Stability and function of secondary Th1 memory cells are dependent on the nature of the secondary stimulus

Journal of Immunology

Volumn 189, Issue 5, 2012, Pages 2348-2355

  Kim, Chulwoo ^a   Jay, David C ^a   Williams, Matthew A ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SURVIVAL; HEPATITIS; IMMUNE RESPONSE; IMMUNOLOGICAL PARAMETERS; LISTERIOSIS; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; LYMPHOCYTE MIGRATION; LYMPHOCYTIC CHORIOMENINGITIS; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SECONDARY CHALLENGE; STIMULUS RESPONSE; TH1 MEMORY CELL; TURNOVER TIME;

AMINO ACID SEQUENCE; ANIMALS; CELL SURVIVAL; CERCOPITHECUS AETHIOPS; CRICETINAE; EPITOPES, T-LYMPHOCYTE; IMMUNIZATION, SECONDARY; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; TH1 CELLS; VERO CELLS;

EID: 84865405358     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200244     Document Type: Article

References (40)

1. Prlic, M., M. A. Williams, and M. J. Bevan. 2007. Requirements for CD8 T-cell priming, memory generation and maintenance. Curr. Opin. Immunol. 19: 315-319.
2. Williams, M. A., and M. J. Bevan. 2007. Effector and memory CTL differentiation. Annu. Rev. Immunol. 25: 171-192.
3. Amanna, I. J., M. K. Slifka, and S. Crotty. 2006. Immunity and immunological memory following smallpox vaccination. Immunol. Rev. 211: 320-337.
4. Hammarlund, E., M. W. Lewis, S. G. Hansen, L. I. Strelow, J. A. Nelson, G. J. Sexton, J. M. Hanifin, and M. K. Slifka. 2003. Duration of antiviral immunity after smallpox vaccination. Nat. Med. 9: 1131-1137.
5. Hammarlund, E., M. W. Lewis, J. M. Hanifin, M. Mori, C. W. Koudelka, and M. K. Slifka. 2010. Antiviral immunity following smallpox virus infection: a case-control study. J. Virol. 84: 12754-12760.
6. Homann, D., L. Teyton, and M. B. A. Oldstone. 2001. Differential regulation of antiviral T-cell immunity results in stable CD8+ but declining CD4+ T-cell memory. Nat. Med. 7: 913-919.
7. Pepper, M., A. J. Pagán, B. Z. Igyártó, J. J. Taylor, and M. K. Jenkins. 2011. Opposing signals from the Bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells. Immunity 35: 583-595.
8. Williams, M. A., E. V. Ravkov, and M. J. Bevan. 2008. Rapid culling of the CD4+ T cell repertoire in the transition from effector to memory. Immunity 28: 533-545.
9. Lenz, D. C., S. K. Kurz, E. Lemmens, S. P. Schoenberger, J. Sprent, M. B. Oldstone, and D. Homann. 2004. IL-7 regulates basal homeostatic proliferation of antiviral CD4+T cell memory. Proc. Natl. Acad. Sci. USA 101: 9357-9362.
10. Surh, C. D., and J. Sprent. 2008. Homeostasis of naive and memory T cells. Immunity 29: 848-862.
11. van Leeuwen, E. M., J. Sprent, and C. D. Surh. 2009. Generation and maintenance of memory CD4(+) T Cells. Curr. Opin. Immunol. 21: 167-172.
12. Janssen, E. M., E. E. Lemmens, T. Wolfe, U. Christen, M. G. von Herrath, and S. P. Schoenberger. 2003. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421: 852-856.
13. Shedlock, D. J., and H. Shen. 2003. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300: 337-339.
14. Sun, J. C., and M. J. Bevan. 2003. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300: 339-342.
15. Bachmann, M. F., P. Wolint, S. Walton, K. Schwarz, and A. Oxenius. 2007. Differential role of IL-2R signaling for CD8+ T cell responses in acute and chronic viral infections. Eur. J. Immunol. 37: 1502-1512.
16. Williams, M. A., A. J. Tyznik, and M. J. Bevan. 2006. Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells. Nature 441: 890-893.
17. Kaech, S. M., and R. Ahmed. 2001. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naïve cells. Nat. Immunol. 2: 415-422.
18. Prlic, M., G. Hernandez-Hoyos, and M. J. Bevan. 2006. Duration of the initial TCR stimulus controls the magnitude but not functionality of the CD8+ T cell response. J. Exp. Med. 203: 2135-2143.
19. van Stipdonk, M. J., G. Hardenberg, M. S. Bijker, E. E. Lemmens, N. M. Droin, D. R. Green, and S. P. Schoenberger. 2003. Dynamic programming of CD8+ T lymphocyte responses. Nat. Immunol. 4: 361-365.
