Multifunctional cytomegalovirus (CMV)-specific CD8+ T cells are not restricted by telomere-related senescence in young or old adults

Immunology

Volumn 144, Issue 4, 2015, Pages 549-560

  Riddell, Natalie E ^a   Griffiths, Stephen J ^a   Rivino, Laura ^b   King, David C B ^b   Teo, Guo H ^b   Henson, Sian M ^a   Cantisan, Sara ^c   Solana, Rafael ^c   Kemeny, David M ^b   Macary, Paul A ^b   Larbi, Anis ^d   Akbar, Arne N ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c UNIVERSITY OF CÓRDOBA   (Spain)

^d AGENCY FOR SCIENCE   (Singapore)

Author keywords

CD8+ T cells; Cytomegalovirus; Multi functional; Senescence; Telomere

Indexed keywords

CD27 ANTIGEN; CD45RA ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 2; QUANTUM DOT; TUMOR NECROSIS FACTOR ALPHA; BIOLOGICAL MARKER; CD45 ANTIGEN; CYTOKINE;

ADULT; AGED; ANTIGEN SPECIFICITY; ARTICLE; ASIAN; CAUCASIAN; CD8+ T LYMPHOCYTE; CELL AGING; COHORT ANALYSIS; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; FLOW CYTOMETRY; FLUORESCENCE IN SITU HYBRIDIZATION; GROUPS BY AGE; HUMAN; HUMAN CELL; LYMPHOCYTE DIFFERENTIATION; NONHUMAN; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; T LYMPHOCYTE SUBPOPULATION; TELOMERE HOMEOSTASIS; THERMOSTABILITY; AGE; AGING; ASIAN CONTINENTAL ANCESTRY GROUP; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CLINICAL TRIAL; COMPARATIVE STUDY; ENGLAND; ETHNOLOGY; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOCYTE ACTIVATION; METABOLISM; MULTICENTER STUDY; PATHOGENICITY; PHENOTYPE; PROCEDURES; SINGAPORE; TELOMERE; TELOMERE SHORTENING; VERY ELDERLY; VIROLOGY; YOUNG ADULT;

ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; AGING; ANTIGENS, CD27; ANTIGENS, CD45; ASIAN CONTINENTAL ANCESTRY GROUP; BIOMARKERS; CD8-POSITIVE T-LYMPHOCYTES; CELL AGING; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; EUROPEAN CONTINENTAL ANCESTRY GROUP; FLOW CYTOMETRY; HUMANS; IMMUNOPHENOTYPING; LONDON; LYMPHOCYTE ACTIVATION; PHENOTYPE; SINGAPORE; TELOMERE; TELOMERE SHORTENING; YOUNG ADULT;

EID: 84924390097     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12409     Document Type: Article

References (46)

