Cell-intrinsic defects in the proliferative response of antiviral memory CD8 T cells in aged mice upon secondary infection

Journal of Immunology

Volumn 184, Issue 9, 2010, Pages 5151-5159

  Decman, Vilma ^a   Laidlaw, Brian J ^a   DiMenna, Lauren J ^a   Abdulla, Sarah ^a   Mozdzanowska, Krystyna ^a   Erikson, Jan ^a   Ertl, Hildegund C J ^a   Wherry, E John ^a  

^a WISTAR INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOPTIVE TRANSFER; AGED; ANIMAL EXPERIMENT; ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELLULAR IMMUNITY; CONTROLLED STUDY; INFLUENZA; INFLUENZA VIRUS; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SECONDARY INFECTION; VIRUS IMMUNITY; AGING; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; COMPARATIVE STUDY; CYTOTOXICITY TEST; DOG; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; ORTHOMYXOVIRUS; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; PATHOPHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION; TRANSPLANTATION; VACCINIA VIRUS; VIROLOGY;

EPITOPE;

ADOPTIVE TRANSFER; AGING; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CYTOTOXICITY TESTS, IMMUNOLOGIC; DOGS; EPITOPES, T-LYMPHOCYTE; GENETIC PREDISPOSITION TO DISEASE; IMMUNODOMINANT EPITOPES; IMMUNOLOGIC MEMORY; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; ORTHOMYXOVIRIDAE; ORTHOMYXOVIRIDAE INFECTIONS; T-LYMPHOCYTE SUBSETS; VACCINIA VIRUS;

EID: 77954478724     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902063     Document Type: Article

References (54)

