Naïve and memory CD8 T cell pool homeostasis in advanced aging: Impact of age and of antigen-specific responses to cytomegalovirus

Age

Volumn 36, Issue 2, 2014, Pages 625-640

  Vescovini, Rosanna ^a   Fagnoni, Francesco Fausto ^b   Telera, Anna Rita ^a   Bucci, Laura ^c   Pedrazzoni, Mario ^a   Magalini, Francesca ^a   Stella, Adriano ^a   Pasin, Federico ^a   Medici, Maria Cristina ^a   Calderaro, Adriana ^a   Volpi, Riccardo ^a   Monti, Daniela ^d   Franceschi, Claudio ^c   Nikolich Žugich, Janko ^e   Sansoni, Paolo ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b Immunohematology and Transfusion Center   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

^d UNIVERSITY OF FLORENCE   (Italy)

^e UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Age; Aging; Cytomegalovirus; Homeostasis; Memory CD8 T cell; Na ve CD8 T cell

Indexed keywords

CD28 ANTIGEN; CYTOMEGALOVIRUS ANTIGEN PP65;

ADULT; AGE; AGED; AGING; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; CYTOMEGALOVIRUS INFECTION; EFFECTOR CELL; FEMALE; HUMAN; HUMAN CELL; LYMPHOCYTE COUNT; MAJOR CLINICAL STUDY; MALE; MEMORY T LYMPHOCYTE; OBSERVATIONAL STUDY; PREDICTION; VIRUS IMMUNITY;

AGED; AGED, 80 AND OVER; AGING; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CROSS-SECTIONAL STUDIES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; FEMALE; FLOW CYTOMETRY; FOLLOW-UP STUDIES; HOMEOSTASIS; HUMANS; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; PHENOTYPE;

EID: 84898868481     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-013-9594-z     Document Type: Article

References (52)

