T cell ageing: Effects of age on development, survival & function

Indian Journal of Medical Research

Volumn 138, Issue NOV, 2013, Pages 595-608

  Salam, Nasir ^a   Rane, Sanket ^a   Das, Rituparna ^a   Faulkner, Matthew ^b   Gund, Rupali ^a   Kandpal, Usha ^a   Lewis, Virginia ^b   Mattoo, Hamid ^a   Prabhu, Savit ^a   Ranganathan, Vidya ^a   Durdik, Jeannine ^b   George, Anna ^a   Rath, Satyajit ^a   Bal, Vineeta ^a  

^a NATIONAL INSTITUTE OF IMMUNOLOGY   (India)

^b UNIVERSITY OF ARKANSAS   (United States)

Author keywords

Adaptive immunity; Ageing; Haematopoietic stem cells; Innate immunity; T cells; TCR repertoire; Thymic involution; Transcription factors

Indexed keywords

B LYMPHOCYTE RECEPTOR; CHEMOKINE; INTERLEUKIN 7; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR; B CELL LYMPHOMA 11B; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CCR9; CHEMOKINE RECEPTOR CXCR4; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; SECONDARY LYMPHOID TISSUE CHEMOKINE; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR 7; TRANSCRIPTION FACTOR GATA 3; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; AGING; AUTOIMMUNITY; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; DENDRITIC CELL; DEVELOPMENTAL STAGE; GENE EXPRESSION; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNOGLOBULIN GENE; INNATE IMMUNITY; INTRACELLULAR SIGNALING; MAJOR HISTOCOMPATIBILITY COMPLEX; MEMORY CELL; NATURAL KILLER CELL; OXIDATIVE STRESS; PHASE 1 CLINICAL TRIAL (TOPIC); PHOSPHORYLATION; REVIEW; SURVIVAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; BIODIVERSITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CELL SURVIVAL; CELLULAR PARAMETERS; HEMATOPOIETIC STEM CELL; IMMUNOCOMPETENCE; INVOLUTION; LYMPHOCYTE FUNCTION; LYMPHOID PROGENITOR CELL; MICROENVIRONMENT; NONHUMAN; PRE T LYMPHOCYTE; T CELL POOL;

ADAPTIVE IMMUNITY; AGING; CD4-POSITIVE T-LYMPHOCYTES; CELL AGING; HEMATOPOIETIC STEM CELLS; HUMANS; IMMUNITY, INNATE; RECEPTORS, ANTIGEN, T-CELL; THYMUS GLAND;

EID: 84891683542     PISSN: 09715916     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (89)

