The immune system and aging: A review

Gynecological Endocrinology

Volumn 30, Issue 1, 2014, Pages 16-22

  Castelo Branco, Camil ^a   Soveral, Iris ^b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b HOSPITAL CLÍNIC   (Spain)

Author keywords

Aging; Immune system; Immunosenescence; Innate and adaptive responses

Indexed keywords

ADAPTIVE IMMUNITY; AGING; AUTOIMMUNITY; B LYMPHOCYTE; DENDRITIC CELL; ENDOCRINE SYSTEM; HUMAN; IMMUNE DEFICIENCY; IMMUNE DYSREGULATION; IMMUNE RESPONSE; IMMUNE SYSTEM; INFLAMMATION; INNATE IMMUNITY; LYMPHOID PROGENITOR CELL; MACROPHAGE; MUCOSA; NATURAL KILLER CELL; NEUTROPHIL; PRIORITY JOURNAL; REVIEW; SENESCENCE; SKIN; SYSTEMATIC REVIEW; T LYMPHOCYTE;

ADAPTIVE IMMUNITY; AGING; ANIMALS; AUTOIMMUNITY; CELL AGING; ENDOCRINE SYSTEM; HUMANS; IMMUNE SYSTEM; IMMUNITY, INNATE; IMMUNOLOGIC DEFICIENCY SYNDROMES; INFLAMMATION;

EID: 84890501668     PISSN: 09513590     EISSN: 14730766     Source Type: Journal    
DOI: 10.3109/09513590.2013.852531     Document Type: Review

References (98)

