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Zihai Li

Title
InstitutionMedical University of South Carolina
DepartmentMicrobiology and Immunology
AddressP.O. Box MSC 955
HO-612B
Hollings Cancer Center - 86 Jonathan Lucas St.
Phone843-792-1034
Fax843-792-9588
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    Collapse Overview 
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    Our laboratory is primarily interested in the mechanism of immune regulation by innate immunity in the context of tumors, infections and autoimmune diseases. By understanding how the immune system deals with microbes, tumors and self, we aim to design effective vaccines and therapeutics against cancer and infectious diseases. Presently our study focuses on two classes of proteins: heat shock proteins (HSPs) and Toll-like receptors (TLRs), both of which have been implicated as master regulators of immunity. We and others have discovered that the function of TLRs is dependent on the integrity of the HSP gp96 (or grp94) in the endoplasmic reticulum. Furthermore, depending on its expression level and its subcellular localization, gp96 can initiate systemic autoimmune disease as well as tumor-specific immunity, both of which have a significant clinical relevance. Using a combination of genetic, cell biological, biochemical and immunological tools, we aim to pinpoint the precise mechanism of TLR-gp96 interaction and define the functions of gp96 in hematopoiesis and in the functions of various cellular components in the immune system. In addition, since gp96 is also an important molecule in mediating the unfolded protein response (UPR), works are ongoing to dissect the roles of gp96 in organ development and oncogenesis, and to develop gp96-specific inhibitors for the treatment of diseases with a heavy pathogenic component of inflammation and metabolic dysregulation. Our study has a broad implication in understanding how the immune system operates physiologically and during pathological conditions, in light of the critical roles of TLRs and the UPR in the evolution, function and regulation of the immune response.

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    Cancer/Other, Minorities, Women-s Health, Cancer, Non-interventional, Men-s Health, Surgery

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    Collapse selected publications
    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Faculty can login to make corrections and additions.
    List All   |   Timeline
    1. Metelli A, Wu BX, Riesenberg B, Guglietta S, Huck JD, Mills C, Li A, Rachidi S, Krieg C, Rubinstein MP, Gewirth DT, Sun S, Lilly MB, Wahlquist AH, Carbone DP, Yang Y, Liu B, Li Z. Thrombin contributes to cancer immune evasion via proteolysis of platelet-bound GARP to activate LTGF-ß. Sci Transl Med. 2020 Jan 08; 12(525). PMID: 31915300.
      View in: PubMed
    2. Karvar S, Ansa-Addo EA, Suda J, Singh S, Zhu L, Li Z, Rockey DC. Moesin, an ERM family member, regulates hepatic fibrosis. Hepatology. 2019 Dec 20. PMID: 31860744.
      View in: PubMed
    3. Riesenberg BP, Ansa-Addo EA, Gutierrez J, Timmers CD, Liu B, Li Z. Cutting Edge: Targeting Thrombocytes to Rewire Anticancer Immunity in the Tumor Microenvironment and Potentiate Efficacy of PD-1 Blockade. J Immunol. 2019 Sep 01; 203(5):1105-1110. PMID: 31358658.
      View in: PubMed
    4. Li P, Zhao R, Fan K, Iwanowycz S, Fan H, Li Z, Liu B. Regulation of dendritic cell function improves survival in experimental sepsis through immune chaperone. Innate Immun. 2019 05; 25(4):235-243. PMID: 31018807.
      View in: PubMed
    5. Dwyer CJ, Knochelmann HM, Smith AS, Wyatt MM, Rangel Rivera GO, Arhontoulis DC, Bartee E, Li Z, Rubinstein MP, Paulos CM. Fueling Cancer Immunotherapy With Common Gamma Chain Cytokines. Front Immunol. 2019; 10:263. PMID: 30842774.
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    6. Luo Z, Li M, Wu Y, Meng Z, Martin L, Zhang L, Ogunrinde E, Zhou Z, Qin S, Wan Z, Westerink MAJ, Warth S, Liu H, Jin P, Stroncek D, Li QZ, Wang E, Wu X, Heath SL, Li Z, Alekseyenko AV, Jiang W. Systemic translocation of Staphylococcus drives autoantibody production in HIV disease. Microbiome. 2019 02 14; 7(1):25. PMID: 30764863.
