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Zihai Li

Zihai Li (born July 1964[citation needed]) is a board-certified medical oncologist, cancer immunologist, and leader in academic medicine. He was recruited to Ohio State University Comprehensive Cancer Center – The James Cancer Hospital & Solove Research Institute (OSUCCC) in 2019 as the founding director of the Pelotonia Institute for Immuno-Oncology.[1] He is a professor of medicine in the Division of Medical Oncology, holds the Klotz Memorial Chair for Cancer Research,[2] and was appointed in 2023 as deputy director for translational research at OSUCCC.[3]

Li's research interests primarily focus on the fields of chaperone biology, immune tolerance, cancer immunology and immunotherapy. He has been continuously funded by the National Institutes of Health (NIH) since 2000, with total funding of over $30 million.[4]


Career

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Following his residency and fellowship, Li began his first joint faculty appointment in the Department of Immunology and Medicine at the University of Connecticut School of Medicine (Farmington, CT). In 2010, he was recruited to the Department of Microbiology and Immunology at the Medical University of South Carolina (MUSC), where he served as chair from 2010-2019. During his tenure as chair, the department doubled its NIH funding and increased its national NIH ranking from 79 to 31. Li was also appointed the leader of the Cancer Immunology Program at MUSC's Hollings Cancer Center (2010-2019). Li was inducted into the American Society of Clinical Investigation (2009)[5] and the Association of American Physicians (2018) and is an elected fellow of the American Association for the Advancement of Science (2021)[6] for his work in the interface of chaperone biology and cancer immunology. Recognizing his history of mentorship, he was awarded the Peggy Schachte Research Mentor Award[7][8] in 2016 from MUSC. In 2022, he received the Mount Sinai Alumni Award for Achievement in Graduate Education.[9]

Contributions to science

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Chaperone biology and immune regulation

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Li has made seminal discoveries studying the immune chaperone gp96 (also called GRP94), a heat shock protein (HSP90)-related, endoplasmic reticulum-resident protein chaperone. His work uncovered that gp96 plays a key role in many physiologic processes, including organ development, innate immunity, and immune tolerance.[10][11][12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][excessive citations] In cancer, its abundant expression is further upregulated, and it promotes oncogenesis through its ever-expanding client network.[35][36][37][38][excessive citations]

Background: In the 1950s, Prehn, Main, Klein, Old, and others demonstrated the existence of protective immunity against cancer in mice using syngeneic tumor models.[39][40][41] This was followed by decades of effort to identify tumor rejection antigens. Pramod Srivastava and Lloyd J. Old isolated a ubiquitous conserved protein, gp96, as a tumor rejection antigen from several chemically induced fibrosarcoma models.[42]

Major contribution to gp96/GRP94 biology: Li defined the ATPase activity of gp96/GRP94,[43] its client network,[11][12][13][14][15][16][17][44][excessive citations] its structure-function relationship,[45][46] and the co-chaperone CNPY3.[15] Furthermore, he established its roles in immunity, hematopoiesis, and cancer. gp96/GRP94 was found to be a major luminal protein of the endoplasmic reticulum in multicellular organisms (not in yeast), and is induced by metabolic stress.[47] However, there were no previous publications regarding the function of gp96/GRP94 when Li began to study this molecule in the 1990s. It was unclear how this unmutated protein could cause animals to generate immunity against a tumor from which it derived. Using a biochemical approach, Li showed for the first time that gp96/GRP94 is a bona fide chaperone of the HSP90 family in that it binds to ATP, processes intrinsic ATPase activity, and chaperones peptides.[43] The ability of gp96/GRP94 to complex with peptides offered a mechanistic explanation for this antigenicity: the chaperoned peptides – not gp96/GRP94 per se – are what produced immunogenicity.

