The tumor antigen NY-ESO-1 mediates direct recognition of melanoma cells by CD4+ T cells after intercellular antigen transfer

Journal of Immunology

Volumn 196, Issue 1, 2016, Pages 64-71

  Fonteneau, Jean Francois ^a   Brilot, Fabienne ^b   Münz, Christian ^c   Gannagé, Monique ^d,e  

^a UNIVERSITÉ DE NANTES   (France)

^b CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY OF GENEVA   (Switzerland)

^e University Hospital   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEASOME; TUMOR ANTIGEN; TUMOR ANTIGEN NY ESO 1; UNCLASSIFIED DRUG; ACETYLCYSTEINE; ATG12 PROTEIN, HUMAN; AUTOPHAGY RELATED PROTEIN 12; BENZYLOXYCARBONYLLEUCYL-LEUCYL-LEUCINE ALDEHYDE; CHLOROQUINE; CTAG1B PROTEIN, HUMAN; EPITOPE; HLA ANTIGEN CLASS 2; LACTACYSTIN; LAMP2 PROTEIN, HUMAN; LEUPEPTIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MEMBRANE PROTEIN; SMALL INTERFERING RNA; SUMO PROTEIN;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; MACROAUTOPHAGY; MELANOMA CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; ADOPTIVE IMMUNOTHERAPY; ANALOGS AND DERIVATIVES; AUTOPHAGY; DENDRITIC CELL; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MELANOMA; RNA INTERFERENCE; TRANSPLANTATION; TUMOR CELL LINE;

ACETYLCYSTEINE; ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 12; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CHLOROQUINE; DENDRITIC CELLS; ENDOCYTOSIS; EPITOPES, T-LYMPHOCYTE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; IMMUNOTHERAPY, ADOPTIVE; LEUPEPTINS; LYMPHOCYTE ACTIVATION; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; MELANOMA; MEMBRANE PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS;

EID: 84953285098     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402664     Document Type: Article

References (37)

