The selection of tumor variants with altered expression of classical and nonclassical MHC class I molecules: Implications for tumor immune escape

Cancer Immunology, Immunotherapy

Volumn 53, Issue 10, 2004, Pages 904-910

  Algarra, Ignacio ^a   García Lora, Angel ^b   Cabrera, Teresa ^b   Ruiz Cabello, Francisco ^b   Garrido, Federico ^b  

^a UNIVERSITY OF JAÉN   (Spain)

^b HOSPITAL UNIVERSITARIO VIRGEN DE LAS NIEVES   (Spain)

Author keywords

Immune escape; MHC class I molecules; Tumor variants

Indexed keywords

HLA ANTIGEN CLASS 1; HLA B ANTIGEN; HLA C ANTIGEN; HLA E ANTIGEN; HLA G ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; BREAST CANCER; CANCER IMMUNOLOGY; CELL DESTRUCTION; CELLULAR IMMUNITY; CONFERENCE PAPER; CYTOLYSIS; EFFECTOR CELL; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENCE; INTESTINE CANCER; LUNG ADENOCARCINOMA; LYMPHOMA; MAJOR HISTOCOMPATIBILITY COMPLEX; METASTASIS; NATURAL KILLER CELL; NONHUMAN; NUDE MOUSE; PHENOTYPE; PRIORITY JOURNAL; SARCOMA; SKIN TUMOR; T LYMPHOCYTE; TUMOR CELL; TUMOR ESCAPE; UTERUS CANCER;

ANIMALS; ANTIGENIC VARIATION; ANTIGENS, NEOPLASM; CLONE CELLS; GENES, MHC CLASS I; H-2 ANTIGENS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; IMMUNOLOGIC SURVEILLANCE; MICE; MICE, KNOCKOUT; MICE, NUDE; MODELS, IMMUNOLOGICAL; NEOPLASMS; SELECTION (GENETICS); T-LYMPHOCYTES, CYTOTOXIC; TUMOR ESCAPE;

EID: 4744373672     PISSN: 03407004     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00262-004-0517-9     Document Type: Conference Paper

References (65)

