Telomerase reverse transcriptase as target for anti-tumor T cell responses in humans

Springer Seminars in Immunopathology

Volumn 27, Issue 1, 2005, Pages 87-104

  Zanetti, Maurizio ^a   Hernandez, Xavier ^b   Langlade Demoyen, Pierre ^c  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^c INSTITUT PASTEUR   (France)

Author keywords

Anti tumor immune response; CD8 T cell immunity; Self tolerance; Telomerase reverse transcriptase

Indexed keywords

HLA A2 ANTIGEN; RIBONUCLEOPROTEIN; TELOMERASE REVERSE TRANSCRIPTASE; TUMOR ANTIGEN; TUMOR VACCINE;

ANTIGENICITY; CANCER CELL; CANCER CONTROL; CELL IMMORTALIZATION; CELLULAR IMMUNITY; DRUG TARGETING; GENE OVEREXPRESSION; HISTOLOGY; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; T LYMPHOCYTE; TUMOR IMMUNITY;

ANTIGENS, NEOPLASM; AUTOIMMUNITY; CD8-POSITIVE T-LYMPHOCYTES; CLINICAL TRIALS; COMBINATORIAL CHEMISTRY TECHNIQUES; CYTOTOXICITY, IMMUNOLOGIC; DNA-BINDING PROTEINS; HUMANS; NEOPLASMS; SELF TOLERANCE; T-LYMPHOCYTES, CYTOTOXIC; TELOMERASE;

EID: 21344455767     PISSN: 03444325     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00281-004-0197-8     Document Type: Review

References (86)