      View in: PubMed
    7. Salem M, Wallace C, Velegraki M, Li A, Ansa-Addo E, Metelli A, Kwon H, Riesenberg B, Wu B, Zhang Y, Guglietta S, Sun S, Liu B, Li Z. GARP Dampens Cancer Immunity by Sustaining Function and Accumulation of Regulatory T Cells in the Colon. Cancer Res. 2019 03 15; 79(6):1178-1190. PMID: 30674536.
      View in: PubMed
    8. Li Z, Song W, Rubinstein M, Liu D. Recent updates in cancer immunotherapy: a comprehensive review and perspective of the 2018 China Cancer Immunotherapy Workshop in Beijing. J Hematol Oncol. 2018 12 21; 11(1):142. PMID: 30577797.
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    9. Lin CY, Kwon H, Rangel Rivera GO, Li X, Chung D, Li Z. Sex Differences in Using Systemic Inflammatory Markers to Prognosticate Patients with Head and Neck Squamous Cell Carcinoma. Cancer Epidemiol Biomarkers Prev. 2018 10; 27(10):1176-1185. PMID: 30049843.
      View in: PubMed
    10. Metelli A, Salem M, Wallace CH, Wu BX, Li A, Li X, Li Z. Immunoregulatory functions and the therapeutic implications of GARP-TGF-ß in inflammation and cancer. J Hematol Oncol. 2018 02 20; 11(1):24. PMID: 29458436.
      View in: PubMed
    11. Kim DS, Song L, Wang J, Wu H, Gu G, Sugi Y, Li Z, Wang H. GRP94 Is an Essential Regulator of Pancreatic ß-Cell Development, Mass, and Function in Male Mice. Endocrinology. 2018 02 01; 159(2):1062-1073. PMID: 29272356.
      View in: PubMed
    12. Wrangle JM, Patterson A, Johnson CB, Neitzke DJ, Mehrotra S, Denlinger CE, Paulos CM, Li Z, Cole DJ, Rubinstein MP. IL-2 and Beyond in Cancer Immunotherapy. J Interferon Cytokine Res. 2018 02; 38(2):45-68. PMID: 29443657.
      View in: PubMed
    13. Wu BX, Li A, Lei L, Kaneko S, Wallace C, Li X, Li Z. Glycoprotein A repetitions predominant (GARP) positively regulates transforming growth factor (TGF) ß3 and is essential for mouse palatogenesis. J Biol Chem. 2017 11 03; 292(44):18091-18097. PMID: 28912269.
      View in: PubMed
    14. Hong F, Liu B, Wu BX, Morreall J, Roth B, Davies C, Sun S, Diehl JA, Li Z. CNPY2 is a key initiator of the PERK-CHOP pathway of the unfolded protein response. Nat Struct Mol Biol. 2017 Oct; 24(10):834-839. PMID: 28869608.
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    15. Thaxton JE, Wallace C, Riesenberg B, Zhang Y, Paulos CM, Beeson CC, Liu B, Li Z. Modulation of Endoplasmic Reticulum Stress Controls CD4+ T-cell Activation and Antitumor Function. Cancer Immunol Res. 2017 08; 5(8):666-675. PMID: 28642246.
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    16. Bartee E, Li Z. In vivo and in situ programming of tumor immunity by combining oncolytics and PD-1 immune checkpoint blockade. Exp Hematol Oncol. 2017; 6:15. PMID: 28546884.
      View in: PubMed
    17. Hua Y, Yang Y, Sun S, Iwanowycz S, Westwater C, Reizis B, Li Z, Liu B. Gut homeostasis and regulatory T cell induction depend on molecular chaperone gp96 in CD11c+ cells. Sci Rep. 2017 05 19; 7(1):2171. PMID: 28526855.
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    18. Zhang J, Liu D, Li G, Staveley-O'Carroll KF, Graff JN, Li Z, Wu JD. Antibody-mediated neutralization of soluble MIC significantly enhances CTLA4 blockade therapy. Sci Adv. 2017 May; 3(5):e1602133. PMID: 28560327.
