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Research, Research Resources, and Publications

Taking a basic science research approach to understanding cancer

Research in the Department of Epigenetics and Molecular Carcinogenesis (EMC) aims to define the mechanisms that control normal cell proliferation, differentiation, survival, and genome maintenance to identify the aberrations in these processes that drive cancer. EMC research focus areas include: Cellular and Molecular Mechanisms of Carcinogenesis; Cancer Genetics and Epigenetics; Genome Integrity - DNA Replication, Recombination and Repair; and Cancer Stem Cells, Apoptosis and Autophagy. EMC hosts research laboratories and research resources on both the North and South MD Anderson campuses in Houston, Texas.

Research

Cellular and Molecular Mechanisms of Carcinogenesis

fluorescence microsocpy image showing localization of proteins SSEA1 and NANOG

The overall goal of our carcinogenesis research is to understand the basic cellular and molecular mechanisms that allow the transformation of normal cells into cancer cells. Defining these mechanisms will help identify new cancer targets and novel strategies for identifying, treating, and preventing cancer.

Departmental carcinogenesis research includes:

Discovering new genetic contributors and drivers of cancers
Identifying genetic and/or therapeutic vulnerabilities in cancers (e.g. CRISPR screens identifying synthetic lethality)
Defining genetic, epigenetic, immunologic, and transcriptional alterations accompanying cancer initiation and progression
Investigating cell signaling pathways involved in cancer induction and progression

Developing novel computational approaches for cancer research

Enormous amounts of data have been generated from high-throughput, genome-wide experimental approaches, thus creating a pressing need for novel computational approaches to mine and interpret complex "-omics" data sets. Understanding these data sets will help define both the players in biological interaction networks and their functions. Research in the department is combining in-silico approaches with wet-lab experiments to identify drivers and attenuators of cancer. Likewise, the development of CRISPR technology has led to new high-throughput approaches such as genome-wide synthetic lethal screens that also benefit from computational approaches, like those being developed in the department to aid the design and interpretation of high-throughput screens.

Researcher pipeting in laminar flow hood

Implementing cutting-edge animal models

Our research relies on the development of genetically engineered animal models for investigating the stepwise molecular changes that occur during carcinogenesis, the function of key genes and gene variants in cancer development, and preclinical prevention and therapeutic studies. A number of existing models are being used for these mechanistic studies, including models for skin, mammary gland, prostate, thymus and blood cancers, but we are also creating novel mouse models using modern knockout/knock-in technologies (e.g. CRISPR-Cas9) to study specific genes and pathways involved in cancer induction and progression.

Making discoveries at the intersection of immunology and tumor biology

Immunotherapy has been hailed as the fourth pillar of cancer therapy joining surgery, chemotherapy, and radiation treatment. Yet, this treatment approach does not work for all patients. Collaborative departmental research has revealed that patients who respond to immunotherapy have antibody responses against their tumors and that the presence of B cells within a tumor may serve as a marker to predict patient immunotherapy response. These findings are leading to new questions about how B cells in tumors affect immunotherapy response.

Examples of faculty members who are defining the Cellular and Molecular Mechanisms of Carcinogenesis:

C. Marcelo Aldaz — Role of WWOX in cancer and disease; genomic determinants controlling development and progression of pre-invasive breast lesions
Shawn Bratton — Autophagy and prostate cancer; caspase-activating complexes
Charles Ishak — Repetitive DNA elements and viral mimicry in tumorigenesis and cancer therapy
Kevin McBride — B cell function and antibody repertoire; B cell lymphoma; role of B cells in immunotherapy response
Ellen Richie — Regulation of thymus development and homeostasis; role of thymic epithelial cells in regulating T-cell development and T-cell receptor repertoire selection
Margarida Almeida Santos — Tumor promoting roles of genome guardians in leukemia
Angela Ting — Role of microbiome-expressed genes in altering host DNA to drive cancer
Richard Wood — Role of DNA polymerase theta in genome stability
Han Xu — Global view of transcriptional and epigenetic regulation using CRISPR screens; machine-learning and statistical algorithms for high-throughput experiments

Cancer Genetics & Epigenetics

Schematic depicting multiple layers of epigenetic influences on chromatin structure

Epigenetic factors that regulate DNA methylation, histone modification and chromatin organization can act as either oncogenes or tumor suppressors. Departmental epigenetics research seeks to define both the normal functions of these factors as well as their roles in cancer formation or suppression.

Readers, Writers and Erasers of Epigenetic Marks

Epigenetic marks include cytosine methylation and hydroxymethylation of DNA and methylation, acetylation, phosphorylation, and ubiquitination of histones. These marks are created by enzymes called "writers." Epigenetic "readers" are effector proteins that bear domains that recognize the specific marks left by the "writers," and epigenetic "erasers" can remove these marks. Thus, multiple epigenomes can be created from a single genome.

Uncovering how epigenetic changes and mutations in epigenetic proteins alter gene expression

The major outcome of epigenetic change is alterations in gene expression. Some epigenetic changes are required for normal development and stem cell differentiation, whereas others are aberrant and can lead to diseases, including immunodeficiency, centromeric region instability and facial anomalies syndrome (ICF) and leukemia and other cancers. Importantly, many epigenetic proteins are mutated in human disease, and epigenetic alterations may be just as important as DNA mutations in driving cancer. In addition to controlling gene transcription, these chromatin-modifying enzymes regulate other processes that require access to DNA, including DNA replication and repair.

The nucleosome is the basic repeating structure of chromatin

Departmental epigenetic research areas include:

Uncovering epigenetic factors controlling developmental reprogramming
Discovering biological roles of histone and non-histone lysine and arginine methylation
Defining the structure and function of epigenetic proteins and epigenetic marks
Finding new cellular functions for ATP-dependent chromatin remodelers
Identifying and characterizing “readers” of epigenetic marks
Understanding the role of histone modifications in DNA repair
Deciphering crosstalk between: histone modifications; histone modifications and DNA methylation; and histone modifications and post-translational modifications of non-histone substrates
Developing technical and computational tools for genome-wide DNA methylation assessment
Defining the functions of DNA methylases and DNA methylation in both normal development and cancer
Understanding the role of DNA methylation-regulated alternative polyadenylation in human health and disease
Defining the contributions of repetitive DNA elements and viral mimicry to cancer initiation and progression and patient therapy response

two researchers use a robotic arm to transfer liquid into multi-well plates

Epigenetics research provides new avenues for cancer treatment

Epimutations, unlike genetic mutations, can be reversed by chemotherapeutic intervention, which makes epigenetic therapy conceptually appealing. Researchers in the department are screening and identifying small-molecule regulators of epigenetic modifiers and evaluating their potential as anti-cancer drugs, providing clear translational relevance to this research.

Making foundational protein arginine methyltransferase inhibitor discoveries

EMC department members worked with Experimental Radiation Oncology to show that the protein arginine methyltransferase CARM1 might be a useful therapeutic target for small cell lung cancer (SCLC) by demonstrating that both CARM1 and its target nuclear factor I B (NFIB) are required for the rapid onset of cancer in a preclinical SCLC model. Further, they showed that CARM1 inhibition combined with etoposide and cisplatin (EP - the current standard of care treatment) led to partial tumor regression in SCLC patient-derived xenograft models, which was superior to that of either CARM1 inhibition or EP alone.

In another example, departmental researchers combined their expertise to use cell culture experiments, computational approaches evaluating cancer cell line RNAi screens, and animal xenograft models to show that small molecule inhibition of CARM1 in CREBBP/EP300-mutated diffuse large B-cell lymphomas (DLBCLs) reduces histone acetyltransferase activity and causes synthetic lethality through downregulation of CBP-target genes. This synthetic interaction reveals the possibility that combination therapy using CARM1 inhibitors with CBP/p300 inhibitors may be useful for treating DLBCLs and other cancers with non-mutated CREBBP/EP300.

Examples of faculty engaged in epigenetics research:

Blaine Bartholomew — ATP-dependent chromatin remodelers influence on chromatin dynamics and non-coding RNA transcription
Mark Bedford — Arginine methylation in cellular processes; development of technologies to identify readers of proteins bearing specific epigenetic marks
Taiping Chen — Biological function of histone methylases and demethylases in development and disease
Xiaodong Cheng — Structure and function of readers, writers, and erasers of DNA modifications and their associated histone modifications
Francesca Cole — Epigenetic regulation of meiotic chromosome organization & pairing
Charles Ishak — DNA repetitive elements in cancer initiation, development and therapeutic response
Margarida Almeida Santos — Epigenetic regulators affecting hematopoietic stem cells
Angela Ting — Defining novel, clinically relevant functions for DNA methylation and the mechanics of DNA methylation in cancer

DNA Replication, Recombination & Repair - Genomic Stability

Mouse meiotic chromosomes (prophase I).

Understanding how DNA is damaged and repaired is fundamental to cancer research

DNA breaks can result from molecularly programmed, intentional DNA damage or non-programmed, incidental DNA damage. Intentional breaks results from specialized cellular processes such as those needed for accurate segregation of chromosomes during meiosis and for creating immune system diversity. In contrast, incidental DNA damage results from exposure to DNA damaging agents from both external and internal sources. External sources include ultraviolet radiation from the sun and chemicals in the environment. Internal sources include reactive chemical species, such as oxygen and water as well as accidental DNA breaks formed during DNA replication. Moreover, many cancer therapies induce irreparable DNA damage leading to cell death. Therefore, investigating how cells respond to and repair DNA damage is important for understanding the causes of cancer and developing new treatments. Research in this area employs a broad range of approaches including protein biochemistry, single-cell genomics, high-resolution microscopy, and genetically engineered mouse models.

scientist pouring a solution into a tray

Departmental research related to genomic stability includes:

Defining molecular mechanisms of DNA double-strand break repair
Discovering new DNA repair pathways and proteins
Defining the functions of DNA polymerases in DNA repair
Characterizing DNA damage and repair processes in normal cell function and in carcinogenesis
Learning how DNA damage and repair contribute to immune system diversity
Unraveling the relationships between DNA damage, chromatin remodeling and DNA repair
Understanding how DNA methylation influences DNA mutation and repair

γ-H2AX foci, in green, mark DNA double-strand breaks

When DNA damage causes cells to go awry

Department investigators are studying the protein machinery involved in several DNA repair pathways, including homologous recombination and DNA end-joining processes for the repair of DNA double-strand breaks, and nucleotide excision repair for the repair of ultraviolet radiation-induced DNA damage and other strand-distorting lesions.

First mammalian HR precursors identified

EMC members uncovered the first evidence of homologous recombination (HR) precursors in mammals. Through molecular and cellular characterizations of >1 million haploid genome equivalents from 13 independent mouse single and double mutant conditions, two distinct recombination precursors were identified that form during mouse meiosis including a double Holliday junction (dHJ) that requires the MutL homolog MLH3, but not its nuclease activity, to form.

Faculty are also uncovering how programmed DNA damage and repair are involved in normal cellular processes, such as meiosis and immune system B cell development, as well as how these normal processes go awry and contribute to cancer and disease.

Other active areas of research include investigations into the actions of DNA polymerases at repair sites, how chromatin-modifying proteins cooperate with the DNA repair machinery to facilitate repair in the context of chromatin, the mechanisms underlying the conversion of DNA damage into the mutations that cause cancer, and the mechanisms that allow cells to tolerate and survive DNA damage.

Examples of faculty members leading the way in DNA Replication, Recombination, and Repair :

Xiaodong Cheng — Role of DNA methylation in DNA mutation and repair
Francesca Cole — DSB repair by homologous recombination during meiosis
Kevin McBride — Role of programmed DNA damage in creating antibody diversity and leading to lymphomagenesis
Margarida Almeida Santos — DNA damage-induced differentiation of stem-like cancer cells
Richard Wood — Nucleotide excision repair, DNA crosslink repair, role of polymerases in DNA damage tolerance

Cancer Stem Cells & Programmed Cell Death

Stem cells in intestinal crypts give rise to all cell types of the intestinal epithelium

Stem cells are undifferentiated cells that are unique in their ability to self-renew to create more stem cells while also being able to create daughter cells that can differentiate into other cell types. Most, if not all, cancerous states reflect inappropriate or incomplete cellular differentiation. Aggressive, therapy resistant cancer cells often resemble stem cells in terms of their transcription profiles and self-renewal capacities. Likewise, unregulated growth, abnormal cell division, and defective apoptotic cell death pathways are hallmark features of tumors.

The goal of research in this area is to define normal stem cell biology and developmental pathways as well as to define genetic, molecular, and biochemical mechanisms that regulate cell proliferation, apoptosis and autophagy and relate these pathways to carcinogenesis.

Person examining a sample with a microscope

Specific research in this area includes:

Defining pathways that govern stem cell biology and embryo development
Understanding DNA damage response in cancer stem cells
Epigenetic modifications in embryonic, adult, and cancer stem cells
Epigenetic mechanisms in early embryos and germ cells
Role of caspases in apoptosis
Apoptosis and autophagy in normal and disease processes

Using stem cells to learn about cancer

Our research using mouse embryonic and adult stem cells has led to several foundational discoveries. For example, research centered on GCN5, a histone acetyltransferase component of the SAGA complex, uncovered a Myc-SAGA axis that is critical for driving stem cells to pluripotency and is essential for the expression of cell-cycle genes driven by MYC overexpression in a mouse model of B cell lymphoma. Studies of SETDB1, a lysine methyltransferase that deposits the repressive H3K9me3 mark, revealed that SETDB1-dependent gene repression is essential for preserving intestinal stem cell identity by modulating the Wnt and Notch signaling pathways. Other research using mouse models of MLL-rearranged acute myeloid leukemia showed that protein arginine methyltransferase 5 (PRMT5) is essential for the initiation and maintenance of MLL-AF9-mediated leukemia and that inhibiting PRMT5 restores normal differentiation to hematopoietic stem cells.

Lysosomes, shown in green in a fibroblast cell, are central to autophagy.

Apoptosis and autophagy: cancer inhibitors and facilitators

Autophagy (self-cannibalism) and apoptosis (programmed cell death) are fundamental cellular processes that provide mechanisms for cell survival (autophagy) and cell death (apoptosis). Autophagy provides cells with means not only to survive cellular stress and to recycle cellular materials and organelles but also to rid themselves of damaged, malformed, or foreign material. Although autophagy helps suppress carcinogenesis, it can also promote tumor progression, metastasis, and cancer therapy resistance. Apoptosis is required for normal organismal development, but also provides a mechanism to stop cells with DNA damage from dividing. Many chemotherapeutics work by causing DNA damage and inducing apoptosis; however, defects in apoptosis contribute to both tumorigenesis and resistance to cancer treatment. Therefore, defining the molecular mechanisms guiding autophagy and apoptosis, and the pathways allowing cross-talk between them, will provide insights into how cells evade and succumb to cancer treatments.

Faculty with research interests in Cancer Stem Cells and Programmed Cell Death:

Blaine Bartholomew — Chromatin remodelers in pluripotency and development
Shawn Bratton — Heat shock- and tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis; caspase-activating complexes and the apoptosome; structure and function of autophagosomes; role of autophagy in prostate cancer
Taiping Chen — Epigenetic regulation of embryonic and adult stem cell behavior and function
Margarida Almeida Santos — Epigenetic regulation of cancer stem cells

EMC Research Resources

Flow Cytometry - EMC

Flow Cytometry-EMC provides cutting-edge resources to dissect the cellular and molecular mechanisms of developmental and disease processes, by aiding researchers in identifying, isolating and quantifying cell types and/or cell subsets, while also offering individualized training on specific instruments and assisting with data analysis and experimental design.

