Heterogeneity in Thymic Emigrants: Implications for Thymectomy and Immunosenescence

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Bains, Iren ^a,b,c,d   Yates, Andrew J ^b   Callard, Robin E ^c,d  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE 7; UNCLASSIFIED DRUG;

ADULT; AGING; ARTICLE; CALCULATION; CD4+ T LYMPHOCYTE; CELL COUNT; CELL DIVISION; CELL MATURATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; LYMPHOCYTE SUBPOPULATION; MATHEMATICAL MODEL; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE; THYMECTOMY;

ADOLESCENT; ADULT; AGE FACTORS; AGING; CD4-POSITIVE T-LYMPHOCYTES; CELL ADHESION MOLECULES; CHILD; CHILD, PRESCHOOL; EMIGRANTS AND IMMIGRANTS; HUMANS; INFANT; INFANT, NEWBORN; MIDDLE AGED; MODELS, BIOLOGICAL; RECEPTOR PROTEIN-TYROSINE KINASES; THYMECTOMY; THYMUS GLAND; YOUNG ADULT;

EID: 84874539245     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049554     Document Type: Article

References (44)

1. Hulstaert F, Hannet I, Deneys V, Munhyeshuli V, Reichert T, et al. (1994) Age-related changes in human blood lymphocyte subpopulations. II. Varying kinetics of percentage and absolute count measurements. Clin Immunol Immunopathol 70: 152-158.
2. Huenecke S, Behl M, Fadler C, Zimmermann S, Bochennek K, et al. (2008) Age-matched lymphocyte subpopulation reference values in childhood and adolescence: application of exponential regression analysis. Eur J Haematol 80: 532-539.
3. Boursalian TE, Golob J, Soper DM, Cooper CJ, Fink PJ, (2004) Continued maturation of thymic emigrants in the periphery. Nat Immunol 5: 418-425.
4. Hosseinzadeh H, Goldschneider I, (1993) Recent thymic emigrants in the rat express a unique antigenic phenotype and undergo post-thymic maturation in peripheral lymphoid tissues. J Immunol 150: 1670-9.
5. Haines CJ, Giffon TD, Lu LS, Lu X, Tessier-Lavigne M, et al. (2009) Human CD4+ T cell recent thymic emigrants are identified by protein tyrosine kinase 7 and have reduced immune function. J Exp Med 206: 275-285.
6. Azevedo RI, Soares MVD, Barata JT, Tendeiro R, Serra-Caetano A, et al. (2009) IL-7 sustains CD31 expression in human naive CD4+ T cells and preferentially expands the CD31+ subset in a PI3K-dependent manner. Blood 113: 2999-3007.
7. Opiela SJ, Koru-Sengul T, Adkins B, (2009) Murine neonatal recent thymic emigrants are phenotypically and functionally distinct from adult recent thymic emigrants. Blood 113: 5635-43.
8. Chu YW, Memon SA, Sharrow SO, Hakim FT, Eckhaus M, et al. (2004) Exogenous IL-7 increases recent thymic emigrants in peripheral lymphoid tissue without enhanced thymic function. Blood 104: 1110-9.
9. Douek DC, McFarland RD, Keiser PH, Gage EA, Massey JM, et al. (1998) Changes in thymic function with age and during the treatment of HIV infection. Nature 396: 690-695.
10. Hazenberg MD, Otto SA, Cohen Stuart JW, Verschuren MC, Borleffs JC, et al. (2000) Increased cell division but not thymic dysfunction rapidly affects the T-cell receptor excision circle content of the naive T cell population in HIV-1 infection. Nat Med 6: 1036-1042.
11. Hazenberg MD, Borghans JAM, de Boer RJ, Miedema F, (2003) Thymic output: a bad TREC record. Nat Immunol 4: 97-99.
12. Bains I, Antia R, Callard R, Yates AJ, (2009) Quantifying the development of the peripheral naive CD4+ T-cell pool in humans. Blood 113: 5480-5487.
13. Kimmig S, Przybylski GK, Schmidt CA, Laurisch K, Mowes B, et al. (2002) Two subsets of naive T helper cells with distinct T cell receptor excision circle content in human adult peripheral blood. J Exp Med 195: 789-794.
14. Kilpatrick RD, Rickabaugh T, Hultin LE, Hultin P, Hausner MA, et al. (2008) Homeostasis of the naive CD4+ T cell compartment during aging. J Immunol 180: 1499-1507.
15. Sauce D, Larsen M, Fastenackels S, Duperrier A, Keller M, et al. (2009) Evidence of premature immune aging in patients thymectomized during early childhood. J Clin Invest 119: 3070-8.
16. Kohler S, Wagner U, Pierer M, Kimmig S, Oppmann B, et al. (2005) Post-thymic in vivo proliferation of naive CD4+ T cells constrains the TCR repertoire in healthy human adults. Eur J Immunol 35: 1987-1994.
17. Linton PJ, Haynes L, Klinman NR, Swain SL, (1996) Antigen-independent changes in naïve CD4 T cells with aging. J Exp Med 184: 1891-900.
18. Steinmann GG, Klaus B, Muller-Hermelink HK, (1985) The involution of the ageing human thymic epithelium is independent of puberty. A morphometric study. Scand J Immunol 22: 563-575.
19. Goronzy JJ, Lee WW, Weyand CM, (2007) Aging and T-cell diversity. Exp Gerontol 42: 400-6.
20. Naylor K, Li G, Vallejo AN, Lee WW, Koetz K, et al. (2005) The influence of age on T cell generation and TCR diversity. J Immunol 174: 7446-7452.
