Processing of tumor antigen differentially impacts the development of helper and effector CD4+ T-cell responses

Molecular Therapy

Volumn 18, Issue 6, 2010, Pages 1224-1232

  Bernard, Dannie ^a   Ventresca, Michael S ^a   Marshall, Laura A ^a   Evelegh, Carole ^a   Wan, Yonghong ^a   Bramson, Jonathan L ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; DOPACHROME TAUTOMERASE; TUMOR ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; CANCER IMMUNIZATION; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; EFFECTOR CELL; FEMALE; HELPER CELL; IMMUNOGENICITY; MELANOMA; MOUSE; NONHUMAN; PROTEIN PROCESSING; GLYCOSYLATION; HUMAN; IMMUNOLOGY; MUTATION;

ADENOVIRIDAE; MURINAE;

ANTIGENS, NEOPLASM; CD4-POSITIVE T-LYMPHOCYTES; GLYCOSYLATION; HUMANS; IMMUNITY, CELLULAR; MUTATION;

EID: 77953135734     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2010.30     Document Type: Article

References (50)

1. Ossendorp, F, Mengedé, E, Camps, M, Filius, R and Melief, CJ (1998). Specifc T helper cell requirement for optimal induction of cytotoxic T lymphocytes against major histocompatibility complex class II negative tumors. J Exp Med 187: 693-702.
2. Wang, JC and Livingstone, AM (2003). Cutting edge: CD4+ T cell help can be essential for primary CD8+ T cell responses in vivo. J Immunol 171: 6339-6343.
3. Gao, FG, Khammanivong, V, Liu, WJ, Leggatt, GR, Frazer, IH and Fernando, GJ (2002). Antigen-specifc CD4+ T-cell help is required to activate a memory CD8+ T cell to a fully functional tumor killer cell. Cancer Res 62: 6438-6441.
4. Janssen, EM, Lemmens, EE, Wolfe, T, Christen, U, von Herrath, MG and Schoenberger, SP (2003). CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421: 852-856.
5. Shedlock, DJ and Shen, H (2003). Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300: 337-339.
6. Topalian, SL, Rivoltini, L, Mancini, M, Ng, J, Hartzman, RJ and Rosenberg, SA (1994). Melanoma-specifc CD4+ T lymphocytes recognize human melanoma antigens processed and presented by Epstein-Barr virus-transformed B cells. Int J Cancer 58: 69-79.
7. Perez, SA, Sotiropoulou, PA, Sotiriadou, NN, Mamalaki, A, Gritzapis, AD, Echner, H et al. (2002). HER-2/neu-derived peptide 884-899 is expressed by human breast, colorectal and pancreatic adenocarcinomas and is recognized by in-vitro-induced specifc CD4(+) T cell clones. Cancer Immunol Immunother 50: 615-624.
8. Schattner, EJ, Mascarenhas, J, Bishop, J, Yoo, DH, Chadburn, A, Crow, MK et al. (1996). CD4+ T-cell induction of Fas-mediated apoptosis in Burkitt's lymphoma B cells. Blood 88: 1375-1382. (Pubitemid 26276813)
9. Thomas, WD and Hersey, P (1998). TNF-related apoptosis-inducing ligand (TRAIL) induces apoptosis in Fas ligand-resistant melanoma cells and mediates CD4 T cell killing of target cells. J Immunol 161: 2195-2200.
10. Echchakir, H, Bagot, M, Dorothée, G, Martinvalet, D, Le Gouvello, S, Boumsell, L et al. (2000). Cutaneous T cell lymphoma reactive CD4+ cytotoxic T lymphocyte clones display a Th1 cytokine profle and use a fas-independent pathway for specifc tumor cell lysis. J Invest Dermatol 115: 74-80.
11. Dighe, AS, Richards, E, Old, LJ and Schreiber, RD (1994). Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFN gamma receptors. Immunity 1: 447-456.
12. Qin, Z and Blankenstein, T (2000). CD4+ T cell-mediated tumor rejection involves inhibition of angiogenesis that is dependent on IFN gamma receptor expression by nonhematopoietic cells. Immunity 12: 677-686.
13. Volpert, OV, Fong, T, Koch, AE, Peterson, JD, Waltenbaugh, C, Tepper, RI et al. (1998). Inhibition of angiogenesis by interleukin 4. J Exp Med 188: 1039-1046.
14. Saleh, M, Davis, ID and Wilks, AF (1997). The paracrine role of tumour-derived mIL-4 on tumour-associated endothelium. Int J Cancer 72: 664-672.
15. Hung, K, Hayashi, R, Lafond-Walker, A, Lowenstein, C, Pardoll, D and Levitsky, H (1998). The central role of CD4(+) T cells in the antitumor immune response. J Exp Med 188: 2357-2368.
