The immune response to melanoma is limited by thymic selection of self-antigens

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Träger, Ulrike ^a,b   Sierro, Sophie ^c   Djordjevic, Gordana ^a,b   Bouzo, Basma ^a,b   Khandwala, Shivani ^a,b   Meloni, Antonella ^d   Mortensen, Monika ^a,b,e   Simon, Anna Katharina ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NIHR OXFORD BIOMEDICAL RESEARCH CENTRE   (United Kingdom)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (Switzerland)

^d UNIVERSITY OF CAGLIARI   (Italy)

^e DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER ANTIBODY; IMMUNOGLOBULIN G; MELANOCYTE PROTEIN PMEL 17; MELANOMA ANTIBODY; TYROSINASE RELATED PROTEIN 2; UNCLASSIFIED DRUG; AUTOANTIGEN; CANCER VACCINE; DOPACHROME ISOMERASE; IMMUNOLOGIC FACTOR; ISOMERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNE POLYENDOCRINOPATHY CANDIDIASIS ECTODERMAL DYSTROPHY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL LEVEL; CELL SPECIFICITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; THYMUS; TUMOR IMMUNITY; ANIMAL; BLOOD; C57BL MOUSE; EPITHELIUM CELL; EXPERIMENTAL MELANOMA; FEMALE; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MOUSE MUTANT; POLYENDOCRINOPATHY; THYMOCYTE; TUMOR CELL LINE;

MUS;

ANIMALS; ANTIBODIES, NEOPLASM; AUTOANTIGENS; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; EPITHELIAL CELLS; FEMALE; GP100 MELANOMA ANTIGEN; HUMANS; IMMUNE TOLERANCE; IMMUNOGLOBULIN G; IMMUNOLOGIC FACTORS; INTRAMOLECULAR OXIDOREDUCTASES; MELANOMA; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; POLYENDOCRINOPATHIES, AUTOIMMUNE; SELF TOLERANCE; THYMOCYTES;

EID: 84859589258     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035005     Document Type: Article

References (37)