1. Silverstein AM (1989) Transplantation and immunogenetics. Academic Press, San Diego
2. Burnet FM (1970) The concept of immunological surveillance. Prog Exp Tumor Res 13:1
3. Burnet FM (1971) Immunological surveillance in neoplasia. Transplant Rev 7:3
4. Offringa R, Burg SH van der, Ossendorp F, et al (2000) Design and evaluation of antigen-specific vaccination strategies against cancer. Curr Opin Immunol 12:576
5. Smyth MJ, Thia KY, Street SE, et al (2000) Perforin-mediated cytotoxicity is critical for surveillance of spontaneous lymphoma. J Exp Med 192:755
6. Yotnda P, Firat H, Garcia-Pons F, et al (1998) Cytotoxic T cell response against the chimeric p210 BCR-ABL protein in patients with chronic myelogenous leukemia. J Clin Invest 101:2290
7. Yotnda P, Garcia F, Peuchmaur M, et al (1998) Cytotoxic T cell response against the chimeric ETV6-AML1 protein in childhood acute lymphoblastic leukemia. J Clin Invest 102:455
8. Molldrem JJ, Lee PP, Wang C, et al (2000) Evidence that specific T lymphocytes may participate in the elimination of chronic myelogenous leukemia. Nat Med 6:1018
9. Boon T, Coulie PG, Van den Eynde B (1997) Tumor antigens recognized by T cells. Immunol Today 18:267
10. Springer G (1984) T and Tn, general carcinoma autoantigens. Science 224:1198
11. Broccoli D, Young JW, Lange T de (1995) Telomerase activity in normal and malignant hematopoietic cells. Proc Natl Acad Sci USA 92:9082
12. Schmidt SM, Schag K, Muller MR, et al (2003) Survivin is a shared tumor-associated antigen expressed in a broad variety of malignancies and recognized by specific cytotoxic T cells. Blood 102:571
13. Kappler JW, Roehm N, Marrack P (1987) T cell tolerance by clonal elimination in the thymus. Cell 49:273
14. Cobbold SP, Adams E, Marshall SE, et al (1996) Mechanisms of peripheral tolerance and suppression induced by monoclonal antibodies to CD4 and CD8. Immunol Rev 149:5
15. Nanda NK, Sercarz EE (1995) Induction of anti-self-immunity to cure cancer. Cell 82:13
16. Theobald M, Biggs J, Hernandez J, et al (1997) Tolerance to p53 by A2.1-restricted cytotoxic T lymphocytes. J Exp Med 185:833
17. Hernandez J, Lee PP, Davis MM, et al (2000) The use of HLA A2.1/p53 peptide tetramers to visualize the impact of self tolerance on the TCR repertoire. J Immunol 164:596
18. Morgan DJ, Kreuwel HT, Fleck S, et al (1998) Activation of low avidity CTL specific for a self epitope results in tumor rejection but not autoimmunity. J Immunol 160:643
19. Sercarz EE, Lehmann PV, Ametani A, et al (1993) Dominance and crypticity of T cell antigenic determinants. Annu Rev Immunol 11:729
20. Yewdell JW, Bennink JR (1999) Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol 17:51
21. Liu GY, Fairchild PJ, Smith RM, et al (1995) Low avidity recognition of self-antigen by T cells permits escape from central tolerance. Immunity 3:407
22. Greider CW, Blackburn EH (1987) The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell 51:887
23. Blackburn EH (1992) Telomerases. Annu Rev Biochem 61:113
24. Blackburn EH (1991) Structure and function of telomeres. Nature 350:569
25. Greider CW (1994) Mammalian telomere dynamics: healing, fragmentation shortening and stabilization. Curr Opin Gen Dev 4:203
26. Counter CM, Avilion AA, LeFeuvre CE, et al (1992) Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J 11:1921
27. Lange T de (1994) Activation of telomerase in a human tumor. Proc Natl Acad Sci USA 91:2882
28. Stewart SA, Ben-Porath I, Carey VJ, et al (2003) Erosion of the telomeric single-strand overhang at replicative senescence. Nat Genet 33:492
29. Kim NW, Piatyszek MA, Prowse KR, et al (1994) Specific association of human telomerase activity with immortal cells and cancer. Science 266:2011
30. Meyerson M, Counter CM, Eaton EN, et al (1997) hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell 90:785
31. Bodnar AG, Ouellette M, Frolkis M, et al (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279:349
32. Lee HW, Blasco MA, Gottlieb GJ, et al (1998) Essential role of mouse telomerase in highly proliferative organs. Nature 392:569
33. Rudolph KL, Chang S, Lee HW, et al (1999) Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell 96:701
34. Greenberg RA, Chin L, Femino A, et al (1999) Short dysfunctional telomeres impair tumorigenesis in the INK4a(delta2/3) cancer-prone mouse. Cell 97:515