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    19. Rachidi S, Metelli A, Riesenberg B, Wu BX, Nelson MH, Wallace C, Paulos CM, Rubinstein MP, Garrett-Mayer E, Hennig M, Bearden DW, Yang Y, Liu B, Li Z. Platelets subvert T cell immunity against cancer via GARP-TGFß axis. Sci Immunol. 2017 May 05; 2(11). PMID: 28763790.
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    20. Majchrzak K, Nelson MH, Bowers JS, Bailey SR, Wyatt MM, Wrangle JM, Rubinstein MP, Varela JC, Li Z, Himes RA, Chan SS, Paulos CM. ß-catenin and PI3Kd inhibition expands precursor Th17 cells with heightened stemness and antitumor activity. JCI Insight. 2017 Apr 20; 2(8). PMID: 28422756.
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    21. Mehrotra S, Britten CD, Chin S, Garrett-Mayer E, Cloud CA, Li M, Scurti G, Salem ML, Nelson MH, Thomas MB, Paulos CM, Salazar AM, Nishimura MI, Rubinstein MP, Li Z, Cole DJ. Vaccination with poly(IC:LC) and peptide-pulsed autologous dendritic cells in patients with pancreatic cancer. J Hematol Oncol. 2017 04 07; 10(1):82. PMID: 28388966.
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    22. Neitzke DJ, Bowers JS, Andrijauskaite K, O'Connell NS, Garrett-Mayer E, Wrangle J, Li Z, Paulos CM, Cole DJ, Rubinstein MP. Murine Th17 cells utilize IL-2 receptor gamma chain cytokines but are resistant to cytokine withdrawal-induced apoptosis. Cancer Immunol Immunother. 2017 Jun; 66(6):737-751. PMID: 28280853.
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    23. Morales C, Li Z. Drosophila canopy b is a cochaperone of glycoprotein 93. J Biol Chem. 2017 04 21; 292(16):6657-6666. PMID: 28275054.
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    24. Hong F, Mohammad Rachidi S, Lundgren D, Han D, Huang X, Zhao H, Kimura Y, Hirano H, Ohara O, Udono H, Meng S, Liu B, Li Z. Mapping the Interactome of a Major Mammalian Endoplasmic Reticulum Heat Shock Protein 90. PLoS One. 2017; 12(1):e0169260. PMID: 28056051.
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    25. Guo B, Fu S, Zhang J, Liu B, Li Z. Targeting inflammasome/IL-1 pathways for cancer immunotherapy. Sci Rep. 2016 10 27; 6:36107. PMID: 27786298.
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    26. Metelli A, Wu BX, Fugle CW, Rachidi S, Sun S, Zhang Y, Wu J, Tomlinson S, Howe PH, Yang Y, Garrett-Mayer E, Liu B, Li Z. Surface Expression of TGFß Docking Receptor GARP Promotes Oncogenesis and Immune Tolerance in Breast Cancer. Cancer Res. 2016 12 15; 76(24):7106-7117. PMID: 27913437.
      View in: PubMed
    27. Zhang J, Zhang K, Li Z, Guo B. ER Stress-induced Inflammasome Activation Contributes to Hepatic Inflammation and Steatosis. J Clin Cell Immunol. 2016 Oct; 7(5). PMID: 27942420.
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    28. Fugle CW, Zhang Y, Hong F, Sun S, Westwater C, Rachidi S, Yu H, Garret-Mayer E, Kirkwood K, Liu B, Li Z. CD24 blunts oral squamous cancer development and dampens the functional expansion of myeloid-derived suppressor cells. Oncoimmunology. 2016; 5(10):e1226719. PMID: 27853649.
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    29. Li Z, Liu D. Cell therapy must be regulated as medicine. Exp Hematol Oncol. 2015; 5:26. PMID: 27547507.
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    30. Liu W, Chen M, Li X, Zhao B, Hou J, Zheng H, Qiu L, Li Z, Meng S. Interaction of Toll-Like Receptors with the Molecular Chaperone Gp96 Is Essential for Its Activation of Cytotoxic T Lymphocyte Response. PLoS One. 2016; 11(5):e0155202. PMID: 27183126.