However, at the time, the physiologic role of gp96/GRP94 remained unclear, in part because the gp96/GRP94 is not present in yeast genetic tools used to study eukaryotic HSPs.[48] Li was the first to use mammalian genetics to uncover the function of GRP94 at the organismal level.[12][49] He discovered that GRP94 is a major chaperone for integrins,[12][14][16][17][excessive citations] Toll-like receptors (TLRs),[14][15] Wnt co-receptors LRP5/6,[11] the platelet receptor for the von Willebrand factor,[50] and the latent TGFβ docking receptor GARP[13] (see illustration). gp96/GRP94 thus masterminds three major signals that regulate T cell immunity: antigens, TLRs, and TGFβ.

illustration of Zihai Li's Contributions to gp96/GRP94

Li also determined that co-chaperones regulate gp96/GRP94 substrate specificity. For instance, gp96/GRP94 folding of TLRs, LRP5/6, and integrins depends on co-chaperones CNPY3,[15] MesD,[11] and GRP78, respectively. Li’s work advanced our understanding of the role of gp96/GRP94 as a key proteostatic switch for controlling innate immunity, immune tolerance, platelet function, and hematopoiesis. Conceptually, it catalyzes the revelation that ancient chaperones have gained specialized function in mammals, opening a new field of developing chaperone-based therapeutics for a variety of diseases. He coined the term “immune chaperone” to describe this family of molecules.[12]

Other contributions

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Li has also made a significant impact on understanding sex as a biological variable in immune responses. He discovered the T cell-intrinsic roles of androgen receptors in conferring CD8 T cell exhaustion in cancer.[51] In addition, he contributed to the first report that loss of the Y chromosome in tumor cells causes T cell dysfunction and increased sensitivity to anti-PD-1 immunotherapy.[52] Li's work has been fundamental in establishing the immunological basis of sex bias in cancer.

Li's other contributions to the field of medicine and biology include the discovery of a molecular key from platelets (via GARP) for cancer immune evasion[53][54] and the first demonstration of CNPY2 as a critical sensor for PERK-mediated unfolded protein response.[55]

