Ageing combines CD4 T cell lymphopenia in secondary lymphoid organs and T cell accumulation in gut associated lymphoid tissue

Immunity and Ageing

Volumn 11, Issue 1, 2014, Pages

  Martinet, Kim Z ^a,b   Bloquet, Stéphane ^b   Bourgeois, Christine ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Age; Ageing; Aging; CD4 T cell homeostasis; CD4 T cell lymphopenia; GALT; Immunology; Immunosenescence; MALT; T cell; T cell homeostasis; T cell lymphopenia

Indexed keywords

ADULT; AGE; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; COLON; CONTROLLED STUDY; FEMALE; INTESTINE LYMPHATIC TISSUE; LAMINA PROPRIA; LYMPHOCYTOPENIA; LYMPHOID ORGAN; MALE; MIDDLE AGED; MOUSE; NONHUMAN; PEYER PATCH; PRIORITY JOURNAL; SMALL INTESTINE; T CELL DEPLETION; ANATOMICAL VARIATION; ANIMAL MODEL; BIOACCUMULATION; CD4+ T LYMPHOCYTE LYMPHOPENIA; CELL COMPARTMENTALIZATION; CELL HETEROGENEITY; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CORRELATIONAL STUDY; DISEASE ASSOCIATION; IMMUNE RESPONSE; LIVER PARENCHYMA; LUNG PARENCHYMA; LYMPHOID TISSUE; MEMORY T LYMPHOCYTE; ORGANOGENESIS; T LYMPHOCYTE;

CD4 ANTIGEN; L SELECTIN; TRANSCRIPTION FACTOR FOXP3;

EID: 84900426713     PISSN: None     EISSN: 17424933     Source Type: Journal    
DOI: 10.1186/1742-4933-11-8     Document Type: Article

References (55)

