Preapoptotic phenotype of viral epitope-specific CD8 T cells precludes memory development and is an intrinsic property of the epitope

Journal of Immunology

Volumn 173, Issue 8, 2004, Pages 5138-5147

  Wang, Xiaoting Z ^a   Brehm, Michael A ^a   Welsh, Raymond M ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; DNA FRAGMENT; EPITOPE; GAMMA INTERFERON; INTERLEUKIN 2; LIPOCORTIN 5; LYSYLALANYLVALYLTYROSYLASPARAGINYLPHENYLALANYLALANYLTHREONYLCYSTEINE; MONOCLONAL ANTIBODY CD3; PHENYLALANYLGLUTAMINYLPROLYLGLUTAMINYLASPARAGINYLGLYCYLGLUTAMINYLPHENYLALANYLISOLEUCINE; UNCLASSIFIED DRUG; VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; CELL TRANSFER; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MALE; MEMORY; MEMORY CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; SPLEEN; T LYMPHOCYTE; VACCINIA VIRUS; VIRUS MENINGITIS; VIRUS STRAIN;

EID: 6344291173     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.8.5138     Document Type: Article

References (55)

1. Ahmed, R., and D. Gray. 1996. Immunological memory and protective immunity: understanding their relation. Science 272:54.
2. Masopust, D., V. Vezys, A. L. Marzo, and L. Lefrancois. 2001. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291:2413.
3. Razvi, E. S., Z. Jiang, B. A. Woda, and R. M. Welsh. 1995. Lymphocyte apoptosis during the silencing of the immune response to acute viral infections in normal, Ipr, and Bcl-2-transgenic mice. Am. J. Pathol. 147:79.
4. Razvi, E. S., and R. M. Welsh. 1993. Programmed cell death of T lymphocytes during acute viral infection: a mechanism for virus-induced immune deficiency. J. Virol. 67:5754.
5. Zhou, S., R. Ou, L. Huang, and D. Moskophidis. 2002. Critical role for perforin-, Fas/FasL-, and TNFR1-mediated cytotoxic pathways in down-regulation of antigen-specific T cells during persistent viral infection. J. Virol. 76:829.
6. Lohman, B. L., and R. M. Welsh. 1998. Apoptotic regulation of T cells and absence of immune deficiency in virus-infected γ-interferon receptor knockout mice. J. Virol. 72:7815.
7. Onami, T. M., L. E. Harrington, M. A. Williams, M. Galvan, C. P. Larsen, T. C. Pearson, N. Manjunath, L. G. Baum, B. D. Pearce, and R. Ahmed. 2002. Dynamic regulation of T cell immunity by CD43. J. Immunol. 168:6022.
8. Zajac, A. J., J. M. Dye, and D. G. Quinn. 2003. Control of lymphocytic choriomeningitis virus infection in granzyme B deficient mice. Virology 305:1.
9. + T cell homeostasis by perforin and interferon-γ. Science 290:1354.
10. + T cells after infection. Nat. Immunol. 3:619.
11. Hockenberry, D., G. Nunez, C. Milliman, R. D. Schreiber, and S. J. Korsmeyer. 1990. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348:334.
12. + T cells. J. Immunol. 164:3950.
13. Lenardo, M., K. M. Chan, F. Hornung, H. McFarland, R. Siegel, J. Wang, and L. Zheng. 1999. Mature T lymphocyte apoptosis-immune regulation in a dynamic and unpredictable antigenic environment. Annu. Rev. Immunol. 17:221.
14. Schluns, K. S., and L. Lefrancois. 2003. Cytokine control of memory T-cell development and survival. Nat. Rev. Immunol. 3:269.
15. Schluns, K. S., W. C. Kieper, S. C. Jameson, and L. Lefrancois. 2000. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat. Immunol. 1:426.
16. Kondrack, R. M., J. Harbertson, J. T. Tan, M. E. McBreen, C. D. Surh, and L. M. Bradley. 2003. Interleukin 7 regulates the survival and generation of memory CD4 cells. J. Exp. Med. 198:1797.
17. 1, on virus-activated T cells. J. Immunol. 171:2804.
18. + T cells. J. Exp. Med. 195:1515.
19. 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.
20. van Engeland, M., L. J. Nieland, F. C. Ramaekers, B. Schutte, and C. P. Reutelingsperger. 1998. Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31:1.
21. Wang, X. Z., S. E. Stepp, M. A. Brehm, H. D. Chen, L. K. Selin, and R. M. Welsh. 2003, Virus-specific CD8 T cells in peripheral tissues are more resistant to apoptosis than those in lymphoid organs. Immunity 18:631.
22. Dillon, S. R., M. Mancini, A. Rosen, and M. S. Schlissel. 2000. Annexin V binds to viable B cells and colocalizes with a marker of lipid rafts upon B cell receptor activation. J. Immunol. 164:1322.
23. Span, L. F., A. H. Pennings, G. Vierwinden, J. B. Boezeman, R. A. Raymakers, and T. de Witte. 2002. The dynamic process of apoptosis analyzed by flow cytometry using Annexin-V/propidium iodide and a modified in situ end labeling technique. Cytometry 47:24.
24. Whitton, J. L., P. J. Southern, and M. B. Oldstone. 1988. Analyses of the cytotoxic T lymphocyte responses to glycoprotein and nucleoprotein components of lymphocytic choriomeningitis virus. Virology 162:321.
