Heat shock protein 90-mediated peptide-selective presentation of cytosolic tumor antigen for direct recognition of tumors by CD4 + T cells

Journal of Immunology

Volumn 188, Issue 8, 2012, Pages 3851-3858

  Tsuji, Takemasa ^a   Matsuzaki, Junko ^b   Caballero, Otavia L ^a,c   Jungbluth, Achim A ^a   Ritter, Gerd ^a   Odunsi, Kunle ^b   Old, Lloyd J ^a   Gnjatic, Sacha ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b ROSWELL PARK CANCER INSTITUTE   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; ENDOSOMAL PROTEINASE; HEAT SHOCK PROTEIN 90; HLA ANTIGEN CLASS 2; NY ESO 1 ANTIGEN; PROTEASOME; PROTEINASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ALLOGENEIC RESTRICTION; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOSOL; FEMALE; HLA RESTRICTION; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNOSURVEILLANCE; MELANOMA CELL; MOLECULAR RECOGNITION; OVARY CANCER; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CLONING, MOLECULAR; CYTOKINES; CYTOSOL; ENDOSOMES; EPITOPES, T-LYMPHOCYTE; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LYMPHOCYTE ACTIVATION; MELANOMA; OVARIAN NEOPLASMS; PEPTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA, SMALL INTERFERING;

EID: 84860319687     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103269     Document Type: Article

References (46)

1. Hanson, H. L., D. L. Donermeyer, H. Ikeda, J. M. White, V. Shankaran, L. J. Old, H. Shiku, R. D. Schreiber, and P. M. Allen. 2000. Eradication of established tumors by CD8+ T cell adoptive immunotherapy. Immunity 13: 265-276.
2. Dudley, M. E., J. R. Wunderlich, P. F. Robbins, J. C. Yang, P. Hwu, D. J. Schwartzentruber, S. L. Topalian, R. Sherry, N. P. Restifo, A. M. Hubicki, et al. 2002. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298: 850-854. (Pubitemid 35231542)
3. Sato, E., S. H. Olson, J. Ahn, B. Bundy, H. Nishikawa, F. Qian, A. A. Jungbluth, D. Frosina, S. Gnjatic, C. Ambrosone, et al. 2005. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc. Natl. Acad. Sci. USA 102: 18538-18543. (Pubitemid 43011261)
4. Watts, C. 2004. The exogenous pathway for antigen presentation on major histocompatibility complex class II and CD1 molecules. Nat. Immunol. 5: 685-692. (Pubitemid 39023297)
5. Shedlock, D. J., and H. Shen. 2003. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300: 337-339. (Pubitemid 36433726)
6. Janssen, E. M., E. E. Lemmens, T. Wolfe, U. Christen, M. G. von Herrath, and S. P. Schoenberger. 2003. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421: 852-856. (Pubitemid 36254145)
7. Houghton, A. N., T. M. Thomson, D. Gross, H. F. Oettgen, and L. J. Old. 1984. Surface antigens of melanoma and melanocytes. Specificity of induction of Ia antigens by human gamma-interferon. J. Exp. Med. 160: 255-269. (Pubitemid 14089794)
8. Schultz, E. S., B. Lethé, C. L. Cambiaso, J. Van Snick, P. Chaux, J. Corthals, C. Heirman, K. Thielemans, T. Boon, and P. van der Bruggen. 2000. A MAGE-A3 peptide presented by HLA-DP4 is recognized on tumor cells by CD4+ cytolytic T lymphocytes. Cancer Res. 60: 6272-6275.
