Shaping and reshaping CD8+ T-cell memory

Nature Reviews Immunology

Volumn 8, Issue 2, 2008, Pages 107-119

  Harty, John T ^a   Badovinac, Vladimir P ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND; CHEMOKINE RECEPTOR CCR7; GAMMA INTERFERON; INTERLEUKIN 12; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIVIRAL ACTIVITY; APOPTOSIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; CELL POPULATION; CELL SHAPE; CELL SURVIVAL; CYTOKINE PRODUCTION; DENDRITIC CELL; EX VIVO STUDY; IMMUNE RESPONSE; IMMUNE STATUS; IMMUNOCOMPETENT CELL; INFLAMMATION; LISTERIA MONOCYTOGENES; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MEMORY T LYMPHOCYTE; NATURAL KILLER CELL; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; VACCINATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; HUMANS; IMMUNOLOGIC MEMORY; INFLAMMATION; LYMPHOCYTE ACTIVATION; MICE; TRANSGENES; VACCINATION;

EID: 38549096234     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri2251     Document Type: Review

References (131)

1. Jameson, S. C. Maintaining the norm: T-cell homeostasis. Nature Rev. Immunol. 2, 547-556 (2002).
2. Blattman, J. N. et al. Estimating the precursor frequency of naive antigen-specific CD8 T cells. J. Exp. Med. 195, 657-664 (2002).
3. Casrouge, A. et al. Size estimate of the αβTCR repertoire of naive mouse splenocytes. J. Immunol. 164, 5782-5787 (2000).
4. Kedzierska, K. et al. Quantification of repertoire diversity of influenza-specific epitopes with predominant public or private TCR usage. J. Immunol. 177, 6705-6712 (2006).
5. Pewe, L. L., Netland, J. M., Heard, S. B. & Perlman, S. Very diverse CD8 T cell clonotypic responses after virus infections. J. Immunol. 172, 3151-3156 (2004).
6. + T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27, 203-213 (2007).
7. Heath, W. R. & Carbone, F. R. Cross-presentation, dendritic cells, tolerance and immunity. Annu. Rev. Immunol. 19, 47-64 (2001).
8. Steinman, R. M., Hawiger, D. & Nussenzweig, M. C. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21, 685-711 (2003).
9. Germain, R. N., Miller, M. J., Dustin, M. L. & Nussenzweig, M. C. Dynamic imaging of the immune system: progress, pitfalls and promise. Nature Rev. Immunol. 6, 497-507 (2006).
10. + T cell response. Immunity 25, 19-29 (2006).
11. Kaech, S. M., Wherry, E. J. & Ahmed, R. Effector and memory T-cell differentiation: implications for vaccine development. Nature Rev. Immunol. 2, 251-262 (2002).
12. + T cells. Immunol. Rev. 211, 81-92 (2006).
13. + T-cell memory. Immunol. Rev. 211, 67-80 (2006).
14. + T cells. Proc. Natl Acad. Sci. USA 98, 6313-6318 (2001).
15. Masopust, D., Vezys, V., Marzo, A. L. & Lefrancois, L. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291, 2413-2417 (2001).
16. + T-cell memory. Nature Med. 7, 913-919 (2001).
17. Becker, T. C. et al. Interleukin 15 is required for proliferative renewal of virus-specific memory CD8 T cells. J. Exp. Med. 195, 1541-1548 (2002).
18. + T cells. J. Exp. Med. 195, 1515-1522 (2002).
19. Schluns, K. S., Kieper, W. C., Jameson, S. C. & Lefrancois, L. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nature Immunol. 1, 426-432 (2000).
20. + cells. J. Exp. Med. 195, 1523-1532 (2002).
21. Hikono, H. et al. T-cell memory and recall responses to respiratory virus infections. Immunol. Rev. 211, 119-132 (2006).
22. + T-cell memory in a model of localized transient infection. Immunol. Rev. 211, 133-145 (2006).