35. Morales CP, Holt SE, Ouellette M, et al (1999) Absence of cancer-associated changes in human fibroblasts immortalized with telomerase. Nat Genet 21:115
36. Hahn WC, Counter CM, Lundberg AS, et al (1999) Creation of human tumour cells with defined genetic elements. Nature 400:464
37. Shay JW, Bacchetti S (1997) A survey of telomerase activity in human cancer. Eur J Cancer 33:787
38. Kim NW (1997) Clinical implications of telomerase in cancer. Eur J Cancer 33:781
39. Nakamura TM, Morin GB, Chapman KB, et al (1997) Telomerase catalytic subunit homologs from fission yeast and human. Science 277:955
40. Sette A, Sidney J, Guercio MF del, et al (1994) Peptide binding to the most frequent HLA-A class I alleles measured by quantitative molecular binding assays. Mol Immunol 31:813
41. Minev B, Hipp J, Firat H, et al (2000) Cytotoxic T cell immunity against telomerase reverse transcriptase in humans. Proc Natl Acad Sci USA 97:4796
42. Vonderheide RH, Hahn WC, Schultze JL, et al (1999) The telomerase catalytic subunit is a widely expressed tumor-associated antigen recognized by cytotoxic T lymphocytes. Immunity 10:673
43. Vonderheide RH, Schultze JL, Anderson KS, et al (2001) Equivalent induction of telomerase-specific cytotoxic T lymphocytes from tumor-bearing patients and healthy individuals. Cancer Res 61:8366
44. Ayyoub M, Migliaccio M, Guillaume P, et al (2001) Lack of tumor recognition by hTERT peptide 540-specific CD8(+) T cells from melanoma patients reveals inefficient antigen processing. Eur J Immunol 31:2642
45. Pascolo S, Bervas N, Ure JM, et al (1997) HLA-A2.1-restricted education and cytolytic activity of CD8(+) T lymphocytes from beta2 microglobulin (beta2m) HLA-A2.1 monochain transgenic H-2Db beta2m double knockout mice. J Exp Med 185:2043
46. Lev A, Denkberg G, Cohen CJ, et al (2002) Isolation and characterization of human recombinant antibodies endowed with the antigen-specific, major histocompatibility complex-restricted specificity of T cells directed toward the widely expressed tumor T-cell epitopes of the telomerase catalytic subunit. Cancer Res 62:3184
47. Colella TA, Bullock TN, Russell LB, et al (2000) Self-tolerance to the murine homologue of a tyrosinase-derived melanoma antigen: implications for tumor immunotherapy. J Exp Med 191:1221
48. Oehen SU, Ohashi PS, Burki K, et al (1994) Escape of thymocytes and mature T cells from clonal deletion due to limiting tolerogen expression levels. Cell Immunol 158:342
49. Kurts C, Sutherland RM, Davey G, et al (1999) CD8 T cell ignorance or tolerance to islet antigens depends on antigen dose. Proc Natl Acad Sci USA 96:12703
50. Sette A, Vitiello A, Reherman B, et al (1994) The relationship between class I binding affinity and immunogenicity of potential cytotoxic T cell epitopes. J Immunol 153:5586
51. Ruppert J, Sidney J, Celis E, et al (1993) Prominent role of secondary anchor residues in peptide binding to HLA-A2.1 molecules. Cell 74:929
52. Tourdot S, Scardino A, Saloustrou E, et al (2000) A general strategy to enhance immunogenicity of low-affinity HLA-A2. 1-associated peptides: implication in the identification of cryptic tumor epitopes. Eur J Immunol 30:3411
53. Pinilla C, Martin R, Gran B, et al (1999) Exploring immunological specificity using synthetic peptide combinatorial libraries. Curr Opin Immunol 11:193
54. Hemmer B, Vergelli M, Pinilla C, et al (1998) Probing degeneracy in T-cell recognition using peptide combinatorial libraries. Immunol Today 19:163
55. Hernandez J, Schoeder K, Blondelle SE, et al (2004) Antigenicity and immunogenicity of peptide analogues of a low affinity peptide of the human telomerase reverse transcriptase tumor antigen. Eur J Immunol 34:2331
56. Staveley-O'Carroll K, Sotomayor E, Montgomery J, et al (1998) Induction of antigen-specific T cell anergy: an early event in the course of tumor progression. Proc Natl Acad Sci USA 95:1178
57. + T cells following immunization. Blood 104:1970
58. + T cells: efficacy is limited by migration away from the site and induction of nonresponsiveness. J Immunol 162:2858
59. Young MR, Wright MA, Matthews JP, et al (1996) Suppression of T cell proliferation by tumor-induced granulocyte-macrophage progenitor cells producing transforming growth factor-beta and nitric oxide. J Immunol 156:1916