1. Janeway CA Jr, Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002; 20: 197-216.
2. Pancer Z, Cooper MD. The evolution of adaptive immunity. Annu Rev Immunol 2006; 24: 497-518.
3. Kondo M, Wagers AJ, Manz MG, Prohaska SS, Scherer DC, Beilhack GF, et al. Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu Rev Immunol 2003; 21: 759-806.
4. Globerson A, Effros RB. Ageing of lymphocytes and lymphocytes in the aged. Immunol Today 2000; 21: 515-21.
5. Desai A, Grolleau-Julius A, Yung R. Leukocyte function in the aging immune system. J Leukoc Biol 2010; 87: 1001-9.
6. Ponnappan S, Ponnappan U. Aging and immune function: molecular mechanisms to interventions. Antioxid Redox Signal 2011; 14: 1551-85.
7. Weng NP. Aging of the immune system: how much can the adaptive immune system adapt? Immunity 2006; 24: 495-9.
8. Solana R, Pawelec G, Tarazona R. Aging and innate immunity. Immunity 2006; 24: 491-4.
9. Plowden J, Renshaw-Hoelscher M, Engleman C, Katz J, Sambhara S. Innate immunity in aging: impact on macrophage function. Aging Cell 2004; 3: 161-7.
10. Renshaw M, Rockwell J, Engleman C, Gewirtz A, Katz J, Sambhara S. Cutting edge: impaired Toll-like receptor expression and function in aging. J Immunol 2002; 169: 4697-701.
11. Gomez CR, Boehmer ED, Kovacs EJ. The aging innate immune system. Curr Opin Immunol 2005; 17: 457-62.
12. Cumberbatch M, Dearman RJ, Kimber I. Influence of ageing on Langerhans cell migration in mice: identification of a putative deficiency of epidermal interleukin-1beta. Immunology 2002; 105: 466-77.
13. Uyemura K, Castle SC, Makinodan T. The frail elderly: role of dendritic cells in the susceptibility of infection. Mech Ageing Dev 2002; 123: 955-62.
14. Chatta GS, Andrews RG, Rodger E, Schrag M, Hammond WP, Dale DC. Hematopoietic progenitors and aging: alterations in granulocytic precursors and responsiveness to recombinant human G-CSF, GM-CSF, and IL-3. J Gerontol 1993; 48: M207-12.
15. Schroder AK, Rink L. Neutrophil immunity of the elderly. Mech Ageing Dev 2003; 124: 419-25.
16. Solana R, Mariani E. NK and NK/T cells in human senescence. Vaccine 2000; 18: 1613-20.
17. LeBien TW, Tedder TF. B lymphocytes: how they develop and function. Blood 2008; 112: 1570-80.
18. Frasca D, Blomberg BB. Aging affects human B cell responses. J Clin Immunol 2011; 31: 430-5.
19. Frasca D, Van der Put E, Riley RL, Blomberg BB. Reduced Ig class switch in aged mice correlates with decreased E47 and activation-induced cytidine deaminase. J Immunol 2004; 172: 2155-62.
20. Haynes L, Maue AC. Effects of aging on T cell function. Curr Opin Immunol 2009; 21: 414-7.
21. Krueger A, Willenzon S, Lyszkiewicz M, Kremmer E, Forster R. CC chemokine receptor 7 and 9 double-deficient hematopoietic progenitors are severely impaired in seeding the adult thymus. Blood 2010; 115: 1906-12.
22. Sambandam A, Maillard I, Zediak VP, Xu L, Gerstein RM, Aster JC, et al. Notch signaling controls the generation and differentiation of early T lineage progenitors. Nat Immunol 2005; 6: 663-70.
23. Radtke F, Wilson A, Stark G, Bauer M, van Meerwijk J, MacDonald HR, et al. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 1999; 10: 547-58.
24. Godfrey DI, Kennedy J, Mombaerts P, Tonegawa S, Zlotnik A. Onset of TCR-beta gene rearrangement and role of TCR-beta expression during CD3-CD4-CD8-thymocyte differentiation. J Immunol 1994; 152: 4783-92.
25. Takahama Y. Journey through the thymus: stromal guides for T-cell development and selection. Nat Rev Immunol 2006; 6: 127-35.