      View in: PubMed
    31. Johnson CB, Wrangle J, Mehrotra S, Li Z, Paulos CM, Cole DJ, Surh CD, Rubinstein MP. Harnessing the IL-7/IL-7Ra axis to improve tumor immunotherapy. Oncoimmunology. 2016 May; 5(5):e1122865. PMID: 27467935.
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    32. Ansa-Addo EA, Thaxton J, Hong F, Wu BX, Zhang Y, Fugle CW, Metelli A, Riesenberg B, Williams K, Gewirth DT, Chiosis G, Liu B, Li Z. Clients and Oncogenic Roles of Molecular Chaperone gp96/grp94. Curr Top Med Chem. 2016; 16(25):2765-78. PMID: 27072698.
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    33. Luo Z, Ma L, Zhang L, Martin L, Wan Z, Warth S, Kilby A, Gao Y, Bhargava P, Li Z, Wu H, Meissner EG, Li Z, Kilby JM, Liao G, Jiang W. Key differences in B cell activation patterns and immune correlates among treated HIV-infected patients versus healthy controls following influenza vaccination. Vaccine. 2016 Apr 07; 34(16):1945-55. PMID: 26721328.
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    34. Liao Q, Liu W, Liu Y, Wang F, Wang C, Zhang J, Chu M, Jiang D, Xiao L, Shao W, Sheng Z, Tao X, Huo L, Yin CC, Zhang Y, Lee G, Huang J, Li Z, Qiu X. Aberrant high expression of immunoglobulin G in epithelial stem/progenitor-like cells contributes to tumor initiation and metastasis. Oncotarget. 2015 Nov 24; 6(37):40081-94. PMID: 26472025.
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    35. Su EW, Moore CJ, Suriano S, Johnson CB, Songalia N, Patterson A, Neitzke DJ, Andrijauskaite K, Garrett-Mayer E, Mehrotra S, Paulos CM, Doedens AL, Goldrath AW, Li Z, Cole DJ, Rubinstein MP. IL-2Ra mediates temporal regulation of IL-2 signaling and enhances immunotherapy. Sci Transl Med. 2015 Oct 28; 7(311):311ra170. PMID: 26511507.
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    36. Anas AA, de Vos AF, Hoogendijk AJ, van Lieshout MH, van Heijst JW, Florquin S, Li Z, van 't Veer C, van der Poll T. Endoplasmic reticulum chaperone gp96 in macrophages is essential for protective immunity during Gram-negative pneumonia. J Pathol. 2016 Jan; 238(1):74-84. PMID: 26365983.
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    37. Rachidi S, Wallace K, Wrangle JM, Day TA, Alberg AJ, Li Z. Neutrophil-to-lymphocyte ratio and overall survival in all sites of head and neck squamous cell carcinoma. Head Neck. 2016 04; 38 Suppl 1:E1068-74. PMID: 26040762.
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    38. Wu BX, Hong F, Zhang Y, Ansa-Addo E, Li Z. GRP94/gp96 in Cancer: Biology, Structure, Immunology, and Drug Development. Adv Cancer Res. 2016; 129:165-90. PMID: 26916005.
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    39. Zhang Y, Ansa-Addo E, Li Z. GP96: safeguarding Treg. Oncotarget. 2015 Aug 21; 6(24):19936-7. PMID: 26164084.
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    40. Zhang L, Li Z, Wan Z, Kilby A, Kilby JM, Jiang W. Humoral immune responses to Streptococcus pneumoniae in the setting of HIV-1 infection. Vaccine. 2015 Aug 26; 33(36):4430-6. PMID: 26141012.
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    41. Lu S, Zhang J, Liu D, Li G, Staveley-O'Carroll KF, Li Z, Wu JD. Nonblocking Monoclonal Antibody Targeting Soluble MIC Revamps Endogenous Innate and Adaptive Antitumor Responses and Eliminates Primary and Metastatic Tumors. Clin Cancer Res. 2015 Nov 01; 21(21):4819-30. PMID: 26106076.