References

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  1. ^ "Pelotonia Institute for Immuno-Oncology Launched at Ohio State With $102,265,000 Investment". The James Cancer Hospital. Retrieved 2024-02-05.
  2. ^ "Education | Zihai Li". LinkedIn. Retrieved 2024-03-14.
  3. ^ "Matthew Ringel, Electra Paskett, Zihai Li named deputy directors at OSUCCC". The Cancer Letter. 2023-12-15. Retrieved 2024-02-05.
  4. ^ "Search results". National Institutes of Health RePORTER. Retrieved 2024-02-05.
  5. ^ "Zihai Li, MD, PhD". American Society for Clinical Investigation. Retrieved 2024-02-05.
  6. ^ "22 AAI Members Named AAAS Fellows". The American Association of Immunologists.
  7. ^ "Spinal cord injury researcher inspires at faculty convocation". web.musc.edu. Retrieved 2024-02-05.
  8. ^ "HCC FACULTY RECOGNIZED at 2016 CONVOCATION" (PDF). MUSC Hollings Cancer Center. p. 8.
  9. ^ "2022 Alumni Reunion and Awards Ceremony". Icahn School of Medicine at Mount Sinai. Retrieved 2024-02-05.
  10. ^ Hong, Feng; Liu, Bei; Chiosis, Gabriela; Gewirth, Daniel T.; Li, Zihai (June 2013). "α7 Helix Region of αI Domain Is Crucial for Integrin Binding to Endoplasmic Reticulum Chaperone gp96". Journal of Biological Chemistry. 288 (25): 18243–18248. doi:10.1074/jbc.m113.468850. ISSN 0021-9258. PMC 3689966. PMID 23671277.
  11. ^ a b c d Liu, Bei; Staron, Matthew; Hong, Feng; Wu, Bill X.; Sun, Shaoli; Morales, Crystal; Crosson, Craig E.; Tomlinson, Stephen; Kim, Ingyu; Wu, Dianqing; Li, Zihai (2013-04-23). "Essential roles of grp94 in gut homeostasis via chaperoning canonical Wnt pathway". Proceedings of the National Academy of Sciences. 110 (17): 6877–6882. Bibcode:2013PNAS..110.6877L. doi:10.1073/pnas.1302933110. ISSN 0027-8424. PMC 3637754. PMID 23572575.
  12. ^ a b c d e Yang, Yi; Liu, Bei; Dai, Jie; Srivastava, Pramod K.; Zammit, David J.; Lefrançois, Leo; Li, Zihai (February 2007). "Heat Shock Protein gp96 Is a Master Chaperone for Toll-like Receptors and Is Important in the Innate Function of Macrophages". Immunity. 26 (2): 215–226. doi:10.1016/j.immuni.2006.12.005. ISSN 1074-7613. PMC 2847270. PMID 17275357.
  13. ^ a b c Zhang, Yongliang; Wu, Bill X.; Metelli, Alessandra; Thaxton, Jessica E.; Hong, Feng; Rachidi, Saleh; Ansa-Addo, Ephraim; Sun, Shaoli; Vasu, Chenthamarakshan; Yang, Yi; Liu, Bei; Li, Zihai (2015-02-02). "GP96 is a GARP chaperone and controls regulatory T cell functions". The Journal of Clinical Investigation. 125 (2): 859–869. doi:10.1172/JCI79014. ISSN 0021-9738. PMC 4319419. PMID 25607841.
  14. ^ a b c d Liu, Bei; Li, Zihai (2008-08-15). "Endoplasmic reticulum HSP90b1 (gp96, grp94) optimizes B-cell function via chaperoning integrin and TLR but not immunoglobulin". Blood. 112 (4): 1223–1230. doi:10.1182/blood-2008-03-143107. ISSN 0006-4971. PMC 2515121. PMID 18509083.
  15. ^ a b c d e Liu, Bei; Yang, Yi; Qiu, Zhijuan; Staron, Matthew; Hong, Feng; Li, Yi; Wu, Shuang; Li, Yunfeng; Hao, Bing; Bona, Robert; Han, David; Li, Zihai (2010-09-21). "Folding of Toll-like receptors by the HSP90 paralogue gp96 requires a substrate-specific cochaperone". Nature Communications. 1 (1): 79. Bibcode:2010NatCo...1...79L. doi:10.1038/ncomms1070. ISSN 2041-1723. PMC 2982182. PMID 20865800.
  16. ^ a b c Liu, Bei; Yang, Yi; Dai, Jie; Medzhitov, Ruslan; Freudenberg, Marina A.; Zhang, Ping L.; Li, Zihai (2006-11-15). "TLR4 Up-Regulation at Protein or Gene Level Is Pathogenic for Lupus-Like Autoimmune Disease". The Journal of Immunology. 177 (10): 6880–6888. doi:10.4049/jimmunol.177.10.6880. ISSN 0022-1767. PMID 17082602.
  17. ^ a b c Staron, Matthew; Yang, Yi; Liu, Bei; Li, Janet; Shen, Yuankai; Zúñiga-Pflücker, Juan Carlos; Aguila, Hector L.; Goldschneider, Irving; Li, Zihai (2010). "Gp96, an endoplasmic reticulum master chaperone for integrins and Toll-like receptors, selectively regulates early T and B lymphopoiesis". Blood. 115 (12): 2380–2390. doi:10.1182/blood-2009-07-233031. PMC 2845896. PMID 19965672. Retrieved 2024-02-05.