1. + T cells. Blood 2006; 107:4781-9.
2. + T helper cells in chronic HCV infection. Hepatology 2005; 41:1019-28.
3. Millington KA, Innes JA, Hackforth S et al. Dynamic relationship between IFN-γ and IL-2 profile of Mycobacterium tuberculosis-specific T cells and antigen load. J Immunol 2007; 178:5217-26.
4. Caccamo N, Guggino G, Meraviglia S et al. Analysis of Mycobacterium tuberculosis-specific CD8 T-cells in patients with active tuberculosis and in individuals with latent infection. PLoS ONE 2009; 4:e5528.
5. Seder RA, Darrah PA, Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 2008; 8:247-58.
6. + T cells in healthy carriers are continuously driven to replicative exhaustion. J Immunol 2005; 175:8218-25.
7. + T cell responses associated with control of viremia. Science 1997; 278:1447-50.
8. + T-cell replicative senescence in human aging. Immunol Rev 2005; 205:147-57.
9. Blackburn EH. Structure and function of telomeres. Nature 1991; 350:569-73.
10. Hodes RJ, Hathcock KS, Weng NP. Telomeres in T and B cells. Nat Rev Immunol 2002; 2:699-706.
11. + T cells: the potential involvement of interleukin-7 in this process. Immunology 2011; 132:326-39.
12. Montpetit AJ, Alhareeri AA, Montpetit M et al. Telomere length: a review of methods for measurement. Nurs Res 2014; 63:289-99.
13. Baerlocher GM, Vulto I, de Jong G, Lansdorp PM. Flow cytometry and FISH to measure the average length of telomeres (flow FISH). Nat Protoc 2006; 1:2365-76.
14. Baerlocher GM, Mak J, Tien T, Lansdorp PM. Telomere length measurement by fluorescence in situ hybridization and flow cytometry: tips and pitfalls. Cytometry 2002; 47:89-99.
15. Reed JR, Vukmanovic-Stejic M, Fletcher JM et al. Telomere erosion in memory T cells induced by telomerase inhibition at the site of antigenic challenge in vivo. J Exp Med 2004; 199:1433-43.
16. Rufer N, Dragowska W, Thornbury G, Roosnek E, Lansdorp PM. Telomere length dynamics in human lymphocyte subpopulations measured by flow cytometry. Nat Biotechnol 1998; 16:743-7.
17. + T cells during acute Epstein-Barr virus infection. Blood 2001; 97:700-7.
18. - memory T cells. J Immunol 2011; 187:2093-100.
19. + T cells. J Exp Med 1997; 186:1407-18.
20. Appay V, van Lier RA, Sallusto F, Roederer M. Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 2008; 73:975-83.
21. Cannon MJ, Schmid DS, Hyde TB. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev Med Virol 2010; 20:202-13.
22. Chidrawar S, Khan N, Wei W, McLarnon A, Smith N, Nayak L, Moss P. Cytomegalovirus-seropositivity has a profound influence on the magnitude of major lymphoid subsets within healthy individuals. Clin Exp Immunol 2009; 155:423-32.
23. + T-cell repertoire, which may be the basis for an imbalance in the cytokine production profile in elderly persons. J Virol 2005; 79:3675-83.
24. Kapoor V, Hakim FT, Rehman N, Gress RE, Telford WG. Quantum dots thermal stability improves simultaneous phenotype-specific telomere length measurement by FISH-flow cytometry. J Immunol Methods 2009; 344:6-14.
25. + T cells. J Clin Invest 2014; 124:4004-16.
26. van de Berg PJ, Griffiths SJ, Yong SL et al. Cytomegalovirus infection reduces telomere length of the circulating T cell pool. J Immunol 2010; 184:3417-23.
27. Crompton JG, Sukumar M, Restifo NP. Uncoupling T-cell expansion from effector differentiation in cell-based immunotherapy. Immunol Rev 2014; 257:264-76.
28. Zhou J, Shen X, Huang J, Hodes RJ, Rosenberg SA, Robbins PF. Telomere length of transferred lymphocytes correlates with in vivo persistence and tumor regression in melanoma patients receiving cell transfer therapy. J Immunol 2005; 175:7046-52.
29. Rosenberg SA, Dudley ME. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr Opin Immunol 2009; 21:233-40.
30. Cawthon RM, Smith KR, O'Brien E, Sivatchenko A, Kerber RA. Association between telomere length in blood and mortality in people aged 60 years or older. Lancet 2003; 361:393-5.
31. Samani NJ, Boultby R, Butler R, Thompson JR, Goodall AH. Telomere shortening in atherosclerosis. Lancet 2001; 358:472-3.
32. Fyhrquist F, Saijonmaa O, Strandberg T. The roles of senescence and telomere shortening in cardiovascular disease. Nat Rev Cardiol 2013; 10:274-83.
33. Cohen S, Janicki-Deverts D, Turner RB, Casselbrant ML, Li-Korotky HS, Epel ES, Doyle WJ. Association between telomere length and experimentally induced upper respiratory viral infection in healthy adults. JAMA 2013; 309:699-705.
34. Levin MJ. Immune senescence and vaccines to prevent herpes zoster in older persons. Curr Opin Immunol 2012; 24:494-500.
35. + T cells in patients with X-linked lymphoproliferative syndrome. Mech Ageing Dev 2005; 126:855-65.
36. Rufer N, Brummendorf TH, Kolvraa S, Bischoff C, Christensen K, Wadsworth L, Schulzer M, Lansdorp PM. 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 1999; 190:157-67.
37. Weng NP, Levine BL, June CH, Hodes RJ. Regulated expression of telomerase activity in human T lymphocyte development and activation. J Exp Med 1996; 183:2471-9.
38. Akbar AN, Beverley PC, Salmon M. Will telomere erosion lead to a loss of T-cell memory? Nat Rev Immunol 2004; 4:737-43.
39. + T cells that re-express CD45RA. J Immunol 2013; 190:5363-72.
40. Ferrando-Martinez S, Ruiz-Mateos E, Hernandez A, Gutierrez E, Rodriguez-Mendez MD, Ordonez A, Leal M. Age-related deregulation of naive T cell homeostasis in elderly humans. Age (Dordr) 2011; 33:197-207.
41. Akbar AN, Henson SM. Are senescence and exhaustion intertwined or unrelated processes that compromise immunity? Nat Rev Immunol 2011; 11:289-95.
42. Nikolich-Zugich J. Ageing and life-long maintenance of T-cell subsets in the face of latent persistent infections. Nat Rev Immunol 2008; 8:512-22.
43. + T cells during persistent infection. Blood 2005; 106:558-65.
44. + T cells to interleukin-7 or interleukin-15 stimulates proliferation without differentiation or loss of telomere length. Immunology 2006; 119:243-53.
45. + memory T-cell subsets in response to antigen or homeostatic cytokines. Blood 2003; 101:4260-6.
46. Passos JF, Nelson G, Wang C et al. Feedback between p21 and reactive oxygen production is necessary for cell senescence. Mol Syst Biol 2010; 6:347.