Selected Recent Publications
2024
Krishnan K Mahadevan, Allison M Dyevoich, Yang Chen, Bingrui Li, Hikaru Sugimoto, Amari M Sockwell, Kathleen M McAndrews, Lakshmi Kavitha Sthanam, Huamin Wang, Shabnam Shalapour, Stephanie S Watowich, Raghu Kalluri. Type I conventional dendritic cells facilitate immunotherapy in pancreatic cancer. 2024 Jun 28;384(6703):eadh4567. doi: 10.1126/science.adh4567. Epub 2024 Jun 28.PMID: 38935717
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. doi: 10.1038/s41375-024-02218-6. Epub 2024 Mar 11.PMID: 38467768
2023
Park JS, Gazzaniga FS, Wu M, Luthens AK, Gillis J, Zheng W, LaFleur MW, Johnson SB, Morad G, Park EM, Zhou Y, Watowich SS, Wargo JA, Freeman GJ, Kasper DL, Sharpe AH. Targeting PD-L2-RGMb overcomes microbiome-related immunotherapy resistance. Nature. 2023 May;617(7960):377-385. doi: 10.1038/s41586-023-06026-3. Epub 2023 May 3. PMID: 37138075.
Zhou Y, Medik YB, Patel B, Zamler DB, Chen S, Chapman T, Schneider S, Park EM, Babcock RL, Chrisikos TT, Kahn LM, Dyevoich AM, Pineda JE, Wong MC, Mishra AK, Cass SH, Cogdill AP, Johnson DH, Johnson SB, Wani K, Ledesma DA, Hudgens CW, Wang J, Wadud Khan MA, Peterson CB, Joon AY, Peng W, Li HS, Arora R, Tang X, Raso MG, Zhang X, Foo WC, Tetzlaff MT, Diehl GE, Clise-Dwyer K, Whitley EM, Gubin MM, Allison JP, Hwu P, Ajami NJ, Diab A, Wargo JA, Watowich SS. Intestinal toxicity to CTLA-4 blockade driven by IL-6 and myeloid infiltration. J Exp Med. 2023 Feb 6;220(2):e20221333. doi: 10.1084/jem.20221333. Epub 2022 Nov 11. PMID: 36367776.
Wang Y, Jenq RR, Wargo JA, Watowich SS. Microbiome influencers of checkpoint blockade-associated toxicity. J Exp Med. 2023 Mar 6;220(3):e20220948. doi: 10.1084/jem.20220948. Epub 2023 Jan 9. PMID: 36622383.
Halsey TM, Thomas AS, Hayase T, Ma W, Abu-Sbeih H, Sun B, Parra ER, Jiang ZD, DuPont HL, Sanchez C, El-Himri R, Brown A, Flores I, McDaniel L, Ortega Turrubiates M, Hensel M, Pham D, Watowich SS, Hayase E, Chang CC, Jenq RR, Wang Y. Microbiome alteration via fecal microbiota transplantation is effective for refractory immune checkpoint inhibitor-induced colitis. Sci Transl Med. 2023 Jun 14;15(700):eabq4006. doi: 10.1126/scitranslmed.abq4006. Epub 2023 Jun 14. PMID: 37315113.
Mahadevan KK, Dyevoich AM, Chen Y, Li B, Sugimoto H, Sockwell AM, McAndrews KM, Wang H, Shalapour S, Watowich SS, Kalluri R. Antigen-presenting type-I conventional dendritic cells facilitate curative checkpoint blockade immunotherapy in pancreatic cancer. bioRxiv. 2023 Mar 6:2023.03.05.531191. doi: 10.1101/2023.03.05.531191. Preprint. PMID: 36945457.