9. Neumann, F., C. Wagner, B. Kubuschok, S. Stevanovic, H. G. Rammensee, and M. Pfreundschuh. 2004. Identification of an antigenic peptide derived from the cancer-testis antigen NY-ESO-1 binding to a broad range of HLA-DR subtypes. Cancer Immunol. Immunother. 53: 589-599. (Pubitemid 38858332)
10. Odunsi, K., F. Qian, J. Matsuzaki, P. Mhawech-Fauceglia, C. Andrews, E. W. Hoffman, L. Pan, G. Ritter, J. Villella, B. Thomas, et al. 2007. Vaccination with an NY-ESO-1 peptide of HLA class I/II specificities induces integrated humoral and T cell responses in ovarian cancer. Proc. Natl. Acad. Sci. USA 104: 12837-12842. (Pubitemid 47255241)
11. Paludan, C., D. Schmid, M. Landthaler, M. Vockerodt, D. Kube, T. Tuschl, and C. Münz. 2005. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307: 593-596. (Pubitemid 40165684)
12. Tewari, M. K., G. Sinnathamby, D. Rajagopal, and L. C. Eisenlohr. 2005. A cytosolic pathway for MHC class II-restricted antigen processing that is proteasome and TAP dependent. Nat. Immunol. 6: 287-294. (Pubitemid 41724766)
13. Zhou, D., P. Li, Y. Lin, J. M. Lott, A. D. Hislop, D. H. Canaday, R. R. Brutkiewicz, and J. S. Blum. 2005. Lamp-2a facilitates MHC class II presentation of cytoplasmic antigens. Immunity 22: 571-581. (Pubitemid 40719193)
14. Taylor, G. S., H. M. Long, T. A. Haigh, M. Larsen, J. Brooks, and A. B. Rickinson. 2006. A role for intercellular antigen transfer in the recognition of EBV-transformed B cell lines by EBV nuclear antigen-specific CD4+ T cells. J. Immunol. 177: 3746-3756. (Pubitemid 44359907)
15. Tsuji, T., N. K. Altorki, G. Ritter, L. J. Old, and S. Gnjatic. 2009. Characterization of preexisting MAGE-A3-specific CD4+ T cells in cancer patients and healthy individuals and their activation by protein vaccination. J. Immunol. 183: 4800-4808.
16. Tsuji, T., J. Matsuzaki, M. P. Kelly, V. Ramakrishna, L. Vitale, L. Z. He, T. Keler, K. Odunsi, L. J. Old, G. Ritter, and S. Gnjatic. 2011. Antibody-targeted NY-ESO-1 to mannose receptor or DEC-205 in vitro elicits dual human CD8+ and CD4+ T cell responses with broad antigen specificity. J. Immunol. 186: 1218-1227.
17. Lautscham, G., T. Haigh, S. Mayrhofer, G. Taylor, D. Croom-Carter, A. Leese, S. Gadola, V. Cerundolo, A. Rickinson, and N. Blake. 2003. Identification of a TAP-independent, immunoproteasome-dependent CD8+ T-cell epitope in Epstein-Barr virus latent membrane protein 2. J. Virol. 77: 2757-2761. (Pubitemid 36222802)
18. Adorini, L., S. J. Ullrich, E. Appella, and S. Fuchs. 1990. Inhibition by brefeldin A of presentation of exogenous protein antigens to MHC class II-restricted T cells. Nature 346: 63-66.
19. Dongre, A. R., S. Kovats, P. deRoos, A. L. McCormack, T. Nakagawa, V. Paharkova-Vatchkova, J. Eng, H. Caldwell, J. R. Yates, III and A. Y. Rudensky. 2001. In vivo MHC class II presentation of cytosolic proteins revealed by rapid automated tandem mass spectrometry and functional analyses. Eur. J. Immunol. 31: 1485-1494. (Pubitemid 32454696)
20. Dengjel, J., O. Schoor, R. Fischer, M. Reich, M. Kraus, M. Müller, K. Kreymborg, F. Altenberend, J. Brandenburg, H. Kalbacher, et al. 2005. Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc. Natl. Acad. Sci. USA 102: 7922-7927. (Pubitemid 40781039)
21. Sahu, R., S. Kaushik, C. C. Clement, E. S. Cannizzo, B. Scharf, A. Follenzi, I. Potolicchio, E. Nieves, A. M. Cuervo, and L. Santambrogio. 2011. Micro-autophagy of cytosolic proteins by late endosomes. Dev. Cell 20: 131-139.
