Stem cell-like plasticity of naïve and distinct memory CD8+ T cell subsets

Seminars in Immunology

Volumn 21, Issue 2, 2009, Pages 62-68

  Stemberger, Christian ^b   Neuenhahn, Michael ^b   Gebhardt, Friedemann E ^b   Schiemann, Matthias ^b   Buchholz, Veit R ^b   Busch, Dirk H ^a,b  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Adoptive T cell transfer; Memory stem cell; Single cell transfer; T cell memory differentiation

Indexed keywords

CYTOKINE;

ADOPTIVE IMMUNOTHERAPY; ALLOGENEIC STEM CELL TRANSPLANTATION; ANTIGEN PRESENTING CELL; CD8+ T LYMPHOCYTE; CELL DIVISION; CELL FATE; CELL LINEAGE; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; HUMAN; IMMUNE DEFICIENCY; LYMPHOCYTE CLONE; LYMPHOCYTE DIFFERENTIATION; MEMORY T LYMPHOCYTE; NONHUMAN; PHENOTYPIC VARIATION; PRE T LYMPHOCYTE; REVIEW; STEM CELL; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; BIOLOGICAL MARKERS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CYTOTOXICITY, IMMUNOLOGIC; HOMEOSTASIS; HUMANS; IMMUNOLOGIC MEMORY; IMMUNOTHERAPY, ADOPTIVE; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; STEM CELLS; T-LYMPHOCYTE SUBSETS;

EID: 62049085970     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smim.2009.02.004     Document Type: Review

References (88)