Patel B, Zhou Y, Babcock RL, Ma F, Zal MA, Kumar D, Medik YB, Kahn LM, Pineda JE, Park EM, Tang X, Raso MG, Zal T, Clise-Dwyer K, Giancotti FG, Colla S, Watowich SS. STAT3 protects HSCs from intrinsic interferon signaling and loss of long-term blood-forming activity. bioRxiv. 2023 Feb 11:2023.02.10.528069. doi: 10.1101/2023.02.10.528069. Preprint. PMID: 3679826
Lulla AR, Akli S, Karakas C, Caruso JA, Warma LD, Fowlkes NW, Rao X, Wang J, Hunt KK, Watowich SS, Keyomarsi K. Neutrophil elastase remodels mammary tumors to facilitate lung metastasis. Mol Cancer Ther. 2023 Oct 5. doi: 10.1158/1535-7163.MCT-23-0414. Online ahead of print. PMID: 37796181
2022
Zhou Y, Medik YB, Patel B, Zamler DB, Chen S, Chapman T, Schneider S, Park EM, Babcock RL, Chrisikos TT, Kahn LM, Dyevoich AM, Pineda JE, Wong MC, Mishra AK, Cass SH, Cogdill AP, Johnson DH, Johnson SB, Wani K, Kedesma DA, Hudgens CW, Wang J, Wadud Kahn MA, Peterson CB, Joon AY, Peng W, Li HS, Arora R, Tang X, Raso MG, Zhang X, Foo WC, Tetzlaff MT, Diehl GE, Clise-Dwyer K, Whitley EM, Gubin MM, Allison JP, Hwu P, Ajami NJ, Diab A, Wargo JA, Watowich SS. Intestinal toxicity to CTLA-4 blockade driven by IL-6 and myeloid infiltration. J Exp Med. 220(2):e20221333. Epub 2022. PMID:3636776
Chrisikos TT, Zhou Y, Kahn LM, Patel B, Denne NL, Brooks A, Shen L, Wang J, Watowich SS. STAT3 inhibits autocrine IFN signaling in type 1 conventional dendritic cells. J Immunol. 209(7):1286-1299. 2022. PMID:36038291
Babcock RL, Zhou Y, Patel B, Chrisikos TT, Kahn LM, Dyevoich AM, Medik YB, Watowich SS. Regulation and function of Id2 in plasmacytoid dendritic cells. Mol Immunol. 148:6-17. 2022. PMID:35640521
Wang Y, Jenq RR, Wargo JA, Watowich SS. Microbiome influencers of checkpoint blockade-associated toxicity. J Exp Med. 2022, in press.
Yuan B, Clowers MJ, Velasco WV, Peng S, Peng Q, Shi Y, Ramos-Castaneda M, Zarghooni M, Yang S, Babcock RL, Chang SH, Heymach JV, Zhang J, Ostrin EJ, Watowich SS, Kadara H, Moghaddam SJ. Targeting IL-1b as an immunepreventive and therapeutic modality for K-ras-mutant lung cancer. JCI Insight. 7(11):e157788. 2022. PMID:35471938.
Zamler DB, Shingu T, Kahn LM, Huntoon K, Kassab C, Ott M, Tomczak K, Liu J, Li Y, Lai I, Zorilla-Veloz R, Yee C, Rai K, Kim BY, Watowich SS, Heimberger AB, Draetta GF, Hu J. Immune landscape of a genetically engineered murine model of glioma compared with human glioma. JCI Insight. 7(12):e148990. 2022. PMID:35653194.
Bhagat A, Shrestha P, Jeyabal P, Peng Z, Watowich SS, Kleinerman ES. Doxorubicin-induced cardiotoxicity is mediated by neutrophils through release of neutrophil elastase. Front Oncol. 12:947604. 2022. PMID:36033503.
Wurster S, Watowich SS, Kontoyiannis DP. Checkpoint inhibitors as immunotherapy for fungal infections: Promises, challenges, and unanswered questions. Front. Front Immunol. 2022 Oct 25;13:1018202. doi: 10.3389/fimmu.2022.1018202. eCollection 2022. PMID: 36389687.