16. Mattes, J, Hulett, M, Xie, W, Hogan, S, Rothenberg, ME, Foster, P et al. (2003). Immunotherapy of cytotoxic T cell-resistant tumors by T helper 2 cells: an eotaxin and STAT6-dependent process. J Exp Med 197: 387-393.
17. Levitsky, HI, Lazenby, A, Hayashi, RJ and Pardoll, DM (1994). In vivo priming of two distinct antitumor effector populations: the role of MHC class I expression. J Exp Med 179: 1215-1224.
18. Leitch, J, Fraser, K, Lane, C, Putzu, K, Adema, GJ, Zhang, QJ et al. (2004). CTL-dependent and-independent antitumor immunity is determined by the tumor not the vaccine. J Immunol 172: 5200-5205.
19. Perez-Diez, A, Joncker, NT, Choi, K, Chan, WF, Anderson, CC, Lantz, O et al. (2007). CD4 cells can be more effcient at tumor rejection than CD8 cells. Blood 109: 5346-5354.
20. Hunder, NN, Wallen, H, Cao, J, Hendricks, DW, Reilly, JZ, Rodmyre, R et al. (2008). Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. N Engl J Med 358: 2698-2703.
21. Lane, C, Leitch, J, Tan, X, Hadjati, J, Bramson, JL and Wan, Y (2004). Vaccination-induced autoimmune vitiligo is a consequence of secondary trauma to the skin. Cancer Res 64: 1509-1514.
22. Kianizad, K, Marshall, LA, Grinshtein, N, Bernard, D, Margl, R, Cheng, S et al. (2007). Elevated frequencies of self-reactive CD8+ T cells following immunization with a xenoantigen are due to the presence of a heteroclitic CD4+ T-cell helper epitope. Cancer Res 67: 6459-6467.
23. Grinshtein, N, Ventresca, M, Margl, R, Bernard, D, Yang, TC, Millar, JB et al. (2009). High-dose chemotherapy augments the effcacy of recombinant adenovirus vaccines and improves the therapeutic outcome. Cancer Gene Ther 16: 338-350.
24. Zhang, S, Bernard, D, Khan, WI, Kaplan, MH, Bramson, JL and Wan, Y (2009). CD4+ T-cell-mediated anti-tumor immunity can be uncoupled from autoimmunity via the STAT4/STAT6 signaling axis. Eur J Immunol 39: 1252-1259.
25. Bloom, MB, Perry-Lalley, D, Robbins, PF, Li, Y, el-Gamil, M, Rosenberg, SA et al. (1997). Identifcation of tyrosinase-related protein 2 as a tumor rejection antigen for the B16 melanoma. J Exp Med 185: 453-459.
26. Steitz, J, Brück, J, Lenz, J, Büchs, S and Tüting, T (2005). Peripheral CD8+ T cell tolerance against melanocytic self-antigens in the skin is regulated in two steps by CD4+ T cells and local infammation: implications for the pathophysiology of vitiligo. J Invest Dermatol 124: 144-150.
27. Golgher, D, Korangy, F, Gao, B, Gorski, K, Jaffee, E, Edidin, M et al. (2001). An immunodominant MHC class II-restricted tumor antigen is conformation dependent and binds to the endoplasmic reticulum chaperone, calreticulin. J Immunol 167: 147-155.
28. Negroiu, G, Dwek, RA and Petrescu, SM (2003). The inhibition of early N-glycan processing targets TRP-2 to degradation in B16 melanoma cells. J Biol Chem 278: 27035-27042.
29. Guevara-Patiño, JA, Engelhorn, ME, Turk, MJ, Liu, C, Duan, F, Rizzuto, G et al. (2006). Optimization of a self antigen for presentation of multiple epitopes in cancer immunity. J Clin Invest 116: 1382-1390.
30. Skipper, JC, Hendrickson, RC, Gulden, PH, Brichard, V, Van Pel, A, Chen, Y et al. (1996). An HLA-A2-restricted tyrosinase antigen on melanoma cells results from posttranslational modifcation and suggests a novel pathway for processing of membrane proteins. J Exp Med 183: 527-534.
31. Wang, S, Bartido, S, Yang, G, Qin, J, Moroi, Y, Panageas, KS et al. (1999). A role for a melanosome transport signal in accessing the MHC class II presentation pathway and in eliciting CD4+ T cell responses. J Immunol 163: 5820-5826.
32. Lepage, S and Lapointe, R (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.
33. Jackson, IJ, Chambers, DM, Tsukamoto, K, Copeland, NG, Gilbert, DJ, Jenkins, NA et al. (1992). A second tyrosinase-related protein, TRP-2, maps to and is mutated at the mouse slaty locus. EMBO J 11: 527-535.