22. Li, Z., A. Menoret, and P. Srivastava. 2002. Roles of heat-shock proteins in antigen presentation and cross-presentation. Curr. Opin. Immunol. 14: 45-51. (Pubitemid 34085106)
23. Smith, V., E. A. Sausville, R. F. Camalier, H. H. Fiebig, and A. M. Burger. 2005. Comparison of 17-dimethylaminoethylamino-17-demethoxy-geldanamycin (17DMAG) and 17-allylamino-17-demethoxygeldanamycin (17AAG) in vitro: effects on Hsp90 and client proteins in melanoma models. Cancer Chemother. Pharmacol. 56: 126-137. (Pubitemid 40884268)
24. Leu, J. I., J. Pimkina, A. Frank, M. E. Murphy, and D. L. George. 2009. A small molecule inhibitor of inducible heat shock protein 70. Mol. Cell 36: 15-27.
25. Sun, L., C. Liang, S. Shirazian, Y. Zhou, T. Miller, J. Cui, J. Y. Fukuda, J. Y. Chu, A. Nematalla, X. Wang, et al. 2003. Discovery of 5-[5-fluoro-2-oxo-1,2-dihydroindol-(3Z)-ylidenemethyl]-2,4-dimethyl-1H-pyrrole- 3-carboxylic acid (2-diethylaminoethyl)amide, a novel tyrosine kinase inhibitor targeting vascular endothelial and platelet-derived growth factor receptor tyrosine kinase. J. Med. Chem. 46: 1116-1119. (Pubitemid 36428215)
26. Bonehill, A., C. Heirman, S. Tuyaerts, A. Michiels, K. Breckpot, F. Brasseur, Y. Zhang, P. Van Der Bruggen, and K. Thielemans. 2004. Messenger RNA-electroporated dendritic cells presenting MAGE-A3 simultaneously in HLA class I and class II molecules. J. Immunol. 172: 6649-6657. (Pubitemid 38669100)
27. Rowell, J. F., A. L. Ruff, F. G. Guarnieri, K. Staveley-O'Carroll, X. Lin, J. Tang, J. T. August, and R. F. Siliciano. 1995. Lysosome-associated membrane protein-1-mediated targeting of the HIV-1 envelope protein to an endosomal/lysosomal compartment enhances its presentation to MHC class II-restricted T cells. J. Immunol. 155: 1818-1828.
28. Baskar, S., L. Glimcher, N. Nabavi, R. T. Jones, and S. Ostrand-Rosenberg. 1995. Major histocompatibility complex class II+B7-1+ tumor cells are potent vaccines for stimulating tumor rejection in tumor-bearing mice. J. Exp. Med. 181: 619-629.
29. Armstrong, T. D., V. K. Clements, B. K. Martin, J. P. Ting, and S. Ostrand-Rosenberg. 1997. Major histocompatibility complex class II-transfected tumor cells present endogenous antigen and are potent inducers of tumor-specific immunity. Proc. Natl. Acad. Sci. USA 94: 6886-6891. (Pubitemid 27281960)
30. Lepage, S., and R. Lapointe. 2006. Melanosomal targeting sequences from gp100 are essential for MHC class II-restricted endogenous epitope presentation and mobilization to endosomal compartments. Cancer Res. 66: 2423-2432.
31. Gnjatic, S., H. Nishikawa, A. A. Jungbluth, A. O. Güre, G. Ritter, E. Jäger, A. Knuth, Y. T. Chen, and L. J. Old. 2006. NY-ESO-1: review of an immunogenic tumor antigen. Adv. Cancer Res. 95: 1-30. (Pubitemid 44088423)
32. Depontieu, F. R., J. Qian, A. L. Zarling, T. L. McMiller, T. M. Salay, A. Norris, A. M. English, J. Shabanowitz, V. H. Engelhard, D. F. Hunt, and S. L. Topalian. 2009. Identification of tumor-associated, MHC class II-restricted phosphopeptides as targets for immunotherapy. Proc. Natl. Acad. Sci. USA 106: 12073-12078.
