Treg suppress CTL responses upon immunization with HSP gp96

European Journal of Immunology

Volumn 39, Issue 11, 2009, Pages 3110-3120

  Liu, Zhen ^a   Li, Xinghui ^a   Qiu, Lipeng ^a   Zhang, Xiaojun ^a   Chen, Lizhao ^a   Cao, Sheng ^a   Wang, Fusheng ^b   Meng, Songdong ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b BEIJING 302 HOSPITAL   (China)

Author keywords

CTL; gp96; Hepatitis B virus; Treg

Indexed keywords

CANCER VACCINE; GLYCOPROTEIN GP 96;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNIZATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG MEGADOSE; FEMALE; LOW DRUG DOSE; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TUMOR IMMUNITY;

ANIMALS; ANTIGENS, NEOPLASM; CELL SEPARATION; CYTOTOXICITY, IMMUNOLOGIC; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HEPATITIS B CORE ANTIGENS; IMMUNIZATION; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEOPLASMS, EXPERIMENTAL; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, REGULATORY;

EID: 70449334144     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939593     Document Type: Article

References (36)

1. Srivastava, P., Roles of heat-shock proteins in innate and adaptive immunity. Nat. Rev. Immunol. 2002. 2: 185-194.
2. Doody, A. D., Kovalchin, J. T., Mihalyo, M. A., Hagymasi, A. T., Drake, C. G. and Adler, A. J., Glycoprotein 96 can chaperone both MHC class I- and class II-restricted epitopes for in vivo presentation, but selectively primes CD8+T cell effector function. J. Immunol. 2004. 172: 6087-6092.
3. Robert, J., Ramanayake, T., Maniero, G. D., Morales, H. and Chida, A. S., Phylogenetic conservation of glycoprotein 96 ability to interact with CD91 and facilitate antigen cross-presentation. J. Immunol. 2008. 180: 3176-3182.
4. + T cells. Cell Stress Chaperones 2006. 11: 364-378.
5. Akutsu, Y., Matsubara, H., Urashima, T., Komatsu, A., Sakata, H., Nishimori, T., Yoneyama, Y. et al. Combination of direct intratumoral administration of dendritic cells and irradiation induces strong systemic antitumor effect mediated by GRP94/gp96 against squamous cell carcinoma in mice. Int. J. Oncol. 2007. 31: 509-515.
6. Yang, Y., Liu, B., Dai, J., Srivastava, P. K., Zammit, D. J., Lefranc-ois, L. and Li, Z., Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 2007. 26: 215-226. (Pubitemid 46329432)
7. Tamura, Y., Peng, P., Liu, K., Daou, M. and Srivastava, P. K., Immunotherapy of tumors with autologous tumor-derived heat shock protein preparations. Science 1997. 278: 117-120. (Pubitemid 27446289)
8. Aalamian, M., Fuchs, E., Gupta, R. and Levey, D. L., Autologous renal cell cancer vaccines using heat shock protein-peptide complexes. Urol. Oncol. 2006. 24: 425-433.
9. SenGupta, D., Norris, P. J., Suscovich, T. J., Hassan-Zahraee, M., Moffett, H. F., Trocha, A., Draenert, R. et al. Heat shock protein-mediated cross-presentation of exogenous HIV antigen on HLA class I and class II. J. Immunol. 2004. 173: 1987-1993. (Pubitemid 38971635)
10. Basta, S., Stoessel, R., Basler, M., van den Broek, M. and Groettrup, M., Cross-presentation of the long-lived lymphocytic choriomeningitis virus nucleoprotein does not require neosynthesis and is enhanced via heat shock proteins. J. Immunol. 2005. 175: 796-805. (Pubitemid 41094961)
11. Testori, A., Richards, J., Whitman, E., Mann, G. B., Lutzky, J., Camacho, L., Parmiani, G. et al. C-100-21 Study Group. Phase III comparison of vitespen, an autologous tumor-derived heat shock protein gp96 peptide complex vaccine, with physician's choice of treatment for stage IV melanoma: the C-100-21 Study Group. J. Clin. Oncol. 2008. 26: 955-962.
12. Li, H., Zhou, M., Han, J., Zhu, X., Dong, T., Gao, G. F. and Tien, P. Generation of murine CTL by a hepatitis B virus-specific peptide and evaluation of the adjuvant effect of heat shock protein glycoprotein 96 and its terminal fragments. J. Immunol. 2005. 174: 195-204. (Pubitemid 40007405)
13. Zhu, X.-D., Li, C.-L., Lang, Z.-W., Gao, G. F. and Tien, P., Significant correlation between expression level of HSP gp96 and the progression of hepatitis B virus induced diseases. World J. Gastroenterol. 2004. 10: 1141-1145.
14. Chandawarkar, R. Y., Wagh, M. S. and Srivastava, P. K. The dual nature of specific immunological activity of tumor-derived gp96 preparations. J. Exp. Med. 1999. 189: 1437-1442.
15. Chandawarkar, R. Y., Wagh, M. S., Kovalchin, J. T. and Srivastava, P., Immune modulation with high-dose heat-shock protein gp96: therapy of murine autoimmune diabetes and encephalomyelitis. Int. Immunol. 2004. 16: 615-624.