1. Derhovanessian E, Solana R, Larbi A, Paweler G. Immunity, ageing and cancer. Immun Ageing 2008;5:11.
2. Tonet AC, Nóbrega OT. Immunosenescence: the association between leukocytes, cytokines and chronic diseases. Rev Brás Geriatr Gerontol 2008;11:259-73.
3. Krabbe KS, Pedersen M, Brunsgaard H. Inflammatory mediators in the elderly. Exp Gerontol 2004;39:687-99.
4. Pawelec G. Immunosenescence: impact in the young as well as the old? Mech Ageing Dev 1999;108:1.
5. Targonski PV, Jacobson RM, Poland GA. Immunosenescence: role and measurement in influenza vaccine response among the elderly. Vaccine 2007;25:3066.
6. Franceschi C, Bonafe M, Valensin S. Human immunosenescence: the prevailing of innate immunity, the failing of clonotypic immunity, and the filling of immunological space. Vaccine 2000; 18: 1717.
7. Fenske NA, Conard CB. Aging skin. Am Fam Physician. 1988;37: 219-30.
8. Kurban RS, Bhawan J. Histologic changes in skin associated with aging. J Dermatol Surg Oncol 1990;16:908-14.
9. Kottner J, Lichterfeld A, Blume-Peytavi U. Maintaining Skin Integrity in the Aged: A Systematic Review. Br J Dermatol 2013;169:528-42.
10. Grewe M. Chronological ageing and photoageing of dendritic cells. Clin Exp Dermatol 2001;26:608-12.
11. Jorissen M, Willems T, Van der Schueren B. Nasal ciliary beat frequency is age independent. Laryngoscope 1998;108:1042-7.
12. Kim SW, Mo JH, Kim JW, et al. Change of nasal function with aging in Korean. Acta Otolaryngol Suppl 2007;(558):90-4.
13. Jafarzadeh A, Sadeghi M, Karam GA, Vazirinejad R. Salivary IgA and IgE levels in healthy subjects: relation to age and gender. Braz Oral Res 2010;24:21-7.
14. Agrawal A, Gupta S. Impact of aging on dendritic cell functions in humans. Ageing Res Rev 2011;10:336-45.
15. Jing Y, Shaheen E, Drake RR, et al. Aging is associated with a numerical and functional decline in plasmacytoid dendritic cells, whereas myeloid dendritic cells are relatively unaltered in human peripheral blood. Human Immunol 2009;70:777-84.
16. Wong C, Goldstein DR. Impact of aging on antigen presentation cell function of dendritic cells. Curr Opin Immunol 2013;25:535-41.
17. Kumar H, Kawai T, Akira S. Pathogen recognition in the innate immune response. Biochem J 2009;420:1-16.
18. Panda A, Qian F, Mohanty S, et al. Age-associated decrease in TLR function in primary human dendritic cells predicts influenza vaccine response. J Immunol 2010;184:2518-27.
19. Agrawal A, Agrawal S, Cao JN, et al. Altered innate immune functioning of dendritic cells in elderly humans: a role of phosphoinositide 3-kinase-signaling pathway. J Immunol 2007; 178:6912-22.
20. Moretto MM, Lawlor EM, Khan IA. Aging mice exhibit a functional defect in mucosal dendritic cell response against an intracellular pathogen. J Immunol 2008;181:7977-84.
21. Stout-Delgado HW, Yang X, Walker WE, et al. Aging impairs IFN regulatory factor 7 up-regulation in plasmacytoid dendritic cells during TLR9 activation. J Immunol 2008;181:6747-56.
22. Camous X, Pera A, Solana R, Larbi A. NK cells in healthy aging and age-associated diseases. J Biomed Biotechnol 2012; 2012:195956.
23. Hazeldine J, Lord JM. The impact of ageing on natural killer cell function and potential consequences for health in older adults. Ageing Res Rev 2013. [Epub ahead of print].
24. Fauriat C, Long EO, Ljunggren HG, Bryceson YT. Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood 2010;115:2167-76.
25. Facchini A, Mariani E, Mariani AR, et al. Increased number of circulating Leu 11+ (CD 16) large granular lymphocytes and decreased NK activity during human ageing. Clin Exp Immunol 1987;68:340-7.
26. Borrego F, Alonso MC, Galiani MD, et al. NK phenotypic markers and IL2 response in NK cells from elderly people. Experimental Gerontology 1999;34:253-65.
27. Hazeldine J, Hampson P, Lord JM. Reduced release and binding of perforin at the immunological synapse underlies the age-related decline in natural killer cell cytotoxicity. Aging Cell 2012;11:751-9.
28. Beli E, Clinthorne JF, Duriancik DM, et al. Natural killer cell function is altered during the primary response of aged mice to influenza infection. Mech Ageing Dev 2011;132:503-10.
29. Fang M, Roscoe F, Sigal LJ. Age-dependent susceptibility to a viral disease due to decreased natural killer cell numbers and trafficking. J Exp Med 2010;207:2369-81.
30. Hayhoe RP, Henson SM, Akbar AN, Palmer DB. Variation of human natural killer cell phenotypes with age: identification of a unique KLRG1-negative subset. Hum Immunol 2010;71:676-81.
31. Mariani E, Meneghetti A, Neri S, et al. Chemokine production by natural killer cells from nonagenarians. Eur J Immunol 2002;32: 1524-9.
32. Borregaard N. Neutrophils, from marrow to microbes. Immunity 2010;33:657-70.
33. Panda A, Arjona A, Sapey E, et al. Human innate immunosenescence: causes and consequences for immunity in old age. Trends Immunol 2009;30:325-33.
34. Chatta GS, Andrews RG, Rodger E, et al. Hematopoietic progenitors and aging: alterations in granulocytic precursors and responsiveness to recombinant human G-CSF, GM-CSF, and IL-3. J Gerontol 1993; 48:M207.
