Melanocyte-specific, cytotoxic T cell responses in vitiligo: The effective variant of melanoma immunity?

Pigment Cell Research

Volumn 18, Issue 4, 2005, Pages 234-242

  Garbelli, Silvia ^a   Mantovani, Stefania ^a   Palermo, Belinda ^a   Giachino, Claudia ^a,b  

^a IRCCS   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Autoimmunity; Cytotoxic T cells; Melanocyte antigens; Tumor immunity

Indexed keywords

ANTINEOPLASTIC AGENT; CELL ANTIGEN; EPITOPE; GLYCOPROTEIN GP 100; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MELAN A; MELANOMA ANTIGEN; MELANOSOMAL MEMBRANE PROTEIN 1; MEMBRANE PROTEIN; MONOPHENOL MONOOXYGENASE; PROTEIN TYROSINE KINASE; T LYMPHOCYTE RECEPTOR; TYROSINASE RELATED PROTEIN 1; TYROSINASE RELATED PROTEIN 2; UNCLASSIFIED DRUG;

ANTIGEN RECOGNITION; AUTOIMMUNITY; CELL DESTRUCTION; CELL LOSS; CELL SPECIFICITY; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; DISEASE ASSOCIATION; ENZYME ACTIVITY; ERADICATION THERAPY; HLA SYSTEM; HUMAN; IMMUNIZATION; IMMUNOTHERAPY; MELANOCYTE; MELANOMA; MELANOMA CELL; PATHOGENESIS; PIGMENT CELL; REVIEW; TUMOR GROWTH; TUMOR IMMUNITY; VITILIGO;

AUTOIMMUNITY; EPIDERMIS; HUMANS; MELANOCYTES; MELANOMA; RECEPTORS, ANTIGEN, T-CELL; SKIN NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC; VITILIGO;

EID: 22744451812     PISSN: 08935785     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0749.2005.00244.x     Document Type: Review

References (99)

1. Abdel-Naser, M.B., Kruger-Krasagakes, S., Krasagakis, K., Gollnick, H., Abdel-Fattah, A., and Orfanos, C.E. (1994). Further evidence for involvement of both cell mediated and humoral immunity in generalized vitiligo. Pigment Cell Res. 7, 1-8.
2. Altman, J.D., Moss, P.A., Goulder, P.J., Barouch, D.H., McHeyzer-Williams, M.G., Bell, J.I., McMichael, A.J., and Davis, M.M. (1996). Phenotypic analysis of antigen-specific T lymphocytes. Science 274, 94-96.
3. Amrani, A., Verdaguer, J., Serra, P., Tafuro, S., Tan, R., and Santamaria, P. (2000). Progression of autoimmune diabetes driven by avidity maturation of a T-cell population. Nature 406, 739-742.
4. Anichini, A., Maccalli, C., Mortarini, R., Salvi, S., Mazzocchi, A., Squarcina, P., Herlyn, M., and Parmiani, G. (1993). Melanoma cells and normal melanocytes share antigens recognized by HLA-A2-restricted cytotoxic T cell clones from melanoma patients. J. Exp. Med. 177, 989-998.
5. Anichini, A., Molla, A., Mortarini, R. et al. (1999). An expanded peripheral T cell population to a cytotoxic T lymphocyte (CTL)-defined, melanocyte-specific antigen in metastatic melanoma patients impacts on generation of peptide-specific CTLs but does not overcome tumor escape from immune surveillance in metastatic lesions. J. Exp. Med. 190, 651-667.
6. al Badri, A.M., Todd, P.M., Garioch, J.J., Gudgeon, J.E., Stewart, D.G., and Goudie, R.B. (1993). An immunohistological study of cutaneous lymphocytes in vitiligo. J. Pathol. 170, 149-155.
7. Bakker, A.B., Schreurs, M.W., de Boer, A.J., Kawakami, Y., Rosenberg, S.A., Adema, G.J., and Figdor, C.G. (1994). Melanocyte lineage-specific antigen gp100 is recognized by melanoma-derived tumor-infiltrating lymphocytes. J. Exp. Med. 179, 1005-1009.