21. Clise-Dwyer K, Huston GE, Buck AL, Duso DK, Swain SL, (2007) Environmental and intrinsic factors lead to antigen unresponsiveness in CD4(+) recent thymic emigrants from aged mice. J Immunol 178: 1321-1331.
22. Macallan DC, Wallace D, Zhang Y, De Lara C, Worth AT, et al. (2004) Rapid turnover of effector-memory CD4(+) T cells in healthy humans. J Exp Med 200: 255-260.
23. Vrisekoop N, den Braber I, de Boer AB, Ruiter AFC, Ackermans MT, et al. (2008) Sparse production but preferential incorporation of recently produced naive T cells in the human peripheral pool. Proc Natl Acad Sci U S A 105: 6115-6120.
24. Shigemura N, Shiono H, Inoue M, Minami M, Ohta M, et al. (2006) Inclusion of the transcervical approach in video-assisted thoracoscopic extended thymectomy (VATET) for myasthenia gravis: a prospective trial. Surg Endosc 20: 1614-8.
25. Terszowski G, M̈uller SM, Bleul CC, Blum C, Schirmbeck R, et al. (2006) Evidence for a functional second thymus in mice. Science 312: 284-7.
26. Bains I, Thíebaut R, Yates AJ, Callard R, (2009) Quantifying thymic export: combining models of naive T cell proliferation and TCR excision circle dynamics gives an explicit measure of thymic output. J Immunol 183: 4329-36.
27. Berzins SP, Boyd RL, Miller JF, (1998) The role of the thymus and recent thymic migrants in the maintenance of the adult peripheral lymphocyte pool. J Exp Med 187: 1839-48.
28. Prelog M, Keller M, Geiger R, Brandstatter A, Wurzner R, et al. (2009) Thymectomy in early childhood: significant alterations of the CD4(+)CD45RA(+)CD62L(+) T cell compartment in later life. Clin Immunol 130: 123-132.
29. Grubeck-Loebenstein B, Wick G, (2002) The aging of the immune system. Adv Immunol 80: 243-84.
30. Phair J, Kauffman CA, Bjornson A, Adams L, Linnemann C Jr, (1978) Failure to respond to influenza vaccine in the aged: correlation with B-cell number and function. J Lab Clin Med 92: 822-8.
31. Cook JM, Gualde N, Hessel L, Mounier M, Michel JP, et al. (1987) Alterations in the human immune response to the hepatitis B vaccine among the elderly. Cell Immunol 109: 89-96.
32. Haynes L, Eaton SM, Burns EM, Randall TD, Swain SL, (2005) Newly generated CD4 T cells in aged animals do not exhibit age-related defects in response to antigen. J Exp Med 201: 845-51.
33. Jones SC, Clise-Dwyer K, Huston G, Dibble J, Eaton S, et al. (2008) Impact of post-thymic cellular longevity on the development of age-associated CD4+ T cell defects. J Immunol 180: 4465-4475.
34. Tsukamoto H, Clise-Dwyer K, Huston GE, Duso DK, Buck AL, et al. (2009) Age-associated increase in lifespan of naive CD4 T cells contributes to T-cell homeostasis but facilitates development of functional defects. Proc Natl Acad Sci U S A 106: 18333-8.
35. Callard RE, Basten A, (1978) Immune function in aged mice. IV. Loss of T cell and B cell function in thymus-dependent antibody responses. Eur J Immunol 8: 552-8.
36. Mancebo E, Clemente J, Sanchez J, Ruiz-Contreras J, De Pablos P, et al. (2008) Longitudinal analysis of immune function in the first 3 years of life in thymectomized neonates during cardiac surgery. Clin Exp Immunol 154: 375-383.
37. Zlamy M, Prelog M, (2009) Thymectomy in early childhood: a model for premature T cell immunosenescence? Rejuvenation Res 12: 249-58.
38. Prelog M, Wilk C, Keller M, Karall T, Orth D, et al. (2008) Diminished response to tick-borne encephalitis vaccination in thymectomized children. Vaccine 26: 595-600.
39. Cho JH, Kim HO, Surh CD, Sprent J, (2010) T cell receptor-dependent regulation of lipid rafts controls naive CD8+ T cell homeostasis. Immunity 32: 214-26.
40. Palmer MJ, Mahajan VS, Chen J, Irvine DJ, Lauffenburger DA, (2011) Signaling thresholds govern heterogeneity in il-7-receptor-mediated responses of näi{dotless}ve cd8(+) t cells. Immunol Cell Biol 89: 581-94.
41. Zamoyska R, Basson A, Filby A, Legname G, Lovatt M, et al. (2003) The influence of the src-family kinases, Lck and Fyn, on T cell differentiation, survival and activation. Immunol Rev 191: 107-18.
42. Feinerman O, Veiga J, Dorfman JR, Germain RN, Altan-Bonnet G, (2008) Variability and robustness in T cell activation from regulated heterogeneity in protein levels. Science 321: 1081-4.
43. Surh CD, Sprent J, (2000) Homeostatic T cell proliferation: how far can T cells be activated to self-ligands? J Exp Med 192: F9-F14.
44. Jenkins MK, Chu HH, McLachlan JB, Moon JJ, (2010) On the composition of the preimmune repertoire of T cells specific for Peptide-major histocompatibility complex ligands. Annu Rev Immunol 28: 275-94.