1. Ahmed I, Hamacher KL (2002) Angiosarcoma in a chronically immunosuppressed renal transplant recipient: report of a case and review of the literature. Am J Dermatopathol 24:330
2. Algarra I, Gaforio JJ, Garrido A, Mialdea MJ, Pérez M, Garrido F (1991) Heterogeneity of MHC-class I antigens in clones of methylcholanthrene induced tumors: implications for local growth and metastasis. Int J Cancer 6:73
3. Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, Spies T (1999) Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285:727
4. + T cells are crucial for the ability of congenic normal mice to reject highly immunogenic sarcomas induced in nude mice with 3-methylcholanthrene. Clin Exp Immunol 121:1365
5. Boon T, Cerottini JC, Van den Eynde B, van der Bruggen P, Van Pel A (1994) Tumor antigens recognized by T lymphocytes. Annu Rev Immunol 12:337
6. Botti C, Seregni E, Ferrari L, Martinetti A, Bombardieri E (1998) Immunosuppressive factors: role in cancer development and progression. Int J Biol Markers 13:51
7. Braud V, Jones EY, McMichael A (1997) The human major histocompatibility complex class Ib molecule HLA-E binds signal sequence-derived peptides with primary anchor residues at positions 2 and 9. Eur J Immunol 27:1164
8. Bukur J, Seliger B (2003) The role of HLA G for protection of human renal cell-carcinoma cells from immune-mediated lysis: implications for immunotherapies. Sem Cancer Biol 13:353
9. Burnet FM (1970) The concept of immunological surveillance. Prog Exp Tumor Res 13:1
10. Cadranel J, Naccache J, Wislez M, Mayaud C (1999) Pulmonary malignancies in the immunocompromised patient. Respiration 66:289
11. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD (2002) Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 3:991
12. Ehrlich P (1909) Ueber den jetzigen Stand der Karzinomforschung (About the current state of the art of cancer research). NedTijdschr Geneesk 5:273
13. Engel AM, Svane IM, Rigaard J, Werdelin O (1997) MCA sarcomas induced in scid mice are more immunogenic than MCA sarcomas induced in congenic, immunocompetent mice. Scand J Immunol 45:463
14. Frumento G, Franchello S, Palmisano GL, Nicotra MR, Giacomini P, Loke YW, Geraghty DE, Maio M, Manzo C, Natali PG, Ferrara GB (2000) Melanomas and melanoma cell lines do not express HLA-G, and the expression cannot be induced by gamma-IFN treatment. Tissue Antigens 56:30
15. Gao Y, Yang W, Pan M, Scully E, Girardi M, Augenlicht LH, Craft J, Yin Z (2003) Gamma delta T cells provide an early source of interferon gamma in tumor immunity. J Exp Med 198:433
16. Garcia-Lora A, Algarra I, Gaforio JJ, Ruiz-Cabello F, Garrido F (2001) Immunoselection by T lymphocytes generates repeated MHC class I deficient metastatic tumor variants. Int J Cancer 91:109
17. Garcia-Lora A, Martinez M, Algarra I, Gaforio JJ, Garrido F (2003) MHC class I-deficient metastatic tumor variants immunoselected by T lymphocytes originate from the coordinated downregulation of APM components. Int J Cancer 106:521
18. Garcia-Lora A, Algarra I, Garrido F (2003) MHC class I antigens, immune surveillance and tumor immune escape. J Cell Physiol 195:346
19. Garrido A, Pérez M, Delgado C, Garrido ML, Rojano J, Algarra I, Garrido F (1986) Influence of class I H-2 gene expression on local tumor growth. Exp Clin Immunogenet 13:98
20. Garrido F, Algarra I (2001) MHC antigens and tumor escape from immune surveillance. Adv Cancer Res 83:117
21. Garrido F, Cabrera T, Concha A, Glew S, Ruiz-Cabello F, Stern PL (1993) Natural history of HLA expression during tumour development. Immunol Today 14:491
22. Garrido F, Ruiz-Cabello F, Cabrera T, Perez-Villar JJ, Lopez-Botet M, Duggan-Keen M, Stern P (1997) Implications for immune surveillance of altered HLA class I phenotypes in human tumors. Immunol Today 18:89
23. Girardi M, Oppenheim DE, Steele CR, Lewis JM, Glusac E, Filler R, Hobby P, Sutton B, Tigelaar RE, Hayday AC (2001) Regulation of cutaneous malignancy by gammadelta T cells. Science 294:605
24. Girardi M, Glusac E, Filler RB, Roberts SJ, Propperova I, Lewis J, Tigelaar RE, Hayday AC (2003) The distinct contributions of murine T cell receptor (TCR)gammadelta+ and TCRalphabeta+ T cells to different stages of chemically induced skin cancer. J Exp Med 198:747
25. Groh V, Steinle A, Bauer S, Spies T (1998) Recognition of stress-induced MHC molecules by intestinal epithelial gammadelta T cells. Science 279:1737
26. Groh V, Rhinehart R, Randolph-Habecker J, Topp MS, Riddell SR, Spies T (2001) Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat Immunol 2:255
27. Haliotis T, Ball JK, Dexter D, Roder JC (1985) Spontaneous and induced primary oncogenesis in natural killer (NK)-cell deficient beige mutant mice. Int J Cancer 35:505
28. Hayashi T, Faustman DL(2002) Development of spontaneous uterine tumors in low molecular mass polypeptide-2 knockout mice. Cancer Res 62:24
29. Jager E, Ringhoffer M, Karbach J, Arand M, Oesch F, Knuth (1996) A Inverse relationship of melanocyte differentiation antigen expression in melanoma tissues and CD8+ cytotoxic-T-cell responses: evidence for immunoselection of antigen-loss variants in vivo. Int J Cancer 66:470
30. Johnsen A, Templeton DJ, Sy MS, Harding CV (1999) Deficiency of transporter for antigen presentation (TAP) in tumor cells allows evasion of immune surveillance and increases tumorigenesis. J Immunol 163:4224
31. Kagi DB, Ledermann B, Burki K, Seiler P, Odermatt B, Olsen KJ, Podack ER, Zinkernagel RM, Hengartner H (1994) Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369:31