8. Becker, J.C., Guldberg, P., Zeuthen, J., Brocker, E.B., and Straten, P.T. (1999). Accumulation of identical T cells in melanoma and vitiligo-like leukoderma. J. Invest. Dermatol. 113, 1033-1038.
9. Boon, T., and Old, L.J. (1997). Cancer Tumor antigens. Curr. Opin. Immunol. 9, 681-683.
10. Boon, T., Cerottini, J.C., Van den Eynde, B., van der Bruggen, P., and Van Pel, A. (1994). Tumor antigens recognized by T lymphocytes. Annu. Rev. Immunol. 12, 337-365 (review).
11. Buckley, W.R., and Lobitz, W.C., Jr (1953). Vitiligo with a raised inflammatory border. AMA Arch. Derm. Syphilol. 67, 316-320.
12. Busch, D.H., and Pamer, E.G. (1999). T cell affinity maturation by selective expansion during infection. J. Exp. Med. 189, 701-710.
13. Bystryn, J.C. (1997). Immune mechanisms in vitiligo. Clin. Dermatol. 15, 853-861 (review).
14. Bystryn, J.C., Rigel, D., Friedman, R.J., and Kopf, A. (1987). Prognostic significance of hypopigmentation in malignant melanoma. Arch. Dermatol. 123, 1053-1055.
15. Castelli, C., Mazzocchi, A., Rini, F., Tarsini, P., Rivoltini, L., Maio, M., Gallino, G., Belli, F., and Parmiani, G. (1998). Immunogenicity of the ALLAVGATK (gp100[17-25]) peptide in HLA-A3.1 melanoma patients. Eur. J. Immunol. 28, 1143-1154.
16. Cole, D.J., Weil, D.P., Shilyansky, J., Custer, M., Kawakami, Y., Rosenberg, S.A., and Nishimura, M.I. (1995). Characterization of the functional specificity of a cloned T-cell receptor heterodimer recognizing the MART-1 melanoma antigen. Cancer Res. 55, 748-752.
17. Coulie, P.G., Brichard, V., Van Pel, A. et al. (1994). A new gene coding for a differentiation antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J. Exp. Med. 180, 35-42.
18. D'Souza, S., Rimoldi, D., Lienard, D., Lejeune, F., Cerottini, J.C., and Romero, P. (1998). Circulating Melan-A/Mart-1 specific cytolytic T lymphocyte precursors in HLA-A2+ melanoma patients have a memory phenotype. Int. J. Cancer 78, 699-706.
19. Das, P.K., van den Wijngaard, R.M., Wankowicz-Kalinska, A., and Le Poole, LC. (2001). A symbiotic concept of autoimmunity and tumour immunity: lessons from vitiligo. Trends Immunol. 22, 130-136.
20. Davis, M.M., and Bjorkman, P.J. (1988). T-cell antigen receptor genes and T-cell recognition. Nature 334, 395-402 (review).
21. Dietrich, P.Y., Walker, P.R., Quiquerez, A.L., Perrin, G., Dutoit, V., Lienard, D., Guillaume, P., Cerottini, J.C., Romero, P., and Valmori, D. (2001). Melanoma patients respond to a cytotoxic T lymphocyte-defined self-peptide with diverse and nonoverlapping T-cell receptor repertoires. Cancer Res. 61, 2047-2054.
22. Dietrich, P.Y., Le Gal, F.A., Dutoit, V. et al. (2003). Prevalent role of TCR alpha-chain in the selection of the preimmune repertoire specific for a human tumor-associated self-antigen. J. Immunol. 170, 5103-5109.
23. Ding, Y.H., Smith, K.J., Garboczi, D.N., Utz, U., Biddison, W.E., and Wiley, D.C. (1998). Two human T cell receptors bind in a similar diagonal mode to the HLA-A2/Tax peptide complex using different TCR amino acids. Immunity 8, 403-411.