  18. ^ Blachere, Nathalie E.; Li, Zihai; Chandawarkar, Rajiv Y.; Suto, Ryuichiro; Jaikaria, Navdeep S.; Basu, Sreyashi; Udono, Heiichiro; Srivastava, Pramod K. (1997). "Heat Shock Protein–Peptide Complexes, Reconstituted in Vitro, Elicit Peptide-specific Cytotoxic T Lymphocyte Response and Tumor Immunity". The Journal of Experimental Medicine. 186 (8): 1315–1322. doi:10.1084/jem.186.8.1315. PMC 2199095. PMID 9334371. Retrieved 2024-02-05.
  19. ^ Zheng, Hong; Dai, Jie; Stoilova, Diliana; Li, Zihai (2001). "Cell Surface Targeting of Heat Shock Protein gp96 Induces Dendritic Cell Maturation and Antitumor Immunity". The Journal of Immunology. 167 (12): 6731–6735. doi:10.4049/jimmunol.167.12.6731. PMID 11739487. Retrieved 2024-02-05.
  20. ^ Audouard, Christophe; Masson, Florent Le; Charry, Colette; Li, Zihai; Christians, Elisabeth S. (2011-02-15). "Oocyte–Targeted Deletion Reveals That Hsp90b1 Is Needed for the Completion of First Mitosis in Mouse Zygotes". PLOS ONE. 6 (2): e17109. Bibcode:2011PLoSO...617109A. doi:10.1371/journal.pone.0017109. ISSN 1932-6203. PMC 3039677. PMID 21358806.
  21. ^ Barton, Elisabeth R.; Park, SooHyun; James, Jose K.; Makarewich, Catherine A.; Philippou, Anastassios; Eletto, Davide; Lei, Hanqin; Brisson, Becky; Ostrovsky, Olga; Li, Zihai; Argon, Yair (September 2012). "Deletion of muscle GRP94 impairs both muscle and body growth by inhibiting local IGF production". The FASEB Journal. 26 (9): 3691–3702. doi:10.1096/fj.11-203026. ISSN 0892-6638. PMC 3425820. PMID 22649033.
  22. ^ Morales, Crystal; Rachidi, Saleh; Hong, Feng; Sun, Shaoli; Ouyang, Xinshou; Wallace, Caroline; Zhang, Yongliang; Garret-Mayer, Elizabeth; Wu, Jennifer; Liu, Bei; Li, Zihai (2014-01-15). "Immune Chaperone gp96 Drives the Contributions of Macrophages to Inflammatory Colon Tumorigenesis". Cancer Research. 74 (2): 446–459. doi:10.1158/0008-5472.can-13-1677. ISSN 0008-5472. PMC 4002507. PMID 24322981.
  23. ^ Metelli, Alessandra; Wu, Bill X.; Fugle, Caroline W.; Rachidi, Saleh; Sun, Shaoli; Zhang, Yongliang; Wu, Jennifer; Tomlinson, Stephen; Howe, Philip H.; Yang, Yi; Garrett-Mayer, Elizabeth; Liu, Bei; Li, Zihai (2016). "Surface Expression of TGFβ Docking Receptor GARP Promotes Oncogenesis and Immune Tolerance in Breast Cancer". Cancer Research. 76 (24): 7106–7117. doi:10.1158/0008-5472.can-16-1456. PMC 5504525. PMID 27913437. Retrieved 2024-02-05.
  24. ^ Huck, John D.; Que, Nanette L.; Hong, Feng; Li, Zihai; Gewirth, Daniel T. (September 2017). "Structural and Functional Analysis of GRP94 in the Closed State Reveals an Essential Role for the Pre-N Domain and a Potential Client-Binding Site". Cell Reports. 20 (12): 2800–2809. doi:10.1016/j.celrep.2017.08.079. ISSN 2211-1247. PMC 5608278. PMID 28930677.
  25. ^ Wu, Bill X.; Li, Anqi; Lei, Liming; Kaneko, Satoshi; Wallace, Caroline; Li, Xue; Li, Zihai (November 2017). "Glycoprotein A repetitions predominant (GARP) positively regulates transforming growth factor (TGF) β3 and is essential for mouse palatogenesis". Journal of Biological Chemistry. 292 (44): 18091–18097. doi:10.1074/jbc.m117.797613. ISSN 0021-9258. PMC 5672034. PMID 28912269.
  26. ^ Thaxton, Jessica E.; Wallace, Caroline; Riesenberg, Brian; Zhang, Yongliang; Paulos, Chrystal M.; Beeson, Craig C.; Liu, Bei; Li, Zihai (2017-08-01). "Modulation of Endoplasmic Reticulum Stress Controls CD4 T-cell Activation and Antitumor Function". Cancer Immunology Research. 5 (8): 666–675. doi:10.1158/2326-6066.cir-17-0081. ISSN 2326-6066. PMC 5585019. PMID 28642246.