26. Kang J, Volkmann A, Raulet DH. Evidence that gammadelta versus alphabeta T cell fate determination is initiated independently of T cell receptor signaling. J Exp Med 2001; 193: 689-98.
27. Masuda K, Kakugawa K, Nakayama T, Minato N, Katsura Y, Kawamoto H. T cell lineage determination precedes the initiation of TCR beta gene rearrangement. J Immunol 2007; 179: 3699-706.
28. Von Boehmer H. Unique features of the pre-T-cell receptor alpha-chain: not just a surrogate. Nat Rev Immunol 2005; 5: 571-7.
29. Porritt HE, Gordon K, Petrie HT. Kinetics of steady-state differentiation and mapping of intrathymic-signaling environments by stem cell transplantation in nonirradiated mice. J Exp Med 2003; 198: 957-62.
30. Klein L, Hinterberger M, Wirnsberger G, Kyewski B. Antigen presentation in the thymus for positive selection and central tolerance induction. Nat Rev Immunol 2009; 9: 833-44.
31. Ashworth TD, Pear WS, Chiang MY, Blacklow SC, Mastio J, Xu L, et al. Deletion-based mechanisms of Notch1 activation in T-ALL: key roles for RAG recombinase and a conserved internal translational start site in Notch1. Blood 2010; 116: 5455-64.
32. Hosoya T, Kuroha T, Moriguchi T, Cummings D, Maillard I, Lim KC, et al. GATA-3 is required for early T lineage progenitor development. J Exp Med 2009; 206: 2987-3000.
33. Weber BN, Chi AW, Chavez A, Yashiro-Ohtani Y, Yang Q, Shestova O, et al. Critical role for TCF-1 in T-lineage specification and differentiation. Nature 2011; 476: 63-8.
34. Zlotoff DA, Sambandam A, Logan TD, Bell JJ, Schwarz BA, Bhandoola A. CCR7 and CCR9 together recruit hematopoietic progenitors to the adult thymus. Blood 2010; 115: 1897-905.
35. Plotkin J, Prockop SE, Lepique A, Petrie HT. Critical role for CXCR4 signaling in progenitor localization and T cell differentiation in the postnatal thymus. J Immunol 2003; 171: 4521-7.
36. Surh CD, Sprent J. Homeostasis of naive and memory T cells. Immunity 2008; 29: 848-62.
37. Takeda S, Rodewald HR, Arakawa H, Bluethmann H, Shimizu T. MHC class II molecules are not required for survival of newly generated CD4+ T cells, but affect their long-term life span. Immunity 1996; 5: 217-28.
38. Tanchot C, Lemonnier FA, Perarnau B, Freitas AA, Rocha B. Differential requirements for survival and proliferation of CD8 naive or memory T cells. Science 1997; 276: 2057-62.
39. Dorfman JR, Stefanova I, Yasutomo K, Germain RN. CD4+ T cell survival is not directly linked to self-MHC-induced TCR signaling. Nat Immunol 2000; 1: 329-35.
40. Goldrath AW, Luckey CJ, Park R, Benoist C, Mathis D. The molecular program induced in T cells undergoing homeostatic proliferation. Proc Natl Acad Sci USA 2004; 101: 16885-90.
41. Hataye J, Moon JJ, Khoruts A, Reilly C, Jenkins MK. Naive and memory CD4+ T cell survival controlled by clonal abundance. Science 2006; 312: 114-6.
42. Lantz O, Grandjean I, Matzinger P, Di Santo JP. Gamma chain required for naive CD4+ T cell survival but not for antigen proliferation. Nat Immunol 2000; 1: 54-8.
43. Tan JT, Dudl E, LeRoy E, Murray R, Sprent J, Weinberg KI, et al. IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc Natl Acad Sci USA 2001; 98: 8732-7.
44. Schluns KS, Kieper WC, Jameson SC, Lefrancois L. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat Immunol 2000; 1: 426-32.
45. Yang Y, An J, Weng NP. Telomerase is involved in IL-7-mediated differential survival of naive and memory CD4+ T cells. J Immunol 2008; 180: 3775-81.
46. Fooksman DR, Vardhana S, Vasiliver-Shamis G, Liese J, Blair DA, Waite J, et al. Functional anatomy of T cell activation and synapse formation. Annu Rev Immunol 2010; 28: 79-105.
47. Smith-Garvin JE, Koretzky GA, Jordan MS. T cell activation. Annu Rev Immunol 2009; 27: 591-619.
