Cytomegalovirus and human immunosenescence

Reviews in Medical Virology

Volumn 19, Issue 1, 2009, Pages 47-56

  Pawelec, Graham ^a,c   Derhovanessian, Evelyna ^a   Larbi, Anis ^a   Strindhall, Jan ^b   Wikby, Anders ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b JÖNKÖPING UNIVERSITY   (Sweden)

^c ZMF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; AGING; BONE; BRAIN; CD4 CD8 RATIO; CELLULAR IMMUNITY; CROSS-SECTIONAL STUDY; CYTOMEGALOVIRUS INFECTION; ENDOCRINE SYSTEM; HEART; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENCE; IMMUNOSENESCENCE; IMMUNOSURVEILLANCE; INCIDENCE; LONGITUDINAL STUDY; LYMPH NODE; LYMPHOCYTE DIFFERENTIATION; MORBIDITY; MORTALITY; PREDICTION; PREVALENCE; REVIEW; SENESCENCE; SKELETAL MUSCLE; T LYMPHOCYTE; VIRUS IMMUNITY; VIRUS REACTIVATION; AGED; ANIMAL; CYTOMEGALOVIRUS; IMMUNITY; IMMUNOLOGY; PHYSIOLOGY;

AGED; AGED, 80 AND OVER; AGING; ANIMALS; CROSS-SECTIONAL STUDIES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; HUMANS; IMMUNITY; LONGITUDINAL STUDIES;

EID: 60549096353     PISSN: 10529276     EISSN: None     Source Type: Journal    
DOI: 10.1002/rmv.598     Document Type: Review

References (79)