2021
Andrews MC, Duong CPM, Gopalakrishnan V, Iebba V, Chen WS, Derosa L, Khan MAW, Cogdill AP, White MG, Wong MC, Ferrere G, Fluckiger A, Roberti MP, Opolon P, Alou MT, Yonekura S, Roh W, Spencer CN, Curbelo IF, Vence L, Reuben A, Johnson S, Arora R, Morad G, Lastrapes M, Baruch EN, Little L, Gumbs C, Cooper ZA, Prieto PA, Wani K, Lazar AJ, Tetzlaff MT, Hudgens CW, Callahan MK, Adamow M, Postow MA, Ariyan CE, Gaudreau PO, Nezi L, Raoult D, Mihalcioiu C, Elkrief A, Pezo RC, Haydu LE, Simon JM, Tawbi HA, McQuade J, Hwu P, Hwu WJ, Amaria RN, Burton EM, Woodman SE, Watowich S, Diab A, Patel SP, Glitza IC, Wong MK, Zhao L, Zhang J, Ajami NJ, Petrosino J, Jenq RR, Davies MA, Gershenwald JE, Futreal PA, Sharma P, Allison JP, Routy B, Zitvogel L, Wargo JA. Gut microbiota signatures are associated with toxicity to combined CTLA-4 and PD-1 blockade. Nat Med 27(8):1432-1441, 8/2021. e-Pub 7/2021. PMID: 34239137.
Marié IJ, Brambilla L, Azzouz D, Chen Z, Baracho GV, Arnett A, Li HS, Liu W, Cimmino L, Chattopadhyay P, Silverman G, Watowich SS, Khor B, Levy DE. Tonic interferon restricts pathogenic IL-17-driven inflammatory disease via balancing the microbiome. Elife 10, 8/2021. e-Pub 8/2021. PMCID: PMC8376249
Spencer CN, McQuade JL, Gopalakrishnan V, McCulloch JA, Vetizou M, Cogdill AP, Khan MAW, Zhang X, White MG, Peterson CB, Wong MC, Morad G, Rodgers T, Badger JH, Helmink BA, Andrews MC, Rodrigues RR, Morgun A, Kim YS, Roszik J, Hoffman KL, Zheng J, Zhou Y, Medik YB, Kahn LM, Johnson S, Hudgens CW, Wani K, Gaudreau PO, Harris AL, Jamal MA, Baruch EN, Perez-Guijarro E, Day CP, Merlino G, Pazdrak B, Lochmann BS, Szczepaniak-Sloane RA, Arora R, Anderson J, Zobniw CM, Posada E, Sirmans E, Simon J, Haydu LE, Burton EM, Wang L, Dang M, Clise-Dwyer K, Schneider S, Chapman T, Anang NAS, Duncan S, Toker J, Malke JC, Glitza IC, Amaria RN, Tawbi HA, Diab A, Wong MK, Patel SP, Woodman SE, Davies MA, Ross MI, Gershenwald JE, Lee JE, Hwu P, Jensen V, Samuels Y, Straussman R, Ajami NJ, Nelson KC, Nezi L, Petrosino JF, Futreal PA, Lazar AJ, Hu J, Jenq RR, Tetzlaff MT, Yan Y, Garrett WS, Huttenhower C, Sharma P, Watowich SS, Allison JP, Cohen L, Trinchieri G, Daniel CR, Wargo JA. Dietary fiber and probiotics influence the gut microbiome and melanoma immunotherapy response. Science. 2021 Dec 24;374(6575):1632-1640. doi: 10.1126/science.aaz7015. Epub 2021 Dec 23. PMID: 34941392
2020
Chrisikos TT, Zhou Y, Li HS, Babcock RL, Wan X, Patel B, Newton K, Mancuso JJ, Watowich SS. STAT3 Inhibits CD103+ cDC1 Vaccine Efficacy in Murine Breast Cancer. Cancers. 2020 Jan; 12(1):128. doi: 10.3390/cancers12010128. PubMed PMID:31947933; PubMedCentral PMCID: PMC7017236.
Wang J, Hasan F, Frey AC, Li HS, Park J, Pan K, Haymaker C, Bernatchez C, Lee DA, Watowich SS, Yee C. Histone deacetylase inhibitors and IL21 cooperate to reprogram human effector CD8+ T cells to memory T cells. Cancer Immunol Res. 2020 Mar 25; doi: 10.1158/2326-6066.CIR-19-0619. [Epub ahead of print]. PubMed PMID: 32213626.
