Cutting edge: The aging immune system reveals the biological impact of direct antigen presentation on CD8 T cell responses

Journal of Immunology

Volumn 199, Issue 2, 2017, Pages 403-407

  Uhrlaub, Jennifer L ^a,b   Smithey, Megan J ^a,b   Nikolich Zugich, Janko ^a,b  

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

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; COWPOX VIRUS; CPXV12 GENE; CPXV203 GENE; CROSS PRESENTATION; IMMUNE EVASION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS GENE; ANIMAL; C57BL MOUSE; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PATHOGENICITY;

HLA ANTIGEN CLASS 1; VIRAL PROTEIN; VIRUS ANTIGEN;

AGING; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; COWPOX VIRUS; CROSS-PRIMING; HISTOCOMPATIBILITY ANTIGENS CLASS I; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; VIRAL PROTEINS;

EID: 85023193088     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1700625     Document Type: Article

References (30)

1. Hanna, W. 1913. Studies in Small-Pox and Vaccination. John Wright and Sons, Ltd., London.
2. Fang, M., F. Roscoe, and L. J. Sigal. 2010. Age-dependent susceptibility to a viral disease due to decreased natural killer cell numbers and trafficking. J. Exp. Med. 207: 2369-2381.
3. Smithey, M. J., K. R. Renkema, B. D. Rudd, and J. Nikolich-? Zugich. 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.
4. Brien, J. D., J. L. Uhrlaub, A. Hirsch, C. A. Wiley, and J. Nikolich-Zugich. 2009. Key role of T cell defects in age-related vulnerability to West Nile virus. J. Exp. Med. 206: 2735-2745.
5. 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.
6. Bhadra, R., M. M. Moretto, J. C. Castillo, C. Petrovas, S. Ferrando-Martinez, U. Shokal, M. Leal, R. A. Koup, I. Eleftherianos, and I. A. Khan. 2014. Intrinsic TGF-β signaling promotes age-dependent CD8+ T cell polyfunctionality attrition. J. Clin. Invest. 124: 2441-2455.
7. 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.
8. Uhrlaub, J. L., J. D. Brien, D. G. Widman, P. W. Mason, and J. Nikolich-Zugich. 2011. Repeated in vivo stimulation of T and B cell responses in old mice generates protective immunity against lethal West Nile virus encephalitis. J. Immunol. 186: 3882-3891.
9. Schuren, A. B., A. I. Costa, and E. J. Wiertz. 2016. Recent advances in viral evasion of the MHC Class I processing pathway. Curr. Opin. Immunol. 40: 43-50.
10. Byun, M., M. C. Verweij, D. J. Pickup, E. J. Wiertz, T. H. Hansen, and W. M. Yokoyama. 2009. Two mechanistically distinct immune evasion proteins of cowpox virus combine to avoid antiviral CD8 T cells. Cell Host Microbe 6: 422-432.
11. McCoy IV, W. H., X. Wang, W. M. Yokoyama, T. H. Hansen, and D. H. Fremont. 2013. Cowpox virus employs a two-pronged strategy to outflank MHCI antigen presentation. Mol. Immunol. 55: 156-158.
12. Alzhanova, D., D. M. Edwards, E. Hammarlund, I. G. Scholz, D. Horst, M. J. Wagner, C. Upton, E. J. Wiertz, M. K. Slifka, and K. Fruh. 2009. Cowpox virus inhibits the transporter associated with antigen processing to evade T cell recognition. Cell Host Microbe 6: 433-445.
13. Dasgupta, A., E. Hammarlund, M. K. Slifka, and K. Fruh. 2007. Cowpox virus evades CTL recognition and inhibits the intracellular transport of MHC class I molecules. J. Immunol. 178: 1654-1661.