23. Lefrancois, L. Development, trafficking, and function of memory T-cell subsets. Immunol. Rev. 211, 93-103 (2006).
24. Marzo, A. L., Yagita, H. & Lefrancois, L. Cutting edge: migration to nonlymphoid tissues results in functional conversion of central to effector memory CD8 T cells. J. Immunol. 179, 36-40 (2007).
25. Sallusto, F., Geginat, J. & Lanzavecchia, A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22, 745-763 (2004).
26. + T cells. Immunol. Rev. 186, 221-233 (2002).
27. Wherry, E. J. et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nature Immunol. 4, 225-234 (2003).
28. Altman, J. D. et al. Phenotypic analysis of antigen-specific T lymphocytes. Science 274, 94-96 (1996).
29. + T cells. J. Immunol. Methods 238, 107-117 (2000).
30. Busch, D. H., Pilip, I. M., Vijh, S. & Pamer, E. G. Coordinate regulation of complex T cell populations responding to bacterial infection. Immunity 8, 353-362 (1998).
31. + T cells during an acute virus infection. Immunity 8, 167-175 (1998).
32. Kearney, E. R., Pape, K. A., Loh, D. Y. & Jenkins, M. K. Visualization of peptide?specific T cell immunity and peripheral tolerance induction in vivo. Immunity 1, 327-339 (1994).
33. Murali-Krishna, K. et al. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8, 177-187 (1998).
34. + T cells that are initially transferred prior to immunization.
35. + T cell effector population size. J. Immunol. 173, 2923-2927 (2004).
36. + T cells initially transferred prior to infection.
37. Probst, H. C., Dumrese, T. & van den Broek, M. F. Cutting edge: competition for APC by CTLs of different specificities is not functionally important during induction of antiviral responses. J. Immunol. 168, 5387-5391 (2002).
38. + T cell response to infection. Immunity 26, 827-841 (2007).
39. Hogquist, K. A. et al. T cell receptor antagonist peptides induce positive selection. Cell 76, 17-27 (1994).
40. Reiner, S. L., Sallusto, F. & Lanzavecchia, A. Division of labor with a workforce of one: challenges in specifying effector and memory T cell fate. Science 317, 622-625 (2007).
41. + T cells after infection. Nature Immunol. 3, 619-626 (2002).
42. + T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nature Immunol. 2, 415-422 (2001).
43. Mercado, R. et al. Early programming of T cell populations responding to bacterial infection. J. Immunol. 165, 6833-6839 (2000).
44. + T-cell generation.
45. + T-cell response. Nature Rev. Immunol. 4, 595-602 (2004).
46. Bennett, S. R. et al. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393, 478-480 (1998).
47. + T-helper and a T-killer cell. Nature 393, 474-478 (1998).
48. Schoenberger, S. P., Toes, R. E., van der Voort, E. I., Offringa, R. & Melief, C. J. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393, 480-483 (1998).
49. + T-cell memory via TRAIL-mediated activation-induced cell death. Nature 434, 88-93 (2005).
50. + T cell memory. Science 297, 2060-2063 (2002).
51. + T lymphocytes. Nature 421, 852-856 (2003).
52. Shedlock, D. J. & Shen, H. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300, 337-339 (2003).
53. Sun, J. C. & Bevan, M. J. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300, 339-342 (2003).
54. + memory T cells. Immunol. Rev. 211, 146-153 (2006).
55. + T cells after acute infection. Nature Immunol. 5, 927-933 (2004).
56. Badovinac, V. P., Messingham, K. A., Griffith, T. S. & Harty, J. T. TRAIL deficiency delays, but does not prevent, erosion in the quality of "helpless" memory CD8 T cells. J. Immunol. 177, 999-1006 (2006).
57. Marzo, A. L. et al. Fully functional memory CD8 T cells in the absence of CD4 T cells. J. Immunol. 173, 969-975 (2004).
