An evolutionary perspective on the mechanisms of immunosenescence

Trends in Immunology

Volumn 30, Issue 7, 2009, Pages 374-381

  Shanley, Daryl P ^a   Aw, Danielle ^b   Manley, Nancy R ^c   Palmer, Donald B ^b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b Development Group   (United Kingdom)

^c University of Georgia ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; CELL AGING; EVOLUTION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOSENESCENCE; INFLAMMATION; LIFE HISTORY; NONHUMAN; PHENOTYPE; REVIEW; SENESCENCE; TH1 CELL; TH2 CELL; THYMUS ATROPHY; THYMUS FUNCTION;

AGING; ANIMALS; EVOLUTION; HUMANS; IMMUNITY, INNATE; REPRODUCTION; T-LYMPHOCYTE SUBSETS; THYMUS GLAND;

EID: 67649410701     PISSN: 14714906     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.it.2009.05.001     Document Type: Review

References (114)

1. Aw D., et al. Immunosenescence: emerging challenges for an ageing population. Immunology 120 (2007) 435-446
2. Pawelec G., et al. Human immunosenescence: is it infectious?. Immunol. Rev. 205 (2005) 257-268
3. Williams P.D., and Day T. Antagonistic pleiotropy, mortality source interactions, and the evolutionary theory of senescence. Evolution 57 (2003) 1478-1488
4. Williams P.D., et al. The shaping of senescence in the wild. Trends Ecol. Evol. 21 (2006) 458-463
5. Sorci G., and Faivre B. Inflammation and oxidative stress in vertebrate host-parasite systems. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364 (2009) 71-83
6. Pawelec G., et al. Impact of aging on innate immunity. J. Leukoc. Biol. 64 (1998) 703-712
7. Siegrist C.-A., and Aspinall R. B-cell responses to vaccination at the extremes of age. Nat. Rev. Immunol. 9 (2009) 185-194
8. Goronzy J.J., and Weyand C.M. T cell development and receptor diversity during aging. Curr. Opin. Immunol. 17 (2005) 468-475
9. Medawar P. An Unsolved Problem of Biology (1952), H.K. Lewis and Co
10. Kirkwood T.B.L., and Austad S.N. Why do we age?. Nature 408 (2000) 233-238
11. Williams G.C. Pleiotropy, natural selection and the evolution of senescence. Evolution 11 (1957) 398-411
12. Kirkwood T.B.L. Evolution of aging. Nature 270 (1977) 301-304
13. Stearns S.C., et al. Experimental evolution of aging, growth, and reproduction in fruitflies. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 3309-3313
14. Rose M., and Charlesworth B. A test of evolutionary theories of senescence. Nature 287 (1980) 141-142
15. Zwaan B., et al. Direct selection on life span in Drosophila melanogaster. Evolution 49 (1995) 649-659
16. Austad S.N. Retarded senescence in an insular population of opossums. J. Zool. (Lond.) 229 (1993) 695-708
17. Bryant M.J., and Reznick D. Comparative studies of senescence in natural populations of guppies. Am. Nat. 163 (2004) 55-68
18. Ricklefs R.E. The evolution of senescence from a comparative perspective. Funct. Ecol. 22 (2008) 379-392
19. Drenos F., and Kirkwood T.B.L. Modelling the disposable soma theory of aging. Mech. Aging Dev. 126 (2005) 99-103
20. Kirkwood T.B.L., and Rose M.R. Evolution of senescence: late survival sacrificed for reproduction. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 332 (1991) 15-24
21. Charlesworth B. Fisher, Medawar, Hamilton and the evolution of aging. Genetics 156 (2000) 927-931
22. Hamilton W.D. The moulding of senescence by natural selection. J. Theor. Biol. 12 (1966) 12-45
23. Sozou P., and Seymour R. To age or not to age. Proc. B. Biol. Sci. 271 (2004) 457-463
24. Lee R.D. Rethinking the evolutionary theory of aging: transfers, not births, shape senescence in social species. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 9637-9642
25. Vaupel J.W., et al. The case for negative senescence. Theor. Popul. Biol. 65 (2004) 339-351
26. Garigan D., et al. Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation. Genetics 161 (2002) 1101-1112
27. Pletcher S.D., et al. Chemical complexity and the genetics of aging. Annu. Rev. Ecol. Evol. Syst. 38 (2007) 299-326