33. Gotter, J., B. Brors, M. Hergenhahn, and B. Kyewski. 2004. Medullary epithelial cells of the human thymus express a highly diverse selection of tissue-specific genes colocalized in chromosomal clusters. J. Exp. Med. 199: 155-166. (Pubitemid 38139246)
34. Srivastava, P. K., A. B. DeLeo, and L. J. Old. 1986. Tumor rejection antigens of chemically induced sarcomas of inbred mice. Proc. Natl. Acad. Sci. USA 83: 3407-3411. (Pubitemid 16043046)
35. Basu, S., R. J. Binder, T. Ramalingam, and P. K. Srivastava. 2001. CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity 14: 303-313. (Pubitemid 32289294)
36. Callahan, M. K., M. Garg, and P. K. Srivastava. 2008. Heat-shock protein 90 associates with N-terminal extended peptides and is required for direct and indirect antigen presentation. Proc. Natl. Acad. Sci. USA 105: 1662-1667. (Pubitemid 351346571)
37. Strbo, N., and E. R. Podack. 2008. Secreted heat shock protein gp96-Ig: an innovative vaccine approach. Am. J. Reprod. Immunol. 59: 407-416. (Pubitemid 351524230)
38. Houlihan, J. L., J. J. Metzler, and J. S. Blum. 2009. HSP90alpha and HSP90beta isoforms selectively modulate MHC class II antigen presentation in B cells. J. Immunol. 182: 7451-7458.
39. Imai, T., Y. Kato, C. Kajiwara, S. Mizukami, I. Ishige, T. Ichiyanagi, M. Hikida, J. Y. Wang, and H. Udono. 2011. Heat shock protein 90 (HSP90) contributes to cytosolic translocation of extracellular antigen for cross-presentation by dendritic cells. Proc. Natl. Acad. Sci. USA 108: 16363-16368.
40. Lich, J. D., J. F. Elliott, and J. S. Blum. 2000. Cytoplasmic processing is a prerequisite for presentation of an endogenous antigen by major histocompatibility complex class II proteins. J. Exp. Med. 191: 1513-1524.
41. Kaushik, S., A. C. Massey, N. Mizushima, and A. M. Cuervo. 2008. Constitutive activation of chaperone-mediated autophagy in cells with impaired macro-autophagy. Mol. Biol. Cell 19: 2179-2192.
42. Nishimura, T., K. Iwakabe, M. Sekimoto, Y. Ohmi, T. Yahata, M. Nakui, T. Sato, S. Habu, H. Tashiro, M. Sato, and A. Ohta. 1999. Distinct role of antigen-specific T helper type 1 (Th1) and Th2 cells in tumor eradication in vivo. J. Exp. Med. 190: 617-627. (Pubitemid 29428646)
43. Quezada, S. A., T. R. Simpson, K. S. Peggs, T. Merghoub, J. Vider, X. Fan, R. Blasberg, H. Yagita, P. Muranski, P. A. Antony, et al. 2010. Tumor-reactive CD4(+) T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts. J. Exp. Med. 207: 637-650.
44. Xie, Y., A. Akpinarli, C. Maris, E. L. Hipkiss, M. Lane, E. K. Kwon, P. Muranski, N. P. Restifo, and P. A. Antony. 2010. Naive tumor-specific CD4(+) T cells differentiated in vivo eradicate established melanoma. J. Exp. Med. 207: 651-667.
45. Hunder, N. N., H. Wallen, J. Cao, D. W. Hendricks, J. Z. Reilly, R. Rodmyre, A. Jungbluth, S. Gnjatic, J. A. Thompson, and C. Yee. 2008. Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. N. Engl. J. Med. 358: 2698-2703. (Pubitemid 351860862)
46. Nishikawa, H., and S. Sakaguchi. 2010. Regulatory T cells in tumor immunity. Int. J. Cancer 127: 759-767.