Reversible senescence in human CD4+CD45RA+CD27 - memory T cells

Journal of Immunology

Volumn 187, Issue 5, 2011, Pages 2093-2100

  Di Mitri, Diletta ^a,b   Azevedo, Rita I ^a,c   Henson, Sian M ^a   Libri, Valentina ^a   Riddell, Natalie E ^a   Macaulay, Richard ^a   Kipling, David ^d   Soares, Maria V D ^c   Battistini, Luca ^b   Akbar, Arne N ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^d CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; CD45RA ANTIGEN; CD57 ANTIGEN; CELL SURFACE MARKER; HISTONE H2AX; KLRG1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; T LYMPHOCYTE RECEPTOR; TELOMERASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELL AGING; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; LYMPHOCYTE DIFFERENTIATION; MEMORY T LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TELOMERE;

ADULT; ANTIGENS, CD27; ANTIGENS, CD45; BLOTTING, WESTERN; CD4-POSITIVE T-LYMPHOCYTES; CELL AGING; CELL DIFFERENTIATION; CELL SEPARATION; FLOW CYTOMETRY; HUMANS; IMMUNOLOGIC MEMORY; IN SITU HYBRIDIZATION, FLUORESCENCE; LYMPHOCYTE ACTIVATION; MIDDLE AGED; P38 MITOGEN-ACTIVATED PROTEIN KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; TELOMERASE;

EID: 80052682032     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100978     Document Type: Article

References (70)

1. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22: 745-763. (Pubitemid 38680440)
2. Akbar, A. N., and S. M. Henson. 2011. Are senescence and exhaustion intertwined or unrelated processes that compromise immunity? Nat. Rev. Immunol. 11: 289-295.
3. Akbar, A. N., L. Terry, A. Timms, P. C. Beverley, and G. Janossy. 1988. Loss of CD45R and gain of UCHL1 reactivity is a feature of primed T cells. J. Immunol. 140: 2171-2178. (Pubitemid 18098471)
4. Appay, V., R. A. Van Lier, F. Sallusto, and M. Roederer. 2008. Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 73: 975-983.
5. Hamann, D., P. A. Baars, M. H. Rep, B. Hooibrink, S. R. Kerkhof-Garde, M. R. Klein, and R. A. Van Lier. 1997. Phenotypic and functional separation of memory and effector human CD8+ T cells. J. Exp. Med. 186: 1407-1418. (Pubitemid 27479800)
6. +T cells from adults respond to recall antigens after CD28 ligation. Int. Immunol. 8: 1737-1742.
7. - T cells: the potential involvement of interleukin-7 in this process. Immunology 132: 326-339.
8. Kimmig, S., G. K. Przybylski, C. A. Schmidt, K. Laurisch, B. Möwes, A. Radbruch, and A. Thiel. 2002. Two subsets of naive T helper cells with distinct T cell receptor excision circle content in human adult peripheral blood. J. Exp. Med. 195: 789-794. (Pubitemid 34259723)
9. Waller, E. C., N. McKinney, R. Hicks, A. J. Carmichael, J. G. Sissons, and M. R. Wills. 2007. Differential costimulation through CD137 (4-1BB) restores proliferation of human virus-specific "effector memory" (CD28-CD45RAHI) CD8+ T cells. Blood 110: 4360-4366. (Pubitemid 351377801)
10. + T cells that re-express CD45RA are apoptosis-resistant memory cells that retain replicative potential. Blood 100: 933-940.
11. Effros, R. B., Z. Cai, and P. J. Linton. 2003. CD8 T cells and aging. Crit. Rev. Immunol. 23: 45-64. (Pubitemid 36875473)
12. Pawelec, G., and E. Derhovanessian. 2011. Role of CMV in immune senescence. Virus Res. 157: 175-179.
13. + T cells. Immunol. Lett. 107: 8-14.
14. Hislop, A. D., G. S. Taylor, D. Sauce, and A. B. Rickinson. 2007. Cellular responses to viral infection in humans: lessons from Epstein-Barr virus. Annu. Rev. Immunol. 25: 587-617. (Pubitemid 46697918)
15. Akbar, A. N., and J. M. Fletcher. 2005. Memory T cell homeostasis and senescence during aging. Curr. Opin. Immunol. 17: 480-485. (Pubitemid 41207950)
16. + T-cell immunity to cytomegalovirus. Hum. Immunol. 65: 456-464.
17. + T-cell differentiation in response to viruses. Nat. Rev. Immunol. 3: 931-939.
18. + T cell response. J. Immunol. 168: 5455-5464.
19. + pool with distinct phenotypic and migratory characteristics. J. Immunol. 167: 212-220.
20. Goronzy, J. J., and C. M. Weyand. 2005. Rheumatoid arthritis. Immunol. Rev. 204: 55-73. (Pubitemid 40460493)
21. Ponchel, F., R. J. Verburg, S. J. Bingham, A. K. Brown, J. Moore, A. Protheroe, K. Short, C. A. Lawson, A. W. Morgan, M. Quinn, et al. 2005. Interleukin-7 deficiency in rheumatoid arthritis: consequences for therapy-induced lymphopenia. Arthritis Res. Ther. 7: R80-R92.
22. + T cell response. J. Immunol. 183: 7919-7930.
23. Campisi, J., and F. d'Adda di Fagagna. 2007. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol. 8: 729-740. (Pubitemid 47312822)
24. Blackburn, E. H. 2005. Telomeres and telomerase: their mechanisms of action and the effects of altering their functions. FEBS Lett. 579: 859-862. (Pubitemid 40361854)
25. 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. (Pubitemid 37442589)
26. d'Adda di Fagagna, F. 2008. Living on a break: cellular senescence as a DNA-damage response. Nat. Rev. Cancer 8: 512-522.
27. Passos, J. F., G. Nelson, C. Wang, T. Richter, C. Simillion, C. J. Proctor, S. Miwa, S. Olijslagers, J. Hallinan, A.Wipat, et al. 2010. Feedback between p21 and reactive oxygen production is necessary for cell senescence. Mol. Syst. Biol. 6: 347.
28. + T cells in healthy carriers are continuously driven to replicative exhaustion. J. Immunol. 175: 8218-8225.
29. Bagley, M. C., T. Davis, M. C. Dix, C. S. Widdowson, and D. Kipling. 2006. Microwave-assisted synthesis of N-pyrazole ureas and the p38alpha inhibitor BIRB 796 for study into accelerated cell ageing. Org. Biomol. Chem. 4: 4158-4164. (Pubitemid 44665188)
30. + T cells. Blood 113: 6619-6628.
31. 473) phosphorylation. J. Immunol. 178: 7710-7719.
32. Reed, J. R., M. Vukmanovic-Stejic, J. M. Fletcher, M. V. Soares, J. E. Cook, C. H. Orteu, S. E. Jackson, K. E. Birch, G. R. Foster, M. Salmon, 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: 1433-1443. (Pubitemid 38685734)
33. Harari, A., F. Vallelian, and G. Pantaleo. 2004. Phenotypic heterogeneity of antigen-specific CD4 T cells under different conditions of antigen persistence and antigen load. Eur. J. Immunol. 34: 3525-3533. (Pubitemid 40012170)
34. Champagne, P., G. S. Ogg, A. S. King, C. Knabenhans, K. Ellefsen, M. Nobile, V. Appay, G. P. Rizzardi, S. Fleury, M. Lipp, et al. 2001. Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 410: 106-111. (Pubitemid 32225845)
35. + T cells expressing the inhibitory killer cell lectin-like receptor G1 (KLRG1). Exp. Gerontol. 38: 911-920.
36. Voehringer, D., C. Blaser, P. Brawand, D. H. Raulet, T. Hanke, and H. Pircher. 2001. Viral infections induce abundant numbers of senescent CD8 T cells. J. Immunol. 167: 4838-4843. (Pubitemid 33009711)