Zhou Y, Slone N, Chrisikos TT, Kyrysyuk O, Babcock RL, Medik YB, Li HS, Kleinerman ES, Watowich SS. Vaccine efficacy against primary and metastatic cancer with in vitro-generated CD103+ conventional dendritic cells. J Immunother Cancer. 2020 Apr;8(1):e000474; doi: 10.1136/jitc-2019-000474. PubMed PMID: 32273347.
Deng S, Ramos-Castaneda M, Velasco WV, Clowers MJ, Gutierrez BA, Noble O, Dong Y, Zarghooni M, Alvarado L, Caetano MS, Yang S, Ostrin EJ, Behrens C, Wistuba II, Stabile LP, Kadara H, Watowich SS, Moghaddam SJ. Interplay between estrogen and Stat3/NF-κB driven immunomodulation in lung cancer. Carcinogenesis. e-Pub 6/2020. PMID: 32603404.
2019
Zuo X, Deguchi Y, Xu W, Liu Y, Li HS, Wei D, Tian R, Chen W, Xu M, Yang Y, Gao S, Jaoude JC, Liu F, Chrieki SP, Moussalli MJ, Gagea M, Sebastian MM, Zheng X, Tan D, Broaddus R, Wang J, Ajami NJ, Swennes AG, Watowich SS, Shureiqi I. PPARD and Interferon Gamma Promote Transformation of Gastric Progenitor Cells and Tumorigenesis in Mice. Gastroenterology. 2019 Jul;157(1):163-178. doi: 10.1053/j.gastro.2019.03.018. Epub 2019 Mar 15. PubMed PMID: 30885780.
Li Y, Yang JY, Xie X, Jie Z, Zhang L, Shi J, Lin D, Gu M, Zhou X, Li HS, Watowich SS, Jain A, Yun Jung S, Qin J, Cheng X, Sun SC. Preventing abnormal NF-κB activation and autoimmunity by Otub1-mediated p100 stabilization. Cell Res. 2019 Jun;29(6):474-485. doi: 10.1038/s41422-019-0174-3. Epub 2019 May 13. PubMed PMID: 31086255.
Yan J, Zhao Q, Gabrusiewicz K, Kong LY, Xia X, Wang J, Ott M, Xu J, Davis RE, Huo L, Rao G, Sun SC,Watowich SS, Heimberger AB, Li S. FGL2 promotes tumor progression in the CNS by suppressing CD103+ dendritic cell differentiation. Nat Commun. 2019 Jan 25;10(1):448. doi: 10.1038/s41467-018-08271-x. PubMed PMID: 30683885.
Chrisikos TT, Zhou Y, Slone N, Babcock R, Watowich SS, Li HS. Molecular regulation of dendritic cell development and function in homeostasis, inflammation, and cancer. Mol Immunol. 2019 Jun;110:24-39. doi:10.1016/j.molimm.2018.01.014. Epub 2018 Mar 15. PubMed PMID: 29549977; PubMed Central PMCID: PMC6139080.
Chu F, Li HS, Liu X, Cao J, Ma W, Ma Y, Weng J, Zhu Z, Cheng X, Wang Z, Liu J, Jiang ZY, Luong AU, Peng W, Wang J, Balakrishnan K, Yee C, Dong C, Davis
RE, Watowich SS, Neelapu SS. CXCR5+CD8+ T cells are a distinct functional subset with an antitumor activity. Leukemia. 2019 Apr 25;. doi: 10.1038/s41375-019-0464-2. [Epub ahead of print] PubMed PMID: 31028278; NIHMSID:NIHMS1523597.