1. Caballero, O. L., and Y. T. Chen. 2009. Cancer/testis (CT) antigens: potential targets for immunotherapy. Cancer Sci. 100: 2014-2021.
2. + T cells from patients with NY-ESO-1-expressing melanoma. J. Immunol. 174: 1751-1759.
3. + T cell responses against NY-ESO-1 in cancer patients: correlation with antibody responses. Proc. Natl. Acad. Sci. USA 100: 8862-8867.
4. Cho, H. J., O. L. Caballero, S. Gnjatic, V. C. Andrade, G. W. Colleoni, A. L. Vettore, H. H. Outtz, S. Fortunato, N. Altorki, C. A. Ferrera, et al. 2006. Physical interaction of two cancer-testis antigens, MAGE-C1 (CT7) and NY-ESO-1 (CT6). Cancer Immun. 6: 12.
5. + T cells: ready for direct attack J. Exp. Med. 203: 805-808.
6. + T-cell subsets mediate immune recognition of Epstein Barr virus nuclear antigen 1 in healthy virus carriers. Blood 109: 1138-1146.
7. Shedlock, D. J., and H. Shen. 2003. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300: 337-339.
8. Bourgeois, C, H. Veiga-Fernandes, A. M. Joret, B. Rocha, and C. Tanchot. 2002. CD8 lethargy in the absence of CD4 help. Eur. J. Immunol. 32: 2199-2207.
9. Cui, W., and S. M. Kaech. 2010. Generation of effector CD8+ T cells and their conversion to memory T cells. Immunol. Rev. 236: 151-166.
10. Perez-Diez, A., N. T. Joncker, K. Choi, W. F Chan, C. C. Anderson, O. Lantz, and P Matzinger. 2007. CD4 cells can be more efficient at tumor rejection than CD8 cells. Blood 109: 5346-5354.
11. Spolski, R., and W. J. Leonard. 2008. Interleukin-21: basic biology and implications for cancer and autoimmunity. Annu. Rev. Immunol. 26: 57-79.
12. + T cells against NY-ESO-1. N. Engl. J. Med. 358: 2698-2703.
13. Labarriere, N., E. Diez, M. C. Pandolfino, C. Viret, Y Guilloux, S. Le Guiner, J. F Fonteneau, B. Dreno, and F Jotereau. 1997. Optimal T cell activation by melanoma cells depends on a minimal level of antigen transcription. J. Immunol. 158: 1238-1245.
14. + and CD8+ T-cell clones using peptide pulsed mature dendritic cells. J. Immunol. Methods 258: 111-126.
15. Somersan, S., M. Larsson, J. F Fonteneau, S. Basu, P Srivastava, and N. Bhardwaj. 2001. Primary tumor tissue lysates are enriched in heat shock proteins and induce the maturation of human dendritic cells. J. Immunol. 167: 4844-4852.
16. Gannage, M., and C. Miinz. 2009. Autophagy in MHC class II presentation of endogenous antigens. Curr. Top. Microbiol. Immunol. 335: 123-140.
17. Yang, Z., and D. J. Klionsky. 2010. Eaten alive: a history of macroautophagy. Nat. Cell Biol. 12: 814-822.
18. Crotzer, V. L., and J. S. Blum. 2008. Cytosol to lysosome transport of intracellular antigens during immune surveillance. Traffic 9: 10-16.
19. 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.
20. Wang, T, Z. Ming, W. Xiaochun, and W. Hong. 2011. Rab7: role of its protein interaction cascades in endo-lysosomal traffic. Cell. Signal. 23: 516-521.
21. + T-cell help in the tumor milieu is required for recruitment and cytolytic function of CD8+ T lymphocytes. Cancer Res. 70: 8368-8377.
22. + T cells have a major "post-licensing" role in CTL mediated anti-tumor immunity. J. Immunol. 165: 6047-6055.
23. + T-cell loss and impairs secondary antitumor responses after successful initial immunotherapy. Nat. Med. 13: 354-360.
24. Robbins, P F, M. El-Gamil, Y F Li, G. Zeng, M. Dudley, and S. A. Rosenberg. 2002. Multiple HLA class Il-restricted melanocyte differentiation antigens are recognized by tumor-infiltrating lymphocytes from a patient with melanoma. J. Immunol. 169: 6036-6047.
25. Pieper, R., R. E. Christian, M. I. Gonzales, M. I. Nishimura, G. Gupta, R. E. Settlage, J. Shabanowitz, S. A. Rosenberg, D. F Hunt, and S. L. Topalian. 1999. Biochemical identification of a mutated human melanoma antigen recognized by CD4(+) T cells. J. Exp. Med. 189: 757-766.
26. Robila, V., M. Ostankovitch, M. L. Altrich-Vanlith, A. C. Theos, S. Drover, M. S. Marks, N. Restifo, and V. H. Engelhard. 2008. MHC class II presentation of gplOO epitopes in melanoma cells requires the function of conventional endosomes and is influenced by melanosomes. J. Immunol. 181: 7843-7852.
27. 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.
28. Tewari, M. K., G Sinnathamby, D. Rajagopal, and L. C. Eisenlohr. 2005. A cytosolic pathway for MHC class Il-restricted antigen processing that is pro-teasome and TAP dependent. Nat. Immunol. 6: 287-294.
29. + T cells. J. Immunol. 177: 3746-3756.
30. Lugini, L., P Matarrese, A. Tinari, F. Lozupone, C. Federici, E. Iessi, M. Gentile, F. Luciani, G. Parmiani, L. Rivoltini, et al. 2006. Cannibalism of live lymphocytes by human metastatic but not primary melanoma cells. Cancer Res. 66: 3629-3638.
31. Federici, C, D. Brambilla, F Lozupone, P Matarrese, A. de Milito, L. Lugini, E. Iessi, S. Cecchetti, M. Marino, M. Perdicchio, et al. 2009. Pleiotropic function of ezrin in human metastatic melanomas. Int. J. Cancer 124: 2804-2812.
32. Van Den Bossche, K., J. M. Naeyaert, and J. Lambert. 2006. The quest for the mechanism of melanin transfer. Traffic 7: 769-778.
33. Benlalam, H., A. Jalil, M. Hasmim, B. Pang, R. Tamouza, M. Mitterrand, Y Godet, N Lamerant, C. Robert, M. F Avril, et al. 2009. Gap junction communication between autologous endothelial and tumor cells induce cross-recognition and elimination by specific CTL. J. Immunol. 182: 2654-2664.
34. Tsuji, T, J. Matsuzaki, O. L. Caballero, A. A. Jungbluth, G. Ritter, K. Odunsi, L. J. Old, and S. Gnjatic. 2012. Heat shock protein 90-mediated peptide-selective presentation of cytosolic tumor antigen for direct recognition of tumors by CD4 (+) T cells. J. Immunol. 188: 3851-3858.
35. Matsuzaki, J., T Tsuji, I. Luescher, L. J. Old, P Shrikant, S. Gnjatic, and K. Odunsi. 2014. Nonclassical antigen-processing pathways are required for MHC class Il-restricted direct tumor recognition by NY-ESO-l-specific CD4(+) T cells. Cancer Immunol. Res. 2: 341-350.
36. Schatton, T, U. Schiitte, N. Y Frank, Q. Zhan, A. Hoerning, S. C. Robles, J. Zhou, F S. Hodi, G. C. Spagnoli, G. F Murphy, and M. H. Frank 2010. Modulation of T-cell activation by malignant melanoma initiating cells. Cancer Res. 70: 697-708.
37. Heslop, H. E., and M. K. Brenner. 2008. The clone ranger? Mol. Ther. 16: 1520-1521.