14. Luteijn, R. D., H. Hoelen, E. Kruse, W. F. van Leeuwen, J. Grootens, D. Horst, M. Koorengevel, J. W. Drijfhout, E. Kremmer, K. Fruh, et al. 2014. Cowpox virus protein CPXV012 eludes CTLs by blocking ATP binding to TAP. J. Immunol. 193: 1578-1589.
15. Byun, M., X. Wang, M. Pak, T. H. Hansen, and W. M. Yokoyama. 2007. Cowpox virus exploits the endoplasmic reticulum retention pathway to inhibit MHC class I transport to the cell surface. Cell Host Microbe 2: 306-315.
16. Bevan, M. J. 1976. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J. Exp. Med. 143: 1283-1288.
17. Bevan, M. J. 2006. Cross-priming. Nat. Immunol. 7: 363-365.
18. Gainey, M. D., J. G. Rivenbark, H. Cho, L. Yang, and W. M. Yokoyama. 2012. Viral MHC class I inhibition evades CD8+ T-cell effector responses in vivo but not CD8+ T-cell priming. Proc. Natl. Acad. Sci. USA 109: E3260-E3267.
19. Rudd, B. D., V. Venturi, G. Li, P. Samadder, J. M. Ertelt, S. S. Way, M. P. Davenport, and J. Nikolich-? Zugich. 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.
20. Pecaut, M. J., A. L. Smith, T. A. Jones, and D. S. Gridley. 2000. Modification of immunologic and hematologic variables by method of CO2 euthanasia. Comp. Med. 50: 595-602.
21. Jenkins, M. K., and J. J. Moon. 2012. The role of naive T cell precursor frequency and recruitment in dictating immune response magnitude. J. Immunol. 188: 4135-4140.
22. Hamilton, S. E., J. M. Schenkel, A. D. Akue, and S. C. Jameson. 2010. IL-2 complex treatment can protect naive mice from bacterial and viral infection. J. Immunol. 185: 6584-6590.
23. Smithey, M. J., S. Brandt, N. E. Freitag, D. E. Higgins, and H. G. Bouwer. 2008. Stimulation of enhanced CD8 T cell responses following immunization with a hyper-antigen secreting intracytosolic bacterial pathogen. J. Immunol. 180: 3406-3416.
24. Smithey, M. J., G. Li, V. Venturi, M. P. Davenport, and J. Nikolich-? Zugich. 2012. Lifelong persistent viral infection alters the naive T cell pool, impairing CD8 T cell immunity in late life. J. Immunol. 189: 5356-5366.
25. 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.
26. Chougnet, C. A., R. I. Thacker, H. M. Shehata, C. M. Hennies, M. A. Lehn, C. S. Lages, and E. M. Janssen. 2015. Loss of phagocytic and antigen crosspresenting capacity in aging dendritic cells is associated with mitochondrial dysfunction. J. Immunol. 195: 2624-2632.
27. Zacca, E. R., M. I. Crespo, R. P. Acland, E. Roselli, N. G. Núnẽz, M. Maccioni, B. A. Maletto, M. C. Pistoresi-Palencia, and G. Morón. 2015. Aging impairs the ability of conventional dendritic cells to cross-prime CD8+ T cells upon stimulation with a TLR7 ligand. PLoS One 10: e0140672.
28. Li, G., M. J. Smithey, B. D. Rudd, and J. Nikolich-? Zugich. 2012. Age-associated alterations in CD8a+ dendritic cells impair CD8 T-cell expansion in response to an intracellular bacterium. Aging Cell 11: 968-977.
29. Hickman, H. D., K. Takeda, C. N. Skon, F. R. Murray, S. E. Hensley, J. Loomis, G. N. Barber, J. R. Bennink, and J. W. Yewdell. 2008. Direct priming of antiviral CD8+ T cells in the peripheral interfollicular region of lymph nodes. Nat. Immunol. 9: 155-165.
30. Richner, J. M., G. B. Gmyrek, J. Govero, Y. Tu, G. J. van der Windt, T. U. Metcalf, E. K. Haddad, J. Textor, M. J. Miller, and M. S. Diamond. 2015. Age-dependent cell trafficking defects in draining lymph nodes impair adaptive immunity and control of West Nile virus infection. PLoS Pathog. 11: e1005027.