Although Flow Cytometry-EMC focuses on EMC users, non-departmental users may also be accommodated, as time and resources permit.

For microscopy services formerly provided by the Flow Cytometry and Cellular Imaging Core-EMC, please see the Advanced Microscopy Core. Please also see the MD Anderson, CCSG-supported, full-service Flow Cytometry and Cellular Imaging Core Facility, directed by Michael Andreeff, M.D., Ph.D.

Flow Cytometry-EMC, located in South Campus Research Building 4, provides assisted use services (hourly fee) to researchers for analytical flow cytometry on all instruments, including the BD LSR Fortessa, BD FACSAria™ Fusion SORP, BD FACSAria™ Fusion and BDAccuri C6PlusTM. Assisted cell sorts are also available on the BD FACSAria™ Fusion SORP and BD FACSAria™ Fusion. Instrument training is mandatory for users wishing to perform unassisted analyses. The fee schedule is listed in iLab. Please contact Pam Whitney (pjwhitney@mdanderson.org) prior to scheduling initial services.

Analytical Flow Cytometry

Flow cytometry is used broadly in cell biological research. Protein expression or specific indicators of cell status can be measured simultaneously for individual cells within a larger, heterogeneous population. Flow Cytometry-EMC provides access to both to advanced instruments and expert staff to meet researcher needs, while specializing in developing complex assays to quantitatively examine cell surface and cytoplasmic antigens, cell cycle, apoptosis, "side populations" and fluorescent transgene expression (e.g. GFP, YFP, RFP and BFP).

Cell Sorting

Flow Cytometry-EMC cell sorting equipment includes a BD FACSAria™ Fusion, 17 parameter, high-speed cell sorter for processing of ≤ BSL2 samples within a biosafety cabinet and a BD FACSAria™ SORP, 18 parameter, high-speed cell sorter. Users can isolate a wide variety of different cell types based on many different combinations of antibody-based stains, fluorescent protein expression, and viability indicators. Cells are detected using BD FACSDiva™ software and can be collected from a single heterogeneous sample into 1-4 tubes, simultaneously.

Recent software upgrades allow for index sorting, letting researchers identify the origin of single cells collected from within the population defined by their experimental parameters. The automatic cell-dispensing unit can dispense single cells into 96- or 384-well plates. The sample chamber and collection apparatus are climate controlled and aerosol contained.

Flow Cytometry-EMC also operates a Miltenyi Biotec autoMACS Pro Cell Separator, an immunomagnetic cell separation system that can be used to enrich or deplete a population of cells prior to sorting on one of our BD instruments.

Other Services

Multi-parameter analysis and sorting
Full-spectrum analysis of fluorescent proteins
autoMACSpro available for depletion/enrichment of cell populations prior to flow experiments
Sorting cells into a variety of tubes and plates including 96- and 384-well plates
Index sorting allowing identification of which experimental population a particular cell was derived
Guidance with experimental design
Consultation and training

First-Time Users and Training

First-time users should contact Pam Whitney (pjwhitney@mdanderson.org) to schedule a consultation before finalizing any experimental plans. This consultation will aid researchers in optimizing their experimental approach, assay design, and fluorescent panels to ensure recovery of meaningful data, and will define user expectations and service costs for the project. Please schedule your appointment at least one week prior to the anticipated date of service to ensure availability of their chosen instrument. Flow personnel can also assist with data analysis using FlowJo software, or they can perform analysis for a specific project, as time permits, for an additional fee.

Instrument training is mandatory for any user who would perform unassisted flow cytometric analyses. Training is provided by Pam Whitney (pjwhitney@mdanderson.org) and requires uninterrupted blocks of time over multiple days. Please note that all users are responsible for archiving their own data. Flow Cytometry-EMC personnel can assist users in learning this practice.

Pam Whitney oversees the day-to-day operations of Flow Cytometry-EMC

Additional Information and Resources

Sample Preparation

Experimental Samples

All samples should be at a concentration of 5.0 x 10⁶cells/ml in appropriate buffer in 12 x 75 FACS tubes or 15 ml conical tubes depending upon instrument.
Bring additional buffer for concentration adjustments.
All samples must be filtered before running on the instruments.

Control Samples

Each experiment must have proper controls. Biological controls for data samples could include isotype controls for antibody staining or stained normal cycling cells for cell cycle analysis.
The instrument setup requires additional controls: unstained cells and single-stained color controls.
Contact Pam Whitney (pjwhitney@mdanderson.org) for more information about the requirements for your experiment.

Spectrum Viewer & Laser Configuration Files

Tissue Culture Hints

Flow Cytometry-EMC is located in South Campus Research Building 4

BD FACSAria™Fusion SORP

The BD FACSAria™Fusion SORP is a 5-laser, 18-parameter, high-speed cell sorter, with automatic cell-dispensing unit, run by platform personnel. This instrument can be used to isolate and capture viable cell subsets or single cells for molecular, genetic and/or functional analyses. This instrument can distinguish many fluorescent proteins, stem cell and side populations, in addition to fluorescent antibody preparations. Cells are detected by digital BD FACSDiva™ software and collected into one or as many as four tubes simultaneously from a single sample. The cell-dispensing unit on this instrument can dispense single cells into 96- or 384-well plates. The sample chamber and collection apparatus are climate-controlled and aerosol-contained. A laser configuration file for this instrument may be downloaded here.

BD FACSAria™ Fusion

The BD FACSAria™ Fusion is a 5-laser, 17-parameter high-speed cell sorter with biosafety cabinet and automatic cell-dispensing unit. It is the primary flow instrument and is run by platform personnel. It can be used to isolate and capture viable cell subsets or single cells for molecular, genetic, and functional analyses. The instrument provides exceptional sensitivity and resolution for optimal multicolor analysis and cell sorting. It allows users to distinguish many fluorescent proteins, fluorescent antibody preparations, and other markers to identify stem cell and side populations. Cells are detected by digital BD FACSDiva™ software and collected into one, or as many as four tubes, simultaneously. The automatic cell-dispensing unit deposits single cells into 96- or 384-well plates. The enhanced stream stability increases sorting purity and efficiency to help isolate minor subsets of cells (e.g. stem cells) for subsequent in vitro and in vivo experiments. This instrument is contained in a bio-safety cabinet permitting analysis of human specimens while ensuring user protection. A laser configuration file for this instrument may be downloaded here.

BD LSRFortessa™

The BD LSRFortessa™ is a 4-laser, 15-parameter cell analyzer equipped with digital BD FACSDiva™ software. It can be used for quantification of cellular subsets based on the expression of surface or intracellular antigens, analysis of apoptosis and cell cycle parameters, and multiparameter analyses. Individualized training on the BD LSRFortessa™ for unassisted operation is available. A laser configuration file for this instrument may be downloaded here.

Miltenyi autoMACS® Pro Separator

The autoMACS® Pro Separator by Miltenyi is an automated high-speed immunomagnetic cell separation system that can process multiple samples at a time. Many cell and tissue types, including whole blood, can be processed with the use of immunomagnetic beads. Cells can be separated using positive selection, depletion, or untouched isolation programs. It can sort more than 10 million cells per second from samples of up to 4×10⁹ total cells. The system reduces manual sample handling and increases reproducibility.

BD Accuri C6Plus™ Cell Analyzer

The newest Flow Cytometry-EMC instrument is a compact, easy-to-use, BD Accuri C6PlusTM 2 laser, 4-parameter cell analyzer. It is optimized for fluorchromes such as FITC, PE, PerCP-Cy™5.5, APC, and BD Horizon Brilliant™ Blue 515 and can analyze fluorescent proteins such as GFP, YFP, and mCherry.

Bioinformatics and Biostatistics Services - EMC

Bioinformatics

EMC Bioinformatics faculty members work collaboratively with investigators to provide novel computational methods, tools and algorithms for the advancement of cancer disease research. Our bioinformatics faculty engage in collaborative research in the areas of bioinformatics, statistical genetics and systems biology to retrieve and analyze various kinds of biological data including DNA/RNA sequences, protein sequences and structures, microarray data and RT-PCR data for the purpose of facilitating biological discovery. Special emphasis is placed on next-generation sequencing data analysis.

Biostatistics

Biostatistics services are augmented with additional support from faculty in the Quantitative Sciences division. Many modern research projects generate data sets that require statistical analyses. Biostatistics staff members provide expertise for such projects and can aid in early project conception, helping develop a fully elaborated study design, and aiding with data collection and analysis. Early statistical planning and incorporating power calculations into study design can help researchers implement more cost-effective projects by helping determine the appropriate size and scope of a study as well as aiding with approaches for more meaningful data collection and analysis.

Research Areas & Projects

Developing working relationships with MD Anderson research faculty and external collaborators to expand the use of advanced computational techniques and statistical analyses, especially as related to next-generation sequencing (e.g. RNA-Seq, DNA-Seq, ChIP-Seq) and DNA methylation analysis
Providing guidance to faculty, students and coworkers in the use of specialized applications, programming, computation and statistical analysis techniques for interpretation of biological data
Conducting computational biology and bioinformatics/biostatistics seminars and workshops for researchers and students
Co-developing or contributing to grant proposals with research faculty, professional colleagues and external collaborators to apply advanced computing and related bioinformatics research to the study of human cancers and disease
Maintaining awareness of emerging computational technologies and new statistical methods, especially to work with large data sets

Bioinformatics and Biostatistics Services-EMC is located in South Campus Research Building 3

Recombinant Antibody Creation and Production Platform

The McBride Lab hosts the Recombinant Antibody Production and Creation Platform (RAPCP). The platform is used to develop custom, recombinant, monoclonal antibodies using a propriety method for isolating single-antigen-specific plasma cells, following inoculation into mice.

Curated antibody-encoding genes are cloned into expression vectors for recombinant antibody production and purification. The antibodies can then be tested in collaboration with the end-user, using a number of assays based on user priorities. The process results in sequence-defined, recombinant antibodies in as few as 30-90 days. For more information, please see the McBride Lab Research page.

Epigenomics Profiling Core (EpiCore)

The Epigenomics Profiling Core (EpiCore) is an institutional resource for epigenomics research that brings scientific expertise, advanced assays, and specialized equipment not otherwise readily available to MD Anderson Cancer Center researchers. The core offers cost-effective, full-service protocols to investigate DNA methylation (Pyrosequencing Methylation Analysis, RRBS, cfMeDIP-seq, WGBS), chromatin accessibility (ATAC-Seq), and DNA-protein interactions (ChIP-Seq and CUT&RUN). This core facilitates researchers’ efforts to define epigenetic mechanisms that alter chromatin and regulate transcription in normal and disease conditions. To learn more, please see the Epigenomics Profiling Core website.

Advanced Microscopy Core (AMC)

The Advanced Microscopy Core enables any number of studies including those centered on cellular protein distribution, cell fate, tumor heterogeneity, drug delivery and tumoricidal activity, DNA damage repair, development, neurodegeneration, cell migration/invasion, angiogenesis and cancer-stroma interactions. Staff can guide users through tissue fixation, permeabilization, vibratome sectioning, and tissue clearing to optimize specific imaging needs and develop pilot applications for investigators. Staff will assist in selecting the optimal instrument, fuorophores, and fluorophore combinations for a user’s particular study, as well as helping users apply image processing software, such as the IMARIS 4-D Image Analysis and Tracking software, for their downstream analyses.

Please see the Advanced Microscopy Core website for more information.

AMC Instruments include:

DeltaVision OMX Blaze V4 Super-Resolution Microscope
Leica TCS SP8 Confocal Microscope with Environmental Chamber
Zeiss LSM880 Confocal Microscope with Airyscan
Leica SP8 DIVE Multiphoton (2-Photon) Microscope
Zeiss Gaussian Lightsheet 7 (LS7) Microscope
LifeCanvas SmartSPIM Lightsheet Microscope
Zeiss Axio Observer Z1
INCell Analyzer 6500 HS Slide/Plate Scanner

Selected Publications

2024

Carvajal-Maldonado D, Li Y, Returan M, Averill AM, Doublié S, Wood RD. J Biol Chem. Dynamic stem-loop extension by Pol θ and templated insertion during DNA repair. 2024 Jul;300(7):107461.

Chen YC, Bhaskara GB, Lu Y, Lin K, Dent SYR. The SAGA acetyltransferase module is required for the maintenance of MAF and MYC oncogenic gene expression programs in multiple myeloma. Genes Dev. 2024 Aug 21. doi: 10.1101/gad.351789.124. Online ahead of print.

Deogharia M, Venegas-Zamora L, Agrawal A, Shi M, Jain AK, McHugh KJ, Altamirano F, Marian AJ, Gurha P. Histone demethylase KDM5 regulates cardiomyocyte maturation by promoting fatty acid oxidation, oxidative phosphorylation, and myofibrillar organization. Cardiovasc Res. 2024 May 7;120(6):630-643.

Du Z, Lin M, Li Q, Guo D, Xue Y, Liu W, Shi H, Chen T, Dan J. The totipotent 2C-like state safeguards genomic stability of mouse embryonic stem cells. J Cell Physiol. 2024 Jun 11. Online ahead of print.

Fijen C, Drogalis Beckham L, Terino D, Li Y, Ramsden DA, Wood RD, Doublié S, Rothenberg E. Sequential requirements for distinct Polθ domains during theta-mediated end joining. Mol Cell. 2024 Apr 18;84(8):1460-1474.e6.

Hardikar S, Ren R, Ying Z, Zhou J, Horton JR, Bramble MD, Liu B, Lu Y, Liu B, Coletta LD, Shen J, Dan J, Zhang X, Cheng X, Chen T. The ICF syndrome protein CDCA7 harbors a unique DNA binding domain that recognizes a CpG dyad in the context of a non-B DNA. Sci Adv. 2024 Aug 23;10(34):eadr0036.

Hogan CH, Owens SM, Reynoso GV, Liao Y, Meyer TJ, Zelazowska MA, Liu B, Li X, Grosskopf AK, Khairallah C, Kirillov V, Reich NC, Sheridan BS, McBride KM, Gewurz BE, Hickman HD, Forrest JC, Krug LT. Multifaceted roles for STAT3 in gammaherpesvirus latency revealed through in vivo B cell knockout models. mBio. 2024 Feb 14;15(2):e0299823.

Kuang X, Salinger A, Benavides F, Muller WJ, Dent SYR*, Koutelou E*. USP22 overexpression fails to augment tumor formation in MMTV-ERBB2 mice but loss of function impacts MMTV promoter activity. PLoS One. 2024 Jan 18;19(1):e0290837. (*Co-corresponding authors)

Larouche JD, Laumont CM, Trofimov A, Vincent K, Hesnard L, Brochu S, Côté C, Humeau JF, Bonneil É, Lanoix J, Durette C, Gendron P, Laverdure JP, Richie ER, Lemieux S, Thibault P, Perreault C. Transposable elements regulate thymus development and function. Elife. 2024 Apr 18;12:RP91037.

Malone CF, Mabe NW, Forman AB, Alexe G, Engel KL, Chen YC, Soeung M, Salhotra S, Basanthakumar A, Liu B, Dent SYR, Stegmaier K. The KAT module of the SAGA complex maintains the oncogenic gene expression program in MYCN-amplified neuroblastoma. Sci Adv. 2024 May 31;10(22):eadm9449.