1. Pawelec, G. 2006. Immunity and ageing in man. Exp. Gerontol. 41: 1239-1242.
2. Sandhu, S. K., and S. B. Mossad. 2001. Influenza in the older adult. Indications for the use of vaccine and antiviral therapy. Geriatrics 56: 43-44, 47-48, 51.
3. Schluger, N. W. 2007. Tuberculosis and nontuberculous mycobacterial infections in older adults. Clin. Chest Med. 28: 773-781, vi.
4. Schmader, K. 2001. Herpes zoster in older adults. Clin. Infect. Dis. 32: 1481-1486.
5. Cook, J. M., N. Gualde, L. Hessel, M. Mounier, J. P. Michel, F. Denis, and M. H. Ratinaud. 1987. Alterations in the human immune response to the hepatitis B vaccine among the elderly. Cell. Immunol. 109: 89-96.
6. Hainz, U., B. Jenewein, E. Asch, K. P. Pfeiffer, P. Berger, and B. Grubeck-Loebenstein. 2005. Insufficient protection for healthy elderly adults by tetanus and TBE vaccines. Vaccine 23: 3232-3235.
7. Haynes, L., and S. L. Swain. 2006. Why aging T cells fail: implications for vaccination. Immunity 24: 663-666.
8. Musher, D.M., A. J. Chapman, A. Goree, S. Jonsson, D. Briles, and R. E. Baughn. 1986. Natural and vaccine-related immunity to Streptococcus pneumoniae. J. Infect. Dis. 154: 245-256.
9. Vu, T., S. Farish, M. Jenkins, and H. Kelly. 2002. A meta-analysis of effectiveness of influenza vaccine in persons aged 65 years and over living in the community. Vaccine 20: 1831-1836.
10. Doria, G., G. Biozzi, D. Mouton, and V. Covelli. 1997. Genetic control of immune responsiveness, aging and tumor incidence. Mech. Ageing Dev. 96: 1-13.
11. Solana, R., G. Pawelec, and R. Tarazona. 2006. Aging and innate immunity. Immunity 24: 491-494.
12. van Duin, D., and A. C. Shaw. 2007. Toll-like receptors in older adults. J. Am. Geriatr. Soc. 55: 1438-1444.
13. Mescher, M. F., J. M. Curtsinger, P. Agarwal, K. A. Casey, M. Gerner, C. D. Hammerbeck, F. Popescu, and Z. Xiao. 2006. Signals required for programming effector and memory development by CD8+ T cells. Immunol. Rev. 211: 81-92.
14. Stout-Delgado, H. W., X. Yang, W. E. Walker, B. M. Tesar, and D. R. Goldstein. 2008. Aging impairs IFN regulatory factor 7 up-regulation in plasmacytoid dendritic cells during TLR9 activation. J. Immunol. 181: 6747-6756.
15. Weng, N. P. 2006. Aging of the immune system: how much can the adaptive immune system adapt? Immunity 24: 495-499.
16. 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.
17. Woodland, D. L., and M. A. Blackman. 2006. Immunity and age: living in the past? Trends Immunol. 27: 303-307.
18. Clambey, E. T., J. White, J. W. Kappler, and P. Marrack. 2008. Identification of two major types of age-associated CD8 clonal expansions with highly divergent properties. Proc. Natl. Acad. Sci. USA 105: 12997-13002.
19. Yager, E. J., M. Ahmed, K. Lanzer, T. D. Randall, D. L. Woodland, and M. A. Blackman. 2008. Age-associated decline in T cell repertoire diversity leads to holes in the repertoire and impaired immunity to influenza virus. J. Exp. Med. 205: 711-723.
20. Ely, K. H., M. Ahmed, J. E. Kohlmeier, A. D. Roberts, S. T. Wittmer, M. A. Blackman, and D. L. Woodland. 2007. Antigen-specific CD8+ T cell clonal expansions develop from memory T cell pools established by acute respiratory virus infections. J. Immunol. 179: 3535-3542.
21. Lang, A., J. D. Brien, I. Messaoudi, and J. Nikolich-Zugich. 2008. Age-related dysregulation of CD8+ T cell memory specific for a persistent virus is independent of viral replication. J. Immunol. 180: 4848-4857.
22. Clambey, E. T., J. W. Kappler, and P. Marrack. 2007. CD8 T cell clonal expansions & aging: a heterogeneous phenomenon with a common outcome. Exp. Gerontol. 42: 407-411.
23. Nishioka, T., J. Shimizu, R. Iida, S. Yamazaki, and S. Sakaguchi. 2006. CD4 +CD25+Foxp3+ T cells and CD4+CD25-Foxp3+ T cells in aged mice. J. Immunol. 176: 6586-6593.
24. Lages, C. S., I. Suffia, P. A. Velilla, B. Huang, G. Warshaw, D. A. Hildeman, Y. Belkaid, and C. Chougnet. 2008. Functional regulatory T cells accumulate in aged hosts and promote chronic infectious disease reactivation. J. Immunol. 181: 1835-1848.
25. Jones, S. C., K. Clise-Dwyer, G. Huston, J. Dibble, S. Eaton, L. Haynes, and S. L. Swain. 2008. Impact of post-thymic cellular longevity on the development of age-associated CD4+ T cell defects. J. Immunol. 180: 4465-4475.
26. Hobbs, M. V., W. O. Weigle, and D. N. Ernst. 1994. Interleukin-10 production by splenic CD4+ cells and cell subsets from young and old mice. Cell. Immunol. 154: 264-272.
27. Haynes, L., S. M. Eaton, E. M. Burns, T. D. Randall, and S. L. Swain. 2003. 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 100: 15053-15058.