24. Dunbar, P.R., Smith, C.L., Chao, D. et al. (2000). A shift in the phenotype of melan-A-specific CTL identifies melanoma patients with an active tumor-specific immune response. J. Immunol. 165, 6644-6652.
25. Ferrone, S., and Marincola, F.M. (1995). Loss of HLA class I antigens by melanoma cells: molecular mechanisms, functional significance and clinical relevance, Immunol. Today 16, 487-494 (review).
26. Garcia, K.C., Degano, M., Pease, L.R., Huang, M., Peterson, P.A., Teyton, L., and Wilson, I.A. (1998). Structural basis of plasticity in T cell receptor recognition of a self peptide-MHC antigen. Science 279, 1166-1172.
27. Gross, A., Tapia, F.J., Mosca, W., Perez, R.M., Briceno, L., Henriquez, J.J., and Convit, J. (1987). Mononuclear cell subpopulations and infiltrating lymphocytes in erythema dyschromicum perstans and vitiligo. Histol. Histopathol. 2, 277-283.
28. Hahne, M., Rimoldi, D., Schroter, M. et al. (1996). Melanoma cell expression of Fas(Apo-1/CD95) ligand: implications for tumor immune escape. Science 274, 1363-1366.
29. Ho, R.C. (1995). Medical management of stage IV malignant melanomas. Medical issues. Cancer 75, 735-741.
30. Houghton, A.N., Real, F.X., Davis, L.J., Cordon-Cardo, C., and Old, L.J. (1987). Phenotypic heterogeneity of melanoma. Relation to the differentiation program of melanoma cells. J. Exp. Med. 165, 812-829.
31. Jager, E., Maeurer, M., Hohn, H. et al. (2000). Clonal expansion of Melan A-specific cytotoxic T lymphocytes in a melanoma patient responding to continued immunization with melanoma-associated peptides. Int. J. Cancer 86, 538-547.
32. Kawakami, Y., and Rosenberg, S.A. (1997). Human tumor antigens recognized by T-cells. Immunol. Res. 16, 313-339 (review).
33. Kawakami, Y., Eliyahu, S., Delgado, C.H., Robbins, P.F., Sakaguchi, K., Appella, E., Yannelli, J.R., Adema, G.J., Miki, T., and Rosenberg, S.A. (1994a). Identification of a human melanoma antigen recognized by tumor-infiltrating lymphocytes associated with in vivo tumor rejection. Proc. Natl. Acad. Sci. U. S. A. 91, 6458-6462.
34. Kawakami, Y., Eliyahu, S., Sakaguchi, K., Robbins, P.F., Rivoltini, L., Yannelli, J.R., Appella, E., and Rosenberg, S.A. (1994b). Identification of the immunodominant peptides of the MART-1 human melanoma antigen recognized by the majority of HLA-A2-restricted tumor infiltrating lymphocytes. J. Exp. Med. 180, 347-352
35. Kawakami, Y., Robbins, P.F., Wang, R.F., Parkhurst, M., Kang, X., and Rosenberg, S.A. (1998). The use of melanosomal proteins in the immunotherapy of melanoma. J. Immunother. 21, 237-246 (review).
36. Khong, HT., and Restifo, N.P. (2002). Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat. Immunol. 3, 999-1005 (review).
37. Lang, K.S., Caroli, C.C., Muhm, A., Wernet, D., Moris, A., Schittek, B., Knauss-Scherwitz, E., Stevanovic, S., Rammensee, H.G., and Garbe, C. (2001). HLA-A2 restricted, melanocyte-specific CD8(+) T lymphocytes detected in vitiligo patients are related to disease activity and are predominantly directed against MelanA/MART1. J. Invest. Dermatol. 116, 891-897.
38. Le Gal, F.A., Avril, M.F., Bosq, J., Lefebvre, P., Deschemin, J.C., Andrieu, M., Dore, M.X., and Guillet, J.G. (2001). Direct evidence to support the role of antigen-specific CD8(+) T cells in melanoma-associated vitiligo. J. Invest. Dermatol. 117, 1464-1470.