16. Hori, S., Nomura, T. and Sakaguchi, S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003. 299: 1057-1061. (Pubitemid 36222930)
17. + natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol. Rev. 2006. 212: 8-27.
18. Manigold, T. and Racanelli, V., T-cell regulation by CD4 regulatory T cells during hepatitis B and C virus infections: facts and controversies. Lancet Infect. Dis. 2007. 7:804-813.
19. Fu, J., Xu, D., Liu, Z., Shi, M., Zhao, P., Fu, B., Zhang, Z. et al. Increased regulatory T cells correlate with CD8 T-cell impairment and poor survival in hepatocellular carcinoma patients. Gastroenterology 2007. 132: 2328-2339. (Pubitemid 46890865)
20. Dai, J., Liu, B., Ngoi, S. M., Sun, S., Vella, A. T. and Li, Z., TLR4 hyperresponsiveness via cell surface expression of heat shock protein gp96 potentiates suppressive function of regulatory T cells. J. Immunol. 2007. 178: 3219-3225. (Pubitemid 46333204)
21. + regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur. J. Immunol. 2004. 34: 336-344.
22. Lutsiak, M. E., Semnani, R. T., De Pascalis, R., Kashmiri, S. V., Schlom, J. and Sabzevari, H., Inhibition of CD4(+)25+T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood 2005. 105: 2862-2868. (Pubitemid 40446280)
23. Buckwalter, M. R. and Srivastava, P. K. "It is the antigen(s), stupid" and other lessons from over a decade of vaccitherapy of human cancer. Semin. Immunol. 2008. 20: 296-300.
24. Filipazzi, P., Valenti, R., Huber, V., Pilla, L., Canese, P., Iero, M., Castelli, C. et al. Identification of a new subset of myeloid suppressor cells in peripheral blood of melanoma patients with modulation by a granulocyte-macrophage colony-stimulation factor-based antitumor vaccine. J. Clin. Oncol. 2007. 25:2546-2553.
25. Yan, J., Liu, X., Wang, Y., Jiang, X., Liu, H., Wang, M., Zhu, X. et al. Enhancing the potency of HBV DNA vaccines using fusion genes of HBV specific antigens and the N-terminal fragment of gp96. J. Gene Med. 2007. 9: 107-121. (Pubitemid 46444488)
26. Di Paolo, N. C., Tuve, S., Ni, S., Hellström, K. E., Hellström, I. and Lieber, A., Effect of adenovirus-mediated heat shock protein expression and oncolysis in combination with low-dose cyclophosphamide treatment on antitumor immune responses. Cancer Res. 2006. 66: 960-969. (Pubitemid 43165964)
27. + regulatory T cells modulate immune tolerance and acute exacerbation on the natural history of chronic hepatitis B virus infection. J. Biomed. Sci. 2007. 14: 43-57.
28. Kondo, Y., Kobayashi, K., Asabe, S., Shiina, M., Niitsuma, H., Ueno, Y., Kobayashi, T. and Shimosegawa T., Vigorous response of cytotoxic T lymphocytes associated with systemic activation of CD8 T lymphocytes in fulminant hepatitis B. Liver Int. 2004. 24: 561-567. (Pubitemid 40028607)
29. Miyake, Y., Iwasaki, Y., Terada, R., Takaguchi, K., Sakaguchi, K. and Shiratori, Y. Systemic inflammatory response syndrome strongly affects the prognosis of patients with fulminant hepatitis B. J. Gastroenterol. 2007. 42: 485-492. (Pubitemid 47050012)
30. Meng, S., Song, J., Rao, Z., Tien, P. and Gao, G. Three-step purification of gp96 from human liver tumor tissues suitable for isolation of gp96-bound peptides. J. Immunol. Methods 2002. 264: 29-35. (Pubitemid 34615888)
31. Meng, S., Gao, T., Gao, G. F. and Tien, P., HBV-specific peptide associated with heat shock protein gp96. Lancet 2001. 357: 528-529. (Pubitemid 32173593)
32. Maini, M. K., Boni, C., Lee, C. K., Larrubia, J. R., Reignat, S., Ogg, G. S., King, A. S. et al. The role of virus-specific CD8(+) cells in liver damage and viral control during persistent hepatitis B virus infection. J. Exp. Med. 2000. 191: 1269-1280.
33. Zanin-Zhorov, A., Cahalon, L., Tal, G., Margalit, R., Lider, O. and Cohen, I. R., Heat shock protein 60 enhances CD4+CD25+regulatory T cell function via innate TLR2 signaling. J. Clin. Invest. 2006. 116: 2022-2032.
34. Warger, T., Hilf, N., Rechtsteiner, G., Haselmayer, P., Carrick, D. M., Jonuleit, H., von Landenberg, P. et al. Interaction of TLR2 and TLR4 ligands with the N-terminal domain of Gp96 amplifies innate and adaptive immune responses. J. Biol. Chem. 2006. 281: 22545-22553.
35. Liu, S., Tobias, R., McClure, S., Styba, G., Shi, Q. and Jackowski, G., Removal of endotoxin from recombinant protein preparations. Clin. Biochem. 1997. 30: 455-463.
36. Gidalevitz, T., Biswas, C., Ding, H., Schneidman-Duhovny, D., Wolfson, H. J., Stevens, F., Radford, S. and Argon, Y., Identification of the N-terminal peptide binding site of glucose-regulated protein 94. J. Biol. Chem. 2004. 279: 16543-16552.