32. Kaplan DH, Shankaran V, Dighe AS, Stockert E, Aguet M, Old LJ, Schreiber RD (1998) Demonstration of an interferon gamma dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci U S A 95:7556
33. Le Bouteiller P (1997) HLA-G: on the track of immunological functions. Eur J Immunogenet 24:397
34. Lehmann F, Marchand M, Hainaut P, Pouillart P, Sastre X, Ikeda H, Boon T, Coulie PG (1995) Differences in the antigens recognized by cytolytic T cells on two successive metastases of a melanoma patient are consistent with immune selection. Eur J Immunol 25:340
35. Llano M, Lee N, Navarro F, Garcia P, Albar JP, Geraghty DE, Lopez-Botet M (1998) HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur J Immunol 28:2854
36. Marin R, Ruiz-Cabello F, Pedrinaci S, Mendez R, Jimenez P, Geraghty DE, Garrido F (2003) Analysis of HLA-E expression in human tumors. Immunogenetics 54:767
37. McClain KL (1997) Immunodeficiency states and related malignancies. Cancer Treat Rev 92:39
38. Mendez R, Serrano A, Jager E, Maleno I, Ruiz Cabello F, Knuth A, Garrido F (2001) Analysis of HLA class I expression in different metastases from two melanoma patients undergoing peptide immunotherapy. Tissue Antigens 57:508
39. Meyer T, Arndt R, Nindl I, Ulrich C, Christophers E, Stockfleth E (2003) Association of human papillomavirus infections with cutaneous tumors in immunosuppressed patients. Transpl Int 16:146
40. Moretta A, Bottino C, Vitale M, Pende D, Biassoni R, Mingari MC, Moretta L (1996) Receptors for HLA class-I molecules in human natural killer cells. Annu Rev Immunol 14:619
41. Nemes B, Zalatnai A, Podder H, Jaray J, Sotonyi P Jr, Schaff Z, Foldes K, Perner F (2000) Papillary microcarcinoma of the thyroid gland in renal transplant patients. Pathol Oncol Res 6:72
42. Otley CC, Pittelkow MR (2000) Skin cancer in liver transplant recipients. Liver Transpl 6:253
43. Pangault C, Amiot L, Caulet-Maugendre S, Brasseur F, Burtin F, Guilloux V, Drenou B, Fauchet R, Onno M (1999) HLA-G protein expression is not induced during malignant transformation. Tissue Antigens. 53:335
44. Pardoll DM (2003) Does the immune system see tumors as foreign or self? Annual Rev Immunol 21:807
45. Paul P, Rouas-Freiss N, Khalil-Daher I, Moreau P, Riteau B, Le Gal FA, Avril MF, Dausset J, Guillet JG, Carosella ED (1998) HLA-G expression in melanoma: a way for tumor cells to escape from immunosurveillance. Proc Natl Acad Sci U S A 95:4510
46. Pérez M, Algarra I, Ljunggren HG, Caballero A, Mialdea MJ, Gaforio JJ, Garrido F (1990) A weakly tumorigenic phenotype with high MHC class I expression is associated with high metastatic potential after surgical removal of the primary murine fibrosarcoma. Int J Cancer 46:258
47. Prehn RT, Main JM (1957) Immunity to methylcholanthrene induced sarcomas. J Natl Cancer Inst 18:769
48. Real LM, Cabrera T, Collado A, Jimenez P, Garcia A, Ruiz-Cabello F, Garrido F (1999) Expression of HLA G in human tumors is not a frequent event. Int J Cancer 81:512
49. Renkvist N, Castelli C, Robbins PF, Parmiani G (2001) A listing of human tumor antigens recognized by T cells. Cancer Immunol Immunother 50:3
50. Restifo NP, Antony PA, Finkelstein SE, Leitner WW, Surman D, Theoret MR, Touloukian CE (2002) Assumptions of the tumor 'escape' hypothesis. Sem Cancer Biol 12:81
51. Seliger B, Cabrera T, Garrido F, Ferrone S (2002) HLA class I antigen abnormalities and immune escape by malignant cells. Sem Cancer Biol 12:3
52. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, Scheriber RD (2001) IFNγ and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 26:1107
53. Smyth MJ, Thia KY, Street SE, MacGregor D, Godfrey DI, Trapani JA (2000) Perforin-mediated cytotoxicity is critical for surveillance of spontaneous lymphoma. J Exp Med 192:755
54. Smyth MJ, Crowe NY, Godfrey DI (2001) NK cells and NKT cells collaborate in host protection from methylcholanthrene-induced fibrosarcoma. Int Immunol 13:459
55. Stern PL (1996) Immunity to human papillomavirus associated cervical neoplasia. Adv Cancer Res 69:175
56. Street SE, Cretney E, Smyth MJ (2001) Perforin and interferon-gamma activities independently control tumor initiation, growth, and metastasis. Blood 97:192
57. Stutman O (1979) Chemical carcinogenesis in nude mice: comparison between nude mice from homozygous matings and heterozygous matings and effect of age and carcinogen dose. J Natl Cancer Inst 62:353
58. Svane IM, Engel AM, Nielsen MB, Ljunggren HG, Rygaard J, Werdelin O (1996) Chemically induced sarcomas from nude mice are more immunogenic than similar sarcomas from congenic normal mice. Eur J Immunol 26:1844
59. Thomas L (1959) Discussion of cellular and humoral aspects of the hypersensitivity states. In: Lawrence HS (ed) Cellular and humoral aspects of the hypersensitive states. Hoeber-Harper, New York, p 529
60. Tomasec P, Braud V, Rickards C, Powell M, McSharry B, Gadola S, Cerundolo V, Borysiewicz L, McMichael A, Wilkinson G (2000) Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287:1031
61. Townsend AR, Rothbard J, Gotch FM, Bahadur G, Wraith D, McMichael AJ (1986) The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell 28:959
62. van den Broek MF, Kagi D, Zinkernagel RM, Hengartner H (1995) Perforin dependence of natural killer cell-mediated tumor control in vivo. Eur J Immunol 25:3514
63. Van den Eynde BJ, Van der Bruggen P (1997) T cell defined tumor antigens. Curr Opin Immunol 9:684
64. Winter P, Schoeneich G, Miersch WD, Klehr HU (1997) Tumour induction as a consequence of immunosuppression after renal transplantation. Int Urol Nephrol 29:701
65. Yokota J (2000) Tumour progression and metastasis. Carcinogenesis 21:497