58. Ramsburg, E. A., Publicover, J. M., Coppock, D. & Rose, J. K. Requirement for CD4 T cell help in maintenance of memory CD8 T cell responses is epitope dependent. J. Immunol. 178, 6350-6358 (2007).
59. Khanolkar, A., Badovinac, V. P. & Harty, J. T. CD8 T cell memory development: CD4 T cell help is appreciated. Immunol. Res. 39, 94-104 (2007).
60. D'Souza, W. N. & Lefrancois, L. IL-2 is not required for the initiation of CD8 T cell cycling but sustains expansion. J. Immunol. 171, 5727-5735 (2003).
61. + memory T cells. Nature 441, 890-893 (2006).
62. Yu, A. et al. Efficient induction of primary and secondary T cell-dependent immune responses in vivo in the absence of functional IL-2 and IL-15 receptors. J. Immunol. 170, 236-242 (2003).
63. Boyman, O., Kovar, M., Rubinstein, M. P., Surh, C. D. & Sprent, J. Selective stimulation of T cell subsets with antibody-cytokine immune complexes. Science 311, 1924-1927 (2006).
64. + T cells that are responding to infection.
65. + T cell differentiation: choosing a path through T-bet. Immunity 27, 180-182 (2007).
66. + T cell fates via the graded expression of T-bet transcription factor. Immunity 27, 281-295 (2007).
67. Murali-Krishna, K. et al. Persistence of memory CD8 T cells in MHC class I-deficient mice. Science 286, 1377-1381 (1999).
68. Klenerman, P. & Hill, A. T cells and viral persistence: lessons from diverse infections. Nature Immunol. 6, 873-879 (2005).
69. Wherry, E. J., Blattman, J. N., Murali-Krishna, K., van der Most, R. & Ahmed, R. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77, 4911-4927 (2003).
70. Wherry, E. J. & Ahmed, R. Memory CD8 T-cell differentiation during viral infection. J. Virol. 78, 5535-5545 (2004).
71. + T cells and facilitate the clearance of chronic LCMV infection.
72. Brooks, D. G. et al. Interleukin-10 determines viral clearance or persistence in vivo. Nature Med. 12, 1301-1309 (2006).
73. Ejrnaes, M. et al. Resolution of a chronic viral infection after interleukin-10 receptor blockade. J. Exp. Med. 203, 2461-2472 (2006).
74. Wherry, E. J., Barber, D. L., Kaech, S. M., Blattman, J. N. & Ahmed, R. Antigen-independent memory CD8 T cells do not develop during chronic viral infection. Proc. Natl Acad. Sci. USA 101, 16004-16009 (2004).
75. high functionally competent memory T cells is compromised by high viral loads and inadequate T cell help. J. Immunol. 174, 5926-5930 (2005).
76. Shin, H., Blackburn, S. D., Blattman, J. N. & Wherry, E. J. Viral antigen and extensive division maintain virus?specific CD8 T cells during chronic infection. J. Exp. Med. 204, 941-949 (2007).
77. Lang, K. S. et al. Inverse correlation between IL-7 receptor expression and CD8 T cell exhaustion during persistent antigen stimulation. Eur. J. Immunol. 35, 738-745 (2005).
78. + T cells.
79. Moskophidis, D., Lechner, F., Pircher, H. & Zinkernagel, R. M. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 362, 758-761 (1993).
80. Vezys, V. et al. Continuous recruitment of naive T cells contributes to heterogeneity of antiviral CD8 T cells during persistent infection. J. Exp. Med. 203, 2263-2269 (2006).
81. + cytotoxic T-cell-mediated pathogenesis during virus infection. Proc. Natl Acad. Sci. USA 93, 14730-14735 (1996).