1. Derhovanessian E, Solana R, Larbi A, Pawelec G. Immunity, ageing and cancer. Immun Ageing 2008, 5:11. 10.1186/1742-4933-5-11, 2564902, 18816370.
2. Fulop T, Larbi A, Witkowski JM, Kotb R, Hirokawa K, Pawelec G. Immunosenescence and cancer. Crit Rev Oncog 2013, 18:489-513. 10.1615/CritRevOncog.2013010597, 24579731.
3. Krupica T, Fry TJ, Mackall CL, Krupica T. Autoimmunity during lymphopenia: a two-hit model. Clin Immunol 2006, 120:121-128. 10.1016/j.clim.2006.04.569, 16766227.
4. Calzascia T, Pellegrini M, Lin A, Garza KM, Elford AR, Shahinian A, Ohashi PS, Mak TW. CD4 T cells, lymphopenia, and IL-7 in a multistep pathway to autoimmunity. Proc Natl Acad Sci U S A 2008, 105:2999-3004. 10.1073/pnas.0712135105, 2268574, 18287017.
5. Wick G, Jansen-Dürr P, Berger P, Blasko I, Grubeck-Loebenstein B. Diseases of aging. Vaccine 2000, 18:1567-1583. 10.1016/S0264-410X(99)00489-2, 10689131.
6. Pawelec G, Larbi A. Immunity and ageing in man: annual review 2006/2007. Exp Gerontol 2008, 43:34-38.
7. Weng N-P. Aging of the immune system: how much can the adaptive immune system adapt?. Immunity 2006, 24:495-499. 10.1016/j.immuni.2006.05.001, 2266981, 16713964.
8. Larbi A, Pawelec G, Wong SC, Goldeck D, Tai JJ-Y, Fulop T. Impact of age on T cell signaling: a general defect or specific alterations?. Ageing Res Rev 2011, 10:370-378. 10.1016/j.arr.2010.09.008, 20933612.
9. Larbi A, Dupuis G, Khalil A, Douziech N, Fortin C, Fülöp T. Differential role of lipid rafts in the functions of CD4+ and CD8+ human T lymphocytes with aging. Cell Signal 2006, 18:1017-1030. 10.1016/j.cellsig.2005.08.016, 16236485.
10. Chen G, Lustig A, Weng N-P. T cell aging: a review of the transcriptional changes determined from genome-wide analysis. Front Immunol 2013, 4:121. 3657702, 23730304.
11. Proust J, Rosenzweig P, Debouzy C, Moulias R. Lymphopenia induced by acute bacterial infections in the elderly: a sign of age-related immune dysfunction of major prognostic significance. Gerontology 1987, 31:178-185.
12. Rea I, Alexander H, Crockard A, Morris T. CD4 lymphopenia in very elderly people. Lancet 1996, 347:328-329.
13. Sauce D, Larsen M, Fastenackels S, Roux A, Gorochov G, Katlama C, Sidi D, Sibony-Prat J, Appay V. Lymphopenia-driven homeostatic regulation of naive T cells in elderly and thymectomized young adults. J Immunol 2012, 189:5541-5548. 10.4049/jimmunol.1201235, 23136199.
14. Bourgeois C, Stockinger B. CD25 + CD4+ regulatory T cells and memory T cells prevent lymphopenia-induced proliferation of naive T cells in transient states of lymphopenia. J Immunol 2006, 177:4558-4566. 10.4049/jimmunol.177.7.4558, 16982893.
15. Den Braber I, Mugwagwa T, Vrisekoop N, Westera L, Mögling R, de Boer AB, Willems N, Schrijver EHR, Spierenburg G, Gaiser K, Mul E, Otto SA, Ruiter AFC, Ackermans MT, Miedema F, Borghans JAM, de Boer RJ, Tesselaar K. Maintenance of peripheral naive T cells is sustained by thymus output in mice but not humans. Immunity 2012, 36:288-297. 10.1016/j.immuni.2012.02.006, 22365666.
16. Mackall C, Fleisher T, Brown M, Andrich M, Chen C, Feuerstein I, Horowitz M, Magrath I, Shad A, Steinberg S, Leonard H, Gress R. Age, thymopoiesis, and CD4+ T-lymphocyte regeneration after intensive chemotherapy. N Engl J Med 1995, 332:143-149. 10.1056/NEJM199501193320303, 7800006.
17. Mosley R, Koker M, Miller R. Idiosyncratic alterations of TCR size distributions affecting both CD4 and CD8 T cell subsets in aging mice. Cell Immunol 1998, 189:10-18. 10.1006/cimm.1998.1369, 9758689.
18. Hall MA, Reid JL, Lanchbury JS. The distribution of human TCR junctional region lengths shifts with age in both CD4 and CD8 T cells. Int Immunol 1998, 10:1407-1419. 10.1093/intimm/10.10.1407, 9796907.