1. Almanzar G, Schwaiger S, Jenewein B, Keller M, Herndler-Brandstetter D, Wurzner R, Schonitzer D, Grubeck-Loebenstein B (2005) Long-term cytomegalovirus infection leads to significant changes in the composition of the CD8+ T-cell repertoire, which may be the basis for an imbalance in the cytokine production profile in elderly persons. J Virol 79(6):3675-3683. doi: 10.1128/JVI.79.6.3675- 3683.2005
2. Boeckh M, Geballe AP (2011) Cytomegalovirus: pathogen, paradigm, and puzzle. J Clin Invest 121(5):1673-1680. doi: 10.1172/JCI45449
3. Chidrawar S, Khan N, Wei W, McLarnon A, Smith N, Nayak L, Moss P (2009) Cytomegalovirus-seropositivity has a profound influence on the magnitude of major lymphoid subsets within healthy individuals. Clin Exp Immunol 155(3):423-432. doi: 10.1111/j.1365-2249.2008.03785.x
4. Cicin-Sain L, Sylwester AW, Hagen SI, Siess DC, Currier N, Legasse AW, Fischer MB, Koudelka CW, Axthelm MK, Nikolich-Zugich J, Picker LJ (2011) Cytomegalovirus-specific T cell immunity is maintained in immunosenescent rhesus macaques. J Immunol 187(4):1722-1732. doi: 10.4049/jimmunol.1100560
5. Demmler GJ (2006) Cytomegalovirus infection: back to the future or no more elephants? Clin Infect Dis 43(9):1152-1153. doi: 10.1086/508204
6. Derhovanessian E, Maier AB, Beck R, Jahn G, Hahnel K, Slagboom PE, de Craen AJ, Westendorp RG, Pawelec G (2010) Hallmark features of immunosenescence are absent in familial longevity. J Immunol 185(8):4618-4624. doi: 10.4049/jimmunol.1001629
7. Derhovanessian E, Maier AB, Hahnel K, Beck R, de Craen AJ, Slagboom EP, Westendorp RG, Pawelec G (2011) Infection with cytomegalovirus but not herpes simplex virus induces the accumulation of late-differentiated CD4+ and CD8+ T-cells in humans. J Gen Virol 92(Pt 12):2746-2756. doi: 10.1099/vir.0.036004-0
8. Fagnoni FF, Vescovini R, Mazzola M, Bologna G, Nigro E, Lavagetto G, Franceschi C, Passeri M, Sansoni P (1996) Expansion of cytotoxic CD8+ CD28- T cells in healthy ageing people, including centenarians. Immunology 88(4):501-507
9. Fagnoni FF, Vescovini R, Passeri G, Bologna G, Pedrazzoni M, Lavagetto G, Casti A, Franceschi C, Passeri M, Sansoni P (2000) Shortage of circulating naive CD8(+) T cells provides new insights on immunodeficiency in aging. Blood 95(9):2860-2868
10. Fagnoni FF, Lozza L, Zibera C, Zambelli A, Ponchio L, Gibelli N, Oliviero B, Pavesi L, Gennari R, Vescovini R, Sansoni P, Da Prada G, Robustelli Della Cuna G (2002) T-cell dynamics after high-dose chemotherapy in adults: elucidation of the elusive CD8+ subset reveals multiple homeostatic T-cell compartments with distinct implications for immune competence. Immunology 106(1):27-37
11. Ferrando-Martinez S, Ruiz-Mateos E, Hernandez A, Gutierrez E, Rodriguez-Mendez Mdel M, Ordonez A, Leal M (2011) Age-related deregulation of naive T cell homeostasis in elderly humans. Age (Dordr) 33(2):197-207. doi: 10.1007/s11357-010-9170-8
12. Ferrando-Martinez S, Romero-Sanchez MC, Solana R, Delgado J, de la Rosa R, Munoz-Fernandez MA, Ruiz-Mateos E, Leal M (2013) Thymic function failure and C-reactive protein levels are independent predictors of all-cause mortality in healthy elderly humans. Age (Dordr) 35(1):251-259. doi: 10.1007/s11357-011-9341- 2
13. Gress RE, Deeks SG (2009) Reduced thymus activity and infection prematurely age the immune system. J Clin Invest 119(10):2884-2887. doi: 10.1172/JCI40855
14. Hadrup SR, Strindhall J, Kollgaard T, Seremet T, Johansson B, Pawelec G, thor Straten P, Wikby A (2006) Longitudinal studies of clonally expanded CD8 T cells reveal a repertoire shrinkage predicting mortality and an increased number of dysfunctional cytomegalovirus-specific T cells in the very elderly. J Immunol 176(4):2645-2653
15. Iancu EM, Corthesy P, Baumgaertner P, Devevre E, Voelter V, Romero P, Speiser DE, Rufer N (2009) Clonotype selection and composition of human CD8 T cells specific for persistent herpes viruses varies with differentiation but is stable over time. J Immunol 183(1):319-331. doi: 10.4049/jimmunol.0803647
16. Kern F, Faulhaber N, Frommel C, Khatamzas E, Prosch S, Schonemann C, Kretzschmar I, Volkmer-Engert R, Volk HD, Reinke P (2000) Analysis of CD8 T cell reactivity to cytomegalovirus using protein-spanning pools of overlapping pentadecapeptides. Eur J Immunol 30(6):1676-1682. doi: 10.1002/1521-4141(200006) 30:6<1676::AID-IMMU1676>3.0.CO;2-V
17. Khan N, Shariff N, Cobbold M, Bruton R, Ainsworth JA, Sinclair AJ, Nayak L, Moss PA (2002) Cytomegalovirus seropositivity drives the CD8 T cell repertoire toward greater clonality in healthy elderly individuals. J Immunol 169(4):1984-1992
