Heightened self-reactivity associated with selective survival, but not expansion, of naïve virus-specific CD8+ T cells in aged mice

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 5, 2016, Pages 1333-1338

  Quinn, Kylie M ^a   Zaloumis, Sophie G ^b   Cukalac, Tania ^a   Kan, Wan Ting ^a   Sng, Xavier Y X ^a   Mirams, Michiko ^a   Watson, Katherine A ^a   McCaw, James M ^b,c,d   Doherty, Peter C ^a,e   Thomas, Paul G ^e   Handel, Andreas ^f   La Gruta, Nicole L ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^e ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^f UNIVERSITY OF GEORGIA   (United States)

Author keywords

Aging; CD44+ virtual memory; CD5; Influenza A virus; Naive CD8+ T cells

Indexed keywords

CD5 ANTIGEN; CD8 ANTIGEN; EPITOPE; HERMES ANTIGEN; T LYMPHOCYTE RECEPTOR;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CELL AGING; CELL EXPANSION; CELL SPECIFICITY; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; FEMALE; INFLUENZA A; INFLUENZA A VIRUS; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE SUBPOPULATION; VIRUS LOAD; VIRUS STRAIN; YOUNG ADULT; ANIMAL; C57BL MOUSE; IMMUNOLOGY;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; MICE; MICE, INBRED C57BL;

EID: 84956657544     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1525167113     Document Type: Article

References (36)