Kettner NM, Vijayaraghavan S, Durak MG, Bui T, Kohansal M, Ha MJ, Liu B, Rao X, Wang J, Yi M, Carey JP, Chen X, Eckols TK, Raghavendra AS, Ibrahim NK, Karuturi MS, Watowich SS, Sahin A, Tweardy DJ, Hunt KK, Tripathy D, Keyomarsi K.Combined inhibition of STAT3 and DNA repair in palbociclib-resistant ER-positive breast cancer. Clin Cancer Res. 2019 Mar 13;. doi: 10.1158/1078-0432.CCR-18-3274. [Epub ahead of print] PubMed PMID: 30867218; NIHMSID:NIHMS1524284.
Nicholson SE, Watowich SS. Introduction to the Special Issue: The tumor microenvironment and molecular regulation of innate immune cells. Mol Immunol. 2019 Jun;110:1-2. doi: 10.1016/j.molimm.2018.10.009. Epub 2018 Oct 11. PMID: 30318379.
2018
Zhang H, Li HS, Hillmer EJ, Zhao Y, Chrisikos TT, Hu H, Wu X, Thompson EJ, Clise-Dwyer K, Millerchip KA, Wei Y, Puebla-Osorio N, Kaushik S, Santos MA, Wang B, Garcia-Manero G, Wang J, Sun SC, Watowich SS. Genetic rescue of lineage-balanced blood cell production reveals a crucial role for STAT3 antiinflammatory activity in hematopoiesis. Proc Natl Acad Sci USA 115(10):E2311-E2319, 3/2018. e-Pub 2/2018. PMCID: PMC5878002.
Chrisikos TT, Zhou Y, Slone N, Babcock R, Watowich SS, Li HS. Molecular regulation of dendritic cell development and function in homeostasis, inflammation, and cancer. Mol Immunol. e-Pub 3/2018. PMID: 29549977.
Fan F, Wang R, Boulbes DR, Zhang H, Watowich SS, Xia L, Ye X, Bhattacharya R, Ellis LM. Macrophage conditioned medium promotes colorectal cancer stem cell phenotype via the hedgehog signaling pathway. PLoS One 13(1):e0190070, 2018. e-Pub 1/2018. PMCID: PMC5749743.
Zhang H, Li HS, Hillmer EJ, Zhao Y, Chrisikos TT, Hu H, Wu X, Thompson EJ, Clise-Dwyer K, Millerchip KA, Wei Y, Puebla-Osorio N, Kaushik S, Santos MA, Wang B, Garcia-Manero G, Wang J, Sun SC, Watowich SS. Genetic rescue of lineage-balanced blood cell production reveals a crucial role for STAT3 antiinflammatory activity in hematopoiesis. Proc Natl Acad Sci USA. 2018 Mar 6;115(10):E2311-E2319. doi: 10.1073/pnas.1713889115. Epub 2018 Feb 20.
Caetano MS, Hassane M, Van HT, Bugarin E, Cumpian AM, McDowell CL, Cavazos CG, Zhang H, Deng S, Diao L, Wang J, Evans SE, Behrens C, Wistuba II, Fuqua SAW, Lin H, Stabile LP, Watowich SS, Kadara H, Moghaddam SJ. Sex specific function of epithelial STAT3 signaling in pathogenesis of K-ras mutant lung cancer. Nat Commun. 2018 Nov 2;9(1):4589. doi: 10.1038/s41467-018-07042-y. PMID: 30389925
Cardona SM, Kim SV, Church KA, Torres VO, Cleary IA, Mendiola AS, Saville SP, Watowich SS, Parker-Thornburg J, Soto-Ospina A, Araque P, Ransohoff RM, Cardona AE. Role of the Fractalkine Receptor in CNS Autoimmune Inflammation: New Approach Utilizing a Mouse Model Expressing the Human CX3CR1I249/M280 Variant. Front Cell Neurosci. 2018 Oct 17;12:365. doi: 10.3389/fncel.2018.00365. eCollection 2018. PMID: 30386211
2017
Kadmon CS, Landers CT, Li HS, Watowich SS, Rodriguez A, King KY. MicroRNA-22 controls interferon alpha production and erythroid maturation in response to infectious stress in mice. Exp Hematol 56:7-15, 2017. e-Pub 2017. PMID: 28911907.