1. Fagnoni FF, Vescovini R, Passeri G, et al. Shortage of circulating naive CD8(+) T cells provides new insights on immunodeficiency in aging. Blood 2000; 95: 2860-2868.
2. Lazuardi L, Jenewein B, Wolf AM, et al. Age-related loss of naive T cells and dysregulation of T-cell/B-cell interactions in human lymph nodes. Immunology 2005; 114: 37-43.
3. Naylor K, Li G, Vallejo AN, et al. The influence of age on T cell generation and TCR diversity. J Immunol 2005; 174: 7446-7452.
4. Hadrup SR, Strindhall J, Kollgaard T, et al. 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 2006; 176: 2645-2653.
5. Zinkernagel RM, Moskophidis D, Kundig T, et al. Effector T-cell induction and T-cell memory versus peripheral deletion of T cells. Immunol Rev 1993; 133: 199-223.
6. Solana R, Pawelec G, Tarazona R. Aging and innate immunity. Immunity 2006; 24: 491-494.
7. Weksler ME, Goodhardt M, Szabo P. The effect of age on B cell development and humoral immunity. Springer Semin Immunopathol 2002; 24: 35-52.
8. Ogata K, An E, Shioi Y, et al. Association between natural killer cell activity and infection in immunologically normal elderly people. Clin Exp Immunol 2001; 124: 392-397.
9. Franceschi C, Capri M, Monti D, et al. Inflammaging and anti-inflammaging: A systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev 2007; 128: 92-105.
10. Kovaiou RD, Herndler-Brandstetter D, Grubeck-Loebenstein B. Age-related changes in immunity: Implications for vaccination in the elderly. Expert Rev Mol Med 2007; 9: 1-17.
11. Khan N, Shariff N, Cobbold M, et al. Cytomegalovirus seropositivity drives the CD8 T cell repertoire toward greater clonality in healthy elderly individuals. J Immunol 2002; 169: 1984-1992.
12. Looney RJ, Falsey A, Campbell D, et al. Role of cytomegalovirus in the T cell changes seen in elderly individuals. Clin Immunol 1999; 90: 213-219.
13. Ouyang Q, Wagner WM, Wikby A, et al. Large numbers of dysfunctional CD8+ T lymphocytes bearing receptors for a single dominant CMV epitope in the very old. J Clin Immunol 2003; 23: 247-257.
14. Pawelec G, Akbar A, Caruso C, et al. Human immunosenescence: is it infectious? Immunol Rev 2005; 205: 257-268.
15. Northfield J, Lucas M, Jones H, et al. Does memory improve with age? CD85j (ILT-2/LIR-1) expression on CD8 T cells correlates with 'memory inflation' in human cytomegalovirus infection. Immunol Cell Biol 2005; 83: 182-188.
16. Pourgheysari B, Khan N, Best D, et al. The cytomegalovirus-specific CD4+ T-cell response expands with age and markedly alters the CD4+ T-cell repertoire. J Virol 2007; 81: 7759-7765.
17. Marshall GS, Stout GG. Cytomegalovirus seroprevalence among women of childbearing age during a 10-year period. Am J Perinatol 2005; 22: 371-376.
18. Colugnati FA, Staras SA, Dollard SC, et al. Incidence of cytomegalovirus infection among the general population and pregnant women in the United States. BMC Infect Dis 2007; 7: 71.
19. Sheevani, Jindal N, Aggarwal A. A pilot seroepidemiological study of cytomegalovirus infection in women of child bearing age. Indian J Med Microbiol 2005; 23: 34-36.
20. Ataman S, Colak D, Gunseren F, et al. Investigation of cytomegalovirus seroepidemiology in Antalya with a population-based cross-sectional study and review of related data in Turkey. Mikrobiyol Bul 2007; 41: 545-555.
21. Staras SA, Dollard SC, Radford KW, et al. Seroprevalence of cytomegalovirus infection in the United States, 1988-1994. Clin Infect Dis 2006; 43: 1143-1151.
22. Hecker M, Qiu D, Marquardt K, et al. Continuous cytomegalovirus seroconversion in a large group of healthy blood donors. Vox Sang 2004; 86: 41-44.
23. Assy N, Gefen H, Schlesinger S, et al. Reactivation versus primary CMV infection after splenectomy in immunocompetent patients. Dig Dis Sci 2007; 52: 3477-3479.
24. Lang KS, Moris A, Gouttefangeas C, et al. High frequency of human cytomegalovirus (HCMV)-specific CD8+ T cells detected in a healthy CMV-seropositive donor. Cell Mol Life Sci 2002; 59: 1076-080.
25. Just-Nubling G, Korn S, Ludwig B, et al. Primary cytomegalovirus infection in an outpatient setting-laboratory markers and clinical aspects. Infection 2003; 31: 318-323.
26. Wreghitt TG, Teare EL, Sule O, et al. Cytomegalovirus infection in immunocompetent patients. Clin Infect Dis 2003; 37: 1603-1606.
27. Rafailidis PI, Mourtzoukou EG, Varbobitis IC, et al. Severe cytomegalovirus infection in apparently immunocompetent patients: a systematic review. Virol J 2008; 5: 47.
28. Limaye AP, Kirby KA, Rubenfeld GD, et al. Cytomegalovirus reactivation in critically ill immunocompetent patients. JAMA 2008; 300: 413-422.
