Two separate defects affecting true naive or virtual memory T cell precursors combine to reduce naive T cell responses with aging

Journal of Immunology

Volumn 192, Issue 1, 2014, Pages 151-159

  Renkema, Kristin R ^a   Li, Gang ^a   Wu, Angela ^a   Smithey, Megan J ^a   Nikolich Žugich, Janko ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE RECEPTOR; INTERLEUKIN 15; INTERLEUKIN 2 RECEPTOR BETA; INTERLEUKIN 7; T LYMPHOCYTE RECEPTOR;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SELECTION; CELL SPECIFICITY; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNE RESPONSE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRE T LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; UPREGULATION; WILD TYPE;

EID: 84891060089     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301453     Document Type: Article

References (43)

1. Murasko, D. M., and J. Jiang. 2005. Response of aged mice to primary virus infections. Immunol. Rev. 205: 285-296.
2. Nikolich-Žugich, J., G. Li, J. L. Uhrlaub, K. R. Renkema, and M. J. Smithey. 2012. Age-related changes in CD8 T cell homeostasis and immunity to infection. Semin. Immunol. 24: 356-364.
3. Woodland, D. L., and M. A. Blackman. 2006. Immunity and age: living in the past? Trends Immunol. 27: 303-307.
4. Naylor, K., G. Li, A. N. Vallejo, W. W. Lee, K. Koetz, E. Bryl, J. Witkowski, J. Fulbright, C. M. Weyand, and J. J. Goronzy. 2005. The influence of age on T cell generation and TCR diversity. J. Immunol. 174: 7446-7452.
5. Cicin-Sain, L., I. Messaoudi, B. Park, N. Currier, S. Planer, M. Fischer, S. Tackitt, D. Nikolich-Žugich, A. Legasse, M. K. Axthelm, et al. 2007. Dramatic increase in naive T cell turnover is linked to loss of naive T cells from old primates. Proc. Natl. Acad. Sci. USA 104: 19960-19965.
6. Messaoudi, I., J. Lemaoult, J. A. Guevara-Patino, B. M. Metzner, and J. Nikolich-Žugich. 2004. Age-related CD8 T cell clonal expansions constrict CD8 T cell repertoire and have the potential to impair immune defense. J. Exp. Med. 200: 1347-1358.
7. Ahmed, M., K. G. Lanzer, E. J. Yager, P. S. Adams, L. L. Johnson, and M. A. Blackman. 2009. Clonal expansions and loss of receptor diversity in the naive CD8 T cell repertoire of aged mice. J. Immunol. 182: 784-792.
8. den Braber, I., T. Mugwagwa, N. Vrisekoop, L. Westera, R. Mögling, A. B. de Boer, N. Willems, E. H. Schrijver, G. Spierenburg, K. Gaiser, et al. 2012. Maintenance of peripheral naive T cells is sustained by thymus output in mice but not humans. Immunity 36: 288-297.
9. Rudd, B. D., V. Venturi, G. Li, P. Samadder, J. M. Ertelt, S. S. Way, M. P. Davenport, and J. Nikolich-Žugich. 2011. Nonrandom attrition of the naive CD8+ T-cell pool with aging governed by T-cell receptor:pMHC interactions. Proc. Natl. Acad. Sci. USA 108: 13694-13699.
10. Haluszczak, C., A. D. Akue, S. E. Hamilton, L. D. Johnson, L. Pujanauski, L. Teodorovic, S. C. Jameson, and R. M. Kedl. 2009. The antigen-specific CD8+ T cell repertoire in unimmunized mice includes memory phenotype cells bearing markers of homeostatic expansion. J. Exp. Med. 206: 435-448.
11. Hogquist, K. A., S. C. Jameson, W. R. Heath, J. L. Howard, M. J. Bevan, and F. R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell 76: 17-27.
