Mechanisms regulating the proliferative potential of human CD8+ T lymphocytes overexpressing telomerase

Journal of Immunology

Volumn 177, Issue 6, 2006, Pages 3657-3668

  Menzel, Olivier ^a   Migliaccio, Marco ^a   Goldstein, Darlene R ^b   Dahoun, Sophie ^c   Delorenzi, Mauro ^a,d   Rufer, Nathalie ^a,e  

^a National Center of Competence in Research in Molecular Oncology   (Switzerland)

^b EPFL   (Switzerland)

^c GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^d SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^e SWISS INST FOR EXP CANCER RESEARCH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; CYCLIN DEPENDENT KINASE INHIBITOR 1; PROTEIN P16INK4A; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE;

ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; HUMAN; HUMAN CELL; KARYOTYPE; LYMPHOCYTE PROLIFERATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; TELOMERE; WESTERN BLOTTING;

EID: 33748507999     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.6.3657     Document Type: Article

References (54)

1. Effros, R. B., and G. Pawelec. 1997. Replicative senescence of T cells: does the Hayflick Limit lead to immune exhaustion? Immunol. Today 18: 450-454.
2. Ben-Porath, I., and R. A. Weinberg. 2004. When cells get stressed: an integrative view of cellular senescence. J. Clin. Invest. 113: 8-13.
3. Narita, M., S. Nunez, E. Heard, A. W. Lin, S. A. Hearn, D. L. Spector, G. J. Hannon, and S. W. Lowe. 2003. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113: 703-716.
4. Wright, W. E., and J. W. Shay. 2001. Cellular senescence as a tumor-protection mechanism: the essential role of counting. Curr. Opm. Genet. Dev. 11: 98-103.
5. Harley, C. B., H. Vaziri, C. M. Counter, and R. C. Allsopp. 1992. The telomere hypothesis of cellular aging. Exp. Gerontol 27: 375-382.
6. d'Adda di Fagagna, F., P. M. Reaper, L. Clay-Farrace, H. Fiegler, P. Carr, T. Von Zglinicki, G. Saretzki, N. P. Carter, and S. P. Jackson. 2003. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426: 194-198.
7. Herbig, U., W. A. Jobling, B. P. Chen, D. J. Chen, and J. M. Sedivy. 2004. Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol. Cell 14: 501-513.
8. Weng, N. P. 2002. Regulation of telomerase expression in human lymphocytes. Springer Semin. Immunopathol. 24: 23-33.
9. Weng, N. P., B. L. Levine, C. H. June, and R. J. Hodes. 1995. Human naive and memory T lymphocytes differ in telomeric length and replicative potential. Proc. Natl. Acad. Sci. USA 92: 11091-11094.
10. Rufer, N., W. Dragowska, G. Thornbury, E. Roosnek, and P. M. Lansdorp. 1998. Telomere length dynamics in human lymphocyte subpopulations measured by flow cytometry. Nat. Biotechnol. 16: 743-747.
11. Rufer, N., T. H. Brummendorf, S. Kolvraa, C. Bischoff, K. Christensen, L. Wadsworth, M. Schulzer, and P. M. Lansdorp. 1999. Telomere fluorescence measurements in granulocytes and T lymphocyte subsets point to a high turnover of hematopoietic stem cells and memory T cells in early childhood. J. Exp. Med. 190: 157-167.
12. Zippelius, A., M. J. Pittet, P. Batard, N. Rufer, M. de Smedt, P. Guillaume, K. Ellefsen, D. Valmori, D. Lienard, J. Plum, et al. 2002. Thymic selection generates a large T cell pool recognizing a self-peptide in humans. J. Exp. Med. 195: 485-494.
13. Alcorta, D. A., Y. Xiong, D. Phelps, G. Hannon, D. Beach, and J. C. Barrett. 1996. Involvement of the cyclin-dependent kinase inhibitor p16 (INK4a) in replicative senescence of normal human fibroblasts. Proc. Natl. Acad. Sci. USA 93: 13742-13747.
14. Stein, G. H., L. F. Drullinger, A. Soulard, and V. Dulic. 1999. Differential roles for cyclin-dependent kinase inhibitors p21 and p16 in the mechanisms of senescence and differentiation in human fibroblasts. Mol. Cell. Biol. 19: 2109-2117.