29. Carter D, Olchovsky D, Pokroy R, et al. Cytomegalovirus-associated colitis causing diarrhea in an immunocompetent patient. World J Gastroenterol 2006; 12: 6898-6899.
30. Galiatsatos P, Shrier I, Lamoureux E, et al. Metaanalysis of outcome of cytomegalovirus colitis in immunocompetent hosts. Dig Dis Sci 2005; 50: 609-616.
31. Stowe RP, Kozlova EV, Yetman DL, et al. Chronic herpesvirus reactivation occurs in aging. Exp Gerontol 2007; 42: 563-570.
32. Musiani M, Zerbini M, Zauli D, et al. Impairment of cytomegalovirus and host balance in elderly subjects. J Clin Pathol 1988; 41: 722-725.
33. Stowe RP, Mehta SK, Ferrando AA, et al. Immune responses and latent herpesvirus reactivation in spaceflight. Aviat Space Environ Med 2001; 72: 884-891.
34. Capri M, Salvioli S, Sevini F, et al. The genetics of human longevity. Ann NY Acad Sci 2006; 1067: 252-263.
35. Schmaltz HN, Fried LP, Xue QL, et al. Chronic cytomegalovirus infection and inflammation are associated with prevalent frailty in communitydwelling older women. J Am Geriatr Soc 2005; 53: 747-754.
36. Barton ES, White DW, Cathelyn JS, et al. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 2007; 447: 326-329.
37. Aiello AE, Haan MN, Pierce CM, et al. Persistent infection, inflammation, and functional impairment in older Latinos. J Gerontol A Biol Sci Med Sci 2008; 63: 610-618.
38. Looney RJ, Falsey A, Campbell D, et al. Role of cytomegalovirus in the T cell changes seen in elderly individuals. Clin Immunol 1999; 90: 213-219.
39. Posnett DN, Sinha R, Kabak S, et al. Clonal populations of T cells in normal elderly humans: the T cell equivalent to "benign monoclonal gammapathy". J Exp Med 1994; 179: 609-618.
40. Olsson J, Wikby A, Johansson B, et al. Age-related change in peripheral blood T-lymphocyte subpopulations and cytomegalovirus infection in the very old: the Swedish longitudinal OCTO immune study. Mech Ageing Dev 2000; 121: 187-201.
41. Remarque E, Pawelec G. T-cell immunosenescence and its clinical relevance in man. Rev Clin Gerontol 1998; 8: 5-14.
42. Koch S, Larbi A, Derhovanessian E, et al. Multiparameter flow cytometric analysis of CD4 and CD8 T cell subsets in young and old people. Immun Ageing 2008; 5: 6.
43. Lanzavecchia A, Sallusto F. Understanding the generation and function of memory T cell subsets. Curr Opin Immunol 2005; 17: 326-332.
44. Rufer N, Dragowska W, Thornbury G, et al. Telomere length dynamics in human lymphocyte subpopulations measured by flow cytometry. Nat Biotechnol 1998; 16: 743-747.
45. Weng NP, Palmer LD, Levine BL, et al. Tales of tails: Regulation of telomere length and telomerase activity during lymphocyte development, differentiation, activation, and aging. Immunol Rev 1997; 160: 43-54.
46. Romero P, Zippelius A, Kurth I, et al. Four functionally distinct populations of human effector-memory CD8+ T lymphocytes. J Immunol 2007; 178: 4112-4119.
47. Effros RB, Pawelec G. Replicative senescence of T cells: does the Hayflick Limit lead to immune exhaustion? Immunol Today 1997; 18: 450-454.
48. Pawelec G, Sansom D, Rehbein A, et al. Decreased proliferative capacity and increased susceptibility to activation-induced cell death in late-passage human CD4+ TCR2+ cultured T cell clones. Exp Gerontol 1996; 31: 655-668.
49. Spaulding C, Guo W, Effros RB. Resistance to apoptosis in human CD8+ T cells that reach replicative senescence after multiple rounds of antigen-specific proliferation. Exp Gerontol 1999; 34: 633-644.
50. Wikby A, Johansson B, Ferguson F, et al. Age-related changes in immune parameters in a very old population of Swedish people: A longitudinal study. Exp Gerontol 1994; 29: 531-541.
51. Pawelec G, Ferguson FG, Wikby A. The SENIEUR protocol after 16 years. Mech Ageing Dev 2001; 122: 132-134.
52. Pawelec G, Ouyang Q, Colonna-Romano G, et al. Is human immunosenescence clinically relevant? Looking for 'immunological risk phenotypes'. Trends Immunol 2002; 23: 330-332.
53. Nilsson BO, Ernerudh J, Johansson B, et al. Morbidity does not influence the T-cell immune risk phenotype in the elderly: Findings in the Swedish NONA Immune Study using sample selection protocols. Mech Ageing Dev 2003; 124: 469-476.
54. Strindhall J, Nilsson BO, Lofgren S, et al. No Immune Risk Profile among individuals who reach 100 years of age: Findings from the Swedish NONA immune longitudinal study. Exp Gerontol 2007; 42: 753-761.
55. Wikby A, Mansson IA, Johansson B, et al. The immune risk profile is associated with age and gender: Findings from three Swedish population studies of individuals 20-100 years of age. Biogerontology 2008; 9: 299-308.