48. Acuto O, Michel F. CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat Rev Immunol 2003; 3: 939-51.
49. Watts TH, DeBenedette MA. T cell co-stimulatory molecules other than CD28. Curr Opin Immunol 1999; 11: 286-93.
50. Riley JL, June CH. The CD28 family: a T-cell rheostat for therapeutic control of T-cell activation. Blood 2005; 105: 13-21.
51. Malek TR. The biology of interleukin-2. Annu Rev Immunol 2008; 26: 453-79.
52. Liao W, Lin JX, Leonard WJ. IL-2 family cytokines: new insights into the complex roles of IL-2 as a broad regulator of T helper cell differentiation. Curr Opin Immunol 2011; 23: 598-604.
53. Sallusto, F, Geginat J, Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 2004; 22: 745-63.
54. Rossi DJ, Bryder D, Zahn JM, Ahlenius H, Sonu R, Wagers AJ, et al. Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci USA 2005; 102: 9194-9.
55. Ito K, Hirao A, Arai F, Takubo K, Matsuoka S, Miyamoto K, et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med 2006; 12: 446-51.
56. Rossi DJ, Bryder D, Weissman IL. Hematopoietic stem cell aging: mechanism and consequence. Exp Gerontol 2007; 42: 385-90.
57. Rossi DJ, Bryder D, Seita J, Nussenzweig A, Hoeijmakers J, Weissman IL. Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 2007; 447: 725-9.
58. Ciofani M, Zuniga-Pflucker JC. The thymus as an inductive site for T lymphopoiesis. Annu Rev Cell Dev Biol 2007; 23: 463-93.
59. Steinmann GG, Klaus B, Muller-Hermelink HK. The involution of the ageing human thymic epithelium is independent of puberty. A morphometric study. Scand J Immunol 1985; 22: 563-75.
60. Flores KG, Li J, Sempowski GD, Haynes BF, Hale LP. Analysis of the human thymic perivascular space during aging. J Clin Invest 1999; 104: 1031-9.
61. Fitzpatrick FT, Kendall MD, Wheeler MJ, Adcock IM, Greenstein BD. Reappearance of thymus of ageing rats after orchidectomy. J Endocrinol 1985; 106: R17-9.
62. Olsen NJ, Olson G, Viselli SM, Gu X, Kovacs WJ. Androgen receptors in thymic epithelium modulate thymus size and thymocyte development. Endocrinology 2001; 142: 1278-83.
63. Min H, Montecino-Rodriguez E, Dorshkind K. Reduction in the developmental potential of intrathymic T cell progenitors with age. J Immunol 2004; 173: 245-50.
64. Mackall CL, Punt JA, Morgan P, Farr AG, Gress RE. Thymic function in young/old chimeras: substantial thymic T cell regenerative capacity despite irreversible age-associated thymic involution. Eur J Immunol 1998; 28: 1886-93.
65. Ortman CL, Dittmar KA, Witte PL, Le PT. Molecular characterization of the mouse involuted thymus: aberrations in expression of transcription regulators in thymocyte and epithelial compartments. Int Immunol 2002; 14: 813-22.
66. Sempowski GD, Hale LP, Sundy JS, Massey JM, Koup RA, Douek DC, et al. Leukemia inhibitory factor, oncostatin M, IL-6, and stem cell factor mRNA expression in human thymus increases with age and is associated with thymic atrophy. J Immunol 2000; 164: 2180-7.
67. Sempowski GD, Gooding ME, Liao HX, Le PT, Haynes BF. T cell receptor excision circle assessment of thymopoiesis in aging mice. Mol Immunol 2002; 38: 841-8.
68. 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.
69. Tsukamoto H, Huston GE, Dibble J, Duso DK, Swain SL. Bim dictates naive CD4 T cell lifespan and the development of age-associated functional defects. J Immunol 2010; 185: 4535-44.
70. Haynes L, Eaton SM, Burns EM, Randall TD, Swain SL. Newly generated CD4 T cells in aged animals do not exhibit age-related defects in response to antigen. J Exp Med 2005; 201: 845-51.