Marshall VA, Cornejo Castro EM, Goodman CA, Labo N, Liu I, Fisher NC, Moore KN, Nair A, Immonen T, Keele BF, Polizzotto MN, Uldrick TS, Mu Y, Saswat T, Krug LT, McBride KM, Lurain K, Ramaswami R, Yarchoan R, Whitby D. Sequencing of Kaposi's Sarcoma Herpesvirus (KSHV) genomes from persons of diverse ethnicities and provenances with KSHV-associated diseases demonstrate multiple infections, novel polymorphisms, and low intra-host variance. PLoS Pathog. 2024 Jul 15;20(7):e1012338.

Mise K, Long J, Galvan DL, Ye Z, Fan G, Sharma R, Serysheva II, Moore TI, Jeter CR, Anna Zal M, Araki M, Wada J, Schumacker PT, Chang BH, Danesh FR. NDUFS4 regulates cristae remodeling in diabetic kidney disease. Nat Commun. 2024 Mar 4;15(1):1965.

Patel B, Zhou Y, Babcock RL, Ma F, Zal MA, Kumar D, Medik YB, Kahn LM, Pineda JE, Park EM, Schneider SM, Tang X, Raso MG, Jeter CR, Zal T, Clise-Dwyer K, Keyomarsi K, Giancotti FG, Colla S, Watowich SS.STAT3 protects hematopoietic stem cells by preventing activation of a deleterious autocrine type-I interferon response. Leukemia. 2024 May;38(5):1143-1155.

Pourebrahim R, Montoya RH, Akiyama H, Ostermann L, Khazaei S, Muftuoglu M, Baran N, Zhao R, Lesluyes T, Liu B, Khoury JD, Gagea M, Van Loo P, Andreeff M. Age-specific induction of mutant p53 drives clonal hematopoiesis and acute myeloid leukemia in adult mice. Cell Rep Med. 2024 May 21;5(5):101558.

Saha D, Animireddy S, Bartholomew B. The SWI/SNF ATP-dependent chromatin remodeling complex in cell lineage priming and early development. Biochem Soc Trans. 2024 Apr 24;52(2):603-616.

Saha D, Animireddy S, Lee J, Thommen A, Murvin MM, Lu Y, Calabrese JM, Bartholomew B. Enhancer switching in cell lineage priming is linked to eRNA, Brg1's AT-hook, and SWI/SNF recruitment. Mol Cell. 2024 May 16;84(10):1855-1869.e5.

Sarkar S, Stitzlein LM, Chandra J. Impact of electronic cigarettes on pediatric, adolescent and young adult leukemia patients. Pediatr Med. 2024 Feb 28;7:3. doi: 10.21037/pm-23-43.

Shanley M, Daher M, Dou J, Li S, Basar R, Rafei H, Dede M, Gumin J, Pantaleόn Garcίa J, Nunez Cortes AK, He S, Jones CM, Acharya S, Fowlkes NW, Xiong D, Singh S, Shaim H, Hicks SC, Liu B, Jain A, Zaman MF, Miao Q, Li Y, Uprety N, Liu E, Muniz-Feliciano L, Deyter GM, Mohanty V, Zhang P, Evans SE, Shpall EJ, Lang FF, Chen K, Rezvani K. Interleukin-21 engineering enhances NK cell activity against glioblastoma via CEBPD. Cancer Cell. 2024 Aug 12;42(8):1450-1466.e11.

Sharma M, Barravecchia I, Teis R, Cruz J, Mumby R, Ziemke EK, Espinoza CE, Krishnamoorthy V, Magnuson B, Ljungman M, Koschmann C, Chandra J, Whitehead CE, Sebolt-Leopold JS, Galban S. Targeting DNA Repair and Survival Signaling in Diffuse Intrinsic Pontine Gliomas to Prevent Tumor Recurrence. Mol Cancer Ther. 2024 Jan 3;23(1):24-34.

Shen L, Ma X, Wang Y, Wang Z, Zhang Y, Pham HQH, Tao X, Cui Y, Wei J, Lin D, Abeywanada T, Hardikar S, Halabelian L, Smith N, Chen T, Barsyte-Lovejoy D, Qiu S, Xing Y, Yang Y. Loss-of-function mutation in PRMT9 causes abnormal synapse development by dysregulation of RNA alternative splicing. Nat Commun. 2024 Apr 1;15(1):2809.

Stitzlein LM, Adams JT, Stitzlein EN, Dudley RW, Chandra J. Current and future therapeutic strategies for high-grade gliomas leveraging the interplay between epigenetic regulators and kinase signaling networks. J Exp Clin Cancer Res. 2024 Jan 5;43(1):12.

Teboul L, Amos-Landgraf J, Benavides FJ, Birling MC, Brown SDM, Bryda E, Bunton-Stasyshyn R, Chin HJ, Crispo M, Delerue F, Dobbie M, Franklin CL, Fuchtbauer EM, Gao X, Golzio C, Haffner R, Hérault Y, Hrabe de Angelis M, Lloyd KCK, Magnuson TR, Montoliu L, Murray SA, Nam KH, Nutter LMJ, Pailhoux E, Pardo Manuel de Villena F, Peterson K, Reinholdt L, Sedlacek R, Seong JK, Shiroishi T, Smith C, Takeo T, Tinsley L, Vilotte JL, Warming S, Wells S, Whitelaw CB, Yoshiki A; Asian Mouse Mutagenesis Resource Association; CELPHEDIA infrastructure; INFRAFRONTIER consortium; International Mammalian Genome Society; International Mouse Phenotyping Consortium; International Society for Transgenic Technologies; Mutant Mouse Resource and Research Centers; Phenomics Australia; RRRC- Rat Resource and Research Center; Pavlovic G. Improving laboratory animal genetic reporting: LAG-R guidelines. Nat Commun. 2024 Jul 2;15(1):5574.

Tiniakou I, Hsu PF, Lopez-Zepeda LS, Garipler G, Esteva E, Adams NM, Jang G, Soni C, Lau CM, Liu F, Khodadadi-Jamayran A, Rodrick TC, Jones D, Tsirigos A, Ohler U, Bedford MT, Nimer SD, Kaartinen V, Mazzoni EO, Reizis B. Genome-wide screening identifies Trim33 as an essential regulator of dendritic cell differentiation. Sci Immunol. 2024 Apr 12;9(94):eadi1023.

Tzetzo SL, Kramer ED, Mohammadpour H, Kim M, Rosario SR, Yu H, Dolan MR, Oturkar CC, Morreale BG, Bogner PN, Stablewski AB, Benavides FJ, Brackett CM, Ebos JML, Das GM, Opyrchal M, Nemeth MJ, Evans SS, Abrams SI. Downregulation of IRF8 in alveolar macrophages by G-CSF promotes metastatic tumor progression. iScience. 2024 Feb 10;27(3):109187.

Wible DJ, Parikh Z, Cho EJ, Chen MD, Mukhopadhyay S, Dalby KN, Varadarajan S, Bratton SB. Unexpected inhibition of the lipid kinase PIKfyve reveals an epistatic role for p38 MAPKs in endolysosomal fission and volume control. Cell Death Dis. 2024 Jan 22;15(1).

Viner C, Ishak CA, Johnson J, Walker NJ, Shi H, Sjöberg-Herrera MK, Shen SY, Lardo SM, Adams DJ, Ferguson-Smith AC, De Carvalho DD, Hainer SJ, Bailey TL, Hoffman MM. Modeling methyl-sensitive transcription factor motifs with an expanded epigenetic alphabet. Genome Biol. 2024 Jan 8;25(1):11.

Xuan F, Xuan H, Huang M, He W, Xu H, Shi X, Wen H.The Tudor-knot Domain of KAT5 Regulates Nucleosomal Substrate Acetylation. J Mol Biol. 2024 Apr 1;436(7):168414.

Zhao F, Deng Y, Yang F, Yan Y, Feng F, Peng B, Gao J, Bedford MT, Li H. Molecular Basis for SPINDOC-Spindlin1 Engagement and Its Role in Transcriptional Attenuation. J Mol Biol. 2024 Apr 1;436(7):168371.

Zhang X, Blumenthal RM, Cheng X. Keep Fingers on the CpG Islands. Epigenomes. 2024 Jun 19;8(2):23.

Zhang X, Blumenthal RM, Cheng X. Updated understanding of the protein-DNA recognition code used by C2H2 zinc finger proteins. Curr Opin Struct Biol. 2024 Aug;87:102836.

Zhang X, Xia F, Zhang X, Blumenthal RM, Cheng X. C2H2 Zinc Finger Transcription Factors Associated with Hemoglobinopathies. J Mol Biol. 2024 Apr 1;436(7):168343.

Zehrbach NM, Oh N, Ishak CA. Insights into LINE-1 reverse transcription guide therapy development. Trends Cancer. 2024 Apr;10(4):286-288.

Zhou J, Chen Q, Ren R, Yang J, Liu B, Horton JR, Chang C, Li C, Maksoud L, Yang Y, Rotili D, Jain AK, Zhang X, Blumenthal RM, Chen T, Gao Y, Valente S, Mai A, Cheng X. Quinoline-based compounds can inhibit diverse enzymes that act on DNA. Cell Chem Biol. 2024 Oct 14:S2451-9456(24)00403-3. doi: 10.1016/j.chembiol.2024.09.007. Online ahead of print.

2023

Beilinson HA, Sevilleja A, Spring J, Benavides F, Beilinson V, Neokosmidis N, Golovkina T. A single dominant locus restricts retrovirus replication in YBR/Ei mice. J Virol. 2023 Aug 31;97(8):e0068523.

Chen Q, Liu B, Zeng Y, Hwang JW, Dai N, Corrêa IR Jr, Estecio MR, Zhang X, Santos MA, Chen T, Cheng X. GSK-3484862 targets DNMT1 for degradation in cells. NAR Cancer. 2023 May 17;5(2):zcad022.

Dan J, Du Z, Zhang J, Chen T. The interplay between H3K36 methylation and DNA methylation in cancer. Cancer Biol Med. 2023 Aug 18;20(8):545-52.

Fan H, Wang F, Zeng A, Murison A, Tomczak K, Hao D, Jelloul FZ, Wang B, Barrodia P, Liang S, Chen K, Wang L, Zhao Z, Rai K, Jain AK, Dick J, Daver N, Futreal A, Abbas HA. Single-cell chromatin accessibility profiling of acute myeloid leukemia reveals heterogeneous lineage composition upon therapy-resistance. Commun Biol. 2023 Jul 21;6(1):765.

Figueroa M, Ma H, Alfayez M, Morales-Mantilla DE, Wang F, Lu Y, Estecio M, King KY, Kleinerman ES, Moghaddam SJ, Daver NG, Andreeff M, Konopleva MY, DiNardo CD, Chandra J. Cigarette smoke exposure accelerates AML progression in FLT3-ITD models. Blood Adv. 2023 Nov 14;7(21):6624-6629.

Gao G, Hausmann S, Flores NM, Benitez AM, Shen J, Yang X, Person MD, Gayatri S, Cheng D, Lu Y, Liu B, Mazur PK, Bedford MT. The NFIB/CARM1 partnership is a driver in preclinical models of small cell lung cancer. Nat Commun. 2023 Jan 23;14(1):363.

Gencel-Augusto J, Su X, Qi Y, Whitley EM, Pant V, Xiong S, Shah V, Lin J, Perez E, Fiorotto ML, Mahmud I, Jain AK, Lorenzi PL, Navin NE, Richie ER, Lozano G. Dimeric p53 Mutant Elicits Unique Tumor-Suppressive Activities through an Altered Metabolic Program. Cancer Discov. 2023 May 4;13(5):1230-1249.

Horton JR, Zhou J, Chen Q, Zhang X, Bedford MT, Cheng X. A complete methyl-lysine binding aromatic cage constructed by two domains of PHF2. J Biol Chem. 2023 Feb;299(2):102862.

Hussain T, Sanchez K, Crayton J, Saha D, Jeter C, Lu Y, Abba M, Seo R, Noebels JL, Fonken L, Aldaz CM. WWOX P47T partial loss-of-function mutation induces epilepsy, progressive neuroinflammation, and cerebellar degeneration in mice phenocopying human SCAR12. Prog Neurobiol. 2023 Apr;223:102425.

Liu KJ, Zelazowska MA, McBride KM. The Longitudinal Analysis of Convergent Antibody VDJ Regions in SARS-CoV-2-Positive Patients Using RNA-Seq. Viruses. 2023 May 26;15(6):1253.

Mahadevan KK, LeBleu VS, Ramirez EV, Chen Y, Li B, Sockwell AM, Gagea M, Sugimoto H, Sthanam LK, Tampe D, Zeisberg M, Ying H, Jain AK, DePinho RA, Maitra A, McAndrews KM, Kalluri R. Elimination of oncogenic KRAS in genetic mouse models eradicates pancreatic cancer by inducing FAS-dependent apoptosis by CD8+ T cells. Dev Cell. 2023 May 4;13(5):1230-1249.

Mu Y, Zelazowska MA, Chen Z, Plummer JB, Dong Q, Krug LT, McBride KM. Divergent structures of Mammalian and gammaherpesvirus uracil DNA glycosylases confer distinct DNA binding and substrate activity. DNA Repair (Amst). 2023 Aug;128:103515.

Patel LR, Stratton SA, McLaughlin M, Krause P, Allton K, Rivas AL, Barbosa D, Hart T, Barton MC. Genome-wide CRISPR-Cas9 screen analyzed by SLIDER identifies network of repressor complexes that regulate TRIM24. iScience. 2023 Jun 14;26(7):107126.

Premkumar T, Paniker L, Kang R, Biot M, Humphrey E, Destain H, Ferranti I, Okulate I, Nguyen H, Kilaru V, Frasca M, Chakraborty P, Cole F. Genetic dissection of crossover mutants defines discrete intermediates in mouse meiosis. Mol Cell. 2023 Aug 17;83(16):2941-2958.e7.

Saha D, Hailu S, Hada A, Lee J, Luo J, Ranish JA, Lin YC, Feola K, Persinger J, Jain A, Liu B, Lu Y, Sen P, Bartholomew B. The AT-hook is an evolutionarily conserved auto-regulatory domain of SWI/SNF required for cell lineage priming. Nat Commun. 2023 Aug 4;14(1):4682.

Santos M, Hwang JW, Bedford MT. CARM1 Arginine Methyltransferase as a Therapeutic Target for Cancer. J Biol Chem. 2023 Aug 1:105124.

Smith KR, Paul S, Dong Q, Anannya O, Oldenburg DG, Forrest JC, McBride KM, Krug LT. Uracil-DNA glycosylase of murine gammaherpesvirus 68 binds cognate viral replication factors independently of its catalytic residues. mSphere. 2023 Oct 24;8(5):e0027823.

Srinivasan J, Vasudev A, Shasha C, Selden HJ, Perez E Jr, LaFleur B, Sinari SA, Krueger A, Richie ER, Ehrlich LIR. The initial age-associated decline in early T-cell progenitors reflects fewer pre-thymic progenitors and altered signals in the bone marrow and thymus microenvironments. Aging Cell. 2023 Aug;22(8):e13870.

Stitzlein LM, Gangadharan A, Walsh LM, Nam D, Espejo AB, Singh MM, Patel KH, Lu Y, Su X, Ezhilarasan R, Gumin J, Singh S, Sulman E, Lang FF, Chandra J. Comparison of pharmacological inhibitors of lysine-specific demethylase 1 in glioblastoma stem cells reveals inhibitor-specific efficacy profiles. Front Neurol. 2023 Apr 4;14:1112207.