25. Daniels, K. A., G. Devora, W. C. Lai, C. L. O'Donnell, M. Bennett, and R. M. Welsh. 2001. Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49H. J. Exp. Med. 194:29.
26. Selin, L. K., M. Y. Lin, K. A. Kraemer, D. M. Pardoll, J. P. Schneck, S. M. Varga, P. A. Santolucito, A. K. Pinto, and R. M. Welsh. 1999. Attrition of T cell memory: selective loss of LCMV epitope-specific memory CD8 T cells following infections with heterologous viruses. Immunity 11:733.
27. + T cells are activated in peripheral blood and accumulate in cerebrospinal fluid from HAM/TSP patients. Proc. Natl. Acad. Sci. USA 95:7568.
28. b major histocompatibility complex class I molecules and presented to cytotoxic T lymphocytes. J. Virol. 69:2297.
29. Whitton, J. L., J. R. Gebhard, H. Lewicki, A. Tishon, and M. B. Oldstone. 1988. Molecular definition of a major cytotoxic T-lymphocyte epitope in the glycoprotein of lymphocytic choriomeningitis virus. J. Virol. 62:687.
30. Brehm, M. A., A. K. Pinto, K. A. Daniels, J. P. Schneck, R. M. Welsh, and L. K. Selin. 2002. T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens. Nat. Immunol. 3:627.
31. + T-lymphocyte responses to multiple epitopes from simian virus 40 (SV40) large T antigen in C57BL/6 mice immunized with SV40, SV40 T-antigen-transformed cells, or vaccinia virus recombinants expressing full-length T antigen or epitope minigenes. J. Virol. 74:6922.
32. Murali-Krishna, K., J. D. Altman, M. Suresh, D. J. Sourdive, A. J. Zajac, J. D. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8:177.
33. Bacso, Z., R. B. Everson, and J. F. Eliason. 2000. The DNA of annexin V-binding apoptotic cells is highly fragmented. Cancer Res. 60:4623.
34. Kim, S. K., M. A. Brehm, R. M. Welsh, and L. K. Selin. 2002. Dynamics of memory T cell proliferation under conditions of heterologous immunity and bystander stimulation. J. Immunol. 169:90.
35. Buchmeier, M. J., R. M. Welsh, F. J. Dutko, and M. B. Oldstone. 1980. The virology and immunobiology of lymphocytic choriomeningitis virus infection. Adv. Immunol. 30:275.
36. 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.
37. + T cells by infected dendritic cells in vivo. Nat. Immunol. 3:265.
38. Kasaian, M. T., and C. A. Biron. 1990. Effects of cyclosporin A on IL-2 production and lymphocyte proliferation during infection of mice with lymphocytic choriomeningitis virus. J. Immunol. 144:299.
39. Shedlock, D. J., and H. Shen. 2003. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300:337.
40. Sun, J. C., and M. J. Bevan. 2003. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300:339.
41. + T lymphocytes. Nature 421:852.
42. + T cells. J. Immunol. 166:7009.
43. + T lymphocyte differentiation as a mechanism for subdominant cytotoxic T lymphocyte responses to a viral antigen. J. Exp. Med. 191:1687.
44. b molecules is controlled by dominant negative elements at peptide non-anchor residues: implications for peptide selection and presentation. J. Biol. Chem. 271:17829.
45. + T cell responses during and after acute lymphocytic choriomeningitis virus infection. J. Immunol. 171:3928.
46. + T cells during viral infection. J. Immunol. 170:4745.
47. van der Most, R. G., K. Murali-Krishna, J. G. Lanier, E. J. Wherry, M. T. Puglielli, J. N. Blattman, A. Sette, and R. Ahmed. 2003. Changing immunodominance patterns in antiviral CD8 T-cell responses after loss of epitope presentation or chronic antigenic stimulation. Virology 315:93.
48. Zajac, A. J., J. N. Blattman, K. Murali-Krishna, D. J. Sourdive, M. Suresh, J. D. Altman, and R. Ahmed. 1998. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 188:2205.
49. Fuller, M. J., and A. J. Zajac. 2003. Ablation of CD8 and CD4 T cell responses by high viral loads. J. Immunol. 170:477.
50. 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.
51. Sallusto, F., D. Lenig, R. Forster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708.
52. + T cell responses from primary to persistent phases of Epstein-Barr virus infection. J. Exp. Med. 195:893.
53. +T cells. J. Immunol. 168:4184.
54. Obar, J. J., S. G. Crist, D. C. Gondek, and E. J. Usherwood. 2004. Different functional capacities of latent and lytic antigen-specific CD8 T cells in murine gammaherpesvirus infection. J. Immunol. 172:1213.
55. Pellegrini, M., G. Belz, P. Bouillet, and A. Strasser. 2003. Shutdown of an acute T cell immune response to viral infection is mediated by the proapoptotic Bcl-2 homology 3-only protein Bim. Proc. Natl. Acad. Sci. USA 100:14175.