39. Le Poole, I.C., Mutis, T., van den Wijngaard, R.M., Westerhof, W., Ottenhoff, T., de Vries, R.R., and Das, P.K. (1993). A novel, antigen-presenting function of melanocytes and its possible relationship to hypopigmentary disorders. J. Immunol. 151, 7284-7292.
40. Le Poole, I.C., van den Wijngaard, R.M., Westerhof, W., and Das, P.K. (1996). Presence of T cells and macrophages in inflammatory vitiligo skin parallels melanocyte disappearance. Am. J. Pathol. 148, 1219-1228.
41. Le Poole, I.C., Wankowicz-Kalinska, A., van den Wijngaard, R.M., Nickoloff, B.J., and Das, P.K. (2004). Autoimmune aspects of depigmentation in vitiligo. J. Invest. Dermatol. Symp. Proc. 9, 68-72.
42. Lee, K.H., Wang, E., Nielsen, M.B., Wunderlich, J., Migueles, S., Connors, M., Steinberg, S.M., Rosenberg, S.A., and Marincola, P.M. (1999a). Increased vaccine-specific T cell frequency after peptide-based vaccination correlates with increased susceptibility to in vitro stimulation but does not lead to tumor regression. J. Immunol. 163, 6292-6300.
43. Lee, P.P., Yee, C., Savage, P.A. et al. (1999b). Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients. Nat. Med. 5, 677-685.
44. + T cells. Cancer Res. 64, 1496-1501.
45. Li, K., Adibzadeh, M., Halder, T., Kaibacher, H., Heinzel, S., Muller, C., Zeuthen, J., and Pawelec, G. (1998). Tumour-specific MHC-class-II-restricted responses after in vitro sensitization to synthetic peptides corresponding to gp100 and Annexin II eluted from melanoma cells. Cancer Immunol. Immunother. 47, 32-38.
46. Loftus, D.J., Castelli, C., Clay, T.M., Squarcina, P., Marincola, F.M., Nishimura, M.I., Parmiani, G., Appella, E., and Rivoltini, L. (1996). Identification of epitope mimics recognized by CTL reactive to the melanoma/melanocyte-derived peptide MART-1 (27-35). J. Exp. Med. 184, 647-657.
47. Maeurer, M.J., Gollin, S.M., Martin, D., Swaney, W., Bryant, J., Castelli, C., Robbins, P., Parmiani, G., Storkus, W.J., and Lotze, M.T. (1996). Tumor escape from immune recognition: lethal recurrent melanoma in a patient associated with downregulation of the peptide transporter protein TAP-1 and loss of expression of the immunodominant MART-1/Melan-A antigen. J. Clin. Invest. 98, 1633-1641.
48. Mandelcorn-Monson, R.L., Shear, N.H., Yau, E., Sambhara, S., Barber, B.H., Spaner, D., and DeBenedette, M.A. (2003). Cytotoxic T lymphocyte reactivity to gp100, MelanA/MART-1, and tyrosinase, in HLA-A2-positive vitiligo patients. J. Invest. Dermatol. 121, 550-556.
49. Mantovani, S., Palermo, B., Garbelli, S., Campanelli, R., Robustelli Delia Cuna, G., Gennari, R., Benvenuto, F., Lantelme, E., and Giachino, C. (2002). Dominant TCR-alpha requirements for a self antigen recognition in humans. J. Immunol. 169, 6253-6260.
50. + T cells in one vitiligo patient. J. Invest. Dermatol. 121, 308-314.
51. Marincola, P.M., Wang, E., Herlyn, M., Seliger, B., and Ferrone, S. (2003). Tumors as elusive targets of T-cell-based active immunotherapy. Trends Immunol. 24, 335-342 (review).
52. McHeyzer-Williams, M.G., and Davis, M.M. (1995). Antigen-specific development of primary and memory T cells in vivo. Science 268, 106-111.