71. Haynes L, Maue AC. Effects of aging on T cell function. Curr Opin Immunol 2009; 21: 414-7.
72. Garcia GG, Miller RA. Single-cell analyses reveal two defects in peptide-specific activation of naive T cells from aged mice. J Immunol 2001; 166: 3151-7.
73. Eisenbraun MD, Tamir A, Miller RA. Altered composition of the immunological synapse in an anergic, age-dependent memory T cell subset. J Immunol 2000; 164: 6105-12.
74. Bining N, Miller RA. Cytokine production by subsets of CD4 memory T cells differing in P-glycoprotein expression: effects of aging. J Gerontol A Biol Sci Med Sci 1997; 52: B137-45.
75. Garcia GG, Miller RA. Age-dependent defects in TCR-triggered cytoskeletal rearrangement in CD4+ T cells. J Immunol 2002; 169: 5021-7.
76. Mattoo H, Faulkner M, Kandpal U, Das R, Lewis V, George A, et al. Naive CD4 T cells from aged mice show enhanced death upon primary activation. Int Immunol 2009; 21: 1277-89.
77. Haynes L, Linton PJ, Eaton SM, Tonkonogy SL, Swain SL. Interleukin 2, but not other common gamma chain-binding cytokines, can reverse the defect in generation of CD4 effector T cells from naive T cells of aged mice. J Exp Med 1999; 190: 1013-24.
78. Eaton SM, Burns EM, Kusser K, Randall TD, Haynes L. Age-related defects in CD4 T cell cognate helper function lead to reductions in humoral responses. J Exp Med 2004; 200: 1613-22.
79. Maue AC, Eaton SM, Lanthier PA, Sweet KB, Blumerman SL, Haynes L. Proinflammatory adjuvants enhance the cognate helper activity of aged CD4 T cells. J Immunol 2009; 182: 6129-35.
80. Haynes L, Eaton SM, Burns EM, Randall TD, Swain SL. CD4 T cell memory derived from young naive cells functions well into old age, but memory generated from aged naive cells functions poorly. Proc Natl Acad Sci USA 2003; 100: 15053-8.
81. Chen Q, Liang WN, Liu GF, Liu M, Xie XQ, Wu J, et al. Case fatality rate of severe acute respiratory syndromes in Beijing. Biomed Environ Sci 2005; 18: 220-6.
82. Vu T, Farish S, Jenkins M, Kelly H. A meta-analysis of effectiveness of influenza vaccine in persons aged 65 years and over living in the community. Vaccine 2002; 20: 1831-6.
83. Vrisekoop N, den Braber I, de Boer AB, Ruiter AF, Ackermans MT, van der Crabben SN, et al. Sparse production but preferential incorporation of recently produced naive T cells in the human peripheral pool. Proc Natl Acad Sci USA 2008; 105: 6115-20.
84. Maletto BA, Ropolo AS, Liscovsky MV, Alignani DO, Glocker M, Pistoresi-Palencia MC. CpG oligodeoxynucleotide functions as an effective adjuvant in aged BALB/c mice. Clin Immunol 2005; 117: 251-61.
85. Chen BJ, Cui X, Sempowski GD, Chao NJ. Growth hormone accelerates immune recovery following allogeneic T-cell-depleted bone marrow transplantation in mice. Exp Hematol 2003; 31: 953-8.
86. Tian ZG, Woody MA, Sun R, Welniak LA, Raziuddin A, Funakoshi S, et al. Recombinant human growth hormone promotes hematopoietic reconstitution after syngeneic bone marrow transplantation in mice. Stem Cells 1998; 16: 193-9.
87. Alpdogan O, Hubbard VM, Smith OM, Patel N, Lu S, Goldberg GL, et al. Keratinocyte growth factor (KGF) is required for postnatal thymic regeneration. Blood 2006; 107: 2453-60.
88. Alpdogan O, Muriglan SJ, Eng JM, Willis LM, Greenberg AS, Kappel BJ, et al. IL-7 enhances peripheral T cell reconstitution after allogeneic hematopoietic stem cell transplantation. J Clin Invest 2003; 112: 1095-107.
89. Mackall CL, Fry TJ, Bare C, Morgan P, Galbraith A, Gress RE. IL-7 increases both thymic-dependent and thymic-independent T-cell regeneration after bone marrow transplantation. Blood 2001; 97: 1491-7.