15. Beausejour, C. M., A. Krtolica, F. Galimi, M. Narita, S. W. Lowe, P. Yaswen, and J. Campisi. 2003. Reversal of human cellular senescence: roles of the p53 and p16 pathways. EMBO J. 22: 4212-4222.
16. Roussel, M. F. 1999. The INK4 family of cell cycle inhibitors in cancer. Oncogene 18: 5311-5317.
17. Lowe, S. W., and C. J. Sherr. 2003. Tumor suppression by Ink4a-Arf: progress and puzzles. Curr. Opin. Genet. Dev. 13: 77-83.
18. Ramirez, R. D., C. P. Morales, B. S. Herbert, J. M. Rohde, C. Passons, J. W. Shay, and W. E. Wright. 2001. Putative telomere-independent mechanisms of replicative aging reflect inadequate growth conditions. Genes Dev. 15: 398-403.
19. Rheinwald, J. G., W. C. Hahn, M. R. Ramsey, J. Y. Wu, Z. Guo, H. Tsao, M. De Luca, C. Catricala, and K. M. O'Toole. 2002. A two-stage, p16(INK4A)- and p53-dependent keratinocyte senescence mechanism that limits replicative potential independent of telomere status. Mol. Cell. Biol. 22: 5157-5172.
20. Chazal, M., C. Marionnet, L. Michel, K. Mollier, J. E. Dazard, V. Della Valle, C. J. Larsen, M. P. Gras, and N. Basset-Seguin. 2002. P16(INK4A) is implicated in both the immediate and adaptative response of human keratinocytes to UVB irradiation. Oncogene 21: 2652-2661.
21. de Magalhaes, J. P., F. Chainiaux, J. Remacle, and O. Toussaint. 2002. Stress-induced premature senescence in BJ and hTERT-BJ1 human foreskin fibroblasts. FEBS Lett. 523: 157-162.
22. + T lymphocytes. J. Immunol. 174: 3335-3343.
23. + T lymphocyte proliferation. J. Immunol. 176: 2173-2182.
24. Vaziri, H., and S. Benchimol. 1998. Reconstitution of telomerase activity in normal human cells leads to elongation of telomeres and extended replicative life span. Curr. Biol. 8: 279-282.
25. Bodnar, A. G., M. Ouellette, M. Frolkis, S. E. Holt, C. P. Chiu, G. B. Morin, C. B. Harley, J. W. Shay, S. Lichtsteiner, and W. E. Wright. 1998. Extension of life-span by introduction of telomerase into normal human cells. Science 279: 349-352.
26. Yang, J., E. Chang, A. M. Cherry, C. D. Bangs, Y. Oei, A. Bodnar, A. Bronstein, C. P. Chiu, and G. S. Herron. 1999. Human endothelial cell life extension by telomerase expression. J. Biol. Chem. 274: 26141-26148.
27. Morales, C. P., S. E. Holt, M. Ouellette, K. J. Kaur, Y. Yan, K. S. Wilson, M. A. White, W. E. Wright, and J. W. Shay. 1999. Absence of cancer-associated changes in human fibroblasts immortalized with telomerase. Nat. Genet. 21: 115-118.
28. Jiang, X. R., G. Jimenez, E. Chang, M. Frolkis, B. Kusler, M. Sage, M. Beeche, A. G. Bodnar, G. M. Wahl, T. D. Tlsty, and C. P. Chiu. 1999. Telomerase expression in human somatic cells does not induce changes associated with a transformed phenotype. Nat. Genet. 21: 111-114.
29. + T cell clones by ectopic expression of telomerase reverse transcriptase. J. Immunol 165: 4239-4245.
30. Rufer, N., M. Migliaccio, J. Antonchuk, R. K. Humphries, E. Roosnek, and P. M. Lansdorp. 2001. Transfer of the human telomerase reverse transcriptase (TERT) gene into T lymphocytes results in extension of replicative potential. Blood 98: 597-603.
31. + helper and regulatory T-cell clones and confers resistance to oxidative stress-induced apoptosis. Blood 101: 4512-4519.
32. Schreurs, M. W., K. B. Scholten, E. W. Kueter, J. J. Ruizendaal, C. J. Meijer, and E. Hooijberg. 2003. In vitro generation and life span extension of human papillomavirus type 16-specific, healthy donor-derived CTL clones. J. Immunol. 171: 2912-2921.
33. Dagarag, M., T. Evazyan, N. Rao, and R. B. Effros. 2004. Genetic manipulation of telomerase in HIV-specific CD8+ T cells: enhanced antiviral functions accompany the increased proliferative potential and telomere length stabilization. J. Immunol. 173: 6303-6311.