1. Miller AJ, Mihm MC Jr, (2006) Melanoma. N Engl J Med 355: 51-65.
2. Castelli C, Rivoltini L, Andreola G, Carrabba M, Renkvist N, et al. (2000) T-cell recognition of melanoma-associated antigens. J Cell Physiol 182: 323-331.
3. Overwijk WW, Restifo NP, (2000) Autoimmunity and the immunotherapy of cancer: targeting the "self" to destroy the "other". Crit Rev Immunol 20: 433-450.
4. Anderson MS, Venanzi ES, Klein L, Chen Z, Berzins SP, et al. (2002) Projection of an immunological self shadow within the thymus by the aire protein. Science 298: 1395-1401.
5. Perheentupa J, (2006) Autoimmune Polyendocrinopathy-Candidiasis-Ectodermal Dystrophy. J Clin Endocrin & Metabolism 91: 2843-2850.
6. Yip L, Su L, Sheng D, Chang P, Atkinson M, et al. (2009) Deaf1 isoforms control the expression of genes encoding peripheral tissue antigens in the pancreatic lymph nodes during type 1 diabetes. Nat Immunol 10: 1026-1033.
7. Mathis D, Benoist C, (2009) Aire. Annu Rev Immunol 27: 287-312.
8. Venanzi ES, Melamed R, Mathis D, Benoist C, (2008) The variable immunological self: genetic variation and nongenetic noise in Aire-regulated transcription. Proc Natl Acad Sci U S A 105: 15860-15865.
9. Jones E, Dahm-Vicker M, Simon AK, Green A, Powrie F, et al. (2002) Depletion of CD25+ regulatory cells results in suppression of melanoma growth and induction of autoreactivity in mice. Cancer Immun 2: 1.
10. Sierro SR, Donda A, Perret R, Guillaume P, Yagita H, et al. (2011) Combination of lentivector immunization and low-dose chemotherapy or PD-1/PD-L1 blocking primes self-reactive T cells and induces anti-tumor immunity. Eur J Immunol 41: 2217-2228.
11. Derbinski J, Schulte A, Kyewski B, Klein L, (2001) Promiscuous gene expression in medullary thymic epithelial cells mirrors the peripheral self. Nat Immunol 2: 1032-1039.
12. Muranski P, Boni A, Antony PA, Cassard L, Irvine KR, et al. (2008) Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood 112: 362-373.
13. Abad JD, Wrzensinski C, Overwijk W, De Witte MA, Jorritsma A, et al. (2008) T-cell receptor gene therapy of established tumors in a murine melanoma model. J Immunother 31: 1-6.
14. Singh V, Ji Q, Feigenbaum L, Leighty RM, Hurwitz AA, (2009) Melanoma progression despite infiltration by in vivo-primed TRP-2-specific T cells. J Immunother 32: 129-139.
15. Jiang W, Anderson MS, Bronson R, Mathis D, Benoist C, (2005) Modifier loci condition autoimmunity provoked by Aire deficiency. J Exp Med 202: 805-815.
16. Gavanescu I, Benoist C, Mathis D, (2008) B cells are required for Aire-deficient mice to develop multi-organ autoinflammation: A therapeutic approach for APECED patients. Proc Natl Acad Sci U S A 105: 13009-13014.
17. Hedstrand H, Ekwall O, Olsson MJ, Landgren E, Kemp EH, et al. (2001) The transcription factors SOX9 and SOX10 are vitiligo autoantigens in autoimmune polyendocrine syndrome type I. J Biol Chem 276: 35390-35395.
18. Hedstrand H, Perheentupa J, Ekwall O, Gustafsson J, Michaelsson G, et al. (1999) Antibodies against hair follicles are associated with alopecia totalis in autoimmune polyendocrine syndrome type I. J Invest Dermatol 113: 1054-1058.
19. Gallimore AM, Simon AK, (2008) Positive and negative influences of regulatory T cells on tumour immunity. Oncogene 27: 5886-5893.
20. Simon AK, Gallimore A, Jones E, Sawitzki B, Cerundolo V, et al. (2002) Fas ligand breaks tolerance to self-antigens and induces tumor immunity mediated by antibodies. Cancer Cell 2: 315-322.
21. Ramsey C, Winqvist O, Puhakka L, Halonen M, Moro A, et al. (2002) Aire deficient mice develop multiple features of APECED phenotype and show altered immune response. Hum Mol Genet 11: 397-409.
22. Schreiber TH, Podack ER, (2009) A critical analysis of the tumour immunosurveillance controversy for 3-MCA-induced sarcomas. Br J Cancer 101: 381-386.
23. Hassler S, Ramsey C, Karlsson MC, Larsson D, Herrmann B, et al. (2006) Aire-deficient mice develop hematopoetic irregularities and marginal zone B-cell lymphoma. Blood 108: 1941-1948.
24. Bockle BC, Wilhelm M, Muller H, Gotsch C, Sepp NT, Oral mucous squamous cell carcinoma-an anticipated consequence of autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED). J Am Acad Dermatol 62: 864-868.
25. Pittet MJ, Zippelius A, Valmori D, Speiser DE, Cerottini JC, et al. (2002) Melan-A/MART-1-specific CD8 T cells: from thymus to tumor. Trends Immunol 23: 325-328.
26. Conteduca G, Ferrera F, Pastorino L, Fenoglio D, Negrini S, et al. The role of AIRE polymorphisms in melanoma. Clin Immunol.
27. Yee C, Thompson JA, Roche P, Byrd DR, Lee PP, et al. (2000) Melanocyte destruction after antigen-specific immunotherapy of melanoma: direct evidence of t cell-mediated vitiligo. J Exp Med 192: 1637-1644.
28. Takase H, Yu CR, Mahdi RM, Douek DC, Dirusso GB, et al. (2005) Thymic expression of peripheral tissue antigens in humans: a remarkable variability among individuals. Int Immunol 17: 1131-1140.
29. Peterson P, Org T, Rebane A, (2008) Transcriptional regulation by AIRE: molecular mechanisms of central tolerance. Nat Rev Immunol 8: 948-957.
30. Niki S, Oshikawa K, Mouri Y, Hirota F, Matsushima A, et al. (2006) Alteration of intra-pancreatic target-organ specificity by abrogation of Aire in NOD mice. J Clin Invest 116: 1292-1301.
31. DeVoss J, Hou Y, Johannes K, Lu W, Liou GI, et al. (2006) Spontaneous autoimmunity prevented by thymic expression of a single self-antigen. J Exp Med 203: 2727-2735.
32. Gavanescu I, Kessler B, Ploegh H, Benoist C, Mathis D, (2007) Loss of Aire-dependent thymic expression of a peripheral tissue antigen renders it a target of autoimmunity. Proc Natl Acad Sci U S A 104: 4583-4587.
33. Derbinski J, Gabler J, Brors B, Tierling S, Jonnakuty S, et al. (2005) Promiscuous gene expression in thymic epithelial cells is regulated at multiple levels. J Exp Med 202: 33-45.
34. Maddison P, Newsom-Davis J, Mills KR, Souhami RL, (1999) Favourable prognosis in Lambert-Eaton myasthenic syndrome and small-cell lung carcinoma. Lancet 353: 117-118.
35. Rosatelli MC, Meloni A, Devoto M, Cao A, Scott HS, et al. (1998) A common mutation in Sardinian autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy patients. Hum Genet 103: 428-434.
36. Salio M, Cella M, Vermi W, Facchetti F, Palmowski M, et al. (2003) Plasmacytoid dendritic cells prime IFN-+-secreting melanoma-specific CD8 lymphocytes and are found in primary melanoma lesions. Eur J Immunol 33: 1052.
37. Quezada SA, Peggs KS, Simpson TR, Shen Y, Littman DR, et al. (2008) Limited tumor infiltration by activated T effector cells restricts the therapeutic activity of regulatory T cell depletion against established melanoma. J Exp Med 205: 2125-2138.