Senescence of T Lymphocytes: Implications for Enhancing Human Immunity

Trends in Immunology

Volumn 37, Issue 12, 2016, Pages 866-876

  Akbar, Arne N ^a   Henson, Sian M ^b   Lanna, Alessio ^a,c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; CELL FUNCTION; HUMAN; IMMUNITY; NUTRIENT; SENESCENCE; T LYMPHOCYTE; ANIMAL; CELL AGING; IMMUNIZATION; IMMUNOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

AGING; ANIMALS; CELL AGING; HUMANS; IMMUNITY; IMMUNIZATION; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84999766469     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2016.09.002     Document Type: Review

References (80)

1. 1 Akbar, A.N., Henson, S.M., Are senescence and exhaustion intertwined or unrelated processes that compromise immunity?. Nat. Rev. Immunol. 11 (2011), 289–295.
2. 2 Di Leonardo, A., et al. DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes Dev. 8 (1994), 2540–2551.
3. 3 Sherr, C.J., DePinho, R.A., Cellular senescence: minireview. Mitotic clock or culture shock?. Cell 102 (2000), 407–410.
4. 4 d'Adda di Fagagna, F., Living on a break: cellular senescence as a DNA-damage response. Nat. Rev. Cancer 8 (2008), 512–522.
5. Ink4a-positive cells shorten healthy lifespan. Nature 530 (2016), 184–189.
6. 6 van Deursen, J.M., The role of senescent cells in ageing. Nature 509 (2014), 439–446.
7. 7 Beverley, P.C.L., Immune memory: the basics and how to trigger an efficient long-term immune memory. J. Comp. Pathol. 142:Suppl. 1 (2010), S91–S95.
8. 8 Ahmed, R., Gray, D., Immunological memory and protective immunity: understanding their relation. Science 272 (1996), 54–60.
9. 9 Akbar, A.N., et al. Will telomere erosion lead to a loss of T-cell memory?. Nat. Rev. Immunol. 4 (2004), 737–743.
10. 10 Nikolich-Zugich, J., Rudd, B.D., Immune memory and aging: an infinite or finite resource?. Curr. Opin. Immunol. 22 (2010), 535–540.
11. 11 Brien, J.D., et al. Key role of T cell defects in age-related vulnerability to West Nile virus. J. Exp. Med. 206 (2009), 2735–2745.
12. 12 Whitehorn, J., Simmons, C.P., The pathogenesis of dengue. Vaccine 29 (2011), 7221–7228.
13. 13 Gupta, M., et al. Persistent infection with Ebola virus under conditions of partial immunity. J. Virol. 78 (2004), 958–967.
14. 14 Grubeck-Loebenstein, B., et al. Immunosenescence and vaccine failure in the elderly. Aging Clin. Exp. Res. 21 (2009), 201–209.
15. 15 Franceschi, C., et al. Biomarkers of immunosenescence within an evolutionary perspective: the challenge of heterogeneity and the role of antigenic load. Exp. Gerontol. 34 (1999), 911–921.
16. − T cells is associated with decreased Akt (Ser473) phosphorylation. J. Immunol. 178 (2007), 7710–7719.
17. 17 Lanna, A., et al. The kinase p38 activated by the metabolic regulator AMPK and scaffold TAB1 drives the senescence of human T cells. Nat. Immunol. 15 (2014), 965–972.
18. + T cells. J. Clin. Invest. 124 (2014), 4004–4016.
19. + T cells in patients with X-linked lymphoproliferative syndrome. Mech. Ageing Dev. 126 (2005), 855–865.
20. 20 van de Berg, P.J., et al. Cytomegalovirus infection reduces telomere length of the circulating T cell pool. J. Immunol. 184 (2010), 3417–3423.
21. 21 Krizhanovsky, V., et al. Senescence of activated stellate cells limits liver fibrosis. Cell 134 (2008), 657–667.
22. 22 Sagiv, A., et al. NKG2D ligands mediate immunosurveillance of senescent cells. Aging 8 (2016), 328–344.
23. 23 Baker, D.J., et al. BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat. Genet 36 (2004), 744–749.