34. Xu, Y, Bartido, S, Setaluri, V, Qin, J, Yang, G and Houghton, AN (2001). Diverse roles of conserved asparagine-linked glycan sites on tyrosinase family glycoproteins. Exp Cell Res 267: 115-125.
35. Mamula, MJ, Gee, RJ, Elliott, JI, Sette, A, Southwood, S, Jones, PJ et al. (1999). Isoaspartyl post-translational modifcation triggers autoimmune responses to self-proteins. J Biol Chem 274: 22321-22327.
36. Depontieu, FR, Qian, J, Zarling, AL, McMiller, TL, Salay, TM, Norris, A et al. (2009). Identifcation of tumor-associated, MHC class II-restricted phosphopeptides as targets for immunotherapy. Proc Natl Acad Sci USA 106: 12073-12078.
37. Housseau, F, Moorthy, A, Langer, DA, Robbins, PF, Gonzales, MI and Topalian, SL (2001). N-linked carbohydrates in tyrosinase are required for its recognition by human MHC class II-restricted CD4(+) T cells. Eur J Immunol 31: 2690-2701.
38. Vlad, AM, Muller, S, Cudic, M, Paulsen, H, Otvos, L Jr, Hanisch, FG et al. (2002). Complex carbohydrates are not removed during processing of glycoproteins by dendritic cells: processing of tumor antigen MUC1 glycopeptides for presentation to major histocompatibility complex class II-restricted T cells. J Exp Med 196: 1435-1446.
39. Doyle, HA and Mamula, MJ (2001). Post-translational protein modifcations in antigen recognition and autoimmunity. Trends Immunol 22: 443-449.
40. Mimura, Y, Mimura-Kimura, Y, Doores, K, Golgher, D, Davis, BG, Dwek, RA et al. (2007). Folding of an MHC class II-restricted tumor antigen controls its antigenicity via MHC-guided processing. Proc Natl Acad Sci USA 104: 5983-5988.
41. Mincheff, M, Zoubak, S, Altankova, I, Tchakarov, S, Makogonenko, Y, Botev, C et al. (2003). Human dendritic cells genetically engineered to express cytosolically retained fragment of prostate-specifc membrane antigen prime cytotoxic T-cell responses to multiple epitopes. Cancer Gene Ther 10: 907-917.
42. Chicz, RM, Urban, RG, Gorga, JC, Vignali, DA, Lane, WS and Strominger, JL (1993). Specifcity and promiscuity among naturally processed peptides bound to HLA-DR alleles. J Exp Med 178: 27-47.
43. Marks, MS, Theos, AC and Raposo, G (2003). Melanosomes and MHC class II antigen-processing compartments: a tinted view of intracellular traffcking and immunity. Immunol Res 27: 409-426.
44. Wu, TC, Guarnieri, FG, Staveley-O'Carroll, K F, Viscidi, R P, Levitsky, HI, Hedrick, L et al. (1995). Engineering an intracellular pathway for major histocompatibility complex class II presentation of antigens. Proc Natl Acad Sci USA 92: 11671-11675.
45. Wang, RF, Wang, X and Rosenberg, SA (1999). Identifcation of a novel major histocompatibility complex class II-restricted tumor antigen resulting from a chromosomal rearrangement recognized by CD4(+) T cells. J Exp Med 189: 1659-1668.
46. Vidalin, O, Tanaka, E, Spengler, U, Trépo, C and Inchauspé, G (1999). Targeting of hepatitis C virus core protein for MHC I or MHC II presentation does not enhance induction of immune responses to DNA vaccination. DNA Cell Biol 18: 611-621.
47. Deng, H, Kowalczyk, D, O, I, Blaszczyk-Thurin, M, Quan Xiang, Z, Giles-Davis, W et al. (2002). A modifed DNA vaccine to p53 induces protective immunity to challenge with a chemically induced sarcoma cell line. Cell Immunol 215: 20-31.
48. Dobaño, C, Rogers, WO, Gowda, K and Doolan, DL (2007). Targeting antigen to MHC Class I and Class II antigen presentation pathways for malaria DNA vaccines. Immunol Lett 111: 92-102.
49. Fung-Leung, W P, Schilham, MW, Rahemtulla, A, Kündig, TM, Vollenweider, M, Potter, J et al. (1991). CD8 is needed for development of cytotoxic T cells but not helper T cells. Cell 65: 443-449.
50. Guyonneau, L, Murisier, F, Rossier, A, Moulin, A and Beermann, F (2004). Melanocytes and pigmentation are affected in dopachrome tautomerase knockout mice. Mol Cell Biol 24: 3396-3403