53. Meije, C.B., Mooi, W.J., Le Poole, I.C., Van Muijen, G.N., and Das, P.K. (2000). Micro-anatomy related antigen expression in melanocytic lesions. J. Pathol. 190, 572-578.
54. Michaelsson, G. (1968). Vitiligo with raised borders. Report of two cases. Acta Derm. Venereol. 48, 158-161.
55. + T cells at tumor site in spite of antitumor immunity to self-antigens in human metastatic melanoma. Cancer Res. 63, 2535-2545.
56. Njoo, M.D., and Westerhof, W. (2001). Vitiligo. Pathogenesis and treatment. Am. J. Clin. Dermatol. 2, 167-181 (review).
57. Nordlund, J.J., Kirkwood, J.M., Forget, B.M., Milton, G., Albert, D.M., and Lerner, A.B. (1983). Vitiligo in patients with metastatic melanoma: a good prognostic sign. J. Am. Acad. Dermatol. 9, 689-696.
58. Ogg, G.S. (2000). Detection of antigen-specific cytotoxic T lymphocytes: significance for investigative dermatology. Clin. Exp. Dermatol. 25, 312-316 (review).
59. Ogg, G.S., Dunbar, R., Romero, P., Chen, J.L., and Cerundolo, V. (1998). High frequency of skin-homing melanocyte-specific cytotoxic T lymphocytes in autoimmune vitiligo. J. Exp. Med. 188, 1203-1208.
60. Old, L.J., and Chen, Y.T. (1998). New paths in human cancer serology. J. Exp. Med. 187, 1163-1167.
61. Ongenae, K., van Geel, N., and Naeyaert, J-M. (2003). Evidence for an autoimmune pathogenesis of vitiligo. Pigment Cell Res. 16, 90-100.
62. Palermo, B., Campanelli, R., Garbelli, S. et al. (2001 a). Specific cytotoxic T lymphocyte responses against Melan-A/MART1, tyrosinase and gp100 in vitiligo by the use of major histocompatibility complex/peptide tetramers: the role of cellular immunity in the etiopathogenesis of vitiligo. J. Invest. Dermatol. 117, 326-332.
63. Palermo, B., Campanelli, R., Mantovani, S. et al. (2001 b). Diverse expansion potential and heterogeneous avidity in tumor-associated antigen-specific T lymphocytes from primary melanoma patients. Eur. J. Immunol. 31, 412-420.
64. Palmowski, M., Salio, M., Dunbar, R.P., and Cerundolo, V. (2002). The use of HLA class I tetramers to design a vaccination strategy for melanoma patients. Immunol. Rev. 188, 155-163 (review).
65. Panelli, M.C., Riker, A., Kammula, U., Wang, E., Lee, K.H., Rosenberg, S.A., and Marincola, F.M. (2000). Expansion of tumor-T cell pairs from fine needle aspirates of melanoma metastases. J. Immunol. 164, 495-504.
66. Parmiani, G. (2001). Melanoma antigens and their recognition by T cells. Keio J. Med. 50, 86-90 (review).
67. Picker, L.J., Michie, S.A., Rott, L.S., and Butcher, E.C. (1990). A unique phenotype of skin-associated lymphocytes in humans. Preferential expression of the HECA-452 epitope by benign and malignant T cells at cutaneous sites. Am. J. Pathol. 136, 1053-1068.
68. Pittet, M.J., Valmori, D., Dunbar, P.R., Speiser, D.E., Lienard, D., Lejeune, F., Fleischhauer, K., Cerundolo, V., Cerottini, J.C., and Romero, P. (1999). High frequencies of naive Melan-A/MART-1-specific CD8(+) T cells in a large proportion of human histocompatibility leukocyte antigen (HLA)-A2 individuals. J. Exp. Med. 190, 705-715.
69. + T cells after vaccination with antigenic peptide. Clin. Cancer Res. 7, 796s-803s.