35. Fortin CF, Larbi A, Dupuis G, et al. GM-CSF activates the Jak/ STAT pathway to rescue polymorphonuclear neutrophils from spontaneous apoptosis in young but not elderly individuals. Biogerontology. 2007;8:173-87.
36. Wenisch C, Patruta S, Daxböck F, et al. Effect of age on human neutrophil function. J Leukoc Biol 2000;67:40-5.
37. Fortin CF, Larbi A, Lesur O, et al. Impairment of SHP-1 downregulation in the lipid rafts of human neutrophils under GMCSF stimulation contributes to their age-related, altered functions. J Leukoc Biol 2006;79:1061-72.
38. Weiskopf D, Weinberger B, Grubeck-Loebenstein B. The aging of the immune system. Transpl Int 2009;22:1041-50.
39. Emanuelli G, Lanzio M, Anfossi T, et al. Influence of age on polymorphonuclear leukocytes in vitro: phagocytic activity in healthy human subjects. Gerontology 1986;32:308.
40. Butcher SK, Chahal H, Nayak L, et al. Senescence in innate immune responses: reduced neutrophil phagocytic capacity and CD16 expression in elderly humans. J Leukoc Biol 2001;70:881.
41. Fulop Jr T, Foris G, Worum I, Leovey A. Age-dependent alterations of Fc gamma receptor-mediated effector functions of human polymorphonuclear leucocytes. Clin Exp Immunol 1985;61:425.
42. Simell B, Vuorela A, Ekström N, et al. Aging reduces the functionality of anti-pneumococcal antibodies and the killing of Streptococcus pneumoniae by neutrophil phagocytosis. Vaccine 2011;29:1929-34.
43. Fortin CF, McDonald PP, Lesur O, Fulop Jr T. Aging and neutrophils: there is still much to do. Rejuvenation Res 2008;11: 873-82.
44. Solana R, Tarazona R, Gayoso I, et al. Innate immunosenescence: effect of aging on cells and receptors of the innate immune system in humans. Semin Immunol 2012;24:331-41.
45. van Duin D, Mohanty S, Thomas V, et al. Age-associated defect in human TLR-1/2 function. J Immunol 2007;178:970-5.
46. van Duin D, Allore HG, Mohanty S, et al. Prevaccine determination of the expression of costimulatory B7 molecules in activated monocytes predicts influenza vaccine responses in young and older adults. J Infect Dis 2007;195:1590-7.
47. Villanueva JL, Solana R, Alonso MC, Peña J. Changes in the expression of HLA-class II antigens on peripheral blood monocytes from aged humans. Dis Markers 1990;8:85-91.
48. Herrero C, Sebastián C, Marqués L, et al. Immunosenescence of macrophages: reduced MHC class II gene expression. Exp Gerontol 2002;37:389.
49. Izgüt-Uysal VN, Ozkaya YG, Ozdemir S, et al. Effect of L-arginine on age-related changes in macrophage phagocytic activity. Immunol Invest 2004;33:287-93.
50. Swift ME, Burns AL, Gray KL, DiPietro LA. Age-related alterations in the inflammatory response to dermal injury. J Invest Dermatol 2001;117:1027-35.
51. Davila DR, Edwards III CK, Arkins S, et al. Interferon-g-induced priming for secretion of superoxide anion and tumor-necrosis factor-a declines in macrophages from aged rats. FASEB J 1990; 4:2906-11.
52. Lansdorp PM, Dragowska W, Thomas TE, et al. Age-related decline in proliferative potential of purified stem cell candidates. Blood Cells 1994;20:376.
53. Beerman I, Bhattacharya D, Zandi S, et al. Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion. Proc Natl Acad Sci USA 2010;107:5465-70.
54. Cho RH, Sieburg HB, Muller-Sieburg CE. A new mechanism for the aging of hematopoietic stem cells: aging changes the clonal composition of the stem cell compartment but not individual stem cells. Blood 2008;111:5553-61.
55. Vaziri H, Dragowska W, Allsopp RC, et al. Evidence for a mitotic clock in human hematopoietic stem cells: loss of telomeric DNA with age. Proc Natl Acad Sci USA 1994;91:9857.
56. Ji H, Ehrlich LI, Seita J, et al. Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature 2010; 467:338-42.
57. Chambers SM, Shaw CA, Gatza C, et al. Aging hematopoietic stem cells decline in function and exhibit epigenetic dysregulation. PLoS Biol 2007;5:e201.
58. Kogut I, Scholz JL, Cancro MP, Cambier JC. B cell maintenance and function in aging. Semin Immunol 2012;24:342-9.
59. Challen GA, Boles NC, Chambers SM, Goodell MA. Distinct hematopoietic stem cell subtypes are differentially regulated by TGF-beta1. Cell Stem Cell 2010;6:265-78.
60. Gibson KL, Wu YC, Barnett Y, et al. B-cell diversity decreases in old age and is correlated with poor health status. Aging Cell 2009;8: 18-25.
61. MacLennan IC. Germinal centers. Annu Rev Immunol 1994;12: 117-39.
62. Chong Y, Ikematsu H, Yamaji K, et al. CD27(+) (memory) B cell decrease and apoptosis-resistant CD27(-) (naive) B cell increase in aged humans: implications for age-related peripheral B cell developmental disturbances. Int Immunol 2005;17:383-90.
63. Ademokun A, Wu YC, Dunn-Walters D. The ageing B cell population: composition and function. Biogerontology. 2010;11: 125-37.
64. Johnson SA, Rozzo SJ, Cambier JC. Aging-dependent exclusion of antigen-inexperienced cells from the peripheral B cell repertoire. J Immunol 2002;168:5014-5023.
65. + B-cell population is important for the development of autoimmunity. Blood 2011;118: 1305-15.
66. Sasaki S, Sullivan M, Narvaez CF, et al. Limited efficacy of inactivated influenza vaccine in elderly individuals is associated with decreased production of vaccine-specific antibodies. J Clin Invest 2011;121:3109-19.