56. Huppert FA, Pinto EM, Morgan K, et al. Survival in a population sample is predicted by proportions of lymphocyte subsets. Mech Ageing Dev 2003; 124: 449-451.
57. Peres A, Bauer M, da Cruz IB, et al. Immunophenotyping and T-cell proliferative capacity in a healthy aged population. Biogerontology 2003; 4: 289-296.
58. Komatsu H, Inui A, Sogo T, et al. Large scale analysis of pediatric antiviral CD8+ T cell populations reveals sustained, functional and mature responses. Immun Ageing 2006; 3: 11.
59. Miles DJ, van der Sande M, Jeffries D, et al. Maintenance of large subpopulations of differentiated CD8 T-cells two years after cytomegalovirus infection in Gambian infants. PLoS ONE. 2008; 3: e2905.
60. Messaoudi I, Lemaoult J, Guevara-Patino JA, et al. Age-related CD8 T cell clonal expansions constrict CD8 T cell repertoire and have the potential to impair immune defense. J Exp Med 2004; 200: 1347-1358.
61. Koch S, Solana R, Dela Rosa O, et al. Human cytomegalovirus infection and T cell immunosenescence: A mini review. Mech Ageing Dev 2006; 127: 538-543.
62. Ouyang Q, Wagner WM, Voehringer D, et al. Age-associated accumulation of CMV-specific CD8+ T cells expressing the inhibitory killer cell lectin-like receptor G1 (KLRG1). Exp Gerontol 2003; 38: 911-920.
63. Almanzar G, Schwaiger S, Jenewein B, et al. Longterm 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 2005; 79: 3675-3683.
64. Benedict CA, Loewendorf A, Garcia Z, et al. Dendritic cell programming by cytomegalovirus stunts naive T cell responses via the PD-L1/PD-1 pathway. J Immunol 2008; 180: 4836-4847.
65. Varani S, Cederarv M, Feld S, et al. Human cytomegalovirus differentially controls B cell and T cell responses through effects on plasmacytoid dendritic cells. J Immunol 2007; 179: 7767-7776.
66. Tabata T, Kawakatsu H, Maidji E, et al. Induction of an epithelial integrin alphavbeta6 in human cytomegalovirus-infected endothelial cells leads to activation of transforming growth factor-beta1 and increased collagen production. Am J Pathol 2008; 172: 1127-1140.
67. Ouyang Q, Wagner WM, Walter S, et al. An age-related increase in the number of CD8+ T cells carrying receptors for an immunodominant Epstein-Barr virus (EBV) epitope is counteracted by a decreased frequency of their antigen-specific responsiveness. Mech Ageing Dev 2003; 124: 477-485.
68. Vescovini R, Telera A, Fagnoni FF, et al. Different contribution of EBV and CMV infections in very long-term carriers to age-related alterations of CD8+ T cells. Exp Gerontol 2004; 39: 1233-1243.
69. Khan N, Hislop A, Gudgeon N, et al. Herpesvirus-specific CD8 T cell immunity in old age: Cytomegalovirus impairs the response to a coresident EBV infection. J Immunol 2004; 173: 7481-7489.
70. Lang A, Brien JD, Messaoudi I, et al. Age-related dysregulation of CD8+ T cell memory specific for a persistent virus is independent of viral replication. J Immunol 2008; 180: 4848-4857.
71. Nikolich-Zugich J. Ageing and life-long maintenance of T-cell subsets in the face of latent persistent infections. Nat Rev Immunol 2008; 8: 512-522.
72. Barber DL, Wherry EJ, Masopust D, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006; 439: 682-687.
73. Jimenez M, Martinez C, Ercilla G, et al. Clinical factors influencing T-cell receptor excision circle (TRECs) counts following allogeneic stem cell transplantation in adults. Transpl Immunol 2006; 16: 52-59.
74. Trzonkowski P, Mysliwska J, Szmit E, et al. Association between cytomegalovirus infection, enhanced proinflammatory response and low level of anti-hemagglutinins during the anti-influenza vaccination-an impact of immunosenescence. Vaccine 2003; 21: 3826-3836.
75. Trzonkowski P, Mysliwska J, Pawelec G, et al. From bench to bedside and back: The SENIEUR Protocol and the efficacy of influenza vaccination in the elderly. Biogerontology 2008; [E-pub ahead of print]
76. Qin W, Jiang J, Chen Q, et al. CpG ODN enhances immunization effects of hepatitis B vaccine in aged mice. Cell Mol Immunol 2004; 1:148-152.
77. Blank C, Mackensen A. Contribution of the PD-L1/PD-1 pathway to T-cell exhaustion: an update on implications for chronic infections and tumor evasion. Cancer Immunol Immunother 2007; 56: 739-745.
78. Provinciali M, Di Stefano G, Colombo M, et al. Adjuvant effect of low-dose interleukin-2 on antibody response to influenza virus vaccination in healthy elderly subjects. Mech Ageing Dev 1994; 77: 75-82.
79. Ben-Yehuda A, Joseph A, Barenholz Y, et al. Immunogenicity and safety of a novel IL-2-supplemented liposomal influenza vaccine (INFLUSOME-VAC) in nursing-home residents. Vaccine 2003; 21: 3169-3178.