70. Ramirez-Montagut, T., Turk, M.J., Wolchok, J.D., Guevara-Patino, J.A., and Houghton, A.N. (2003). Immunity to melanoma: unraveling the relation of tumor immunity and autoimmunity. Oncogene 22, 3180-3187.
71. Rees, W., Bender, J., Teague, T.K., Kedl, R.M., Crawford, F., Marrack, P., and Kappler, J. (1999). An inverse relationship between T cell receptor affinity and antigen dose during CD4(+) T cell responses in vivo and in vitro. Proc. Natl. Acad. Sci. U. S. A. 96, 9781-9786.
72. Reinherz, E.L., Tan, K., Tang, L. et al. (1999). The crystal structure of a T cell receptor in complex with peptide and MHC class II. Science 286, 1913-1921.
73. Rivoltini, L., Kawakami, Y., Sakaguchi, K. et al. (1995). Induction of tumor-reactive CTL from peripheral blood and tumor-infiltrating lymphocytes of melanoma patients by in vitro stimulation with an immunodominant peptide of the human melanoma antigen MART-1. J. Immunol. 154, 2257-2265.
74. + CTL clones resist Fas ligand-induced apoptosis and use Fas/Fas ligand-independent mechanisms for tumor killing. J. Immunol. 161, 1220-1230.
75. Rivoltini, L., Carrabba, M., Huber, V. et al. (2002). Immunity to cancer: attack and escape in T lymphocyte-tumor cell interaction, Immunol. Rev. 188, 97-113 (review).
76. Robbins, P.F., and Kawakami, Y. (1996). Human tumor antigens recognized by T cells. Curr. Opin. Immunol. 8, 628-636 (review).
77. Romero, P., Dunbar, P.R., Valmori, D., Pittet, M., Ogg, G.S., Rimoldi, D., Chen, J.L., Lienard, D., Cerottini, J.C., and Cerundolo, V. (1998). Ex vivo staining of metastatic lymph nodes by class I major histocompatibility complex tetramers reveals high numbers of antigen-experienced tumor-specific cytolytic T lymphocytes. J. Exp. Med. 188, 1641-1650.
78. Romero, P., Valmori, D., Pittet, M.J. et al. (2002). Antigenicity and immunogenicity of Melan-A/MART-1 derived peptides as targets for tumor reactive CTL in human melanoma. Immunol. Rev. 188, 81-96 (review).
79. Rosenberg, S.A. (1997). Cancer vaccines based on the identification of genes encoding cancer regression antigens. Immunol. Today 18, 175-182 (review).
80. Rosenberg, S.A., Yannelli, J.R., Yang, J.C., Topalian, S.L., Schwartzentruber, D.J., Weber, J.S., Parkinson, D.R., Seipp, C.A., Einhorn, J.H., and White, D.E. (1994). Treatment of patients with metastatic melanoma with autologous tumor-infiltrating lymphocytes and interleukin 2. J. Natl. Cancer Inst. 86, 1159-1166.
81. Savage, P.A., Boniface, J.J., and Davis, M.M. (1999). A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity 10, 485-492.
82. Schallreuter, K.U., Levenig, C., Kuhnl, P., Loliger, C., Hohl-Tehari, M., and Berger, J. (1993). Histocompatibility antigens in vitiligo: Hamburg study on 102 patients from northern Germany. Dermatology 187, 186-192.
83. Scheibenbogen, C., Schmittel, A., Keilholz, U., Allgauer, T., Hofmann, U., Max, R., Thiel, E., and Schadendorf, D. (2000). Phase 2 trial of vaccination with tyrosinase peptides and granulocyte-macrophage colony-stimulating factor in patients with metastatic melanoma. J. Immunother. 23, 275-281.
84. Sensi, M., Salvi, S., Castelli, C., Maccalli, C., Mazzocchi, A., Mortarini, R., Nicolini, G., Herlyn, M., Parmiani, G., and Anichini, A. (1993). T cell receptor (TCR) structure of autologous melanoma-reactive cytotoxic T lymphocyte (CTL) clones: tumor-infiltrating lymphocytes overexpress in vivo the TCR beta chain sequence used by an HLA-A2-restricted and melanocyte-lineage- specific CTL clone. J. Exp. Med. 178, 1231-1246.