20. Obst, R., H.-M. van Santen, D. Mathis, and C. Benoist. 2005. Antigen persistence is required throughout the expansion phase of a CD4(+) T cell response. J. Exp. Med. 201: 1555-1565.
21. Ravkov, E. V., and M. A. Williams. 2009. The magnitude of CD4+ T cell recall responses is controlled by the duration of the secondary stimulus. J. Immunol. 183: 2382-2389.
22. Williams, M. A., and M. J. Bevan. 2004. Shortening the infectious period does not alter expansion of CD8 T cells but diminishes their capacity to differentiate into memory cells. J. Immunol. 173: 6694-6702.
23. Gett, A. V., F. Sallusto, A. Lanzavecchia, and J. Geginat. 2003. T cell fitness determined by signal strength. Nat. Immunol. 4: 355-360.
24. Jelley-Gibbs, D. M., D. M. Brown, J. P. Dibble, L. Haynes, S. M. Eaton, and S. L. Swain. 2005. Unexpected prolonged presentation of influenza antigens promotes CD4 T cell memory generation. J. Exp. Med. 202: 697-706.
25. Lanzavecchia, A., and F. Sallusto. 2002. Progressive differentiation and selection of the fittest in the immune response. Nat. Rev. Immunol. 2: 982-987.
26. Román, E., E. Miller, A. Harmsen, J. Wiley, U. H. Von Andrian, G. Huston, and S. L. Swain. 2002. CD4 effector T cell subsets in the response to influenza: heterogeneity, migration, and function. J. Exp. Med. 196: 957-968.
27. Swain, S. L., J. N. Agrewala, D. M. Brown, D. M. Jelley-Gibbs, S. Golech, G. Huston, S. C. Jones, C. Kamperschroer, W. H. Lee, K. K. McKinstry, et al. 2006. CD4+ T-cell memory: generation and multi-faceted roles for CD4+ T cells in protective immunity to influenza. Immunol. Rev. 211: 8-22.
28. McHeyzer-Williams, M. G., and M. M. Davis. 1995. Antigen-specific development of primary and memory T cells in vivo. Science 268: 106-111.
29. Savage, P. A., J. J. Boniface, and M. M. Davis. 1999. A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity 10: 485-492.
30. Oxenius, A., M. F. Bachmann, R. M. Zinkernagel, and H. Hengartner. 1998. Virus-specific MHC-class II-restricted TCR-transgenic mice: effects on humoral and cellular immune responses after viral infection. Eur. J. Immunol. 28: 390-400.
31. Ahmed, R., A. Salmi, L. D. Butler, J. M. Chiller, and M. B. Oldstone. 1984. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J. Exp. Med. 160: 521-540.
32. Shen, H., M. K. Slifka, M. Matloubian, E. R. Jensen, R. Ahmed, and J. F. Miller. 1995. Recombinant Listeria monocytogenes as a live vaccine vehicle for the induction of protective anti-viral cell-mediated immunity. Proc. Natl. Acad. Sci. USA 92: 3987-3991.
33. Slifka, M. K., H. Shen, M. Matloubian, E. R. Jensen, J. F. Miller, and R. Ahmed. 1996. Antiviral cytotoxic T-cell memory by vaccination with recombinant Listeria monocytogenes. J. Virol. 70: 2902-2910.
34. Homann, D., H. Lewicki, D. Brooks, J. Eberlein, V. Mallet-Designé, L. Teyton, and M. B. Oldstone. 2007. Mapping and restriction of a dominant viral CD4+ T cell core epitope by both MHC class I and MHC class II. Virology 363: 113-123.
35. Darrah, P. A., D. T. Patel, P. M. De Luca, R.W. Lindsay, D. F. Davey, B. J. Flynn, S. T. Hoff, P. Andersen, S. G. Reed, S. L. Morris, et al. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13: 843-850.
36. Seder, R. A., P. A. Darrah, and M. Roederer. 2008. T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 8: 247-258.
37. Marshall, H. D., A. Chandele, Y. W. Jung, H. Meng, A. C. Poholek, I. A. Parish, R. Rutishauser, W. Cui, S. H. Kleinstein, J. Craft, and S. M. Kaech. 2011. Differential expression of Ly6C and T-bet distinguish effector and memory Th1 CD4(+) cell properties during viral infection. Immunity 35: 633-646.
38. Slifka, M. K., and J. L. Whitton. 2001. Functional avidity maturation of CD8(+) T cells without selection of higher affinity TCR. Nat. Immunol. 2: 711-717.
39. Whitmire, J. K., N. Benning, and J. L. Whitton. 2006. Precursor frequency, nonlinear proliferation, and functional maturation of virus-specific CD4+ T cells. J. Immunol. 176: 3028-3036.
40. Purton, J. F., J. T. Tan, M. P. Rubinstein, D. M. Kim, J. Sprent, and C. D. Surh. 2007. Antiviral CD4+ memory T cells are IL-15 dependent. J. Exp. Med. 204: 951-961.