34. Lindvall, C., M. Hou, T. Komurasaki, C. Zheng, M. Henriksson, J. M. Sedivy, M. Bjorkholm, B. T. Teh, M. Nordenskjold, and D. Xu. 2003. Molecular characterization of human telomerase reverse transcriptase-immortalized human fibroblasts by gene expression profiling: activation of the epiregulin gene. Cancer Res. 63: 1743-1747.
35. Smith, L. L., H. A. Coller, and J. M. Roberts. 2003. Telomerase modulates expression of growth-controlling genes and enhances cell proliferation. Nat. Cell Biol. 5: 474-479.
36. + T lymphocytes overexpressing hTERT. Blood 106: 43-50.
37. + T lymphocytes. Blood 106: 2663-2670.
38. + T subsets based on gene expression and replicative history analysis. Methods Mol. Med. 109: 265-284.
39. Bolstad, B. M., F. Collin, J. Brettschneider, K. Simpson, L. Cope, R.A. Irizarry, and T. P. Speed. 2005. Quality assessment of Affymetrix gene chip data. In: Bioinformatics and Computational Biology Solutions Using R and Bioconductor, R. Gentleman, V. Carey, W. Huber, R. Irizarry, and S. Dutoit, eds. Springer, Heidelberg, 33-47.
40. Irizarry, R. A., B. M. Bolstad, F. Collin, L. M. Cope, B. Hobbs, and T. P. Speed. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31: e15.
41. Bolstad, B. M., R. A. Irizarry, M. Astrand, and T. P. Speed. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
42. Lonnstedt, I., and T. P. Speed. 2002. Replicated microarray data. Statistica Sinica 12: 31-46.
43. Smyth, G. K. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3: article 3.
44. Henthorn, P., M. Kiledjian, and T. Kadesch. 1990. Two distinct transcription factors that bind the immunoglobulin enhancer microE5/κ 2 motif. Science 247: 467-470.
45. Ben-Porath, I., and R. A. Weinberg. 2005. The signals and pathways activating cellular senescence. Int. J. Biochem. Cell Biol. 37: 961-976.
46. Bergqvist, I., M. Eriksson, J. Saarikettu, B. Eriksson, B. Corneliussen, T. Grundstrom, and D. Holmberg. 2000. The basic helix-loop-helix transcription factor E2-2 is involved in T lymphocyte development. Eur. J. Immunol. 30: 2857-2863.
47. Stewart, S. A., W. C. Hahn, B. F. O'Connor, E. N. Banner, A. S. Lundberg, P. Modha, H. Mizuno, M. W. Brooks, M. Fleming, D. B. Zimonjic, et al. 2002. Telomerase contributes to tumorigenesis by a telomere length-independent mechanism. Proc. Natl. Acad. Sci. USA 99: 12606-12611.
48. Shi, S., S. Gronthos, S. Chen, A. Reddi, C. M. Counter, P. G. Robey, and C. Y. Wang. 2002. Bone formation by human postnatal bone marrow stromal stem cells is enhanced by telomerase expression. Nat. Biotechnol. 20: 587-591.
49. Oh, H., G. E. Taffet, K. A. Youker, M. L. Entman, P. A. Overbeek, L. H. Michael, and M. D. Schneider. 2001. Telomerase reverse transcriptase promotes cardiac muscle cell proliferation, hypertrophy, and survival. Proc. Natl. Acad. Sci. USA 98: 10308-10313.
50. MacKenzie, K. L., S. Franco, C. May, M. Sadelain, and M. A. Moore. 2000. Mass cultured human fibroblasts overexpressing hTERT encounter a growth crisis following an extended period of proliferation. Exp. Cell Res. 259: 336-350.
51. + T lymphocyte immortalization. J. Immunol. 165: 4978-4984.
52. Milyavsky, M., I. Shats, N. Erez, X. Tang, S. Senderovich, A. Meerson, Y. Tabach, N. Goldfinger, D. Ginsberg, C. C. Harris, and V. Rotter. 2003. Prolonged culture of telomerase-immortalized human fibroblasts leads to a premalignant phenotype. Cancer Res. 63: 7147-7157.
53. Noble, J. R., Z. H. Zhong, A. A. Neumann, J. R. Melki, S. J. Clark, and R. R. Reddel. 2004. Alterations in the p16(INK4a) and p53 tumor suppressor genes of hTERT-immortalized human fibroblasts. Oncogene 23: 3116-3121.
54. Gorbunova, V., A. Seluanov, and O. M. Pereira-Smith. 2003. Evidence that high telomerase activity may induce a senescent-like growth arrest in human fibroblasts. J. Biol. Chem. 278: 7692-7698.