24. + T cells: the potential involvement of interleukin-7 in this process. Immunol. 132 (2011), 326–339.
25. − memory T cells. J. Immunol. 187 (2011), 2093–2100.
26. + T cells by both hTERT downregulation and induction of p38 MAPK signaling. J. Immunol. 191 (2013), 3744–3752.
27. + T-cell proliferation by distinct pathways. Eur. J. Immunol. 45 (2015), 1441–1451.
28. + T cells. Blood 113 (2009), 6619–6628.
29. − T cells from rheumatoid arthritis patients. J. Immunol. 161 (1998), 1018–1025.
30. null T cells are associated with defects in apoptotic pathways. J. Immunol. 165 (2000), 6301–6307.
31. 31 Appay, V., et al. Accelerated immune senescence and HIV-1 infection. Exp. Gerontol. 42 (2007), 432–437.
32. + T cells in healthy carriers are continuously driven to replicative exhaustion. J. Immunol. 175 (2005), 8218–8225.
33. + T cells. J. Exp. Med. 186 (1997), 1407–1418.
34. 34 Khan, N., et al. Cytomegalovirus seropositivity drives the CD8 T cell repertoire toward greater clonality in healthy elderly individuals. J. Immunol. 169 (2002), 1984–1992.
35. 35 Das, A., et al. Functional skewing of the global CD8 T cell population in chronic hepatitis B virus infection. J. Exp. Med. 205 (2008), 2111–2124.
36. + T-lymphocyte telomere length is related to fibrosis stage, clinical outcome and treatment response in chronic hepatitis C virus infection. J. Hepatol. 53 (2010), 252–260.
37. + T cell efficacy in vaccination and disease. Nat. Med. 14 (2008), 623–628.
38. + T cell differentiation. J. Clin. Invest. 120 (2010), 4077–4090.
39. 39 Hislop, A.D., et al. Cellular responses to viral infection in humans: lessons from Epstein–Barr virus. Annu. Rev. Immunol. 25 (2007), 587–617.
40. + T cells during persistent infection. Blood 106 (2005), 558–565.
41. + T cell responses to EBV contrast with CD8 responses in breadth of lytic cycle antigen choice and in lytic cycle recognition. J. Immunol. 187 (2011), 92–101.
42. + T cells that re-express CD45RA are apoptosis-resistant memory cells that retain replicative potential. Blood 100 (2002), 933–940.
43. + T cells are not restricted by telomere-related senescence in young or old adults. Immunol. 144 (2015), 549–560.
44. 44 Passos, J.F., et al. Feedback between p21 and reactive oxygen production is necessary for cell senescence. Mol. Syst. Biol., 6, 2010, 347.
45. 45 Davis, T., et al. Evaluating the role of p38 MAP kinase in growth of Werner syndrome fibroblasts. Ann. N. Y. Acad. Sci. 1197 (2010), 45–48.
46. 46 Cong, Y-S., et al. Human telomerase and its regulation. Microbiol. Mol. Biol. Rev. 66 (2002), 407–425.
47. 47 Salvador, J.M., et al. Alternative p38 activation pathway mediated by T cell receptor-proximal tyrosine kinases. Nat. Immunol. 6 (2005), 390–395.
48. 48 Reed, J.R., et al. Telomere erosion in memory T cells induced by telomerase inhibition at the site of antigenic challenge in vivo. J. Exp. Med. 199 (2004), 1433–1443.
49. 49 Patterson, H., et al. Protein kinase inhibitors in the treatment of inflammatory and autoimmune diseases. Clin. Exp. Immunol. 176 (2014), 1–10.
50. 50 Powell, J.D., et al. Regulation of immune responses by mTOR. Annu. Rev. Immunol. 30 (2012), 39–68.
51. + T lymphocytes. Cell Death Dis., 5, 2014, e1294.
52. 52 Terman, A., Brunk, U.T., The aging myocardium: roles of mitochondrial damage and lysosomal degradation. Heart Lung Circ. 14 (2005), 107–114.