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    42. Patel HJ, Patel PD, Ochiana SO, Yan P, Sun W, Patel MR, Shah SK, Tramentozzi E, Brooks J, Bolaender A, Shrestha L, Stephani R, Finotti P, Leifer C, Li Z, Gewirth DT, Taldone T, Chiosis G. Structure-activity relationship in a purine-scaffold compound series with selectivity for the endoplasmic reticulum Hsp90 paralog Grp94. J Med Chem. 2015 May 14; 58(9):3922-43. PMID: 25901531.
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    43. Rachidi S, Sun S, Li Z. Endoplasmic reticulum heat shock protein gp96/grp94 is a pro-oncogenic chaperone, not a tumor suppressor. Hepatology. 2015 May; 61(5):1766-7. PMID: 25163410.
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    44. Liu D, Sun W, Hou J, Yuan R, Li Z. Pass quantity, focus on quality. J Hematol Oncol. 2015 Mar 18; 8:27. PMID: 25886529.
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    45. Gudi R, Haycraft CJ, Bell PD, Li Z, Vasu C. Centrobin-mediated regulation of the centrosomal protein 4.1-associated protein (CPAP) level limits centriole length during elongation stage. J Biol Chem. 2015 Mar 13; 290(11):6890-902. PMID: 25616662.
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    46. Zhang Y, Wu BX, Metelli A, Thaxton JE, Hong F, Rachidi S, Ansa-Addo E, Sun S, Vasu C, Yang Y, Liu B, Li Z. GP96 is a GARP chaperone and controls regulatory T cell functions. J Clin Invest. 2015 Feb; 125(2):859-69. PMID: 25607841.
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    47. Li Y, Chitnis N, Nakagawa H, Kita Y, Natsugoe S, Yang Y, Li Z, Wasik M, Klein-Szanto AJ, Rustgi AK, Diehl JA. PRMT5 is required for lymphomagenesis triggered by multiple oncogenic drivers. Cancer Discov. 2015 Mar; 5(3):288-303. PMID: 25582697.
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    48. Salem ML, El-Badawy AS, Li Z. Immunobiology and signaling pathways of cancer stem cells: implication for cancer therapy. Cytotechnology. 2015 Oct; 67(5):749-59. PMID: 25516358.
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    49. Jiang W, Zhang L, Lang R, Li Z, Gilkeson G. Sex differences in monocyte activation in systemic lupus erythematosus (SLE). PLoS One. 2014; 9(12):e114589. PMID: 25485543.
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    50. Rachidi S, Sun S, Wu BX, Jones E, Drake RR, Ogretmen B, Cowart LA, Clarke CJ, Hannun YA, Chiosis G, Liu B, Li Z. Endoplasmic reticulum heat shock protein gp96 maintains liver homeostasis and promotes hepatocellular carcinogenesis. J Hepatol. 2015 Apr; 62(4):879-88. PMID: 25463537.
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    51. Guo B, Li Z. Endoplasmic reticulum stress in hepatic steatosis and inflammatory bowel diseases. Front Genet. 2014; 5:242. PMID: 25120559.
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    52. Zhang L, Luo Z, Sieg SF, Funderburg NT, Yu X, Fu P, Wu H, Jiao Y, Gao Y, Greenspan NS, Harding CV, Kilby JM, Li Z, Lederman MM, Jiang W. Plasmacytoid dendritic cells mediate synergistic effects of HIV and lipopolysaccharide on CD27+ IgD- memory B cell apoptosis. J Virol. 2014 Oct; 88(19):11430-41. PMID: 25056888.
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    53. Bailey SR, Nelson MH, Himes RA, Li Z, Mehrotra S, Paulos CM. Th17 cells in cancer: the ultimate identity crisis. Front Immunol. 2014; 5:276. PMID: 24987392.
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    54. Thaxton JE, Liu B, Zheng P, Liu Y, Li Z. Deletion of CD24 impairs development of heat shock protein gp96-driven autoimmune disease through expansion of myeloid-derived suppressor cells. J Immunol. 2014 Jun 15; 192(12):5679-86. PMID: 24808359.
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    55. Thaxton JE, Li Z. To affinity and beyond: harnessing the T cell receptor for cancer immunotherapy. Hum Vaccin Immunother. 2014; 10(11):3313-21. PMID: 25483644.