18. Khan N, Hislop A, Gudgeon N, Cobbold M, Khanna R, Nayak L, Rickinson AB, Moss PA (2004) Herpesvirus-specific CD8 T cell immunity in old age: cytomegalovirus impairs the response to a coresident EBV infection. J Immunol 173(12):7481-7489
19. Khan N, Best D, Bruton R, Nayak L, Rickinson AB, Moss PA (2007) T cell recognition patterns of immunodominant cytomegalovirus antigens in primary and persistent infection. J Immunol 178(7):4455-4465
20. Koch S, Larbi A, Ozcelik D, Solana R, Gouttefangeas C, Attig S, Wikby A, Strindhall J, Franceschi C, Pawelec G (2007) Cytomegalovirus infection: a driving force in human T cell immunosenescence. Ann N Y Acad Sci 1114:23-35. doi: 10.1196/annals.1396.043
21. Lachmann R, Bajwa M, Vita S, Smith H, Cheek E, Akbar A, Kern F (2012) Polyfunctional T cells accumulate in large human cytomegalovirus-specific T cell responses. J Virol 86(2):1001-1009
22. Lang A, Nikolich-Zugich J (2011) Functional CD8 T cell memory responding to persistent latent infection is maintained for life. J Immunol 187(7):3759-3768. doi: 10.4049/jimmunol.1100666
23. Lang A, Brien JD, Nikolich-Zugich J (2009) Inflation and long-term maintenance of CD8 T cells responding to a latent herpesvirus depend upon establishment of latency and presence of viral antigens. J Immunol 183(12):8077-8087. doi: 10.4049/jimmunol.0801117
24. Leng SX, Qu T, Semba RD, Li H, Yao X, Nilles T, Yang X, Manwani B, Walston JD, Ferrucci L, Fried LP, Margolick JB, Bream JH (2011) Relationship between cytomegalovirus (CMV) IgG serology, detectable CMV DNA in peripheral monocytes, and CMV pp 65(495-503)-specific CD8+ T cells in older adults. Age (Dordr) 33(4):607-614. doi: 10.1007/s11357-011-9205-9
25. Litjens NH, de Wit EA, Betjes MG (2011) Differential effects of age, cytomegalovirus-seropositivity and end-stage renal disease (ESRD) on circulating T lymphocyte subsets. Immun Ageing 8(1):2. doi: 10.1186/1742-4933-8-2
26. Looney RJ, Falsey A, Campbell D, Torres A, Kolassa J, Brower C, McCann R, Menegus M, McCormick K, Frampton M, Hall W, Abraham GN (1999) Role of cytomegalovirus in the T cell changes seen in elderly individuals. Clin Immunol 90(2):213-219. doi: 10.1006/clim.1998.4638
27. McElhaney JE, Effros RB (2009) Immunosenescence: what does it mean to health outcomes in older adults? Curr Opin Immunol 21(4):418-424. doi: 10.1016/j.coi.2009.05.023
28. Messaoudi I, Warner J, Fischer M, Park B, Hill B, Mattison J, Lane MA, Roth GS, Ingram DK, Picker LJ, Douek DC, Mori M, Nikolich-Zugich J (2006) Delay of T cell senescence by caloric restriction in aged long-lived nonhuman primates. Proc Natl Acad Sci U S A 103(51):19448-19453. doi: 10.1073/pnas.0606661103
29. Miles DJ, van der Sande M, Jeffries D, Kaye S, Ojuola O, Sanneh M, Cox M, Palmero MS, Touray ES, Waight P, Rowland-Jones S, Whittle H, Marchant A (2008) Maintenance of large subpopulations of differentiated CD8 T-cells two years after cytomegalovirus infection in Gambian infants. PLoS One 3(8):e2905. doi: 10.1371/journal.pone.0002905
30. Moss P (2010) The emerging role of cytomegalovirus in driving immune senescence: a novel therapeutic opportunity for improving health in the elderly. Curr Opin Immunol 22(4):529-534. doi: 10.1016/j.coi.2010.07.001
31. Natali A, Valcavi P, Medici MC, Dieci E, Montali S, Chezzi C (1997) Cytomegalovirus infection in an Italian population: antibody prevalence, virus excretion and maternal transmission. New Microbiol 20(2):123-133
32. Ouyang Q, Wagner WM, Zheng W, Wikby A, Remarque EJ, Pawelec G (2004) Dysfunctional CMV-specific CD8(+) T cells accumulate in the elderly. Exp Gerontol 39(4):607-613. doi: 10.1016/j.exger.2003.11.016
33. Pawelec G (2006) Immunity and ageing in man. Exp Gerontol 41(12):1239-1242. doi: 10.1016/j.exger.2006.09.005
34. Pawelec G, Koch S, Franceschi C, Wikby A (2006) Human immunosenescence: does it have an infectious component? Ann N Y Acad Sci 1067:56-65. doi: 10.1196/annals.1354.009
35. Pawelec G, Akbar A, Beverley P, Caruso C, Derhovanessian E, Fulop T, Griffiths P, Grubeck-Loebenstein B, Hamprecht K, Jahn G, Kern F, Koch SD, Larbi A, Maier AB, Macallan D, Moss P, Samson S, Strindhall J, Trannoy E, Wills M (2010) Immunosenescence and Cytomegalovirus: where do we stand after a decade? Immun Ageing 7:13. doi: 10.1186/1742-4933-7-13