1. CDC (2013) Influenza Activity - United States, 2012-13 Season and Composition of the 2013-14 Influenza Vaccine, Report Mamw. Available at www.cdc.gov/mmwr/preview/mmwrhtml/mm6223a5.htm. Accessed January 6, 2016.
2. Gardner EM, Gonzalez EW, Nogusa S, Murasko DM (2006) Age-related changes in the immune response to influenza vaccination in a racially diverse, healthy elderly population. Vaccine 24(10):1609-1614.
3. Nikolich-Žugich J (2014) Aging of the T cell compartment in mice and humans: From no naive expectations to foggy memories. J Immunol 193(6):2622-2629.
4. Decman V, et al. (2010) Cell-intrinsic defects in the proliferative response of antiviral memory CD8 T cells in aged mice upon secondary infection. J Immunol 184(9):5151-5159.
5. Jiang J, Fisher EM, Murasko DM (2013) Intrinsic defects in CD8 T cells with aging contribute to impaired primary antiviral responses. Exp Gerontol 48(6):579-586.
6. Renkema KR, Li G, Wu A, Smithey MJ, Nikolich-Žugich J (2014) Two separate defects affecting true naive or virtual memory T cell precursors combine to reduce naive T cell responses with aging. J Immunol 192(1):151-159.
7. Tscharke DC, Croft NP, Doherty PC, La Gruta NL (2015) Sizing up the key determinants of the CD8(+) T cell response. Nat Rev Immunol 15(11):705-716.
8. Cukalac T, et al. (2014) The influenza virus-specific CTL immunodominance hierarchy in mice is determined by the relative frequency of high-avidity T cells. J Immunol 192(9):4061-4068.
9. Jenkins MK, Moon JJ (2012) The role of naive T cell precursor frequency and recruitment in dictating immune response magnitude. J Immunol 188(9):4135-4140.
10. La Gruta NL, et al. (2010) Primary CTL response magnitude in mice is determined by the extent of naive T cell recruitment and subsequent clonal expansion. J Clin Invest 120(6):1885-1894.
11. Ahmed M, et al. (2009) Clonal expansions and loss of receptor diversity in the naive CD8 T cell repertoire of aged mice. J Immunol 182(2):784-792.
12. Goronzy JJ, Lee WW, Weyand CM (2007) Aging and T-cell diversity. Exp Gerontol 42(5):400-406.
13. Yager EJ, et al. (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(3):711-723.
14. Decman V, et al. (2012) Defective CD8 T cell responses in aged mice are due to quantitative and qualitative changes in virus-specific precursors. J Immunol 188(4):1933-1941.
15. Chiu B-C, Martin BE, Stolberg VR, Chensue SW (2013) Cutting edge: Central memory CD8 T cells in aged mice are virtual memory cells. J Immunol 191(12):5793-5796.
16. Rudd BD, et al. (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(33):13694-13699.
17. Dash P, et al. (2011) Paired analysis of TCRα and TCRβ chains at the single-cell level in mice. J Clin Invest 121(1):288-295.
18. Kedzierska K, Turner SJ, Doherty PC (2004) Conserved T cell receptor usage in primary and recall responses to an immunodominant influenza virus nucleoprotein epitope. Proc Natl Acad Sci USA 101(14):4942-4947.
19. La Gruta NL, et al. (2008) Epitope-specific TCRbeta repertoire diversity imparts no functional advantage on the CD8+ T cell response to cognate viral peptides. Proc Natl Acad Sci USA 105(6):2034-2039.
20. Turner SJ, Diaz G, Cross R, Doherty PC (2003) Analysis of clonotype distribution and persistence for an influenza virus-specific CD8+ T cell response. Immunity 18(4):549-559.
21. Thomas PG, etal. (2007) Hidden epitopes emerge in secondary influenza virus-specific CD8+ T cell responses. J Immunol 178(5):3091-3098.
22. Valkenburg SA, et al. (2012) Early priming minimizes the age-related immune compromise of CD8+ T cell diversity and function. PLoS Pathog 8(2):e1002544.
23. Po JL, Gardner EM, Anaraki F, Katsikis PD, Murasko DM (2002) Age-associated decrease in virus-specific CD8+ T lymphocytes during primary influenza infection. Mech Ageing Dev 123(8):1167-1181.
24. Moon JJ, et al. (2007) Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27(2):203-213.
25. Obar JJ, Khanna KM, Lefrançois L (2008) Endogenous naive CD8+ T cell precursor frequency regulates primary and memory responses to infection. Immunity 28(6):859-869.
26. Cukalac T, et al. (2015) Paired TCRap analysis of virus-specific CD8(+) T cells exposes diversity in a previously defined 'narrow' repertoire. Immunol Cell Biol 93(9):804-814.
27. Azzam HS, et al. (1998) CD5 expression is developmentally regulated by T cell receptor (TCR) signals and TCR avidity. J Exp Med 188(12):2301-2311.
28. Mandl JN, Monteiro JP, Vrisekoop N, Germain RN (2013) T cell-positive selection uses self-ligand binding strength to optimize repertoire recognition of foreign antigens. Immunity 38(2):263-274.
29. Fulton RB, et al. (2015) The TCR's sensitivity to self peptide-MHC dictates the ability of naive CD8(+) T cells to respond to foreign antigens. Nat Immunol 16(1):107-117.
30. Chu HH, Moon JJ, Kruse AC, Pepper M, Jenkins MK (2010) Negative selection and peptide chemistry determine the size of naive foreign peptide-MHC class II-specific CD4+ T cell populations. J Immunol 185(8):4705-4713.
31. Akue AD, Lee JY, Jameson SC (2012) Derivation and maintenance of virtual memory CD8 T cells. J Immunol 188(6):2516-2523.
32. Haluszczak C, etal. (2009) The antigen-specificCD8+Tcell repertoire in unimmunized mice includes memory phenotype cells bearing markers of homeostatic expansion. J Exp Med 206(2):435-448.
33. Takada K, Jameson SC (2009) Self-class I MHC molecules support survival of naive CD8 T cells, but depress their functional sensitivity through regulation of CD8 expression levels. J Exp Med 206(10):2253-2269.
34. La Gruta NL, Turner SJ, Doherty PC (2004) Hierarchies in cytokine expression profiles for acute and resolving influenza virus-specific CD8+ T cell responses: Correlation of cytokine profile and TCR avidity. J Immunol 172(9):5553-5560.
35. Wang Y, Naumann U, Wright ST, Warton DI (2012) mvabund - an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3:471-474.
36. Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3:89-101.