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    56. Hong F, Wu BX, Li Z. Molecular regulation of macrophages in unleashing cancer-related inflammation. Oncoimmunology. 2014 Jan 01; 3(1):e27659. PMID: 24778928.
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    57. Li Z, Chen L, Rubinstein MP. Cancer immunotherapy: are we there yet? Exp Hematol Oncol. 2013 Dec 10; 2(1):33. PMID: 24326015.
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    58. Morales C, Rachidi S, Hong F, Sun S, Ouyang X, Wallace C, Zhang Y, Garret-Mayer E, Wu J, Liu B, Li Z. Immune chaperone gp96 drives the contributions of macrophages to inflammatory colon tumorigenesis. Cancer Res. 2014 Jan 15; 74(2):446-59. PMID: 24322981.
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    59. Zhang Y, Helke KL, Coelho SG, Valencia JC, Hearing VJ, Sun S, Liu B, Li Z. Essential role of the molecular chaperone gp96 in regulating melanogenesis. Pigment Cell Melanoma Res. 2014 Jan; 27(1):82-9. PMID: 24024552.
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    60. Hua Y, White-Gilbertson S, Kellner J, Rachidi S, Usmani SZ, Chiosis G, Depinho R, Li Z, Liu B. Molecular chaperone gp96 is a novel therapeutic target of multiple myeloma. Clin Cancer Res. 2013 Nov 15; 19(22):6242-51. PMID: 24077352.
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    61. An N, Lin YW, Mahajan S, Kellner JN, Wang Y, Li Z, Kraft AS, Kang Y. Pim1 serine/threonine kinase regulates the number and functions of murine hematopoietic stem cells. Stem Cells. 2013 Jun; 31(6):1202-12. PMID: 23495171.
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    62. Hong F, Liu B, Chiosis G, Gewirth DT, Li Z. a7 helix region of aI domain is crucial for integrin binding to endoplasmic reticulum chaperone gp96: a potential therapeutic target for cancer metastasis. J Biol Chem. 2013 Jun 21; 288(25):18243-8. PMID: 23671277.
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    63. Liu B, Staron M, Hong F, Wu BX, Sun S, Morales C, Crosson CE, Tomlinson S, Kim I, Wu D, Li Z. Essential roles of grp94 in gut homeostasis via chaperoning canonical Wnt pathway. Proc Natl Acad Sci U S A. 2013 Apr 23; 110(17):6877-82. PMID: 23572575.
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    64. Rachidi SM, Qin T, Sun S, Zheng WJ, Li Z. Molecular profiling of multiple human cancers defines an inflammatory cancer-associated molecular pattern and uncovers KPNA2 as a uniform poor prognostic cancer marker. PLoS One. 2013; 8(3):e57911. PMID: 23536776.
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    65. Pandey JP, Li Z. The forgotten tale of immunoglobulin allotypes in cancer risk and treatment. Exp Hematol Oncol. 2013 Feb 20; 2(1):6. PMID: 23425356.
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    66. Liu B, Staron M, Li Z. Murine but not human basophil undergoes cell-specific proteolysis of a major endoplasmic reticulum chaperone. PLoS One. 2012; 7(6):e39442. PMID: 22724016.
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    67. Wu S, Dole K, Hong F, Noman AS, Issacs J, Liu B, Li Z. Chaperone gp96-independent inhibition of endotoxin response by chaperone-based peptide inhibitors. J Biol Chem. 2012 Jun 08; 287(24):19896-903. PMID: 22532561.
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    68. Li Z, Hsueh CT, Liu D. Publish, not perish: Introducing Experimental Hematology & Oncology. Exp Hematol Oncol. 2012 Mar 26; 1(1):1. PMID: 23210503.
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    69. Liu B, Yang Y, Qiu Z, Staron M, Hong F, Li Y, Wu S, Li Y, Hao B, Bona R, Han D, Li Z. Folding of Toll-like receptors by the HSP90 paralogue gp96 requires a substrate-specific cochaperone. Nat Commun. 2010 Sep 21; 1:79. PMID: 20865800.
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