60. Rosenberg SA (2001) Progress in human tumour immunology and immunotherapy. Nature 411:380
61. Brousset P, al Saati T, Zenou RC, et al (1998) Telomerase activity might persist in the human thymus throughout life. Mol Pathol 51:170
62. Gross DA, Graff-Dubois S, Opolon P, et al (2004) High vaccination efficiency of low-affinity epitopes in antitumor immunotherapy. J Clin Invest 113:425
63. Greider CW (1998) Telomerase activity, cell proliferation, and cancer. Proc Natl Acad Sci USA 95:90
64. Notaro R, Cimmino A, Tabarini D, et al (1997) In vivo telomere dynamics of human hematopoietic stem cells. Proc Natl Acad Sci USA 94:13782
65. Weng NP, Granger L, Hodes RJ (1997) Telomere lengthening and telomerase activation during human B cell differentiation. Proc Natl Acad Sci USA 94:10827
66. Weng NP, Levine BL, June CH, et al (1996) Regulated expression of telomerase activity in human T lymphocyte development and activation. J Exp Med 183:2471
67. Liu K, Hodes RJ, Weng N (2001) Cutting edge: telomerase activation in human T lymphocytes does not require increase in telomerase reverse transcriptase (hTERT) protein but is associated with hTERT phosphorylation and nuclear translocation. J Immunol 166:4826
68. Valenzuela HF, Effros RB (2002) Divergent telomerase and CD28 expression patterns in human CD4 and CD8T cells following repeated encounters with the same antigenic stimulus. Clin Immunol 105:117
69. + T cells. J Exp Med 198:569
70. Dudley ME, Wunderlich JR, Robbins PF, et al (2002) Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298:850
71. Hernandez J, Garcia-Pons F, Lone LC, et al (2002) Identification of a human telomerase reverse transcriptase peptide of low affinity for HLA-A2.1 that induces CTL and mediates lysis of tumor cells. Proc Natl Acad Sci USA 99:12275
72. Reed JR, Vukmanovic-Stejic M, Fletcher JM, et al (2004) Telomere erosion in memory T cells induced by telomerase inhibition at the site of antigenic challenge in vivo. J Exp Med 199:1433
73. Streilein JW (1995) Unraveling immune privilege. Science 270:1158
74. Bellgrau D, Gold D, Selawry H, et al (1995) A role for CD95 ligand in preventing graft rejection. Nature 377:630
75. Ditzian-Kadanoff R (1999) Testicular-associated immune deviation and prevention of adjuvant-induced arthritis by three tolerization methods. Scand J Immunol 50:150
76. Vonderheide RH, Anderson KS, Hahn WC, et al (2001) Characterization of HLA-A3-restricted cytotoxic T lymphocytes reactive against the widely expressed tumor antigen telomerase. Clin Cancer Res 7:3343
77. Arai J, Yasukawa M, Ohminami H, et al (2001) Identification of human telomerase reverse transcriptase-derived peptides that induce HLA-A24-restricted antileukemia cytotoxic T lymphocytes. Blood 97:2903
78. Lee TD (1990) Distribution of HLA antigens in North American Caucasians, North American Blacks and Orientals. In: Lee J (ed) The HLA System. Springer, New York, pp 141-178
79. Fernandez-Vina MA, Falco M, Sun Y, et al (1992) DNA typing for HLA class I alleles: I. Subsets of HLA-A2 and of-A28. Hum Immunol 33:163
80. Krausa P, Brywka M 3rd, Savage D, et al (1995) Genetic polymorphism within HLA-A*02: significant allelic variation revealed in different populations. Tissue Antigens 45:223
81. Parham P, Ohta T (1996) Population biology of antigen presentation by MHC class I molecules. Science 272:67
82. Sette A, Sidney J (1999) Nine major HLA class I supertypes account for the vast preponderance of HLA-A and -B polymorphism. Immunogenetics 50:201
83. + T lymphocytes. Clin Cancer Res 10:828
84. Zanetti M (2003) Protocol #0207: a phase I, escalating dose, open-label evaluation of safety, feasibility, and tolerability of transgenic lymphocyte immunization (TLI) vaccine subjects with histologically proven prostate adenocarcinoma. Hum Gene Ther 14:301
85. Su Z, Dannull J, Heiser A, et al (2003) Immunological and clinical responses in metastatic renal cancer patients vaccinated with tumor RNA-transfected dendritic cells. Cancer Res 63:2127
86. Parkhurst MR, Riley JP, Igarashi T, et al (2004) Immunization of patients with the hTERT:540 peptide induces peptide-reactive T lymphocytes that do not recognize tumors endogenously expressing telomerase. Clin Cancer Res 10:4688