82. Greenwald, R. J., Freeman, G. J. & Sharpe, A. H. The B7 family revisited. Annu. Rev. Immunol. 23, 515-548 (2005).
83. Watts, T. H. TNF/TNFR family members in costimulation of T cell responses. Annu. Rev. Immunol. 23, 23-68 (2005).
84. + T cells. J. Immunol. 162, 3256-3562 (1999).
85. Curtsinger, J. M., Valenzuela, J. O., Agarwal, P., Lins, D. & Mescher, M. F. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J. Immunol. 174, 4465-4469 (2005).
86. + T cells in vivo. J. Immunol. 163, 2561-2567 (1999).
87. Aichele, P. et al. CD8 T cells specific for lymphocytic choriomeningitis virus require type I IFN receptor for clonal expansion. J. Immunol. 176, 4525-4529 (2006).
88. Curtsinger, J. M., Johnson, C. M. & Mescher, M. F. CD8 T cell clonal expansion and development of effector function require prolonged exposure to antigen, costimulation, and signal 3 cytokine. J. Immunol. 171, 5165-5171 (2003).
89. Kolumam, G. A., Thomas, S., Thompson, L. J., Sprent, J. & Murali-Krishna, K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J. Exp. Med. 202, 637-650 (2005).
90. + T cell homeostasis. J. Immunol. 176, 735-739 (2006).
91. + T cells to increase their abundance during virus infection. J. Exp. Med. 201, 1053-1059 (2005).
92. Mitchell, T. C. et al. Immunological adjuvants promote activated T cell survival via induction of Bcl-3. Nature Immunol. 2, 397-402 (2001).
93. Thomas, S., Kolumam, G. A. & Murali-Krishna, K. Antigen presentation by nonhemopoietic cells amplifies clonal expansion of effector CD8 T cells in a pathogen?specific manner. J. Immunol. 178, 5802-5811 (2007).
94. Way, S. S., Havenar-Daughton, C., Kolumam, G. A., Orgun, N. N. & Murali-Krishna, K. IL-12 and type-I IFN synergize for IFN-γ production by CD4 T cells, whereas neither are required for IFN-γ production by CD8 T cells after Listeria monocytogenes infection. J. Immunol. 178, 4498-4505 (2007).
95. Thompson, L. J., Kolumam, G. A., Thomas, S. & Murali-Krishna, K. Innate inflammatory signals induced by various pathogens differentially dictate the IFN?I dependence of CD8 T cells for clonal expansion and memory formation. J. Immunol. 177, 1746-1754 (2006).
96. Cousens, L. P. et al. Two roads diverged: interferon α/β- and interleukin 12-mediated pathways in promoting T cell interferon γ responses during viral infection. J. Exp. Med. 189, 1315-1328 (1999).
97. Ou, R., Zhou, S., Huang, L. & Moskophidis, D. Critical role for α/β and γ interferons in persistence of lymphocytic choriomeningitis virus by clonal exhaustion of cytotoxic T cells. J. Virol. 75, 8407-8423 (2001).
98. Fuller, M. J., Khanolkar, A., Tebo, A. E. & Zajac, A. J. Maintenance, loss, and resurgence of T cell responses during acute, protracted, and chronic viral infections. J. Immunol. 172, 4204-4214 (2004).
99. Fuller, M. J. & Zajac, A. J. Ablation of CD8 and CD4 T cell responses by high viral loads. J. Immunol. 170, 477-486 (2003).
100. Gallimore, A. et al. Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes. J. Exp. Med. 187, 1383-1393 (1998).
101. Zhou, S., Ou, R., Huang, L. & Moskophidis, D. 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, 829-840 (2002).
102. Nguyen, L. T. et al. TNF receptor 1 (TNFR1) and CD95 are not required for T cell deletion after virus infection but contribute to peptide?induced deletion under limited conditions. Eur. J. Immunol. 30, 683-688 (2000).
103. Reich, A., Korner, H., Sedgwick, J. D. & Pircher, H. Immune down-regulation and peripheral deletion of CD8 T cells does not require TNF receptor-ligand interactions nor CD95 (Fas, APO?1). Eur. J. Immunol. 30, 678-682 (2000).