Stroik S, Carvajal-Garcia J, Gupta D, Edwards A, Luthman A, Wyatt DW, Dannenberg RL, Feng W, Kunkel TA, Gupta GP, Hedglin M, Wood R, Doublié S, Rothenberg E, Ramsden DA. Stepwise requirements for polymerases δ and θ in theta-mediated end joining. Nature. 2023 Nov;623(7988):836-841.

Thiyagarajan T, Ponnusamy S, Hwang DJ, He Y, Asemota S, Young KL, Johnson DL, Bocharova V, Zhou W, Jain AK, Petricoin EF, Yin Z, Pfeffer LM, Miller DD, Narayanan R. Inhibiting androgen receptor splice variants with cysteine-selective irreversible covalent inhibitors to treat prostate cancer. Proc Natl Acad Sci U S A. 2023 Jan 3;120(1):e2211832120.

Wang Y, Bedford MT. Effectors and effects of arginine methylation. Biochem Soc Trans. 2023 Apr 26;51(2):725-734.

Yang J, Horton JR, Liu B, Corces VG, Blumenthal RM, Zhang X, Cheng X. Structures of CTCF-DNA complexes including all 11 zinc fingers. Nucleic Acids Res. 2023 Sep 8;51(16):8447-8462.

Ying Z, Hardikar S, Plummer JB, Hamidi T, Liu B, Chen Y, Shen J, Mu Y, McBride KM, Chen T. Enhanced CD19 activity in B cells contributes to immunodeficiency in mice deficient in the ICF syndrome gene Zbtb24. Cell Mol Immunol. 2023 Dec;20(12):1487-1498

Xu L, Xuan H, He W, Zhang L, Huang M, Li K, Wen H, Xu H, Shi X. TAZ2 truncation confers overactivation of p300 and cellular vulnerability to HDAC inhibition. Nat Commun. 2023 Sep 2;14(1):5362.

Zhang L, He W, Fu R, Wang S, Chen Y, Xu H. Guide-specific loss of efficiency and off-target reduction with Cas9 variants. Nucleic Acids Res. 2023 Oct 13;51(18):9880-9893.

Zheng C, Wei Y, Zhang P, Xu L, Zhang Z, Lin K, Hou J, Lv X, Ding Y, Chiu Y, Jain A, Islam N, Malovannaya A, Wu Y, Ding F, Xu H, Sun M, Chen X, Chen Y. CRISPR/Cas9 screen uncovers functional translation of cryptic lncRNA-encoded open reading frames in human cancer. J Clin Invest. 2023 Mar 1;133(5):e159940.

Zheng C, Wei Y, Zhang P, Lin K, He D, Teng H, Manyam G, Zhang Z, Liu W, Lee HRL, Tang X, He W, Islam N, Jain A, Chiu Y, Cao S, Diao Y, Meyer-Gauen S, Höök M, Malovannaya A, Li W, Hu M, Wang W, Xu H, Kopetz S, Chen Y. CRISPR-Cas9-based functional interrogation of unconventional translatome reveals human cancer dependency on cryptic non-canonical open reading frames. Nat Struct Mol Biol. 2023 Nov 6. Online ahead of print

Zhou J, Deng Y, Iyamu ID, Horton JR, Yu D, Hajian T, Vedadi M, Rotili D, Mai A, Blumenthal RM, Zhang X, Huang R, Cheng X. Comparative Study of Adenosine Analogs as Inhibitors of Protein Arginine Methyltransferases and a Clostridioides difficile-specific DNA Adenine Methyltransferase. ACS Chem Biol. 2023 Apr 21;18(4):734-745.

Zhou J, Horton JR, Menna M, Fiorentino F, Ren R, Yu D, Hajian T, Vedadi M, Mazzoccanti G, Ciogli A, Weinhold E, Hüben M, Blumenthal RM, Zhang X, Mai A, Rotili D, Cheng X. Systematic Design of Adenosine Analogs as Inhibitors of a Clostridioides difficile-Specific DNA Adenine Methyltransferase Required for Normal Sporulation and Persistence. J Med Chem. 2023 Jan 12;66(1):934-950.

2022

Basu S, Dong Y, Kumar R, Jeter C, Tang DG. Slow-cycling (dormant) cancer cells in therapy resistance, cancer relapse and metastasis. Semin Cancer Biol. 2022 Jan;78:90-103.

Carvajal-Maldonado D, Drogalis Beckham L, Wood RD, Doublié S. When DNA Polymerases Multitask: Functions Beyond Nucleotidyl Transfer. Front Mol Biosci. 2022 Jan 7;8:815845

Chen YC, Koutelou E, Dent SYR. Now open: Evolving insights to the roles of lysine acetylation in chromatin organization and function. Mol Cell. 2022 Feb 17;82(4):716-727.

Cheng X, Blumenthal RM. Mediating and maintaining methylation while minimizing mutation: Recent advances on mammalian DNA methyltransferases. Curr Opin Struct Biol. 2022 Aug;75:102433.

Dan J, Chen T. Genetic Studies on Mammalian DNA Methyltransferases. Adv Exp Med Biol. 2022;1389:111-136.

Darbaniyan F, Zheng H, Kanagal-Shamanna R, Lockyer P, Montalban-Bravo G, Estecio M, Lu Y, Soltysiak KA, Chien KS, Yang H, Sasaki K, Class C, Ganan-Gomez I, Do KA, Garcia-Manero G, Wei Y. Transcriptomic Signatures of Hypomethylating Agent Failure in Myelodysplastic Syndromes and Chronic Myelomonocytic Leukemia. Exp Hematol. 2022 Nov;115:44-53.

Fabre ML, Canzoneri R, Gurruchaga A, Lee J, Tatineni P, Kil H, Lacunza E, Aldaz CM*, Abba MC*. MALINC1 an Immune-Related Long Non-Coding RNA Associated with Early-Stage Breast Cancer Progression. Cancers (Basel). 2022 Jun 7;14(12):2819. (*co-corresponding authors)

Fedoriw A#, Shi L#, O'Brien S, Smitheman KN, Wang Y, Hou J, Sherk C, Rajapurkar S, Laraio J, Williams LJ, Xu C, Han G, Feng Q, Bedford MT, Wang L, Barbash O, Kruger RG, Hwu P, Mohammad HP, Peng W. Inhibiting Type I arginine methyltransferase activity promotes the T cell mediated antitumor immune response. Cancer Immunol Res. 2022 Apr 1;10(4):420-436. (#equal contribution)

Fontes F, Rocha S, Sánchez R, Pessina P, Sebastian M, Benavides F, Breijo M. Detection of high antibodies titers against rat leukemia virus in an outbreak of reproductive disorders and lymphomas in Wistar rats. Lab Anim. 2022 Mar 31:236772221085356. doi: 10.1177/00236772221085356. Online ahead of print.

Fu* R, He W*, Dou J, Villarreal OD, Bedford E, Wang H, Hou C, Zhang L, Wang Y, Ma D, Chen Y, Gao X, Depken M, Xu H. Systematic decomposition of sequence determinants governing CRISPR/Cas9 specificity. Nat Commun. 2022 Jan 25;13(1):474. (*equal contribution)

Horton JR, Pathuri S, Wong K, Ren R, Rueda L, Fosbenner DT, Heerding DA, McCabe MT, Pappalardi MB, Zhang X, King BW, Cheng X. Structural characterization of dicyanopyridine containing DNMT1-selective, non-nucleoside inhibitors. Structure. 2022 Jun 2;30(6):793-802.e5.

Huang P, Peslak SA, Ren R, Khandros E, Qin K, Keller CA, Giardine B, Bell HW, Lan X, Sharma M, Horton JR, Abdulmalik O, Chou ST, Shi J, Crossley M, Hardison RC, Cheng X, Blobel GA. HIC2 controls developmental hemoglobin switching by repressing BCL11A transcription. Nat Genet. 2022 Sep;54(9):1417-1426

Huang YH, Chen CW, Sundaramurthy V, Słabicki M, Hao D, Watson CJ, Tovy A, Reyes JM, Dakhova O, Crovetti BR, Galonska C, Lee M, Brunetti L, Zhou Y, Tatton-Brown K, Huang Y, Cheng X, Meissner A, Valk PJM, Van Maldergem L, Sanders MA, Blundell JR, Li W, Ebert BL, Goodell MA. Systematic Profiling of DNMT3A Variants Reveals Protein Instability Mediated by the DCAF8 E3 Ubiquitin Ligase Adaptor. Cancer Discov. 2022 Jan;12(1):220-235.

Iannelli G, Milite C, Marechal N, Cura V, Bonnefond L, Troffer-Charlier N, Feoli A, Rescigno D, Wang Y, Cipriano A, Viviano M, Bedford MT, Cavarelli J, Castellano S, Sbardella G. Turning Nonselective Inhibitors of Type I Protein Arginine Methyltransferases into Potent and Selective Inhibitors of Protein Arginine Methyltransferase 4 through a Deconstruction-Reconstruction and Fragment-Growing Approach. J Med Chem. 2022 Apr 28. doi: 10.1021/acs.jmedchem.2c00252. Online ahead of print.

Kannan S, Irwin ME, Herbrich SM, Cheng T, Patterson LL, Aitken MJL, Bhalla K, You MJ, Konopleva M, Zweidler-McKay PA, Chandra J. Targeting the NRF2/HO-1 Antioxidant Pathway in FLT3-ITD-Positive AML Enhances Therapy Efficacy. Antioxidants (Basel). 2022 Apr 5;11(4):717.

Khan FI, Rehman T, Sameena F, Hussain T*, AlAjmi MF, Lai D, Khan MKA. Investigating the binding mechanism of topiramate with bovine serum albumin using spectroscopic and computational methods. J Mol Recognit. 2022 Jul;35(7):e2958. (*postdoctoral fellow with C.M. Aldaz)

Kim KB, Kabra A, Kim DW, Xue Y*, Huang Y, Hou PC, Zhou Y, Miranda LJ, Park JI, Shi X, Bender TP, Bushweller JH, Park KS. KIX domain determines a selective tumor-promoting role for EP300 and its vulnerability in small cell lung cancer. Sci Adv. 2022 Feb 18;8(7):eabl4618. (*graduate student with X. Shi)

Koutelou E, Dent SYR. Navigating EMT with COMPASS and PRC2. Nat Cell Biol. 2022 Apr;24(4):412-414. (News & Views article)

Lancaster JN, Keatinge-Clay DE, Srinivasan J, Li Y, Selden HJ, Nam S, Richie ER, Ehrlich LIR. Central tolerance is impaired in the middle-aged thymic environment. Aging Cell. 2022 Jun;21(6):e13624. PMID: 35561351

Liao Y, Chen CH, Xiao T, de la Peña Avalos B, Dray EV, Cai C, Gao S, Shah N, Zhang Z, Feit A, Xue P, Liu Z, Yang M, Lee JH, Xu H, Li W, Mei S, Pierre RS, Shu S, Fei T, Duarte M, Zhao J, Bradner JE, Polyak K, Kantoff PW, Long H, Balk SP, Liu XS, Brown M, Xu K. Inhibition of EZH2 transactivation function sensitizes solid tumors to genotoxic stress. Proc Natl Acad Sci U S A. 2022 Jan 18;119(3):e2105898119.

Liu Y, Iqbal A, Li W, Ni Z, Wang Y, Ramprasad J, Abraham KJ, Zhang M, Zhao DY, Qin S, Loppnau P, Jiang H, Guo X, Brown PJ, Zhen X, Xu G, Mekhail K, Ji X, Bedford MT, Greenblatt JF, Min J. A small molecule antagonist of SMN disrupts the interaction between SMN and RNAP II. Nat Commun. 2022 Sep 16;13(1):5453.

Meng H, Gonzales NM, Jung SY, Lu Y, Putluri N, Zhu B, Dacso CC, Lonard DM, O'Malley BW. Defining the mammalian coactivation of hepatic 12-h clock and lipid metabolism. Cell Rep. 2022 Mar 8;38(10):110491.

Miglioranza Scavuzzi B, van Drongelen V, Kaur B, Fox JC, Liu J, Mesquita-Ferrari RA, Kahlenberg JM, Farkash EA, Benavides F, Miller FW, Sawalha AH, Holoshitz J. The lupus susceptibility allele DRB1*03:01 encodes a disease-driving epitope. Commun Biol. 2022 Jul 28;5(1):751.

Moyret-Lalle C, Prodhomme MK*, Burlet D, Kashiwagi A, Petrilli V, Puisieux A, Seimiya H, Tissier A. Role of EMT in the DNA damage response, double-strand break repair pathway choice and its implications in cancer treatment. Cancer Sci. 2022 May 9. doi: 10.1111/cas.15389. Online ahead of print. (*Prodhomme is a postdoc in the Wood lab)

Mustachio LM, Roszik J . Single-Cell Sequencing: Current Applications in Precision Onco-Genomics and Cancer Therapeutics. Cancers (Basel). 2022 Jan 28;14(3):657.

Ozirmak Lermi N, Gray SB, Bowen CM, Reyes-Uribe L, Dray BK, Deng N, Harris RA, Raveendran M, Benavides F, Hodo CL, Taggart MW, Colbert Maresso K, Sinha KM, Rogers J, Vilar E. Comparative molecular genomic analyses of a spontaneous rhesus macaque model of mismatch repair-deficient colorectal cancer. PLoS Genet. 2022 Apr 21;18(4):e1010163.

Park D, Gharghabi M, Reczek CR, Plow R, Yungvirt C, Aldaz CM, Huebner K. Wwox Binding to the Murine Brca1-BRCT Domain Regulates Timing of Brip1 and CtIP Phospho-Protein Interactions with This Domain at DNA Double-Strand Breaks, and Repair Pathway Choice. Int J Mol Sci. 2022 Mar 28;23(7):3729.

Perez CJ, Mecklenburg L, Fernandez A, Cantero M, de Souza T, Lin K, Dent SYR, Montoliu L, Awgulewitsch A, Benavides, F. Naked (N) mutant mice carry a nonsense mutation in the homeobox of Hoxc13. Exp Dermatol. 2022 Mar;31(3):330-340.

Piya S, Yang Y, Bhattacharya S, Sharma P, Ma H, Mu H, He H, Ruvolo V, Baran N, Davis RE, Jain AK, Konopleava M, Kantarjian H, Andreeff M, You MJ, Borthakur G. Targeting the NOTCH1-MYC-CD44 axis in leukemia-initiating cells in T-ALL. Leukemia. 2022 May;36(5):1261-1273.

Ren R#, Horton JR#, Hong S, Cheng X. Recent Advances on DNA Base Flipping: A General Mechanism for Writing, Reading, and Erasing DNA Modifications. Adv Exp Med Biol. 2022;1389:295-315. (#equal contribution)

Soundararajan R, Viscuse P, Pilie P, Liu J, Logotheti S, Laberiano Fernández C, Lorenzini D, Hoang A, Lu W, Soto LMS, Wistuba II, Xu M, Song X, Shepherd PDA, Navone NM, Tidwell RSS, Lozano G, Logothetis C, Zhang J, Long JP, Estecio MR, Tzelepi V, Aparicio AM. Genotype-to-Phenotype Associations in the Aggressive Variant Prostate Cancer Molecular Profile (AVPC-m) Components. Cancers (Basel). 2022 Jun 30;14(13):3233.