28. Zerofsky M., et al. Aging of the innate immune response in Drosophila melanogaster. Aging Cell 4 (2005) 103-108
29. Amdam G.V., et al. Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Exp. Gerontol. 39 (2004) 767-773
30. Holmes D., and Austad S. Declining immunity with age in the wild. Sci. Aging Knowl. Environ. 2004 (2004) pe22
31. Palacios M., et al. Immunosenescence in some but not all immune components in a free-living vertebrate, the tree swallow. Proc. Biol. Sci. 274 (2007) 951-957
32. Adams A.A., et al. Advanced age in horses affects divisional history of T cells and inflammatory cytokine production. Mech. Ageing Dev. 129 (2008) 656-664
33. Blount D.G., et al. Age-related alterations to immune parameters in Labrador retriever dogs. Vet. Immunol. Immunopathol. 108 (2005) 399-407
34. Campbell D.J., et al. Age-related differences in parameters of feline immune status. Vet. Immunol. Immunopathol. 100 (2004) 73-80
35. Katepalli M.P., et al. The effect of age and telomere length on immune function in the horse. Dev. Comp. Immunol. 32 (2008) 1409-1415
36. Jackson J.A., et al. Review series on helminths, immune modulation and the hygiene hypothesis: immunity against helminths and immunological phenomena in modern human populations: coevolutionary legacies?. Immunology 126 (2009) 18-27
37. Lee H.H., et al. Delayed maturation of an IL-12-producing dendritic cell subset explains the early Th2 bias in neonatal immunity. J. Exp. Med. 205 (2008) 2269-2280
38. Singh R.R., et al. Neonatal peptide exposure can prime T cells and, upon subsequent immunization, induce their immune deviation: implications for antibody vs. T cell-mediated autoimmunity. J. Exp. Med 183 (1996) 1613-1621
39. Chen N., and Field E.H. Enhanced type 2 and diminished type 1 cytokines in neonatal tolerance. Transplantation 59 (1995) 933-941
40. Forsthuber T., et al. Induction of TH1 and TH2 immunity in neonatal mice. Science 271 (1996) 1728-1730
41. Yu P., et al. Fetal exposure to high-avidity TCR ligand enhances expansion of peripheral T regulatory cells. J. Immunol. 181 (2008) 73-80
42. Miller J.F. Immunological function of the thymus. Lancet 2 (1961) 748-749
43. Aspinall R., and Andrew D. Thymic atrophy in the mouse is a soluble problem of the thymic environment. Vaccine 18 (2000) 1629-1637
44. Savino W. The thymus is a common target organ in infectious diseases. PLoS Pathog. 2 (2006) e62
45. Howard J.K., et al. Leptin protects mice from starvation-induced lymphoid atrophy and increases thymic cellularity in ob/ob mice. J. Clin. Invest. 104 (1999) 1051-1059
46. Kendall M.D., and Clarke A.G. The thymus in the mouse changes its activity during pregnancy: a study of the microenvironment. J. Anat. 197 (2000) 393-411
47. Gruver A.L., and Sempowski G.D. Cytokines, leptin, and stress-induced thymic atrophy. J. Leukoc. Biol. 84 (2008) 915-923
48. Ciriaco E., et al. Age-related changes in the avian primary lymphoid organs (thymus and bursa of Fabricius). Microsc. Res. Tech. 62 (2003) 482-487
49. Plytycz B., et al. Age-dependent changes in thymuses in the European common frog, Rana temporaria. J. Exp. Zool 273 (1995) 451-460
50. Danilova N., et al. T cells and the thymus in developing zebrafish. Dev. Comp. Immunol. 28 (2004) 755-767
51. Lam S.H., et al. Morphologic transformation of the thymus in developing zebrafish. Dev. Dyn. 225 (2002) 87-94
52. Torroba M., and Zapata A. Aging of the vertebrate immune system. Microsc. Res. Tech. 62 (2003) 477-481
53. Bertho J.-M., et al. Phenotypic and immunohistological analyses of the human adult thymus: evidence for an active thymus during adult life. Cell. Immunol. 179 (1997) 30-40
54. Steinmann G.G., et al. The involution of the aging human thymic epithelium is independent of puberty. Scand. J. Immunol. 22 (1985) 563-575
55. Sempowski G.D., et al. T cell receptor excision circle assessment of thymopoiesis in aging mice. Mol. Immunol. 38 (2002) 841-848
56. Gray D.H., et al. Developmental kinetics, turnover and stimulatory capacity of thymic epithelial cells. Blood 108 (2006) 3777-3785