104. + T cells. J. Immunol. 164, 3950-3954 (2000).
105. Hildeman, D. A. et al. Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. Immunity 16, 759-767 (2002).
106. Pellegrini, M., Belz, G., Bouillet, P. & Strasser, A. 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, 14175-14180 (2003).
107. Hildeman, D., Jorgensen, T., Kappler, J. & Marrack, P. Apoptosis and the homeostatic control of immune responses. Curr. Opin. Immunol. 19, 516-521 (2007).
108. Plas, D. R., Rathmell, J. C. & Thompson, C. B. Homeostatic control of lymphocyte survival: potential origins and implications. Nature Immunol. 3, 515-521 (2002).
109. + T-cell responses during chronic viral infection. J. Virol. 80, 8627-8638 (2006).
110. lo effector T cells and limits T cell memory. Eur. J. Immunol. 36, 1694-1706 (2006).
111. Wojciechowski, S. et al. Bim/Bcl-2 balance is critical for maintaining naive and memory T cell homeostasis. J. Exp. Med. 204, 1665-1675 (2007).
112. + T cell homeostasis by perforin and interferon-γ. Science 290, 1354-1358 (2000).
113. Tewari, K., Nakayama, Y. & Suresh, M. Role of direct effects of IFN-γ on T cells in the regulation of CD8 T cell homeostasis. J. Immunol. 179, 2115-2125 (2007).
114. + T cell memory. J. Immunol. 179, 1190-1197 (2007).
115. + T cell contraction is controlled by early inflammation. Nature Immunol. 5, 809-817 (2004).
116. Haring, J. S. & Harty, J. T. Aberrant contraction of antigen-specific CD4 T cells after infection in the absence of γ interferon or its receptor. Infect. Immun. 74, 6252-6263 (2006).
117. + T cells responding to infection. J. Immunol. 174, 6791-6802 (2005).
118. Refaeli, Y., Van Parijs, L., Alexander, S. I. & Abbas, A. K. Interferon-γ is required for activation-induced death of T lymphocytes. J. Exp. Med. 196, 999-1005 (2002).
119. Pearce, E. L. & Shen, H. Generation of CD8 T cell memory is regulated by IL?12. J. Immunol. 179, 2074-2081 (2007).
120. Chang, J. T. et al. Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 315, 1687-1691 (2007). This paper suggests that a single T cell can promote diverse cell fates through an asymmetric initial cell division.
121. + T cell generation after acute infection. J. Immunol. 179, 53-63 (2007).
122. Kaech, S. M., Hemby, S., Kersh, E. & Ahmed, R. Molecular and functional profiling of memory CD8 T cell differentiation. Cell 111, 837-851 (2002).
123. + T-cell responses following peptide-DC vaccination.
124. + memory T lymphocyte precursors following peptide immunization. J. Immunol. 175, 4400-4407 (2005).
125. + T-cell memory determined by clonal burst size. Nature 369, 652-654 (1994).
126. Harty, J. T. & Bevan, M. J. Specific immunity to Listeria monocytogenes in the absence of IFN-γ. Immunity 3, 109-117 (1995).
127. Woodland, D. L. Jump-starting the immune system: prime-boosting comes of age. Trends Immunol. 25, 98-104 (2004).
128. + T cells undergoing primary and secondary responses to infection in the same host. J. Immunol. 170, 4933-4942 (2003).
129. + T cells to apoptosis in vivo. J. Immunol. 169, 3760-3770 (2002).
130. + T cells are more protective but slower to acquire a central-memory phenotype. J. Exp. Med. 203, 919-932 (2006).
131. Unsoeld, H. & Pircher, H. Complex memory T-cell phenotypes revealed by coexpression of CD62L and CCR7. J. Virol. 79, 4510-4513 (2005).