Srour N, Villarreal OD, Hardikar S, Yu Z, Preston S, Miller WH Jr, Szewczyk MM, Barsyte-Lovejoy D, Xu H, Chen T, del Rincón SV, Richard S. PRMT7 ablation stimulates anti-tumor immunity and sensitizes melanoma to immune checkpoint blockade. Cell Rep. 2022 Mar 29;38(13):110582.

Tu SM, Estecio MR, Lin SH, Zacharias NM. Stem Cell Theory of Cancer: Rude Awakening or Bad Dream from Cancer Dormancy? Cancers (Basel). 2022 Jan 27;14(3):655.

Van HT, Harkins PR, Patel A, Jain AK, Lu Y, Bedford MT, Santos MA. Methyl-lysine readers PHF20 and PHF20L1 define two distinct gene expression-regulating NSL complexes. J Biol Chem. 2022 Mar;298(3):101588.

Vanson S, Li Y, Wood RD, Doublié S.Probing the structure and function of polymerase θ helicase-like domain. DNA Repair (Amst). 2022 Aug;116:103358.

Wang Y, Person MD, Bedford MT. Pan-methylarginine antibody generation using PEG linked GAR motifs as antigens. Methods. 2022 Apr;200:80-86.

Wang Z, Lu Y, Fornage M, Jiao L, Shen J, Li D, Wei P. Identification of novel susceptibility methylation loci for pancreatic cancer in a two-phase epigenome-wide association study. Epigenetics. 2022 Nov;17(11):1357-1372.

Wood RD, Doublié S. Genome Protection by DNA Polymerase θ. Annu Rev Genet. 2022 Nov 30;56:207-228.

Yang J*, Gupta E*, Horton JR, Blumenthal RM, Zhang X, Cheng X. DNA Repair. Differential ETS1 binding to T:G mismatches within a CpG dinucleotide contributes to C-to-T somatic mutation rate of the IDH2 hotspot at codon Arg140. DNA Repair DNA Repair (Amst). 2022 Apr;298(4):101751. (*equal contribution)

Yu D, Dai N, Wolf EJ, Corrêa IR Jr, Zhou J, Wu T, Blumenthal RM, Zhang X, Cheng X. Enzymatic characterization of mRNA cap adenosine-N6 methyltransferase PCIF1 activity on uncapped RNAs. J Biol Chem. 2022 Apr;298(4):101751

Yu D, Zhou J, Chen Q, Wu T, Blumenthal RM, Zhang X, Cheng X. Enzymatic Characterization of In Vitro Activity of RNA Methyltransferase PCIF1 on DNA. Biochemistry. 2022 May 23;61(11):1005-13.

Zhou J, Horton JR, Yu D, Ren R, Blumenthal RM, Zhang X, Cheng X. Repurposing epigenetic inhibitors to target the Clostridioides difficile-specific DNA adenine methyltransferase and sporulation regulator CamA. Epigenetics. 2022 Sep;17(9):970-981.

Zhao S, Habib SL, Senejani AG, Sebastian M, Kidane D. Role of Base Excision Repair in Innate Immune Cells and Its Relevance for Cancer Therapy. Biomedicines. 2022 Feb 26;10(3):557.

Zhang Y, Li Y, Chachad D, Liu B, Godavarthi JD, Williams-Villalobo A, Lasisi L, Xiong S, Matin A. In silico analysis of DND1 and its co-expressed genes in human cancers. Biochem Biophys Rep. 2022 Jan 13;29:101206.

Zhang Y, Williams-Villalobo A, Godavarthi JD, Shakoor F, Xiong S, Liu B. Integrative bioinformatic analysis of p53 and pathway alterations in two different lung cancer subtypes. Biochem Biophys Rep. 2022 Dec 7;33:101404.

2021

Abba MC, Fabre ML, Lee J, Tatineni P, Kil H, Aldaz CM. HOTAIR Modulated Pathways in Early-Stage Breast Cancer Progression. Front Oncol. 2021 Nov 17;11:783211.

Bailey CP, Wang R, Figueroa M, Zhang S, Wang L, Chandra J. Computational immune infiltration analysis of pediatric high-grade gliomas (pHGGs) reveals differences in immunosuppression and prognosis by tumor location. Comput Syst Oncol. 2021 Sep;1(3):e1016.

Ben Yamin B#, Ahmed-Seghir S#, Tomida J#, Despras E, Pouvelle C, Yurchenko A, Goulas J, Corre R, Delacour Q, Droin N, Dessen P, Goidin D, Lange SS, Bhetawal S, Mitjavila-Garcia MT, Baldacci G, Nikolaev S, Cadoret JC*, Wood RD*, Kannouche PL*. DNA polymerase zeta contributes to heterochromatin replication to prevent genome instability. EMBO J. 2021 Nov 2;40(21):e104543. (#equal contributions as first authors, *equal contributions as senior authors)

Carvajal-Maldonado D, Wood RD. Regulating Polθ in Breast Cancer. Cancer Res. 2021 Mar 15;81(6):1441-1442.

Chen J, Horton J, Sagum C, Zhou J, Cheng X, Bedford MT. Histone H3 N-terminal mimicry drives a novel network of methyl-effector interactions. Biochem J. 2021 May 28;478(10):1943-1958.

Chen LM, Chai JC, Liu B, Strutt TM, McKinstry KK, Chai KX. Prostasin regulates PD-L1 expression in human lung cancer cells. Biosci Rep. 2021 Jul 30;41(7):BSR20211370.

Cheng T, Kiser K, Grasse L, Iles L, Bartholomeusz G, Samaniego F, Orlowski RZ, Chandra J. Expression of histone deacetylase (HDAC) family members in bortezomib-refractory multiple myeloma and modulation by panobinostat. Cancer Drug Resist. 2021;4(4):888-902.

Chen YC, Dent SYR. Conservation and diversity of the eukaryotic SAGA coactivator complex across kingdoms. Epigenetics Chromatin. 2021 Jun 10;14(1):26.

Dejima H, Hu X, Chen R, Zhang J, Fujimoto J, Parra ER, Haymaker C, Hubert SM, Duose D, Solis LM, Su D, Fukuoka J, Tabata K, Pham HHN, Mcgranahan N, Zhang B, Ye J, Ying L, Little L, Gumbs C, Chow CW, Estecio MR, Godoy MCB, Antonoff MB, Sepesi B, Pass HI, Behrens C, Zhang J, Vaporciyan AA, Heymach JV, Scheet P, Lee JJ, Wu J, Futreal PA, Reuben A, Kadara H, Wistuba II, Zhang J. Immune evolution from preneoplasia to invasive lung adenocarcinomas and underlying molecular features. Nat Commun. 2021 May 11;12(1):2722.

DiNardo CD, Beird HC, Estecio M, Hardikar S, Takahashi K, Bannon SA, Borthakur G, Jabbour E, Gumbs C, Khoury JD, Routbort M, Gong T, Kondo K, Kantarjian H, Garcia-Manero G, Chen T, Futreal PA. Germline DNMT3A mutation in familial acute myeloid leukaemia. Epigenetics. 2021 May;16(5):567-576.

Genois MM, Gagné JP, Yasuhara T, Jackson J, Saxena S, Langelier MF, Ahel I, Bedford MT, Pascal JM, Vindigni A, Poirier GG, Zou L. CARM1 regulates replication fork speed and stress response by stimulating PARP1. Mol Cell. 2021 Feb 18;81(4):784-800.e8

He W, Wang H, Wei Y, Jiang Z, Tang Y, Chen Y, Xu H. GuidePro: A multi-source ensemble predictor for prioritizing sgRNAs in CRISPR/Cas9 protein knockouts. Bioinformatics. 2021 Jan 4:btaa1068.

Hu X, Estecio MR, Chen R, Reuben A, Wang L, Fujimoto J, Carrot-Zhang J, McGranahan N, Ying L, Fukuoka J, Chow CW, Pham HHN, Godoy MCB, Carter BW, Behrens C, Zhang J, Antonoff MB, Sepesi B, Lu Y, Pass HI, Kadara H, Scheet P, Vaporciyan AA, Heymach JV, Wistuba II, Lee JJ, Futreal PA, Su D, Issa JJ, Zhang J. Evolution of DNA methylome from precancerous lesions to invasive lung adenocarcinomas. Nat Commun. 2021 Jan 29;12(1):687.

Jung YS, Stratton SA, Lee SH, Kim MJ, Jun S, Zhang J, Zheng B, Cervantes CL, Cha JH, Barton MC, Park JI. TMEM9-v-ATPase Activates Wnt/β-Catenin Signaling via APC Lysosomal Degradation for Liver Regeneration and Tumorigenesis. Hepatology. 2021 Feb;73(2):776-794.

Koutelou E, Farria AT, Dent SYR. Complex functions of Gcn5 and PCAF in development and disease. Biochim Biophys Acta Gene Regul Mech. 2021 Feb;1864(2):194609.

Kuang X, McAndrew MJ, Mustachio LM, Chen YC, Atanassov BS, Lin K, Lu Y, Shen J, Salinger A, Macatee T, Dent SYR*, Koutelou E*. Usp22 Overexpression Leads to Aberrant Signal Transduction of Cancer-Related Pathways but Is Not Sufficient to Drive Tumor Formation in Mice. Cancers (Basel). 2021 Aug 25;13(17):4276. (*co-corresponding authors)

Lan X, Ren R, Feng R, Ly LC, Lan Y, Zhang Z, Aboreden N, Qin K, Horton JR, Grevet JD, Mayuranathan T, Abdulmalik O, Keller CA, Giardine B, Hardison RC, Crossley M, Weiss MJ, Cheng X, Shi J, Blobel GA. ZNF410 Uniquely Activates the NuRD Component CHD4 to Silence Fetal Hemoglobin Expression. Mol Cell. 2021 Jan 21;81(2):239-254.e8.

Llorens-Agost M, Ensminger M, Le HP, Gawai A, Liu J, Cruz-García A, Bhetawal S, Wood RD, Heyer WD, Löbrich M. POLθ-mediated end joining is restricted by RAD52 and BRCA2 until the onset of mitosis. Nat Cell Biol. 2021 Oct;23(10):1095-1104.

Manickavinayaham S, Dennehey BK, Johnson DG. Direct Regulation of DNA Repair by E2F and RB in Mammals and Plants: Core Function or Convergent Evolution? Cancers (Basel). 2021 Feb 24;13(5):934.

Martin SK, Tomida J, Wood RD. Disruption of DNA polymerase ζ engages an innate immune response. Cell Rep. 2021 Feb 23;34(8):108775.

Morales F, Corrales E, Zhang B, Vásquez M, Santamaría-Ulloa C, Quesada H, Sirito M, Estecio MR, Monckton DG, Krahe R. Myotonic dystrophy type 1 (DM1) clinical subtypes and CTCF site methylation status flanking the CTG expansion are mutant allele length-dependent. Hum Mol Genet. 2021 Dec 27;31(2):262-274.

Muradova E, Patel N, Sell B, Bittencourt BB, Ojeda SS, Adelmann CH, Cen L, Cheng CH, Shen J, Davis CM, Ehli EA, Newberg JY, Cherpelis B, Black MA, Mann MB, Mitragotri S, Tsai KY. Noninvasive Assessment of Epidermal Genomic Markers of UV Exposure in Skin. J Invest Dermatol. 2021 Jan;141(1):124-131.e2.

Pappalardi MB, Keenan K, Cockerill M, Kellner WA, Stowell A, Sherk C, Wong K, Pathuri S, Briand J, Steidel M, Chapman P, Groy A, Wiseman AK, McHugh CF, Campobasso N, Graves AP, Fairweather E, Werner T, Raoof A, Butlin RJ, Rueda L, Horton JR, Fosbenner DT, Zhang C, Handler JL, Muliaditan M, Mebrahtu M, Jaworski JP, McNulty DE, Burt C, Eberl HC, Taylor AN, Ho T, Merrihew S, Foley SW, Rutkowska A, Li M, Romeril SP, Goldberg K, Zhang X, Kershaw CS, Bantscheff M, Jurewicz AJ, Minthorn E, Grandi P, Patel M, Benowitz AB, Mohammad HP, Gilmartin AG, Prinjha RK, Ogilvie D, Carpenter C, Heerding D, Baylin SB, Jones PA, Cheng X, King BW, Luengo JI, Jordan AM, Waddell I, Kruger RG, McCabe MT. Discovery of a first-in-class reversible DNMT1-selective inhibitor with improved tolerability and efficacy in acute myeloid leukemia. Nat Cancer. 2021 Oct;2(10):1002-1017.

Park D, Gharghabi M, Schrock MS, Plow R, Druck T, Yungvirt C, Aldaz CM, Huebner K. Interaction of Wwox with Brca1 and associated complex proteins prevents premature resection at double-strand breaks and aberrant homologous recombination. DNA Repair (Amst). 2022 Feb;110:103264.

Shah VV*, Duncan AD*, Jiang S*, Stratton SA, Allton KL, Yam C, Jain A, Krause PM, Lu Y, Cai S, Tu Y, Zhou X, Zhang X, Jiang Y, Carroll CL, Kang Z, Liu B, Shen J, Gagea M, Manu SM, Huo L, Gilcrease M, Powell RT, Guo L, Stephan C, Davies PJ, Parker-Thornburg J, Lozano G, Behringer RR, Piwnica-Worms H, Chang JT, Moulder SL, Barton MC. Mammary-specific expression of Trim24 establishes a mouse model of human metaplastic breast cancer. Nat Commun. 2021 Sep 10;12(1):5389. (*co-first authors)

Srinivasan J, Lancaster JN, Singarapu N, Hale LP, Ehrlich LIR, Richie ER. Age-Related Changes in Thymic Central Tolerance. Front Immunol. 2021 Apr 22;12:676236. (Review)

Sun M#, Wang Y#, Zheng C#, Wei Y, Hou J, Zhang P, He W, Lv X, Ding Y, Liang H, Hon CC, Chen X, Xu H*, Chen Y*. Systematic functional interrogation of human pseudogenes using CRISPRi. Genome Biol. 2021 Aug 23;22(1):240. (#equal contribution, *co-corresponding authors)

Toraason E, Horacek A, Clark C, Glover ML, Adler VL, Premkumar T, Salagean A, Cole F, Libuda DE. Meiotic DNA break repair can utilize homolog-independent chromatid templates in C. elegans. Curr Biol. 2021 Apr 12;31(7):1508-1514.e5.

Trinh A, Gil Del Alcazar CR, Shukla SA, Chin K, Chang YH, Thibault G, Eng J, Jovanović B, Aldaz CM, Park SY, Jeong J, Wu C, Gray J, Polyak K. Genomic Alterations during the In Situ to Invasive Ductal Breast Carcinoma Transition Shaped by the Immune System. Mol Cancer Res. 2021 Apr;19(4):623-635.

Wright T, Wang Y, Bedford MT. The Role of the PRMT5-SND1 Axis in Hepatocellular Carcinoma. Epigenomes. 2021 Mar;5(1):2. (Review)

Yang F, Chen J, Liu B, Gao G, Sebastian M, Jeter C, Shen J, Person MD, Bedford MT. SPINDOC binds PARP1 to facilitate PARylation. Nat Commun. 2021 Nov 4;12(1):6362.