57. Ortman C.L., et al. Molecular characterization of the mouse involuted thymus: aberrations in expression of transcription regulators in thymocyte and epithelial compartments. Int. Immunol. 14 (2002) 813-822
58. Hale J.S., et al. Thymic output in aged mice. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 8447-8452
59. Chen L., et al. Foxn1 is required to maintain the postnatal thymic microenvironment in a dosage-sensitive manner. Blood 113 (2009) 567-574
60. Min B., et al. Neonates support lymphopenia-induced proliferation. Immunity 18 (2003) 131-140
61. Schuler T., et al. Cutting edge: IL-7-dependent homeostatic proliferation of CD8+ T cells in neonatal mice allows the generation of long-lived natural memory T cells. J. Immunol. 172 (2004) 15-19
62. Min H., et al. Reassessing the role of growth hormone and sex steroids in thymic involution. Clin. Immunol. 118 (2006) 117-123
63. Sutherland J.S., et al. Activation of thymic regeneration in mice and humans following androgen blockade. J. Immunol. 175 (2005) 2741-2753
64. George A.J.T., and Ritter M.A. Thymic involution with aging: obsolescence or good housekeeping?. Immunol. Today 17 (1996) 267-272
65. Dorshkind K., et al. The aging immune system: is it ever too old to become young again?. Nat. Rev. Immunol. 9 (2009) 57-62
66. Aw D., et al. Architectural changes in the thymus of aging mice. Aging Cell 7 (2008) 158-167
67. Dowling M.R., and Hodgkin P.D. Why does the thymus involute? A selection-based hypothesis. Trends Immunol. 30 (2009) 295-300
68. Dowling M.R., and Hodgkin P.D. Modelling naive T-cell homeostasis: consequences of heritable cellular lifespan during aging. Nat. Rev. Immuol. Cell Biol (2009) 10.1038/icb.2009.11
69. Tyan M.L. Age-related decrease in mouse T cell progenitors. J. Immunol. 118 (1977) 846-851
70. Sudo K., et al. Age-associated characteristics of murine hematopoietic stem cells. J. Exp. Med. 192 (2000) 1273-1280
71. Zhu X., et al. Lymphohematopoietic progenitors do not have a synchronized defect with age-related thymic involution. Aging Cell 6 (2007) 663-672
72. Heng T.S.P., et al. Effects of castration on thymocyte development in two different models of thymic involution. J. Immunol. 175 (2005) 2982-2993
73. Min H., et al. Reduction in the developmental potential of intrathymic T cell progenitors with age. J. Immunol. 173 (2004) 245-250
74. Gui J., et al. The aged thymus shows normal recruitment of lymphohematopoietic progenitors but has defects in thymic epithelial cells. Int. Immunol. 19 (2007) 1201-1211
75. Clise-Dwyer K., et al. Environmental and intrinsic factors lead to antigen unresponsiveness in CD4+ recent thymic emigrants from aged mice. J. Immunol. 178 (2007) 1321-1331
76. Eaton S.M., et al. Bone marrow precursor cells from aged mice generate CD4 T cells that function well in primary and memory responses. J. Immunol. 181 (2008) 4825-4831
77. Aw D., et al. Is thymocyte development functional in the aged?. Impact Aging 1 (2009) 146-153
78. Aw D., et al. Phenotypical and morphological changes in the thymic microenvironment from aging mice. Biogerontology 10 (2009) 311-322
79. Li L., et al. Cellular mechanism of thymic involution. Scand. J. Immunol. 57 (2003) 410-422
80. Mackall C.L., et al. Thymic function in young/old chimeras: substantial thymic T cell regenerative capacity despite irreversible age-associated thymic involution. Eur. J. Immunol. 28 (1998) 1886-1893
81. Leposavic G., et al. Age-associated changes in CD90 expression on thymocytes and in TCR-dependent stages of thymocyte maturation in male rats. Exp. Gerontol. 41 (2006) 574-589
82. Aspinall R., et al. Old rhesus macaques treated with Interleukin-7 show increased TREC levels and respond well to influenza vaccination. Rejuvenation Res. 10 (2007) 5-18
83. Alpdogan O., et al. Keratinocyte growth factor (KGF) is required for postnatal thymic regeneration. Blood 107 (2006) 2453-2460
84. Min D., et al. Sustained thymopoiesis and improvement in functional immunity induced by exogenous KGF administration in murine models of aging. Blood 109 (2007) 2529-2537