12. Barnden, M. J., J. Allison, W. R. Heath, and F. R. Carbone. 1998. Defective TCR expression in transgenic mice constructed using cDNA-based a- and b-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76: 34-40.
13. Pircher, H., P. S. Ohashi, R. L. Boyd, H. Hengartner, and K. Brduscha. 1994. Evidence for a selective and multi-step model of T cell differentiation: CD4+ CD8low thymocytes selected by a transgenic T cell receptor on major histocompatibility complex class I molecules. Eur. J. Immunol. 24: 1982-1987.
14. Mueller, S. N., W. Heath, J. D. McLain, F. R. Carbone, and C. M. Jones. 2002. Characterization of two TCR transgenic mouse lines specific for herpes simplex virus. Immunol. Cell Biol. 80: 156-163.
15. Smithey, M. J., K. R. Renkema, B. D. Rudd, and J. Nikolich-Žugich. 2011. Increased apoptosis, curtailed expansion and incomplete differentiation of CD8+ T-cells combine to decrease clearance of L. monocytogenes in old mice. Eur. J. Immunol. 41: 1352-1364.
16. Kedl, R. M., and M. F. Mescher. 1997. Migration and activation of antigenspecific CD8+ T cells upon in vivo stimulation with allogeneic tumor. J. Immunol. 159: 650-663.
17. Akue, A. D., J. Y. Lee, and S. C. Jameson. 2012. Derivation and maintenance of virtual memory CD8 T cells. J. Immunol. 188: 2516-2523.
18. Weinreich, M. A., O. A. Odumade, S. C. Jameson, and K. A. Hogquist. 2010. T cells expressing the transcription factor PLZF regulate the development of memory-like CD8+ T cells. Nat. Immunol. 11: 709-716.
19. Sprent, J., and C. D. Surh. 2011. Normal T cell homeostasis: the conversion of naive cells into memory-phenotype cells. Nat. Immunol. 12: 478-484.
20. Padovan, E., G. Casorati, P. Dellabona, S. Meyer, M. Brockhaus, and A. Lanzavecchia. 1993. Expression of two T cell receptor a chains: dual receptor T cells. Science 262: 422-424.
21. Heath, W. R., F. R. Carbone, P. Bertolino, J. Kelly, S. Cose, and J. F. Miller. 1995. Expression of two T cell receptor a chains on the surface of normal murine T cells. Eur. J. Immunol. 25: 1617-1623.
22. Alam, S. M., and N. R. Gascoigne. 1998. Posttranslational regulation of TCRVa allelic exclusion during T cell differentiation. J. Immunol. 160: 3883-3890.
23. Wilson, A., H. Pircher, P. Ohashi, and H. R. MacDonald. 1992. Analysis of immature (CD42CD82) thymic subsets in T-cell receptor ab transgenic mice. Dev. Immunol. 2: 85-94.
24. Jiang, J., D. Gross, P. Elbaum, and D. M. Murasko. 2007. Aging affects initiation and continuation of T cell proliferation. Mech. Ageing Dev. 128: 332-339.
25. Song, L., Y. H. Kim, R. K. Chopra, J. J. Proust, J. E. Nagel, A. A. Nordin, and W. H. Adler. 1993. Age-related effects in T cell activation and proliferation. Exp. Gerontol. 28: 313-321.
26. Hertogh-Huijbregts, A., C. Vissinga, J. Rozing, and L. Nagelkerken. 1990. Impairment of CD3-dependent and CD3-independent activation pathways in CD4+ and in CD8+ T cells from old CBA/RIJ mice. Mech. Ageing Dev. 53: 141-155.
27. Lages, C. S., I. Lewkowich, A. Sproles, M. Wills-Karp, and C. Chougnet. 2010. Partial restoration of T-cell function in aged mice by in vitro blockade of the PD-1/PD-L1 pathway. Aging Cell 9: 785-798.
28. Moon, J. J., H. H. Chu, M. Pepper, S. J. McSorley, S. C. Jameson, R. M. Kedl, and M. K. Jenkins. 2007. Naive CD4+ T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27: 203-213.