85. Skipper, J.C., Hendrickson, R.C., Gulden, P.H. et al. (1996). An HLA-A2-restricted tyrosinase antigen on melanoma cells results from posttranslational modification and suggests a novel pathway for processing of membrane proteins. J. Exp. Med. 183, 527-534.
86. + and CD4+ T cells. Forum (Genova). 10, 256-270 (review).
87. Thomson, T.M., Real, F.X., Murakami, S., Cordon-Cardo, C., Old, L.J., Houghton, A.N. (1988). Differentiation antigens of melanocytes and melanoma: analysis of melanosome and cell surface markers of human pigmented cells with monoclonal antibodies. J. Invest. Dermatol. 90, 459-466.
88. Thurner, B., Haendle, I., Roder, C. et al. (1999). Vaccination with mage-3A1 peptide-pulsed mature, monocyte-derived dendritic cells expands specific cytotoxic T cells and induces regression of some metastases in advanced stage IV melanoma. J. Exp. Med. 190, 1669-1678.
89. Valmori, D., Fonteneau, J.F., Lizana, C.M., Gervois, N., Lienard, D., Rimoldi, D., Jongeneel, V., Jotereau, F., Cerottini, J.C., and Romero, P. (1998). Enhanced generation of specific tumor-reactive CTL in vitro by selected Melan-A/MART-1 immunodominant peptide analogues. J. Immunol. 160, 1750-1758.
90. + T cells in melanoma patients. J. Immunol. 165, 533-538.
91. Van den Eynde, B.J., and van der Bruggen, P. (1997). T cell defined tumor antigens. Curr. Opin. Immunol. 9, 684-693 (review).
92. Vijayasaradhi, S., Bouchard, B., Houghton, A.N. (1990). The melanoma antigen gp75 is the human homologue of the mouse b (brown) locus gene product. J. Exp. Med. 171, 1375-1380.
93. Wankowicz-Kalinska, A., Le Poole, C., van den Wijngaard, R., Storkus, W.J., and Das, P.K. (2003a). Melanocyte-specific immune response in melanoma and vitiligo: two faces of the same coin? Pigment Cell Res. 16, 254-260 (review).
94. + T cells to Type-1-like is associated with melanocyte loss in human vitiligo. Lab. Invest. 83, 683-695.
95. van den Wijngaard, R., Wankowicz-Kalinska, A., Le Poole, C., Tigges, B., Westerhof, W., and Das, P. (2000). Local immune response in skin of generalized vitiligo patients. Destruction of melanocytes is associated with the prominent presence of CLA+ T cells at the perilesional site. Lab. Invest. 80, 1299-1309.
96. van den Wijngaard, R., Wankowicz-Kalinska, A., Pals, S., Weening, J., and Das, P. (2001). Autoimmune melanocyte destruction in vitiligo. Lab. Invest. 81, 1061-1067.
97. Yee, C., Thompson, J.A., Roche, P., Byrd, D.R., Lee, P.P., Piepkorn, M., Kenyon, K., Davis, M.M., Riddell, S.R., and Greenberg, P.D. (2000). Melanocyte destruction after antigen-specific immunotherapy of melanoma: direct evidence of t cell-mediated vitiligo. J. Exp. Med. 192, 1637-1644.
98. Yokosuka, T., Takase, K., Suzuki, M., Nakagawa, Y., Taki, S., Takahashi, H., Fujisawa, T., Arase, H., and Saito, T. (2002). Predominant role of T cell receptor (TCR)-alpha chain in forming preimmune TCR repertoire revealed by clonal TCR reconstitution system. J. Exp. Med. 195, 991-1001.
99. Zippelius, A., Pittet, M.J., Batard, P. et al. (2002). Thymic selection generates a large T cell pool recognizing a self-peptide in humans. J. Exp. Med. 195, 485-494.