37. Tanaka, T., H. D. Halicka, F. Traganos, K. Seiter, and Z. Darzynkiewicz. 2007. Induction of ATM activation, histone H2AX phosphorylation and apoptosis by etoposide: relation to cell cycle phase. Cell Cycle 6: 371-376.
38. Weng, N. P., B. L. Levine, C. H. June, and R. J. Hodes. 1996. Regulated expression of telomerase activity in human T lymphocyte development and activation. J. Exp. Med. 183: 2471-2479.
39. Bryl, E., A. N. Vallejo, E. L. Matteson, J. M. Witkowski, C. M. Weyand, and J. J. Goronzy. 2005. Modulation of CD28 expression with anti-tumor necrosis factor alpha therapy in rheumatoid arthritis. Arthritis Rheum. 52: 2996-3003. (Pubitemid 41447078)
40. Parish, S. T., J. E. Wu, and R. B. Effros. 2009. Modulation of T lymphocyte replicative senescence via TNF-alpha inhibition: role of caspase-3. J. Immunol. 182: 4237-4243.
41. Berenson, L. S., J. Yang, B. P. Sleckman, T. L. Murphy, and K. M. Murphy. 2006. Selective requirement of p38alpha MAPK in cytokine-dependent, but not antigen receptor-dependent, Th1 responses. J. Immunol. 176: 4616-4621.
42. Dodeller, F., and H. Schulze-Koops. 2006. The p38 mitogen-activated protein kinase signaling cascade in CD4 T cells. Arthritis Res. Ther. 8: 205.
43. Li, C., P. Beavis, A. C. Palfreeman, P. Amjadi, A. Kennedy, and F. M. Brennan. 2011. Activation of p38 mitogen-activated protein kinase is critical step for acquisition of effector function in cytokine-activated T cells, but acts as a negative regulator in T cells activated through the T-cell receptor. Immunology 132: 104-110.
44. Iwasa, H., J. Han, and F. Ishikawa. 2003. Mitogen-activated protein kinase p38 defines the common senescence-signalling pathway. Genes Cells 8: 131-144. (Pubitemid 36511698)
45. Haq, R., J. D. Brenton, M. Takahashi, D. Finan, A. Finkielsztein, S. Damaraju, R. Rottapel, and B. Zanke. 2002. Constitutive p38HOG mitogen-activated protein kinase activation induces permanent cell cycle arrest and senescence. Cancer Res. 62: 5076-5082. (Pubitemid 34987550)
46. Bagley, M. C., T. Davis, P. G. S. Murziani, C. S. Widdowson, and D. Kipling. 2010. Use of p38 MAPK Inhibitors for the Treatment of Werner Syndrome. Pharmaceuticals 3: 1842-1872.
47. Davis, T., M. A. Bachler, F. S. Wyllie, M. C. Bagley, and D. Kipling. 2010. Evaluating the role of p38 MAP kinase in growth of Werner syndrome fibroblasts. Ann. N.Y. Acad. Sci. 1197: 45-48.
48. Akbar, A. N., P. C. Beverley, and M. Salmon. 2004. Will telomere erosion lead to a loss of T-cell memory? Nat. Rev. Immunol. 4: 737-743. (Pubitemid 39223079)
49. Hodes, R. J., K. S. Hathcock, and N. P. Weng. 2002. Telomeres in T and B cells. Nat. Rev. Immunol. 2: 699-706. (Pubitemid 37328727)
50. Effros, R. B. 2004. Replicative senescence of CD8 T cells: effect on human ageing. Exp. Gerontol. 39: 517-524. (Pubitemid 38402077)
51. Goronzy, J. J., H. Fujii, and C. M. Weyand. 2006. Telomeres, immune aging and autoimmunity. Exp. Gerontol. 41: 246-251.
52. + T subsets with distinct replicative history and partial effector functions. Blood 102: 1779-1787.
53. Nikolich-Zugich, J., and B. D. Rudd. 2010. Immune memory and aging: an infinite or finite resource? Curr. Opin. Immunol. 22: 535-540.
54. Akbar, A. N., and M. Vukmanovic-Stejic. 2007. Telomerase in T lymphocytes: use it and lose it? J. Immunol. 178: 6689-6694.
55. - T cells: their role in the age-associated decline of immune function. Trends Immunol. 30: 306-312.
56. + T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 8: 379-385.
57. Von Zglinicki, T., G. Saretzki, J. Ladhoff, F. d'Adda di Fagagna, and S. P. Jackson. 2005. Human cell senescence as a DNA damage response. Mech. Ageing Dev. 126: 111-117. (Pubitemid 40018484)
58. + T cells in patients with X-linked lymphoproliferative syndrome. Mech. Ageing Dev. 126: 855-865.
59. + T cell-mediated antimicrobial activity against Mycobacterium tuberculosis in humans. J. Clin. Invest. 119: 1167-1177.
60. Geginat, J., F. Sallusto, and A. Lanzavecchia. 2001. Cytokine-driven proliferation and differentiation of human naive, central memory, and effector memory CD4+ T cells. J. Exp. Med. 194: 1711-1719. (Pubitemid 34028651)
61. Fujii, H., L. Shao, I. Colmegna, J. J. Goronzy, and C. M. Weyand. 2009. Telomerase insufficiency in rheumatoid arthritis. Proc. Natl. Acad. Sci. USA 106: 4360-4365.
62. Khan, N. 2007. The immunological burden of human cytomegalovirus infection. Arch. Immunol. Ther. Exp. (Warsz.) 55: 299-308.
63. high populations. J. Immunol. 173: 5843-5851.
64. Wherry, E. J., J. N. Blattman, K. Murali-Krishna, R. Van der Most, and R. Ahmed. 2003. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77: 4911-4927. (Pubitemid 36402840)
65. Zajac, A. J., J. N. Blattman, K. Murali-Krishna, D. J. Sourdive, M. Suresh, J. D. Altman, and R. Ahmed. 1998. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 188: 2205-2213. (Pubitemid 29028493)
66. Kuchroo, V. K., V. Dardalhon, S. Xiao, and A. C. Anderson. 2008. New roles for TIM family members in immune regulation. Nat. Rev. Immunol. 8: 577-580.
67. + T cells. Immunol. Rev. 192: 131-142.
68. Zarubin, T., and J. Han. 2005. Activation and signaling of the p38 MAP kinase pathway. Cell Res. 15: 11-18. (Pubitemid 41653958)
69. Fulop, T., A. Larbi, J. M. Witkowski, J. McElhaney, M. Loeb, A. Mitnitski, and G. Pawelec. 2010. Aging, frailty and age-related diseases. Biogerontology 11: 547-563.
70. Weyand, C. M., J. W. Fulbright, and J. J. Goronzy. 2003. Immunosenescence, autoimmunity, and rheumatoid arthritis. Exp. Gerontol. 38: 833-841. (Pubitemid 36957956)