53. 53 Phadwal, K., et al. A novel method for autophagy detection in primary cells: impaired levels of macroautophagy in immunosenescent T cells. Autophagy 8 (2012), 677–689.
54. 54 Tchkonia, T., et al. Cellular senescence and the senescent secretory phenotype: therapeutic opportunities. J. Clin. Invest. 123 (2013), 966–972.
55. 55 Franceschi, C., et al. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann. N. Y. Acad. Sci. 908 (2000), 244–254.
56. 56 Hohensinner, P.J., et al. Telomere dysfunction, autoimmunity and aging. Aging Dis. 2 (2011), 524–537.
57. 57 Wentzensen, I.M., et al. The association of telomere length and cancer: a meta-analysis. Cancer Epidemiol. Biomarkers Prev. 20 (2011), 1238–1250.
58. 58 Chou, J.P., Effros, R.B., T cell replicative senescence in human aging. Curr. Pharm. Des. 19 (2013), 1680–1698.
59. 59 Schönland, S.O., et al. Premature telomeric loss in rheumatoid arthritis is genetically determined and involves both myeloid and lymphoid cell lineages. Proc. Natl. Acad. Sci. U.S.A. 100 (2003), 13471–13476.
60. 60 Campisi, J., Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120 (2005), 513–522.
61. 61 Sweeney, S.E., The as-yet unfulfilled promise of p38 MAPK inhibitors. Nat. Rev. Rheumatol. 5 (2009), 475–477.
62. +CD28- T-cells. PLoS ONE, 7, 2012, e33939.
63. 63 Ho, P-C., Liu, P-S., Metabolic communication in tumors: a new layer of immunoregulation for immune evasion. J. Immunother. Cancer, 4, 2016, 4.
64. 64 Wherry, E.J., et al. Low CD8 T-cell proliferative potential and high viral load limit the effectiveness of therapeutic vaccination. J. Virol. 79 (2005), 8960–8968.
65. 65 Riella, L.V., et al. Role of the PD-1 pathway in the immune response. Am. J. Transplant. 12 (2012), 2575–2587.
66. 66 Mahoney, K.M., et al. Combination cancer immunotherapy and new immunomodulatory targets. Nat. Rev. Drug Discov. 14 (2015), 561–584.
67. 67 Pearce, E.L., Pearce, E.J., Metabolic pathways in immune cell activation and quiescence. Immunity 38 (2013), 633–643.
68. 68 Ho, P-C., et al. Phosphoenolpyruvate is a metabolic checkpoint of anti-tumor T cell responses. Cell 162 (2015), 1217–1228.
69. 69 Hayflick, L., Moorhead, P.S., The serial cultivation of human diploid cell strains. Exp. Cell Res. 25 (1961), 585–621.
70. 70 von Zglinicki, T., et al. Human cell senescence as a DNA damage response. Mech. Ageing Dev. 126 (2005), 111–117.
71. 71 Blasco, M.A., Telomerase beyond telomeres. Nat. Rev. Cancer 2 (2002), 627–633.
72. 72 Weng, N.P., Telomere and adaptive immunity. Mech. Ageing Dev. 129 (2008), 60–66.
73. 73 Blagosklonny, M.V., Cell cycle arrest is not senescence. Aging 3 (2011), 94–101.
74. 74 Freund, A., et al. Inflammatory networks during cellular senescence: causes and consequences. Trends Mol. Med. 16 (2010), 238–246.
75. 75 Coppe, J.P., et al. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu. Rev. Pathol. 5 (2010), 99–118.
76. 76 Montpetit, A.J., et al. Telomere length: a review of methods for measurement. Nurs. Res. 63 (2014), 289–299.
77. 77 Baerlocher, G.M., et al. Flow cytometry and FISH to measure the average length of telomeres (flow FISH). Nat. Protoc. 1 (2006), 2365–2376.
78. + T subsets with distinct replicative history and partial effector functions. Blood 102 (2003), 1779–1787.
79. 79 de Jesus, B.B., Blasco, M.A., Assessing cell and organ senescence biomarkers. Circ. Res. 111 (2012), 97–109.
80. 80 Hewitt, G., et al. Telomeres are favoured targets of a persistent DNA damage response in ageing and stress-induced senescence. Nat. Commun., 3, 2012, 708.