29. Tscharke, D. C., G. Karupiah, J. Zhou, T. Palmore, K. R. Irvine, S. M. Haeryfar, S. Williams, J. Sidney, A. Sette, J. R. Bennink, and J. W. Yewdell. 2005. Identification of poxvirus CD8+ T cell determinants to enable rational design and characterization of smallpox vaccines. J. Exp. Med. 201: 95-104.
30. Brien, J. D., J. L. Uhrlaub, and J. Nikolich-Žugich. 2007. Protective capacity and epitope specificity of CD8+ T cells responding to lethal West Nile virus infection. Eur. J. Immunol. 37: 1855-1863.
31. Goronzy, J. J., G. Li, M. Yu, and C. M. Weyand. 2012. Signaling pathways in aged T cells: a reflection of T cell differentiation, cell senescence and host environment. Semin. Immunol. 24: 365-372.
32. Decman, V., B. J. Laidlaw, T. A. Doering, J. Leng, H. C. Ertl, D. R. Goldstein, and E. J. Wherry. 2012. Defective CD8 T cell responses in aged mice are due to quantitative and qualitative changes in virus-specific precursors. J. Immunol. 188: 1933-1941.
33. Lai, D., J. Zhu, T. Wang, J. Hu-Li, M. Terabe, J. A. Berzofsky, C. Clayberger, and A. M. Krensky. 2011. KLF13 sustains thymic memory-like CD8+ T cells in BALB/c mice by regulating IL-4-generating invariant natural killer T cells. J. Exp. Med. 208: 1093-1103.
34. Ji, Q., A. Perchellet, and J. M. Goverman. 2010. Viral infection triggers central nervous system autoimmunity via activation of CD8+ T cells expressing dual TCRs. Nat. Immunol. 11: 628-634.
35. Lemaire, M. M., L. Dumoutier, G. Warnier, C. Uyttenhove, J. Van Snick, M. de Heusch, M. Stevens, and J. C. Renauld. 2011. Dual TCR expression biases lung inflammation in DO11.10 transgenic mice and promotes neutrophilia via microbiota-induced Th17 differentiation. J. Immunol. 187: 3530-3537.
36. Su, L. F., B. A. Kidd, A. Han, J. J. Kotzin, and M. M. Davis. 2013. Virus-specific CD4+ memory-phenotype T cells are abundant in unexposed adults. Immunity 38: 373-383.
37. Li, S. P., Z. Cai, W. Shi, A. Brunmark, M. Jackson, and P. J. Linton. 2002. Early antigen-specific response by naive CD8 T cells is not altered with aging. J. Immunol. 168: 6120-6127.
38. Plowden, J., M. Renshaw-Hoelscher, S. Gangappa, C. Engleman, J. M. Katz, and S. Sambhara. 2004. Impaired antigen-induced CD8+ T cell clonal expansion in aging is due to defects in antigen presenting cell function. Cell. Immunol. 229: 86-92.
39. Norian, L. A., and P. M. Allen. 2004. No intrinsic deficiencies in CD8+ T cellmediated antitumor immunity with aging. J. Immunol. 173: 835-844.
40. Miller, R. A., and O. Stutman. 1981. Decline, in aging mice, of the anti-2,4,6-trinitrophenyl (TNP) cytotoxic T cell response attributable to loss of Lyt-2-, interleukin 2-producing helper cell function. Eur. J. Immunol. 11: 751-756.
41. Effros, R. B., and R. L. Walford. 1983. The immune response of aged mice to influenza: diminished T-cell proliferation, interleukin 2 production and cytotoxicity. Cell. Immunol. 81: 298-305.
42. Po, J. L., E. M. Gardner, F. Anaraki, P. D. Katsikis, and D. M. Murasko. 2002. Age-associated decrease in virus-specific CD8+ T lymphocytes during primary influenza infection. Mech. Ageing Dev. 123: 1167-1181.
43. Effros, R. B., and G. Pawelec. 1997. Replicative senescence of T cells: does the Hayflick Limit lead to immune exhaustion? Immunol. Today 18: 450-454.