85. Rossi S.W., et al. Keratinocyte growth factor (KGF) enhances postnatal T-cell development via enhancements in proliferation and function of thymic epithelial cells. Blood 109 (2007) 3803-3811
86. Klasing K.C. The costs of immunity. Acta Zoologica Sinica 50 (2004) 961-969
87. Hurtado A., et al. The role of helminthes in human evolution: implications for global health in the 21st century. In: Elton S., and O'Higgins P. (Eds). Medicine and Evolution: Current Applications, Future Prospects (2008), Taylor and Francis 152-178
88. Råberg L., et al. Basal metabolic rate and the evolution of the adaptive immune system. Proc. Biol. Sci. 269 (2002) 817-821
89. Franceschi C., et al. Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech. Ageing Dev. 128 (2007) 92-105
90. Van Bodegom D., et al. Regulation of human life histories. Annals N.Y. Acad. Sci. 1100 (2007) 84-97
91. Franceschi C., et al. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann. N. Y. Acad. Sci 908 (2000) 208-218
92. Licastro F., et al. Innate immunity and inflammation in aging: a key for understanding age-related diseases. Immun. Ageing 2 (2005) 8
93. Vasto S., et al. Inflammation, aging and cancer. Mech. Ageing Dev. 130 (2009) 40-45
94. Ottaviani E., et al. Ecoimmunology: is there any room for the neuroendocrine system?. Bioessays 30 (2008) 868-874
95. Finch C.E., and Crimmins E.M. Inflammatory exposure and historical changes in human life-spans. Science 305 (2004) 1736-1739
96. Crimmins E.M., and Finch C.E. Infection, inflammation, height, and longevity. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 498-503
97. Gurven M., et al. Aging and inflammation in two epidemiological worlds. J. Gerontol. A Biol. Sci. Med. Sci. 63 (2008) 196-199
98. McDade T.W., et al. Maintenance versus growth: investigating the costs of immune activation among children in lowland Bolivia. Am. J. Phys. Anthropol. 136 (2008) 478-484
99. McDade T.W. Life history, maintenance, and the early origins of immune function. Am. J. Hum. Biol. 17 (2005) 81-94
100. Moore S.E., et al. Season of birth predicts mortality in rural Gambia. Nature 388 (1997) 434
101. Collinson A.C., et al. Birth season and environmental influences on patterns of thymic growth in rural Gambian infants. Acta Paediatr. 92 (2003) 1014-1020
102. McDade T.W. Life history theory and the immune system: steps toward a human ecological immunology. Am. J. Phys. Anthropol. 122 S37 (2003) 100-125
103. Zuk M., and Stoehr A. Immune defense and host life history. Am. Nat. 160 (2002) S9-S22
104. Fedorka K.M., et al. Immune suppression and the cost of reproduction in the ground cricket, Allonemobius socius. Evolution 58 (2004) 2478-2485
105. Helle S., et al. Accelerated immunosenescence in preindustrial twin mothers. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 12391-12396
106. Raghupathy R. Th 1-type immunity is incompatible with successful pregnancy. Immunol. Today 18 (1997) 478-482
107. Westendorp R.G.J., et al. Optimizing human fertility and survival. Nat. Med. 7 (2001) 873
108. Drenos F., et al. Trade-off mediated effects on the genetics of human survival caused by increasingly benign living conditions. Biogerontology 7 (2006) 287-295
109. Wilson J.N., et al. A hallmark of balancing selection is present at the promoter region of interleukin 10. Genes Immun. 7 (2006) 680-683
110. Medawar P. Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. Symp. Soc. Exp. Biol. 7 (1953) 320-338
111. Lesser K.J., et al. Naturally occurring genetic variation in the age-specific immune response of Drosophila melanogaster. Aging Cell 5 (2006) 293-295
112. Salminen A., et al. Activation of innate immunity system during aging: NF-kB signaling is the molecular culprit of inflamm-aging. Ageing Res. Rev. 7 (2008) 83-105
113. Taub D.D. Neuroendocrine interactions in the immune system. Cell. Immunol. 252 (2008) 1-6
114. Pawelec G., et al. T cells and aging. Front. Biosci. 7 (2002) d59-d99