36. Pignatelli S, Lazzarotto T, Gatto MR, Dal Monte P, Landini MP, Faldella G, Lanari M (2010) Cytomegalovirus gN genotypes distribution among congenitally infected newborns and their relationship with symptoms at birth and sequelae. Clin Infect Dis 51(1):33-41. doi: 10.1086/653423
37. Pita-Lopez ML, Gayoso I, DelaRosa O, Casado JG, Alonso C, Munoz-Gomariz E, Tarazona R, Solana R (2009) Effect of ageing on CMV-specific CD8 T cells from CMV seropositive healthy donors. Immun Ageing 6:11. doi: 10.1186/1742-4933-6-11
38. Pitcher CJ, Hagen SI, Walker JM, Lum R, Mitchell BL, Maino VC, Axthelm MK, Picker LJ (2002) Development and homeostasis of T cell memory in rhesus macaque. J Immunol 168(1):29-43
39. Sauce D, Larsen M, Fastenackels S, Duperrier A, Keller M, Grubeck-Loebenstein B, Ferrand C, Debre P, Sidi D, Appay V (2009) Evidence of premature immune aging in patients thymectomized during early childhood. J Clin Invest 119(10):3070-3078. doi: 10.1172/JCI39269
40. Snyder CM, Cho KS, Bonnett EL, van Dommelen S, Shellam GR, Hill AB (2008) Memory inflation during chronic viral infection is maintained by continuous production of short-lived, functional T cells. Immunity 29(4):650-659. doi: 10.1016/j.immuni.2008.07.017
41. Sylwester AW, Mitchell BL, Edgar JB, Taormina C, Pelte C, Ruchti F, Sleath PR, Grabstein KH, Hosken NA, Kern F, Nelson JA, Picker LJ (2005) Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J Exp Med 202(5):673-685. doi: 10.1084/jem.20050882
42. Turner JE, Aldred S, Witard OC, Drayson MT, Moss PM, Bosch JA (2010) Latent cytomegalovirus infection amplifies CD8 T-lymphocyte mobilisation and egress in response to exercise. Brain Behav Immun 24(8):1362-1370. doi: 10.1016/j.bbi.2010.07.239
43. van de Berg PJ, van Stijn A, Ten Berge IJ, van Lier RA (2008) A fingerprint left by cytomegalovirus infection in the human T cell compartment. J Clin Virol 41(3):213-217. doi: 10.1016/j.jcv.2007.10.016
44. van de Berg PJ, Griffiths SJ, Yong SL, Macaulay R, Bemelman FJ, Jackson S, Henson SM, ten Berge IJ, Akbar AN, van Lier RA (2010) Cytomegalovirus infection reduces telomere length of the circulating T cell pool. J Immunol 184(7):3417-3423. doi: 10.4049/jimmunol.0903442
45. Vescovini R, Telera A, Fagnoni FF, Biasini C, Medici MC, Valcavi P, di Pede P, Lucchini G, Zanlari L, Passeri G, Zanni F, Chezzi C, Franceschi C, Sansoni P (2004) Different contribution of EBV and CMV infections in very long-term carriers to age-related alterations of CD8+ T cells. Exp Gerontol 39(8):1233-1243. doi: 10.1016/j.exger.2004.04.004
46. Vescovini R, Biasini C, Fagnoni FF, Telera AR, Zanlari L, Pedrazzoni M, Bucci L, Monti D, Medici MC, Chezzi C, Franceschi C, Sansoni P (2007) Massive load of functional effector CD4+ and CD8+ T cells against cytomegalovirus in very old subjects. J Immunol 179(6):4283-4291
47. Vescovini R, Biasini C, Telera AR, Basaglia M, Stella A, Magalini F, Bucci L, Monti D, Lazzarotto T, Dal Monte P, Pedrazzoni M, Medici MC, Chezzi C, Franceschi C, Fagnoni FF, Sansoni P (2010) Intense antiextracellular adaptive immune response to human cytomegalovirus in very old subjects with impaired health and cognitive and functional status. J Immunol 184(6):3242-3249. doi: 10.4049/jimmunol.0902890
48. Vezys V, Masopust D, Kemball CC, Barber DL, O'Mara LA, Larsen CP, Pearson TC, Ahmed R, Lukacher AE (2006) Continuous recruitment of naive T cells contributes to heterogeneity of antiviral CD8 T cells during persistent infection. J Exp Med 203(10):2263-2269. doi: 10.1084/jem.20060995
49. Wallace DL, Masters JE, De Lara CM, Henson SM, Worth A, Zhang Y, Kumar SR, Beverley PC, Akbar AN, Macallan DC (2011) Human cytomegalovirus-specific CD8(+) T-cell expansions contain long-lived cells that retain functional capacity in both young and elderly subjects. Immunology 132(1):27-38. doi: 10.1111/j.1365-2567.2010.03334.x
50. Weinberger B, Lazuardi L, Weiskirchner I, Keller M, Neuner C, Fischer KH, Neuman B, Wurzner R, Grubeck-Loebenstein B (2007) Healthy aging and latent infection with CMV lead to distinct changes in CD8+ and CD4+ T-cell subsets in the elderly. Hum Immunol 68(2):86-90. doi: 10.1016/j.humimm.2006.10.019
51. Weng NP, Akbar AN, Goronzy J (2009) CD28(-) T cells: their role in the age-associated decline of immune function. Trends Immunol 30(7):306-312. doi: 10.1016/j.it.2009.03.013
52. Wikby A, Johansson B, Olsson J, Lofgren S, Nilsson BO, Ferguson F (2002) Expansions of peripheral blood CD8 T-lymphocyte subpopulations and an association with cytomegalovirus seropositivity in the elderly: the Swedish NONA immune study. Exp Gerontol 37(2-3):445-453