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  28. ^ Wallace, Caroline H.; Wu, Bill X.; Salem, Mohammad; Ansa-Addo, Ephraim A.; Metelli, Alessandra; Sun, Shaoli; Gilkeson, Gary; Shlomchik, Mark J.; Liu, Bei; Li, Zihai (2018-04-05). "B lymphocytes confer immune tolerance via cell surface GARP-TGF-β complex". JCI Insight. 3 (7). doi:10.1172/jci.insight.99863. ISSN 0021-9738. PMC 5928869. PMID 29618665.
  29. ^ Salem, Mohammad; Wallace, Caroline; Velegraki, Maria; Li, Anqi; Ansa-Addo, Ephraim; Metelli, Alessandra; Kwon, Hyunwoo; Riesenberg, Brian; Wu, Bill; Zhang, Yongliang; Guglietta, Silvia; Sun, Shaoli; Liu, Bei; Li, Zihai (2019-03-15). "GARP Dampens Cancer Immunity by Sustaining Function and Accumulation of Regulatory T Cells in the Colon". Cancer Research. 79 (6): 1178–1190. doi:10.1158/0008-5472.can-18-2623. ISSN 0008-5472. PMC 6420855. PMID 30674536.
  30. ^ Riesenberg, Brian P.; Ansa-Addo, Ephraim A.; Gutierrez, Jennifer; Timmers, Cynthia D.; Liu, Bei; Li, Zihai (2019-09-01). "Cutting Edge: Targeting Thrombocytes to Rewire Anticancer Immunity in the Tumor Microenvironment and Potentiate Efficacy of PD-1 Blockade". The Journal of Immunology. 203 (5): 1105–1110. doi:10.4049/jimmunol.1900863. ISSN 0022-1767. PMC 7304159. PMID 31358658.
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  33. ^ Iwanowycz, Stephen; Ngoi, Soo; Li, Yingqi; Hill, Megan; Koivisto, Christopher; Parrish, Melodie; Guo, Beichu; Li, Zihai; Liu, Bei (2021-09-08). "Type 2 dendritic cells mediate control of cytotoxic T cell resistant tumors". JCI Insight. 6 (17). doi:10.1172/jci.insight.145885. ISSN 0021-9738. PMC 8492342. PMID 34283809.
  34. ^ Li, Anqi; Chang, Yuzhou; Song, No-Joon; Wu, Xingjun; Chung, Dongjun; Riesenberg, Brian P.; Velegraki, Maria; Giuliani, Giuseppe D.; Das, Komal; Okimoto, Tamio; Kwon, Hyunwoo; Chakravarthy, Karthik B.; Bolyard, Chelsea; Wang, Yi; He, Kai (2022-09-01). "Selective targeting of GARP-LTGFβ axis in the tumor microenvironment augments PD-1 blockade via enhancing CD8 T cell antitumor immunity". Journal for ImmunoTherapy of Cancer. 10 (9): e005433. doi:10.1136/jitc-2022-005433. ISSN 2051-1426. PMC 9472209. PMID 36096533.
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  36. ^ Hua, Yunpeng; White-Gilbertson, Shai; Kellner, Joshua; Rachidi, Saleh; Usmani, Saad Z.; Chiosis, Gabriela; DePinho, Ronald; Li, Zihai; Liu, Bei (2013-11-14). "Molecular Chaperone gp96 Is a Novel Therapeutic Target of Multiple Myeloma". Clinical Cancer Research. 19 (22): 6242–6251. doi:10.1158/1078-0432.ccr-13-2083. ISSN 1078-0432. PMC 3851294. PMID 24077352.
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  53. ^ Rachidi, Saleh; Metelli, Alessandra; Riesenberg, Brian; Wu, Bill X.; Nelson, Michelle H.; Wallace, Caroline; Paulos, Chrystal M.; Rubinstein, Mark P.; Garrett-Mayer, Elizabeth; Hennig, Mirko; Bearden, Daniel W.; Yang, Yi; Liu, Bei; Li, Zihai (2017-05-05). "Platelets subvert T cell immunity against cancer via GARP-TGFβ axis". Science Immunology. 2 (11). doi:10.1126/sciimmunol.aai7911. ISSN 2470-9468. PMC 5539882. PMID 28763790.
  54. ^ Metelli, Alessandra; Wu, Bill X.; Riesenberg, Brian; Guglietta, Silvia; Huck, John D.; Mills, Catherine; Li, Anqi; Rachidi, Saleh; Krieg, Carsten; Rubinstein, Mark P.; Gewirth, Daniel T.; Sun, Shaoli; Lilly, Michael B.; Wahlquist, Amy H.; Carbone, David P. (2020-01-08). "Thrombin contributes to cancer immune evasion via proteolysis of platelet-bound GARP to activate LTGF-β". Science Translational Medicine. 12 (525). doi:10.1126/scitranslmed.aay4860. ISSN 1946-6234. PMC 7814995. PMID 31915300.
  55. ^ Hong, Feng; Liu, Bei; Wu, Bill X.; Morreall, Jordan; Roth, Brady; Davies, Christopher; Sun, Shaoli; Diehl, J. Alan; Li, Zihai (October 2017). "CNPY2 is a key initiator of the PERK–CHOP pathway of the unfolded protein response". Nature Structural & Molecular Biology. 24 (10): 834–839. doi:10.1038/nsmb.3458. ISSN 1545-9985. PMC 6102046. PMID 28869608.
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