19. Buchholz VR, Neuenhahn M, Busch DH. CD8+ T cell differentiation in the aging immune system: until the last clone standing. Curr Opin Immunol 2011, 23:549-554. 10.1016/j.coi.2011.05.002, 21664807.
20. LeMaoult J, Messaoudi I, Manavalan JS, Potvin H, Nikolich-Zugich D, Dyall R, Szabo P, Weksler ME, Nikolich-Zugich J. Age-related dysregulation in CD8 T cell homeostasis: kinetics of a diversity loss. J Immunol 2000, 165(5):2367-2373. 10.4049/jimmunol.165.5.2367, 10946259.
21. Aspinall R. Age-associated thymic atrophy in the mouse is due to a deficiency affecting rearrangement of the TCR during intrathymic T cell development. J Immunol 1997, 158:3037-3045.
22. 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, 28:1886-1893. 10.1002/(SICI)1521-4141(199806)28:06<1886::AID-IMMU1886>3.0.CO;2-M, 9645370.
23. Aspinall R, Pitts D, Lapenna A, Mitchell W. Immunity in the elderly: the role of the thymus. J Comp Pathol 2010, 142(Suppl):S111-S115.
24. Linton PJ, Dorshkind K. Age-related changes in lymphocyte development and function. Nat Immunol 2004, 5:133-139.
25. Miller RA. The aging immune system: primer and prospectus. Science 1996, 273:70-74. 10.1126/science.273.5271.70, 8658199.
26. Lefebvre JS, Maue AC, Eaton SM, Lanthier PA, Tighe M, Haynes L. The aged microenvironment contributes to the age-related functional defects of CD4 T cells in mice. Aging Cell 2012, 11:732-740. 10.1111/j.1474-9726.2012.00836.x, 3444657, 22607653.
27. Zediak VP, Maillard I, Bhandoola A. Multiple prethymic defects underlie age-related loss of T progenitor competence. Blood 2007, 110:1161-1167. 10.1182/blood-2007-01-071605, 1939899, 17456721.
28. Czesnikiewicz-Guzik M, Lee W-W, Cui D, Hiruma Y, Lamar DL, Yang Z-Z, Ouslander JG, Weyand CM, Goronzy JJ. T cell subset-specific susceptibility to aging. Clin Immunol 2008, 127:107-118. 10.1016/j.clim.2007.12.002, 2435295, 18222733.
29. Lerner A, Yamada T, Miller RA. Pgp-1hi T lymphocytes accumulate with age in mice and respond poorly to concanavalin A. Eur J Immunol 1989, 19:977-982. 10.1002/eji.1830190604, 2666144.
30. Bell EB, Sparshott SM. The peripheral T-cell pool: regulation by non-antigen induced proliferation?. Semin Immunol 1997, 9:347-353. 10.1006/smim.1997.0092, 9405263.
31. Kieper WC, Jameson SC. Homeostatic expansion and phenotypic conversion of naive T cells in response to self peptide/MHC ligands. Proc Natl Acad Sci U S A 1999, 96:13306-13311. 10.1073/pnas.96.23.13306, 23943, 10557316.
32. Bourgeois C, Stockinger B. T cell homeostasis in steady state and lymphopenic conditions. Immunol Lett 2006, 107:89-92. 10.1016/j.imlet.2006.08.001, 16963128.
33. Ganusov VV, De Boer RJ. Do most lymphocytes in humans really reside in the gut?. Trends Immunol 2007, 28:514-518. 10.1016/j.it.2007.08.009, 17964854.
34. Mackall CL, Granger L, Sheard MA, Cepeda R, Gress RE. T-cell regeneration after bone marrow transplantation: differential CD45 isoform expression on thymic-derived versus thymic-independent progeny. Blood 1993, 82:2585-2594.
35. Bourgeois C, Hao Z, Rajewsky K, Potocnik AJ, Stockinger B. Ablation of thymic export causes accelerated decay of naive CD4 T cells in the periphery because of activation by environmental antigen. Proc Natl Acad Sci U S A 2008, 105:8691-8696. 10.1073/pnas.0803732105, 2438401, 18562288.
36. Jankovic V, Messaoudi I, Nikolich-Zugich J. Phenotypic and functional T-cell aging in rhesus macaques (Macaca mulatta): differential behavior of CD4 and CD8 subsets. Blood 2013, 102:3244-3251.
37. Tanchot C, Rocha B. The organization of mature T-cell pools. Immunol Today 1998, 19:575-579. 10.1016/S0167-5699(98)01344-9, 9864949.