Yang J, Horton JR, Akdemir KC, Li J, Huang Y, Kumar J, Blumenthal RM, Zhang X, Cheng X. Preferential CEBP binding to T:G mismatches and increased C-to-T human somatic mutations. Nucleic Acids Res. 2021 May 21;49(9):5084-5094.

Yang Y, Ren R, Ly LC, Horton JR, Li F, Quinlan KGR, Crossley M, Shi Y, Cheng X. Structural basis for human ZBTB7A action at the fetal globin promoter. Cell Rep. 2021 Sep 28;36(13):109759.

Yu D#, Horton JR#, Yang J, Hajian T, Vedadi M, Sagum CA, Bedford MT, Blumenthal RM, Zhang X, Cheng X. Human MettL3-MettL14 RNA adenine methyltransferase complex is active on double-stranded DNA containing lesions. Nucleic Acids Res. 2021 Nov 18;49(20):11629-11642. (#equal contribution)

Zhou J#, Horton JR#, Blumenthal RM, Zhang X, Cheng X. Clostridioides difficile specific DNA adenine methyltransferase CamA squeezes and flips adenine out of DNA helix. Nat Commun. 2021 Jun 8;12(1):3436. (#equal contribution)

2020

Abba MC, Canzoneri R, Gurruchaga A, Lee J, Tatineni P, Kil H, Lacunza E, Aldaz CM. LINC00885 a Novel Oncogenic Long Non-Coding RNA Associated with Early Stage Breast Cancer Progression. Int J Mol Sci. 2020 Oct 8;21(19):7407.

Benavides F, Rülicke T, Prins JB, Bussell J, Scavizzi F, Cinelli P, Herault Y, Wedekind D. Genetic quality assurance and genetic monitoring of laboratory mice and rats: FELASA Working Group Report. Lab Anim. 2020 Apr;54(2):135-148.

Bhardwaj SK, Hailu SG, Olufemi L, Brahma S, Kundu S, Hota SK, Persinger J, Bartholomew B. Dinucleosome specificity and allosteric switch of the ISW1a ATP-dependent chromatin remodeler in transcription regulation. Nat Commun. 2020 Nov 20;11(1):5913.

Farria AT, Plummer JB, Salinger AP, Shen J, Lin K, Lu Y, McBride KM, Koutelou E, Dent SYR. Transcriptional Activation of MYC-Induced Genes by GCN5 Promotes B-cell Lymphomagenesis. Cancer Res. 2020 Dec 15;80(24):5543-5553.

Hardikar S, Ying Z, Zeng Y, Zhao H, Liu B, Veland N, McBride K, Cheng X, Chen T. The ZBTB24-CDCA7 axis regulates HELLS enrichment at centromeric satellite repeats to facilitate DNA methylation. Protein Cell. 2020 Mar;11(3):214-218.

Helmink BA, Reddy SM, Gao J, Zhang S, Basar R, Thakur R, Yizhak K, Sade-Feldman M, Blando J, Han G, Gopalakrishnan V, Xi Y, Zhao H, Amaria RN, Tawbi HA, Cogdill AP, Liu W, LeBleu VS, Kugeratski FG, Patel S, Davies MA, Hwu P, Lee JE, Gershenwald JE, Lucci A, Arora R, Woodman S, Keung EZ, Gaudreau PO, Reuben A, Spencer CN, Burton EM, Haydu LE, Lazar AJ, Zapassodi R, Hudgens CW, Ledesma DA, Ong S, Bailey M, Warren S, Rao D, Krijgsman O, Rozeman EA, Peeper D, Blank CU, Schumacher TN, Butterfield LH, Zelazowska MA, McBride KM, Kalluri R, Allison J, Petitprez F, Fridman WH, Sautès-Fridman C, Hacohen N, Rezvani K, Sharma P, Tetzlaff MT, Wang L, Wargo JA. B cells and tertiary lymphoid structures promote immunotherapy response. Nature. 2020 Jan;577(7791):549-555.

Hwang T, Reh S, Dunbayev Y, Zhong Y, Takata Y, Shen J, McBride KM, Murnane JP, Bhak J, Lee S, Wood RD, Takata KI. Defining the mutation signatures of DNA polymerase θ in cancer genomes. NAR Cancer. 2020 Sep;2(3):zcaa017.

Jain K, Fraser CS, Marunde MR, Parker MM, Sagum C, Burg JM, Hall N, Popova IK, Rodriguez KL, Vaidya A, Krajewski K, Keogh MC, Bedford MT*, Strahl BD.* Characterization of the plant homeodomain (PHD) reader family for their histone tail interactions. Epigenetics Chromatin. 2020 Jan 24;13(1):3 (*Co-corresponding authors)

Kumar A, Zhong Y, Albrecht A, Sang PB, Maples A, Liu Z, Vinayachandran V, Reja R, Lee CF, Kumar A, Chen J, Xiao J, Park B, Shen J, Liu B, Person MD, Trybus KM, Zhang KYJ, Pugh BF, Kamm KE, Milewicz DM, Shen X*, Kapoor P*. Actin R256 Mono-methylation Is a Conserved Post-translational Modification Involved in Transcription. Cell Rep. 2020 Sep 29;32(13):108172. (*co-corresponding authors)

Kumar J, Kaur G, Ren R, Lu Y, Lin K, Li J, Huang Y, Patel A, Barton MC, Macfarlan T, Zhang X, Cheng X. KRAB domain of ZFP568 disrupts TRIM28-mediated abnormal interactions in cancer cells. NAR Cancer. 2020 Jun;2(2):zcaa007.

Shen Y, Gao G, Yu X, Kim H, Wang L, Xie L, Schwarz M, Chen X, Guccione E, Liu J*, Bedford MT*, Jin J*. Discovery of First-in-Class Protein Arginine Methyltransferase 5 (PRMT5) Degraders. J Med Chem. 2020 Sep 10;63(17):9977-9989. (*Co-corresponding authors)

Turner OC, Aeffner F, Bangari DS, High W, Knight B, Forest T, Cossic B, Himmel LE, Rudmann DG, Bawa B, Muthuswamy A, Aina OH, Edmondson EF, Saravanan C, Brown DL, Sing T, Sebastian MM. Society of Toxicologic Pathology Digital Pathology and Image Analysis Special Interest Group Article*: Opinion on the Application of Artificial Intelligence and Machine Learning to Digital Toxicologic Pathology. Toxicol Pathol. 2020 Feb;48(2):277-294.

Veazey KJ, Cheng D, Lin K, Villarreal OD, Gao G, Perez-Oquendo M, Van HT, Stratton SA, Green M, Xu H, Lu Y, Bedford MT, Santos MA. CARM1 inhibition reduces histone acetyltransferase activity causing synthetic lethality in CREBBP/EP300-mutated lymphomas. Leukemia. 2020 Jun 24. doi: 10.1038/s41375-020-0908-8.

Woodcock CB, Horton JR, Zhou J, Bedford MT, Blumenthal RM, Zhang X, Cheng X. Biochemical and structural basis for YTH domain of human YTHDC1 binding to methylated adenine in DNA. Nucleic Acids Res. 2020 Oct 9;48(18):10329-10341.

Zelazowska MA, Dong Q, Plummer JB, Zhong Y, Liu B, Krug LT, McBride KM. Gammaherpesvirus-infected germinal center cells express a distinct immunoglobulin repertoire. Life Sci Alliance. 2020 Feb 6;3(3):e201900526.

Zeng Y*, Ren R*, Kaur G, Hardikar S, Ying Z, Babcock L, Gupta E, Zhang X, Chen T#, Cheng X#. The inactive Dnmt3b3 isoform preferentially enhances Dnmt3b-mediated DNA methylation. Genes Dev. 2020 Oct 1;34(21-22):1546-58. (*co-first authors, #co-corresponding authors)

2019

Bao J, Di Lorenzo A, Lin K, Lu Y, Zhong Y, Sebastian MM, Muller WJ, Yang Y, Bedford MT. (2019) Mouse models of overexpression reveal distinct oncogenic roles for different type I protein arginine methyltransferases. Cancer Res. 79(1):21-32.

Gao G, Zhang L, Villarreal OD, He W, Su D, Bedford E, Moh P, Shen J, Shi X, Bedford MT, Xu H. (2019) PRMT1 loss sensitizes cells to PRMT5 inhibition. Nucleic Acids Res. 47(10):5038-5048.

He W, Zhang L, Villarreal OD, Fu R, Bedford E, Dou J, Patel AY, Bedford MT, Shi X, Chen T, Bartholomew B, Xu H. (2019) De novo identification of essential protein domains from CRISPR-Cas9 tiling-sgRNA knockout screens. Nat Commun. 10(1):4541.

Hussain T, Kil H, Hattiangady B, Lee J, Kodali M, Shuai B, Attaluri S, Takata Y, Shen J, Abba MC, Shetty AK, Aldaz CM. (2019) Wwox deletion leads to reduced GABA-ergic inhibitory interneuron numbers and activation of microglia and astrocytes in mouse hippocampus. Neurobiol Dis. 121:163-176.

Koutelou E, Wang L, Schibler A, Chao HP, Kuang X, Lin K, Lu Y, Shen J, Jeter CR, Salinger A, Wilson M, Chen YC, Atanassov BS, Tang DG, Dent SY. (2019) Usp22 controls multiple signaling pathways that are essential for vasculature formation in the mouse placenta. Development. Feb 22;146(4). pii: dev174037. ]

Manickavinayaham S, Vélez-Cruz R, Biswas AK, Bedford E, Klein BJ, Kutateladze TG, Liu B, Bedford MT, Johnson DG. (2019) E2F1 acetylation directs p300/CBP-mediated histone acetylation at DNA double-strand breaks to facilitate repair. Nat Commun. 10(1):4951.

McBride KM, Kil H, Mu Y, Plummer JB, Lee J, Zelazowski MJ, Sebastian M, Abba MC, Aldaz CM. (2019) Wwox Deletion in Mouse B Cells Leads to Genomic Instability, Neoplastic Transformation, and Monoclonal Gammopathies. Front Oncol. 9:517.

Patel L, Kang R, Rosenberg SC, Qiu Y, Raviram R, Chee S, Hu R, Ren B, Cole F,* Corbett KD*. (2019) Dynamic reorganization of the genome shapes the recombination landscape in meiotic prophase. Nat Struct Mol Biol. 26(3):164-174. (*co-corresponding authors)

Ren R, Hardikar S, Horton JR, Lu Y, Zeng Y, Singh AK, Lin K, Coletta LD, Shen J, Lin Kong CS, Hashimoto H, Zhang X, Chen T, Cheng X. (2019) Structural basis of specific DNA binding by the transcription factor ZBTB24. Nucleic Acids Res. 47(16):8388-8398.

Wible DJ, Chao HP, Tang DG, Bratton SB. (2019) ATG5 cancer mutations and alternative mRNA splicing reveal a conjugation switch that regulates ATG12-ATG5-ATG16L1 complex assembly and autophagy. Cell Discov. 5:42.

Veland N, Lu Y, Hardikar S, Gaddis S, Zeng Y, Liu B, Estecio MR, Takata Y, Lin K, Tomida MW, Shen J, Saha D, Gowher H, Zhao H, Chen T. (2019) DNMT3L facilitates DNA methylation partly by maintaining DNMT3A stability in mouse embryonic stem cells. Nucleic Acids Res. 47(1):152-167.

2018

Appikonda S, Thakkar KN, Shah PK, Dent SYR, Andersen JN, Barton MC. (2018) Cross-talk between chromatin acetylation and SUMOylation of tripartite motif-containing protein 24 (TRIM24) impacts cell adhesion. J Biol Chem. 293(19):7476-7485.

Bao J, Perez CJ, Kim J, Zhang H, Murphy CJ, Hamidi T, Jaubert J, Platt CD, Chou J, Deng M, Zhou MH, Huang Y, Gaitán-Peñas H, Guénet JL, Lin K, Lu Y, Chen T, Bedford MT, Dent SY, Richburg JH, Estévez R, Pan HL, Geha RS, Shi Q, Benavides F. (2018) Deficient LRRC8A-dependent volume-regulated anion channel activity is associated with male infertility in mice. JCI Insight. 3(16):e99767.

Bao J, Rousseaux S, Shen J, Lin K, Lu Y, Bedford MT. The arginine methyltransferase CARM1 represses p300•ACT•CREMτ activity and is required for spermiogenesis. (2018) Nucleic Acids Res. 46(9):4327-4343.

Brahma S, Ngubo M, Paul S, Udugama M, Bartholomew B. (2018) The Arp8 and Arp4 module acts as a DNA sensor controlling INO80 chromatin remodeling. Nat Commun. 90(1):3309

Cheng D, Vemulapalli V, Lu Y, Shen J, Aoyagi S, Fry CJ, Yang Y, Foulds CE, Stossi F, Treviño LS, Mancini MA, O’Malley BW, Walker CL, Boyer TG, Bedford MT. (2018) CARM1 methylates MED12 to regulate its RNA binding ability. Life Sci Alliance. 1(5):e201800117.

Das P, Veazey KJ, Van HT, Kaushik S, Lin K, Lu Y, Ishii M, Kikuta J, Ge K, Nussenzweig A, Santos MA. (2018) Histone methylation regulator PTIP is required to maintain normal and leukemic bone marrow niches. Proc Natl Acad Sci U S A. 2018 Oct 23;115(43):E10137-E10146. pii: 201806019.

Franco HL, Nagari A, Malladi V, Li W, Xi Y, Richardson D, Allton KL, Tanaka K, Li J, Murakami S, Keyomarsi K, Bedford MT, Shi X, Li W, Barton MC, Dent SYR, Kraus WL. (2018) Enhancer transcription reveals subtype-specific gene expression programs controlling breast cancer pathogenesis. Genome Res. 28(2):159-170.

Hamidi T, Singh AK, Veland N, Vemulapalli V, Chen J, Hardikar S, Bao J, Fry CJ, Yang V, Lee KA, Guo A, Arrowsmith CH, Bedford MT, Chen T. (2018) Identification of Rpl29 as a major substrate of the lysine methyltransferase Set7/9. J Biol Chem. 293(33):12770-12780.

Jain AK, Barton MC. (2018) p53: emerging roles in stem cells, development and beyond. Development. 145(8): dev158360.

Kaushik S, Liu F, Veazey KJ, Gao G, Das P, Neves LF, Lin K, Zhong Y, Lu Y, Giuliani V, Bedford MT, Nimer SD, Santos MA. (2018) Genetic deletion or small-molecule inhibition of the arginine methyltransferase PRMT5 exhibit anti-tumoral activity in mouse models of MLL-rearranged AML. Leukemia. 32(2):499-509.

Kang R, Zelazowski MJ, Cole F. (2018) Missing the Mark: PRDM9-dependent methylation is required for meiotic DSB targeting. Mol Cell. 69(5):725-727.

Singarapu N, Ma K, Reeh KAG, Shen J, Lancaster JN, Yi S, Xie H, Orkin SH, Manley NR, Ehrlich LIR, Jiang N, Richie ER. (2018) Polycomb repressive complex 2 is essential for development and maintenance of a functional TEC compartment. Sci Rep. 8(1):14335.

Wang L, Koutelou E, Hirsch C, McCarthy R, Schibler A, Lin K, Lu Y, Jeter C, Shen J, Barton MC, Dent SYR. (2018) GCN5 regulates FGF signaling and activates selective MYC target genes during early embryoid body differentiation. Stem Cell Reports. 10(1):287-299

Wible DJ, Bratton SB. (2018) Reciprocity in ROS and autophagic signaling. Curr Opin Toxicol. 7:28-36.