Xiao Y, Zou Q, Xie X, Liu T, Li HS, Jie Z, Jin J, Hu H, Manyam G, Zhang L, Cheng X, Wang H, Marie I, Levy DE, Watowich SS, Sun SC. The kinase TBK1 functions in dendritic cells to regulate T cell homeostasis, autoimmunity, and antitumor immunity. J Exp Med 214(5):1493-1507, 2017. e-Pub 2017. PMID: 28356390.
Ni L, Wang L, Yao C, Ni Z, Liu F, Gong C, Zhu X, Yan X, Watowich SS, Lee DA, Zhu S. The histone deacetylase inhibitor valproic acid inhibits NKG2D expression in natural killer cells through suppression of STAT3 and HDAC3. Sci Rep 7:45266, 2017. e-Pub 2017. PMID: 28338101.
2016
Li HS, Jin J, Liang X, Matatall KA, Ma Y, Zhang H, Ullrich SE, King KY, Sun SC, Watowich SS. Loss of c-Kit and bone marrow failure upon conditional removal of the GATA-2 C-terminal zinc finger domain in adult mice. Eur J Haematol 97(3):261-70, 2016. e-Pub 2016. PMID: 26660446.
Li HS, Liu C, Xiao Y, Chu F, Liang X, Peng W, Hu J, Neelapu SS, Sun SC, Hwu P, Watowich SS. Bypassing STAT3-mediated inhibition of the transcriptional regulator ID2 improves the antitumor efficacy of dendritic cells. Sci Signal 9(447):ra94, 2016. e-Pub 2016. PMID: 27678219.
Caetano MS, Zhang H, Cumpian AM, Gong L, Unver N, Ostrin EJ, Daliri S, Chang SH, Ochoa CE, Hanash S, Behrens C, Wistuba II, Sternberg C, Kadara H, Ferreira CG, Watowich SS, Moghaddam SJ. IL6 Blockade Reprograms the Lung Tumor Microenvironment to Limit the Development and Progression of K-ras-Mutant Lung Cancer. Cancer Res 76(11):3189-99, 2016. e-Pub 2016. PMID: 27197187.
Hillmer EJ, Zhang H, Li HS, Watowich SS. STAT3 Signaling in Immunity. Cytokine Growth Factor Rev. 2016 Oct;31:1-15. doi: 10.1016/j.cytogfr.2016.05.001. Epub 2016 May 9. Review. PMID:27185365. PMCID:PMC5050093.
2015
Huang X, Li J, Dorta-Estremera S, Di Domizio J, Anthony SM, Watowich SS, Popkin D, Liu Z, Brohawn P, Yao Y, Schluns KS, Lanier LL, Cao W. Neutrophils Regulate Humoral Autoimmunity by Restricting Interferon-γ Production via the Generation of Reactive Oxygen Species. Cell Rep 12(7):1120-32, 2015. e-Pub 2015. PMID: 26257170.
Mao F, Xu M, Zuo X, Yu J, Xu W, Moussalli MJ, Elias E, Li HS, Watowich SS, Shureiqi I. 15-Lipoxygenase-1 suppression of colitis-associated colon cancer through inhibition of the IL-6/STAT3 signaling pathway. FASEB J 29(6):2359-70, 2015. e-Pub 2015. PMID: 25713055.
2014
Zhang H, Hu H, Greeley N, Jin J, Matthews AJ, Ohashi E, Caetano MS, Li HS, Wu X, Mandal PK, McMurray JS, Moghaddam SJ, Sun SC, Watowich SS. STAT3 restrains RANK- and TLR4-mediated signalling by suppressing expression of the E2 ubiquitin-conjugating enzyme Ubc13. Nat Commun 5:5798, 2014. e-Pub 2014. PMID: 25503582.
Li HS, Watowich SS. Innate immune regulation by STAT-mediated transcriptional mechanisms. Immunol Rev. 2014 Sep;261(1):84-101. doi: 10.1111/imr.12198. PMID: 25123278.