67. Dunn-Walters DK, Banerjee M, Mehr R. Effects of age on antibody affinity maturation. Biochem Soc Trans 2003;31:447-8.
68. Roukens AH, Soonawala D, Joosten SA, et al. Elderly subjects have a delayed antibody response and prolonged viraemia following yellow fever vaccination: a prospective controlled cohort study. PLoS One 2011;6:e27753.
69. Nagele EP, Han M, Acharya NK, et al. Natural IgG autoantibodies are abundant and ubiquitous in human sera, and their number is influenced by age, gender, and disease. PLoS One 2013;8:e60726.
70. Schenkein JG, Park S, Nahm MH. Pneumococcal vaccination in older adults induces antibodies with low opsonic capacity and reduced antibody potency. Vaccine 2008;26:5521-6.
71. 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.
72. Moro-García MA, Alonso-Arias R, López-Larrea C. Molecular mechanisms involved in the aging of the T-cell immune response. Curr Genomics 2012;13:589-602.
73. Hazenberg MD, Verschuren MC, Hamann D, et al. T cell receptor excision circles as markers for recent thymic emigrants: basic aspects, technical approach, and guidelines for interpretation. J Mol Med 2001;79:631-40.
74. Douek DC, McFarland RD, Keiser PH, et al. Changes in thymic function with age and during the treatment of HIV infection. Nature 1998;396:690-5.
75. Ferrando-Martínez S. Thymopoiesis in elderly human is associated with systemic inflammatoruy status. Age 2009;31:87-97.
76. Gupta S, Bi R, Su K, et al. Characterization of naïve, memory and effector CD8+ T cells: effect of age. Exp Gerontol 2004;39:545-50.
77. Ferrando-Martínez S, Ruiz-Mateos E, Hernández A, et al. Age-related deregulation of naive T cell homeostasis in elderly humans. Age 2011;33:197-207.
78. Fagnoni FF, Vescovini R, Passeri G, et al. Shortage of circulating naive CD8(+) T cells provides new insights on immunodeficiency in aging. Blood 2000;95:2860-8.
79. Finney HM, Akbar AN, Lawson AD. Activation of resting human primary T cells with chimeric receptors: costimulation from CD28, inducible costimulator, CD134, and CD137 in series with signals from the TCR zeta chain. J Immunol 2004;172:104-13.
80. Vallejo AN. CD28 extinction in human T cells: altered functions and the program of T-cell senescence. Immunol Rev 2005;205:158-69.
81. Sansoni P, Fagnoni F, Vescovini R, et al. T lymphocyte proliferative capability to defined stimuli and costimulatory CD28 pathway is not impaired in healthy centenarians. Mech. Ageing Dev 1997;96: 127-36.
82. Weyand CM, Brandes JC, Schmidt D, et al. Functional properties of CD4+ CD28- T cells in the aging immune system. Mech Ageing Dev 1998;102:131-47.
83. Nociari MM, Telford W, Russo C. Postthymic development of CD28-CD8+ T cell subset: age-associated expansion and shift from memory to naive phenotype. J Immunol 1999;162:3327-35.
84. Vallejo AN, Schirmer M, Weyand CM, Goronzy JJ. Clonality and longevity of CD4+CD28null T cells are associated with defects in apoptotic pathways. J Immunol 2000;165:6301-7.
85. Valenzuela HF, Effros RB. Divergent telomerase and CD28 expression patterns in human CD4 and CD8 T cells following repeated encounters with the same antigenic stimulus. Clin Immunol 2002;105:117-25.
86. Abedin S, Michel JJ, Lemster B, Vallejo AN. Diversity of NKR expression in aging T cells and in T cells of the aged: the new frontier into the exploration of protective immunity in the elderly. Exp Gerontol 2005;40:537-48.
87. Fagnoni FF, Vescovini R, Mazzola M, et al. Expansion of cytotoxic CD8+ CD28- T cells in healthy ageing people, including centenarians. Immunology 1996;88:501-7.
88. Moro-García MA, Alonso-Arias R, López-Larrea C. When aging reaches CD4+ T-cells: phenotypic and functional changes. Front Immunol 2013;4:107.
89. Brown DM, Lee S, Garcia-Hernandez ML, Swain SL. Multifunctional CD4 cells expressing gamma interferon and perforin mediate protection against lethal influenza virus infection. J Virol 2012;86:6792-803.
90. Tarazona R, DelaRosa O, Alonso C, et al. Increased expression of NK cell markers on T lymphocytes in aging and chronic activation of the immune system reflects the accumulation of effector/ senescent T cells. Mech Ageing Dev 2000;121:77-88.
91. Sansoni P, Vescovini R, Fagnoni F, et al. The immune system in extreme longevity. Exp Gerontol 2008;43:61-5.
92. 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.
93. Franceschi C, Bonafè M, Valensin S, et al. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann NY Acad Sci 2000;908:244-54.
94. Bruunsgaard H, Andersen-Ranberg K, Jeune B, et al. A high plasma concentration of TNF-alpha is associated with dementia in centenarians. J Gerontol 1999;54A:M357-64.
95. Griffin WS. Inflammation and neurodegenerative diseases. Am J Clin Nutr 2006;83:470S-4S.
96. Pradhan AD, Manson JE, Rifai N, et al. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 2000;286:327-34.
97. Lio D, Candore G, Crivello A, et al. Opposite effects of interleukin 10 common gene polymorphisms in cardiovascular diseases and in successful ageing: genetic background of male centenarians is protective against coronary heart disease. J Med Genet 2004;41: 790-4.
98. Gavazzi G, Herrmann F, Krause KH. Aging and infectious diseases in the developing world. Clin Infect Dis 2004;39:83-91.