28. Shi, J., and R. A. Miller. 1993. Differential tyrosine-specific protein phosphorylation in mouse T lymphocyte subsets. Effect of age. J. Immunol. 151: 730-739.
29. Tamir, A., M. D. Eisenbraun, G. G. Garcia, and R. A. Miller. 2000. Age-dependent alterations in the assembly of signal transduction complexes at the site of T cell/ APC interaction. J. Immunol. 165: 1243-1251.
30. Eaton, S. M., E. M. Burns, K. Kusser, T. D. Randall, and L. Haynes. 2004. Age-related defects in CD4 T cell cognate helper function lead to reductions in humoral responses. J. Exp. Med. 200: 1613-1622.
31. 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.
32. Ernst, D. N., W. O. Weigle, D. N. McQuitty, A. L. Rothermel, and M. V. Hobbs. 1989. Stimulation of murine T cell subsets with anti-CD3 antibody. Age-related defects in the expression of early activation molecules. J. Immunol. 142: 1413-1421.
33. Kapasi, Z. F., K. Murali-Krishna, M. L. McRae, and R. Ahmed. 2002. Defective generation but normal maintenance of memory T cells in old mice. Eur. J. Immunol. 32: 1567-1573.
34. Murasko, D. M., and J. Jiang. 2005. Response of aged mice to primary virus infections. Immunol. Rev. 205: 285-296.
35. Doherty, P. C. 1977. Diminished T cell surveillance function in old mice infected with lymphocyte choriomeningitis virus. Immunology 32: 751-754.
36. 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.
37. Effros, R. B., and R. L. Walford. 1983. Diminished T-cell response to influenza virus in aged mice. Immunology 49: 387-392.
38. 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.
39. Effros, R. B., and R. L. Walford. 1984. The effect of age on the antigen-presenting mechanism in limiting dilution precursor cell frequency analysis. Cell. Immunol. 88: 531-539.
40. Wherry, E. J., J. N. Blattman, K. Murali-Krishna, R. van der Most, and R. Ahmed. 2003. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77: 4911-4927.
41. Mozdzanowska, K., K. Maiese, and W. Gerhard. 2000. Th cell-deficient mice control influenza virus infection more effectively than Th- and B cell-deficient mice: evidence for a Th-independent contribution by B cells to virus clearance. J. Immunol. 164: 2635-2643.
42. Buchmeier, M. J., and A. J. Zajac. 1999. Lymphocytic choriomeningitis virus. In Persistent Viral Infections. R. Ahmed, and I. S. Y. Chen, eds. Wiley, New York, p. 575-605.
43. Wherry, E. J., V. Teichgräber, T. C. Becker, D. Masopust, S. M. Kaech, R. Antia, U. H. von Andrian, and R. Ahmed. 2003. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 4: 225-234.
44. Kaech, S. M., J. T. Tan, E. J. Wherry, B. T. Konieczny, C. D. Surh, and R. Ahmed. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4: 1191-1198.
45. Hikono, H., J. E. Kohlmeier, S. Takamura, S. T. Wittmer, A. D. Roberts, and D. L. Woodland. 2007. Activation phenotype, rather than central- or effectormemory phenotype, predicts the recall efficacy of memory CD8+ T cells. J. Exp. Med. 204: 1625-1636.
46. Lefrançois, L. 2006. Development, trafficking, and function of memory T-cell subsets. Immunol. Rev. 211: 93-103.
47. Badovinac, V. P., J. S. Haring, and J. T. Harty. 2007. Initial T cell receptor transgenic cell precursor frequency dictates critical aspects of the CD8(+) T cell response to infection. Immunity 26: 827-841.
48. Sarkar, S., V. Teichgräber, V. Kalia, A. Polley, D. Masopust, L. E. Harrington, R. Ahmed, and E. J. Wherry. 2007. Strength of stimulus and clonal competition impact the rate of memory CD8 T cell differentiation. J. Immunol. 179: 6704-6714.
49. Sarkar, S., V. Kalia, W. N. Haining, B. T. Konieczny, S. Subramaniam, and R. Ahmed. 2008. Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J. Exp. Med. 205: 625-640.
50. Joshi, N. S., W. Cui, A. Chandele, H. K. Lee, D. R. Urso, J. Hagman, L. Gapin, and S. M. Kaech. 2007. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27: 281-295.
51. Valenzuela, H. F., and R. B. Effros. 2002. Divergent telomerase and CD28 expression patterns in human CD4 and CD8 T cells following repeated encounters with the same antigenic stimulus. Clin. Immunol. 105: 117-125.
52. Boucher, N., T. Dufeu-Duchesne, E. Vicaut, D. Farge, R. B. Effros, and F. Schächter. 1998. CD28 expression in T cell aging and human longevity. Exp. Gerontol. 33: 267-282.
53. Henson, S. M., and A. N. Akbar. 2009. KLRG1-more than a marker for T cell senescence. Age 31: 285-291.
54. Kenyon, C. 2005. The plasticity of aging: insights from long-lived mutants. Cell 120: 449-460.