38. Ma A, Koka R, Burkett P. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol 2006, 24:657-679. 10.1146/annurev.immunol.24.021605.090727, 16551262.
39. Utsuyama M, Hirokawa K. Age-related changes of splenic T cells in mice-a flow cytometric analysis. Mech Ageing Dev 1987, 40:89-102. 10.1016/0047-6374(87)90037-6, 2891881.
40. Stienen A, Feyen O, Niehues T. Effect of age on homeostasis of lymphocytes in an interleukin-7-deficient mouse model. Eur Cytokine Netw 2011, 22:63-72.
41. Ishimoto Y, Tomiyama-Miyaji C, Watanabe H, Yokoyama H, Ebe K, Tsubata S, Aoyagi Y, Abo T. Age-dependent variation in the proportion and number of intestinal lymphocyte subsets, especially natural killer T cells, double-positive CD4+ CD8+ cells and B220+ T cells, in mice. Immunology 2004, 113:371-377. 10.1111/j.1365-2567.2004.01961.x, 1782573, 15500624.
42. Menzies FM, Henriquez FL. Immunomodulation by the Female Sex Hormones. Open Infect Dis J 2009, 3:61-72.
43. Strindhall J, Skog M, Ernerudh J, Bengner M, Löfgren S, Matussek A, Nilsson BO, Wikby A. The inverted CD4/CD8 ratio and associated parameters in 66-year-old individuals: the Swedish HEXA immune study. Age (Dordr) 2013, 35:985-991. 10.1007/s11357-012-9400-3, 3636392, 22415616.
44. Gupta S, Su H, Bi R, Agrawal S, Gollapudi S. Life and death of lymphocytes: a role in immunesenescence. Immun ageing I A 2005, 2:12.
45. Posnett DN, Sinha R, Kabak S, Russo C. Clonal populations of T cells in normal elderly humans: the T cell equivalent to " benign monoclonal gammapathy" . J Exp Med 1994, 179:609-618. 10.1084/jem.179.2.609, 2191374, 8294871.
46. Hingorani R, Choi I, Akolkar P, Gulwani-akolkar B, Pergolizzi R, Silver J, Gregersen PK. Clonal Predominance of T Cell Receptors Within the CD8+ CD45RO + Subset in Normal Human Subjects. J Immunol 1993, 151(10):5762-5769.
47. Ahmed M, Lanzer KG, Yager EJ, Adams PS, Johnson LL, Blackman MA. Clonal expansions and loss of receptor diversity in the naive CD8 T cell repertoire of aged mice. J Immunol 2009, 182:784-792. 10.4049/jimmunol.182.2.784, 2724652, 19124721.
48. Callahan JE, Kappler JW, Marrack P. Unexpected expansions of CD8-bearing cells in old mice. J Immunol 1993, 151:6657-6669.
49. Gruver AL, Hudson LL, Sempowski GD. Immunosenescence of ageing. 2007, 211(2):144-156.
50. Honda K, Littman DR. The microbiome in infectious disease and inflammation. Annu Rev Immunol 2012, 30:759-795. 10.1146/annurev-immunol-020711-074937, 22224764.
51. Kamada N, Seo S-U, Chen GY, Núñez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 2013, 13:321-335. 10.1038/nri3430, 23618829.
52. Veazey RS, DeMaria M, Chalifoux LV, Shvetz DE, Pauley DR, Knight HL, Rosenzweig M, Johnson RP, Desrosiers RC, Lackner AA. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 1998, 280:427-431. 10.1126/science.280.5362.427, 9545219.
53. Sheridan BS, Lefrançois L. Regional and mucosal memory T cells. Nat Immunol 2011, 131:485-491.
54. Sathaliyawala T, Kubota M, Yudanin N, Turner D, Camp P, Thome JJC, Bickham KL, Lerner H, Goldstein M, Sykes M, Kato T, Farber DL. Distribution and compartmentalization of human circulating and tissue-resident memory T cell subsets. Immunity 2013, 38:187-197. 10.1016/j.immuni.2012.09.020, 3557604, 23260195.
55. Schulthess J, Meresse B, Ramiro-Puig E, Montcuquet N, Darche S, Bègue B, Ruemmele F, Combadière C, Di Santo JP, Buzoni-Gatel D, Cerf-Bensussan N. Interleukin-15-dependent NKp46+ innate lymphoid cells control intestinal inflammation by recruiting inflammatory monocytes. Immunity 2012, 37:108-121. 10.1016/j.immuni.2012.05.013, 22705105.