2017

Bae N, Viviano M, Su X, Lv J, Cheng D, Sagum C, Castellano S, Bai X, Johnson C, Khalil MI, Shen J, Chen K, Li H, Sbardella G, Bedford MT. (2017) Developing Spindlin1 small-molecule inhibitors by using protein microarrays. Nat Chem Biol. 13(7):750-756.

Brahma S, Udugama MI, Kim J, Hada A, Bhardwaj SK, Hailu SG, Lee TH, Bartholomew B. (2017) INO80 exchanges H2A.Z for H2A by translocating on DNA proximal to histone dimers. Nat Commun. 8:15616.

Carr SM, Munro S, Sagum CA, Fedorov O, Bedford MT, La Thangue NB. (2017) Tudor-domain protein PHF20L1 reads lysine methylated retinoblastoma tumour suppressor protein. Cell Death Differ. 24(12):2139-2149.

Dan J, Rousseau P, Hardikar S, Veland N, Wong J, Autexier C, Chen T. (2017) Zscan4 inhibits maintenance DNA methylation to facilitate telomere elongation in mouse embryonic stem cells. Cell Rep. 20(8):1936-1949.

Espejo AB, Gao G, Black K, Gayatri S, Veland N, Kim J, Chen T, Sudol M, Walker C, Bedford MT. (2017) PRMT5 C-terminal phosphorylation modulates a 14-3-3/PDZ interaction switch. J Biol Chem. 292(6):2255-2265.

Li J, Xi Y, Li W, McCarthy RL, Stratton SA, Zou W, Li W, Dent SY, Jain AK, Barton MC. (2017) TRIM28 interacts with EZH2 and SWI/SNF to activate genes that promote mammosphere formation. Oncogene. 36(21):2991-3001.

Manandhar M, Lowery MG, Boulware KS, Lin KH, Lu Y, Wood RD. (2017) Transcriptional consequences of XPA disruption in human cell lines. DNA Repair (Amst). 57:76-90.

Mi W, Guan H, Lyu J, Zhao D, Xi Y, Jiang S, Andrews FH, Wang X, Gagea M, Wen H, Tora L, Dent SYR, Kutateladze TG, Li W, Li H, Shi X. (2017) YEATS2 links histone acetylation to tumorigenesis of non-small cell lung cancer. Nat Commun. 8(1):1088

Mu Y, Zelazowska MA, McBride KM. (2017) Phosphorylation promotes activation-induced cytidine deaminase activity at the Myc oncogene. J Exp Med. 214(12):3543-3552.

Ortiz GJ, Li Y, Post SM, Pant V, Xiong S, Larsson CA, El-Naggar AK, Johnson DG, Lozano G. (2017) Contrasting effects of an Mdm2 functional polymorphism on tumor phenotypes. Oncogene. 37(3):332-340.

Takata KI, Reh S, Yousefzadeh MJ, Zelazowski MJ, Bhetawal S, Trono D, Lowery MG, Sandoval M, Takata Y, Lu Y, Lin K, Shen J, Kusewitt DF, McBride KM, Cole F, Wood RD. (2017) Analysis of DNA polymerase ν function in meiotic recombination, immunoglobulin class-switching, and DNA damage tolerance. PLoS Genet. 13(6):e1006818.

Schrock MS, Batar B, Lee J, Druck T, Ferguson B, Cho JH, Akakpo K, Hagrass H, Heerema NA, Xia F, Parvin JD, Aldaz CM, Huebner K. (2017) Wwox-Brca1 interaction: role in DNA repair pathway choice. Oncogene. 2017 Apr 20;36(16):2215-2227.

Veland N, Hardikar S, Zhong Y, Gayatri S, Dan J, Strahl BD, Rothbart SB, Bedford MT, Chen T. (2017) The arginine methyltransferase PRMT6 regulates DNA methylation and contributes to global DNA hypomethylation in cancer. Cell Rep. 21(12):3390-3397

Wan L*, Wen H*, Li Y, Lyu J, Xi Y, Hoshii T, Joseph JK, Wang X, Loh YE, Erb MA, Souza AL, Bradner JE, Shen L, Li W, Allis CD, Armstrong SA, Shi X. (2017) ENL links histone acetylation to oncogenic gene expression in acute myeloid leukaemia. Nature. 543(7644):265-269 (*equal contribution)

Zelazowski MJ, Sandoval M, Paniker L, Hamilton HM, Han J, Gribbell MA, Kang R, Cole F. (2017) Age-dependent alterations in meiotic recombination cause chromosome segregation errors in spermatocytes. Cell. 171(3):601-614.e13.

Zhu F, Willette-Brown J, Song NY, Lomada D, Song Y, Xue L, Gray Z, Zhao Z, Davis SR, Sun Z, Zhang P, Wu X, Zhan Q, Richie ER, Hu Y. (2017) Autoreactive T cells and chronic fungal infection drive esophageal carcinogenesis. Cell Host Microbe. 21(4):478-493.

2009-2016

2016

Atanassov BS, Mohan RD, Lan X, Kuang X, Lu Y, Lin K, McIvor E, Li W, Zhang Y, Florens L, Byrum SD, Mackintosh SG, Calhoun-Davis T, Koutelou E, Wang L, Tang DG, Tackett AJ, Washburn MP, Workman JL, Dent SY. (2016) ATXN7L3 and ENY2 coordinate activity of multiple H2B deubiquitinases important for cellular proliferation and tumor growth. Mol Cell. 62(4):558-71.

Bain VE, Gordon J, O’Neil JD, Ramos I, Richie ER, Manley NR. (2016) Tissue-specific roles for sonic hedgehog signaling in establishing thymus and parathyroid organ fate. Development. 143(21):4027-4037.

Jain AK, Xi Y, McCarthy R, Allton K, Akdemir KC, Patel LR, Aronow B, Lin C, Li W, Yang L, Barton MC. (2016) LncPRESS1 is a p53-regulated LncRNA that safeguards pluripotency by disrupting SIRT6-mediated de-acetylation of histone H3K56. Mol Cell. 64(5):967-981

Lange SS, Tomida J, Boulware KS, Bhetawal S, Wood RD. (2016) The polymerase activity of mammalian DNA Pol ζ Is specifically required for cell and embryonic viability. PLoS Genet. 12(1):e1005759.

Li Y, Sabari BR, Panchenko T, Wen H, Zhao D, Guan H, Wan L, Huang H, Tang Z, Zhao Y, Roeder RG, Shi X, Allis CD, Li H. (2016) Molecular coupling of histone crotonylation and active transcription by AF9 YEATS domain. Mol Cell. 62(2):181-93.

Stuckey JI, Dickson BM, Cheng N, Liu Y, Norris JL, Cholensky SH, Tempel W, Qin S, Huber KG, Sagum C, Black K, Li F, Huang XP, Roth BL, Baughman BM, Senisterra G, Pattenden SG, Vedadi M, Brown PJ, Bedford MT, Min J, Arrowsmith CH, James LI, Frye SV. (2016) A cellular chemical probe targeting the chromodomains of Polycomb repressive complex 1. Nat Chem Biol. 12(3):180-7.

Vélez-Cruz R, Manickavinayaham S, Biswas AK, Clary RW, Premkumar T, Cole F, Johnson DG. (2016) RB localizes to DNA double-strand breaks and promotes DNA end resection and homologous recombination through the recruitment of BRG1. Genes Dev. 2016 Nov 15;30(22):2500-2512.

Wu CC, Lee S, Malladi S, Chen MD, Mastrandrea NJ, Zhang Z, Bratton SB. (2016) The Apaf-1 apoptosome induces formation of caspase-9 homo- and heterodimers with distinct activities. Nat Commun. 2016 Nov 24;7:13565

Zhang D, Park D, Zhong Y, Lu Y, Rycaj K, Gong S, Chen X, Liu X, Chao HP, Whitney P, Calhoun-Davis T, Takata Y, Shen J, Iyer VR, Tang DG. (2016) Stem cell and neurogenic gene-expression profiles link prostate basal cells to aggressive prostate cancer. Nat Commun. 7:10798.

Zhang X, Peng D, Xi Y, Yuan C, Sagum CA, Klein BJ, Tanaka K, Wen H, Kutateladze TG, Li W, Bedford MT, Shi X. (2016) G9a-mediated methylation of ERα links the PHF20/MOF histone acetyltransferase complex to hormonal gene expression. Nat Commun. 7:10810.

2015

Hirsch CL, Coban Akdemir Z, Wang L, Jayakumaran G, Trcka D, Weiss A, Hernandez JJ, Pan Q, Han H, Xu X, Xia Z, Salinger AP, Wilson M, Vizeacoumar F, Datti A, Li W, Cooney AJ, Barton MC, Blencowe BJ, Wrana JL, Dent SY. (2015) Myc and SAGA rewire an alternative splicing network during early somatic cell reprogramming. Genes Dev.29(8):803-16.

Hu SB, Xiang JF, Li X, Xu Y, Xue W, Huang M, Wong CC, Sagum CA, Bedford MT, Yang L, Cheng D, Chen LL. (2015) Protein arginine methyltransferase CARM1 attenuates the paraspeckle-mediated nuclear retention of mRNAs containing IRAlus. Genes Dev. 29(6):630-45.

Kapoor P, Bao Y, Xiao J, Espejo A, Yang L, Bedford MT, Peng G, Shen X. (2015) Phosphorylation-Dependent Enhancement of Rad53 Kinase Activity through the INO80 Chromatin Remodeling Complex. Mol Cell. 58(5):863-9.

Kapoor P, Bao Y, Xiao J, Luo J, Shen J, Persinger J, Peng G, Ranish J, Bartholomew B, Shen X. (2015) Regulation of Mec1 kinase activity by the SWI/SNF chromatin remodeling complex. Genes Dev. 29(6):591-602.

Li M, Hada A, Sen P, Olufemi L, Hall MA, Smith BY, Forth S, McKnight JN, Patel A, Bowman GD, Bartholomew B, Wang MD. (2015) Dynamic regulation of transcription factors by nucleosome remodeling. Elife. 4. doi: 10.7554/eLife.06249.

Pathiraja TN, Thakkar KN, Jiang S, Stratton S, Liu Z, Gagea M, Shi X, Shah PK, Phan L, Lee MH, Andersen J, Stampfer M, Barton MC. (2015) TRIM24 links glucose metabolism with transformation of human mammary epithelial cells. Oncogene. 34(22):2836-45.

Yang Y, Hadjikyriacou A, Xia Z, Gayatri S, Kim D, Zurita-Lopez C, Kelly R, Guo A, Li W, Clarke SG, Bedford MT. (2015) PRMT9 is a type II methyltransferase that methylates the splicing factor SAP145. Nat Commun. 6:6428.

2014

Biswas AK, Mitchell DL, Johnson DG (2014) E2F1 responds to ultraviolet radiation by directly stimulating DNA repair and suppressing carcinogenesis. Cancer Res. 74(12):3369-77.

Cole F, Baudat F, Grey C, Keeney S, de Massy B, Jasin M (2014) Mouse tetrad analysis provides insights into recombination mechanisms and hotspot evolutionary dynamics. Nat Genet. 46(10):1072-80.

Jin M, Zhang T, Liu C, Badeaux MA, Liu B, Liu R, Jeter C, Chen X, Vlassov AV, Tang DG (2014) miRNA-128 suppresses prostate cancer by inhibiting BMI-1 to inhibit tumor-initiating cells. Cancer Res. 74(15):4183-95.

Li Y, Wen H, Xi Y, Tanaka K, Wang H, Peng D, Ren Y, Jin Q, Dent SYR., Li W, Li H, Shi X (2014) AF9 YEATS Domain Links Histone Acetylation to DOT1L-Mediated H3K79 Methylation. Cell.159(3):558-71.

Reeh KA, Cardenas KT, Bain VE, Liu Z, Laurent M, Manley NR, Richie, ER (2014) Ectopic TBX1 suppresses thymic epithelial cell differentiation and proliferation during thymus organogenesis. Development. 141(15):2950-8.

Wen H, Li Y, Xi Y, Jiang S, Stratton S, Peng D, Tanaka K, Ren Y, Xia Z, Wu J, Li B, Barton MC, Li W, Li H, Shi X (2014) ZMYND11 links histone H3.3K36me3 to transcription elongation and tumour suppression. Nature. 508(7495):263-8.

Yang Y, McBride KM, Hensley S, Lu Y, Chedin F, Bedford MT (2014) Arginine methylation facilitates the recruitment of TOP3B to chromatin to prevent R loop accumulation. Mol Cell. 53(3):484-97.

Yousefzadeh MJ, Wyatt DW, Takata K, Mu Y, Hensley SC, Tomida J, Bylund, GO, Doublie S, Johansson E, Ramsden DA, McBride KM and Wood, RD (2014) Mechanism of Suppression of Chromosomal Instability by DNA Polymerase POLQ. PLoS Genet. 10(10):e1004654.

2013

Badeaux MA, Jeter CR, Gong S, Liu B, Suraneni MV, Rundhaug J, Fischer SM, Yang T, Kusewitt D, Tang DG. (2013) In vivo functional studies of tumor-specific retrogene NanogP8 in transgenic animals. Cell Cycle. 12(15):2395-408.

Chen K, Wilson MA, Hirsch C, Watson A, Liang S, Lu Y, Li W, Dent SY (2013) Stabilization of the promoter nucleosomes in nucleosome-free regions by the yeast Cyc8-Tup1 corepressor. Genome Res. 23:312-22.

Johnson DG, Dent SY (2013) Chromatin: receiver and quarterback for cellular signals. Cell. 152(4):685-9.

Kapoor P, Chen M, Winkler DD, Luger K, Shen X (2013) Evidence for monomeric actin function in INO80 chromatin remodeling. Nat Struct Mol Biol. 20(4):426-32.

Kim SJ, Wong PK. (2013) ROS upregulation during the early phase of retroviral infection plays an important role in viral establishment in the host cell. J Gen Virol. 94(Pt 10):2309-17.

Kim SJ, Zhao H, Hardikar S, Singh AK, Goodell MA, Chen T. (2013) A DNMT3A mutation common in AML exhibits dominant-negative effects in murine ES cells. Blood. 2013 Dec 12;122(25):4086-9.

Lange SS, Bedford E, Reh S, Wittschieben JP, Carbajal S, Kusewitt DF, DiGiovanni J, Wood RD (2013) Dual role for mammalian DNA polymerase zeta in maintaining genome stability and proliferative responses. Proc Natl Acad Sci U S A. 110(8):E687-96.

Li J, Zhao Z, Carter C, Ehrlich LI, Bedford MT, Richie ER (2013) Coactivator-associated arginine methyltransferase 1 regulates fetal hematopoiesis and thymocyte development. J Immunol. 190(2):597-604.

Mikulec CD, Rundhaug JE, Simper MS, Lubet RA, Fischer SM. (2013) The chemopreventive efficacies of nonsteroidal anti-inflammatory drugs: the relationship of short-term biomarkers to long-term skin tumor outcome. Cancer Prev Res (Phila). 6(7):675-85.

Perez CJ, Dumas A, Vallières L, Guénet JL, Benavides F. (2013) Several classical mouse inbred strains, including DBA/2, NOD/Lt, FVB/N, and SJL/J, carry a putative loss-of-function allele of Gpr84. J Hered. 2013 Jul-Aug;104(4):565-71.

Takata K, Reh S, Tomida J, Person MD, Wood RD. (2013) Human DNA helicase HELQ participates in DNA interstrand crosslink tolerance with ATR and RAD51 paralogs. Nat Commun. 2013;4:2338.

Yeh TC, Bratton SB (2013) Caspase-dependent regulation of the ubiquitin-proteasome system through direct substrate targeting. Proc Natl Acad Sci U S A. 110(35):14284-9.

Zhao H, Chen T. (2013) Tet family of 5-methylcytosine dioxygenases in mammalian development. J Hum Genet. 58(7):421-7.

2012

Badeaux AI, Yang Y, Cardenas K, Vemulapalli V, Chen K, Kusewitt D, Richie E, Li W, Bedford MT (2012). Loss of the methyl lysine effector protein PHF20 impacts the expression of genes regulated by the lysine acetyltransferase MOF. J Biol Chem. 287(1):429-37.

Biswas AK, Johnson DG. (2012) Transcriptional and nontranscriptional functions of E2F1 in response to DNA damage. Cancer Res. 72(1):13-7.

Chen YC, Gatchel JR, Lewis RW, Mao CA, Grant PA, Zoghbi HY, Dent SY (2012) Gcn5 loss-of-function accelerates cerebellar and retinal degeneration in a SCA7 mouse model. Hum Mol Genet. 21(2):394-405.

Ferguson BW, Gao X, Kil H, Lee J, Benavides F, Abba MC, Aldaz CM (2012) Conditional Wwox deletion in mouse mammary gland by means of two Cre recombinase approaches. PLoS One. 7(5):e36618.

Lange SS, Wittschieben JP, Wood RD (2012) DNA polymerase zeta is required for proliferation of normal mammalian cells. Nucleic Acids Res. 40 (10):4473-82.

Lu M, Liu Z, Yu H, Wang LE, Li G, Sturgis EM, Johnson DG, Wei Q (2012) Combined effects of E2F1 and E2F2 polymorphisms on risk and early onset of squamous cell carcinoma of the head and neck. Mol Carcinog. 51 Suppl 1:E132-41.

Mitchell D, Paniker L, Godar D (2012) Nucleotide excision repair is reduced in oral epithelial tissues compared with skin. Photochem Photobiol. 88(4):1027-32.

Qin J, Liu X, Laffin B, Chen X, Choy G, Jeter CR, Calhoun-Davis T, Li H, Palapattu GS, Pang S, Lin K, Huang J, Ivanov I, Li W, Suraneni MV, Tang DG (2012) The PSA(-/lo) prostate cancer cell population harbors self-renewing long-term tumor-propagating cells that resist castration. Cell Stem Cell. 10(5):556-69.

Regunathan R, Woo J, Pierce MC, Polydorides AD, Raoufi M, Roayaie S, Schwartz M, Labow D, Shin D, Suzuki R, Bhutani MS, Coghlan LG, Richards-Kortum R, Anandasabapathy S, Kim MK. (2012) Feasibility and preliminary accuracy of high-resolution imaging of the liver and pancreas using FNA compatible microendoscopy (with video). Gastrointest Endosc. 76(2):293-300.

2011

Atanassov BS, Dent SY. (2011) USP22 regulates cell proliferation by deubiquitinating the transcriptional regulator FBP1. EMBO Rep. 12(9):924-30.

Atanassov BS, Koutelou E, Dent SY. (2011) The role of deubiquitinating enzymes in chromatin regulation. FEBS Lett. 585(13):2016-23.

Benavides F, Perez C, Blando J, Contreras O, Shen J, Coussens LM, Fischer SM, Kusewitt DF, DiGiovanni J, Conti CJ. (2011) Protective role of cathepsin L in mouse skin carcinogenesis. Mol Carcinog. 51(4):352-61.

Butler JS, Zurita-Lopez CI, Clarke SG, Bedford MT, Dent SY. (2011) Protein-arginine methyltransferase 1 (PRMT1) methylates Ash2L, a shared component of mammalian histone H3K4 methyltransferase complexes. J Biol Chem. 286(14):12234-44.

Chen J, Zhu F, Weaks RL, Biswas AK, Guo R, Li Y, Johnson DG. (2011) E2F1 promotes the recruitment of DNA repair factors to sites of DNA double-strand breaks. Cell Cycle. 10(8):1287-94.

Fernandez AA, Garcia R, Paniker L, Trono D, Mitchell DL. (2011) An experimental population study of nucleotide excision repair as a risk factor for UVB-induced melanoma. Photochem Photobiol. 87(2):335-41.

Fischer SM, Hawk ET, Lubet RA. (2011) Coxibs and other nonsteroidal anti-inflammatory drugs in animal models of cancer chemoprevention. Cancer Prev Res (Phila). 4(11):1728-35.

Guo R, Chen J, Mitchell DL, Johnson DG (2011) GCN5 and E2F1 stimulate nucleotide excision repair by promoting H3K9 acetylation at sites of damage. Nucleic Acids Res. 39(4):1390-7.

Jeter CR, Liu B, Liu X, Chen X, Liu C, Calhoun-Davis T, Repass J, Zaehres H, Shen JJ, Tang DG. (2011) NANOG promotes cancer stem cell characteristics and prostate cancer resistance to androgen deprivation. Oncogene. 30(36):3833-45.

Kim J, Hwangbo J, Wong PK. (2011) p38 MAPK-Mediated Bmi-1 down-regulation and defective proliferation in ATM-deficient neural stem cells can be restored by Akt activation. PLoS One. 2011 Jan 28;6(1):e16615

Lashinger LM, Malone LM, Brown GW, Daniels EA, Goldberg JA, Otto G, Fischer SM, Hursting SD. (2011) Rapamycin partially mimics the anticancer effects of calorie restriction in a murine model of pancreatic cancer. Cancer Prev Res (Phila). 4(7):1041-51.

Latham JA, Chosed RJ, Wang S, Dent SY (2011) Chromatin signaling to kinetochores: transregulation of Dam1 methylation by histone H2B ubiquitination. Cell. 146(5):709-19.

Li H, Tang DG. (2011) Prostate cancer stem cells and their potential roles in metastasis. J Surg Oncol. 103(6):558-62.

Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S, Wiggins JF, Bader AG, Fagin R, Brown D, Tang DG (2011) The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med. 17(2):211-5.

Perez C, Parker-Thornburg J, Mikulec C, Kusewitt DF, Fischer SM, Digiovanni J, Conti CJ, Benavides F. (2011) SKHIN/Sprd, a new genetically defined inbred hairless mouse strain for UV-induced skin carcinogenesis studies. Exp Dermatol. 21(3):217-20.

Rahn JJ, Rowley B, Lowery MP, Coletta LD, Limanni T, Nairn RS, Adair GM. (2011) Effects of varying gene targeting parameters on processing of recombination intermediates by ERCC1-XPF. DNA Repair (Amst). 10(2):188-98.

Spannhoff A, Kim YK, Raynal NJ, Gharibyan V, Su MB, Zhou YY, Li J, Castellano S, Sbardella G, Issa JP, Bedford MT (2011) Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Reports. 12(3):238-43.

Surh I, Rundhaug J, Pavone A, Mikulec C, Abel E, Fischer SM. (2011) Upregulation of the EP1 receptor for prostaglandin E2 promotes skin tumor progression. Mol Carcinog. 50(6):458-68.

Yan L, Della Coletta L, Powell KL, Shen J, Thames H, Aldaz CM, MacLeod MC. (2011) Activation of the canonical Wnt/beta-catenin pathway in ATF3-induced mammary tumors. PLoS One. 6(1):e16515.

2010

Alexander A, Cai SL, Kim J, Nanez A, Sahin M, MacLean KH, Inoki K, Guan KL, Shen J, Person MD, Kusewitt D, Mills GB, Kastan MB, Walker CL (2010) ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc Natl Acad Sci U S A.107:4153-8.

Bredfeldt TG, Greathouse KL, Safe SH, Hung MC, Bedford MT, Walker CL. (2010) Xenoestrogen-induced regulation of EZH2 and histone methylation via estrogen receptor signaling to PI3K/AKT. Mol Endocrinol. 24(5):993-1006

Jain A, Bacolla A, Chakraborty P, Grosse F, Vasquez KM. (2010) Human DHX9 helicase unwinds triple-helical DNA structures. Biochemistry. 49(33):6992-9

Kha DT, Wang G, Natrajan N, Harrison L, Vasquez KM. Pathways for double-strand break repair in genetically unstable Z-DNA-forming sequences. J Mol Biol. 2010 398(4):471-80.

Kim D, Lee J, Cheng D, Li J, Carter C, Richie E, Bedford MT. (2010) Enzymatic activity is required for the in vivo functions of CARM1. J Biol Chem. 285(2):1147-52

Guo R, Chen J, Zhu F, Biswas AK, Berton TR, Mitchell DL, Johnson DG (2010) E2F1 localizes to sites of UV-induced DNA damage to enhance nucleotide excision repair. J Biol Chem. 285:19308-15.

Mitchell DL, Fernandez AA, Nairn RS, Garcia R, Paniker L, Trono D, Thames HD, Gimenez-Conti I (2010) Ultraviolet A does not induce melanomas in a Xiphophorus hybrid fish model. Proc Natl Acad Sci U S A. 107(20):9329-34.

Perez CJ, Jaubert J, Guénet JL, Barnhart KF, Ross-Inta CM, Quintanilla VC, Aubin I, Brandon JL, Otto NW, DiGiovanni J, Gimenez-Conti I, Giulivi C, Kusewitt DF, Conti CJ, Benavides F. (2010) Two hypomorphic alleles of mouse argininosuccinate synthetase as a new animal model of citrullinemia type I and other hyperammonemic syndromes. Am J Pathol. 177(4):1958-68.

Pusapati RV, Weaks RL, Rounbehler RJ, McArthur MJ, Johnson DG. (2010) E2F2 suppresses Myc-induced proliferation and tumorigenesis. Mol Carcinog. 49(2):152-6.

Rundhaug JE, Fischer SM. (2010) Molecular mechanisms of mouse skin tumor promotion. Cancers (Basel). 2(2):436-82

Short JD, Dere R, Houston KD, Cai SL, Kim J, Bergeron JM, Shen J, Liang J, Bedford MT, Mills GB, Walker CL. (2010) AMPK-mediated phosphorylation of murine p27 at T197 promotes binding of 14-3-3 proteins and increases p27 stability. Mol Carcinog. 49(5):429-39.

Yang Y, Lu Y, Espejo A, Wu J, Xu W, Liang S, Bedford MT (2010) TDRD3 is an effector molecule for arginine-methylated histone marks. Mol Cell. 40(6):1016-23.

Zhu F, Dollé ME, Berton TR, Kuiper RV, Capps C, Espejo A, McArthur MJ, Bedford MT, van Steeg H, de Vries A, Johnson DG (2010) Mouse models for the p53 R72P polymorphism mimic human phenotypes. Cancer Res. 70(14):5851-9.

2009

Abba MC, Hu Y, Levy CC, Gaddis S, Kittrell FS, Hill J, Bissonnette RP, Brown PH, Medina D, Aldaz CM. (2009) Identification of modulated genes by three classes of chemopreventive agents at preneoplastic stages in a p53-null mouse mammary tumor model. Cancer Prev Res (Phila). 2(2):175-84.

Blando J, Portis M, Benavides F, Alexander A, Mills G, Dave B, Conti CJ, Kim J, Walker CL. (2009) PTEN deficiency is fully penetrant for prostate adenocarcinoma in C57BL/6 mice via mTOR-dependent growth. Am J Pathol. 174(5):1869-79.

Bua DJ, Kuo AJ, Cheung P, Liu CL, Migliori V, Espejo A, Casadio F, Bassi C, Amati B, Bedford MT, Guccione E, Gozani O. Epigenome microarray platform for proteome-wide dissection of chromatin-signaling networks. (2009) PLoS One. 4(8):e6789.

Chen X, Schneider-Broussard R, Hollowell D, McArthur M, Jeter CR, Benavides F, DiGiovanni J, Tang DG. (2009) Abnormal differentiation, hyperplasia and embryonic/perinatal lethality in BK5-T/t transgenic mice. Differentiation. 77(3):324-34.

Falbo KB, Alabert C, Katou Y, Wu S, Han J, Wehr T, Xiao J, He X, Zhang Z, Shi Y, Shirahige K, Pasero P, and Shen X (2009) Involvement of a chromatin remodeling complex in damage tolerance during DNA replication. Nat Struct Mol Biol. 16(11):1167-72.

Griffith AV, Cardenas K, Carter C, Gordon J, Iberg A, Engleka K, Epstein JA, Manley NR, Richie ER (2009) Increased thymus- and decreased parathyroid-fated organ domains in Splotch mutant embryos. Dev Biol. 327(1):216-27.

Jeter CR, Badeaux M, Choy G, Chandra D, Patrawala L, Liu C, Calhoun-Davis T, Zaehres H, Daley GQ, Tang DG. (2009) Functional evidence that the self-renewal gene NANOG regulates human tumor development. Stem Cells. 2009 May;27(5):993-1005.

Kim DJ, Kataoka K, Sano S, Connolly K, Kiguchi K, DiGiovanni J. (2009) Targeted disruption of Bcl-xL in mouse keratinocytes inhibits both UVB- and chemically induced skin carcinogenesis. Mol Carcinog. 48(10):873-85.

Kuang X, Scofield VL, Yan M, Stoica G, Liu N, Wong PK. (2009) Attenuation of oxidative stress, inflammation and apoptosis by minocycline prevents retrovirus-induced neurodegeneration in mice. Brain Res. 1286:174-84.

Liu B, Zhu F, Xia X, Park E, Hu Y. (2009) A tale of terminal differentiation: IKKalpha, the master keratinocyte regulator. Cell Cycle. 8(4):527-31.

Liu Y, Nairn RS, Vasquez KM. (2009) Targeted gene conversion induced by triplex-directed psoralen interstrand crosslinks in mammalian cells. Nucleic Acids Res. 37(19):6378-88.

Ludes-Meyers JH, Kil H, Parker-Thornburg J, Kusewitt DF, Bedford MT, Aldaz CM. (2009) Generation and characterization of mice carrying a conditional allele of the Wwox tumor suppressor gene. PLoS One. 4(11):e7775.

Repass JF, Laurent MN, Carter C, Reizis B, Bedford MT, Cardenas K, Narang P, Coles M, Richie ER. (2009) IL7-hCD25 and IL7-Cre BAC transgenic mouse lines: new tools for analysis of IL-7 expressing cells. Genesis. 47(4):281-7.

Scofield VL, Yan M, Kuang X, Kim SJ, Crunk D, Wong PK. (2009) The drug monosodium luminol (GVT) preserves thymic epithelial cell cytoarchitecture and allows thymocyte survival in mice infected with the T cell-tropic, cytopathic retrovirus ts1. Immunol Lett. 122(2):159-69.

Shirley SH, Rundhaug JE, Tian J, Cullinan-Ammann N, Lambertz I, Conti CJ, Fuchs-Young R. (2009) Transcriptional regulation of estrogen receptor-alpha by p53 in human breast cancer cells. Cancer Res. 69(8):3405-14.

Zhao J, Jain A, Iyer RR, Modrich PL, Vasquez KM. (2009) Human HMGB1 directly facilitates interactions between nucleotide excision repair proteins on triplex-directed psoralen interstrand crosslinks. DNA Repair (Amst). ;8(7):865-72.