1. Altman J.D., Moss P.A., Goulder P.J., Barouch D.H., McHeyzer-Williams M.G., Bell J.I., et al. Phenotypic analysis of antigen-specific T lymphocytes. Science 274 (1996) 94-96
2. Kearney E.R., Pape K.A., Loh D.Y., and Jenkins M.K. Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity 1 (1994) 327-339
3. Knabel M., Franz T.J., Schiemann M., Wulf A., Villmow B., Schmidt B., et al. Reversible MHC multimer staining for functional isolation of T-cell populations and effective adoptive transfer. Nat Med 8 (2002) 631-637
4. Jung T., Schauer U., Heusser C., Neumann C., and Rieger C. Detection of intracellular cytokines by flow cytometry. J Immunol Methods 159 (1993) 197-207
5. Busch D.H., Pilip I.M., Vijh S., and Pamer E.G. Coordinate regulation of complex T cell populations responding to bacterial infection. Immunity 8 (1998) 353-362
6. Stemberger C., Neuenhahn M., Buchholz V.R., and Busch D.H. Origin of CD8+ effector and memory T cell subsets. Cell Mol Immunol 4 (2007) 399-405
7. Pantaleo G., and Koup R.A. Correlates of immune protection in HIV-1 infection: what we know, what we don't know, what we should know. Nat Med 10 (2004) 806-810
8. Masopust D., Vezys V., Marzo A.L., and Lefrancois L. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291 (2001) 2413-2417
9. Sallusto F., Lenig D., Forster R., Lipp M., and Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401 (1999) 708-712
10. Joshi N.S., Cui W., Chandele A., Lee H.K., Urso D.R., Hagman J., et al. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27 (2007) 281-295
11. Sarkar S., Kalia V., Haining W.N., Konieczny B.T., Subramaniam S., and Ahmed R. Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J Exp Med 205 (2008) 625-640
12. Kamimura D., and Bevan M.J. Naive CD8+ T cells differentiate into protective memory-like cells after IL-2 anti IL-2 complex treatment in vivo. J Exp Med 204 (2007) 1803-1812
13. Geginat J., Lanzavecchia A., and Sallusto F. Proliferation and differentiation potential of human CD8+ memory T-cell subsets in response to antigen or homeostatic cytokines. Blood 101 (2003) 4260-4266
14. Huster K.M., Stemberger C., and Busch D.H. Protective immunity towards intracellular pathogens. Curr Opin Immunol 18 (2006) 458-464
15. Huster K.M., Koffler M., Stemberger C., Schiemann M., Wagner H., and Busch D.H. Unidirectional development of CD8+ central memory T cells into protective Listeria-specific effector memory T cells. Eur J Immunol 36 (2006) 1453-1464
16. Castellino F., and Germain R.N. Cooperation between CD4+ and CD8+ T cells: when, where, and how. Annu Rev Immunol 24 (2006) 519-540
17. Kaech S.M., Tan J.T., Wherry E.J., Konieczny B.T., Surh C.D., and Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol 4 (2003) 1191-1198
18. Huster K.M., Busch V., Schiemann M., Linkemann K., Kerksiek K.M., Wagner H., et al. Selective expression of IL-7 receptor on memory T cells identifies early CD40L-dependent generation of distinct CD8+ memory T cell subsets. Proc Natl Acad Sci USA 101 (2004) 5610-5615
19. van Stipdonk M.J., Lemmens E.E., and Schoenberger S.P. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat Immunol 2 (2001) 423-429
20. Kaech S.M., and Ahmed R. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat Immunol 2 (2001) 415-422
21. Mercado R., Vijh S., Allen S.E., Kerksiek K., Pilip I.M., and Pamer E.G. Early programming of T cell populations responding to bacterial infection. J Immunol 165 (2000) 6833-6839
22. Bevan M.J., and Fink P.J. The CD8 response on autopilot. Nat Immunol 2 (2001) 381-382
23. Prlic M., Hernandez-Hoyos G., and Bevan M.J. Duration of the initial TCR stimulus controls the magnitude but not functionality of the CD8+ T cell response. J Exp Med 203 (2006) 2135-2143
24. Tewari K., Walent J., Svaren J., Zamoyska R., and Suresh M. Differential requirement for Lck during primary and memory CD8+ T cell responses. Proc Natl Acad Sci USA 103 (2006) 16388-16393
25. Reiner S.L., Sallusto F., and Lanzavecchia A. Division of labor with a workforce of one: challenges in specifying effector and memory T cell fate. Science 317 (2007) 622-625
26. Wherry E.J., Teichgraber V., Becker T.C., Masopust D., Kaech S.M., Antia R., et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 4 (2003) 225-234
27. Kaech S.M., Hemby S., Kersh E., and Ahmed R. Molecular and functional profiling of memory CD8 T cell differentiation. Cell 111 (2002) 837-851
28. Opferman J.T., Ober B.T., and Ashton-Rickardt P.G. Linear differentiation of cytotoxic effectors into memory T lymphocytes. Science 283 (1999) 1745-1748
29. Lanzavecchia A., and Sallusto F. Dynamics of T lymphocyte responses: intermediates, effectors, and memory cells. Science 290 (2000) 92-97
30. Lauvau G., Vijh S., Kong P., Horng T., Kerksiek K., Serbina N., et al. Priming of memory but not effector CD8 T cells by a killed bacterial vaccine. Science 294 (2001) 1735-1739
31. Wong P., Lara-Tejero M., Ploss A., Leiner I., and Pamer E.G. Rapid development of T cell memory. J Immunol 172 (2004) 7239-7245
32. Manjunath N., Shankar P., Wan J., Weninger W., Crowley M.A., Hieshima K., et al. Effector differentiation is not prerequisite for generation of memory cytotoxic T lymphocytes. J Clin Invest 108 (2001) 871-878
33. Zhang M., Byrne S., Liu N., Wang Y., Oxenius A., and Ashton-Rickardt P.G. Differential survival of cytotoxic T cells and memory cell precursors. J Immunol 178 (2007) 3483-3491
34. Zhang Y., Joe G., Hexner E., Zhu J., and Emerson S.G. Host-reactive CD8+ memory stem cells in graft-versus-host disease. Nat Med 11 (2005) 1299-1305
35. Gett A.V., Sallusto F., Lanzavecchia A., and Geginat J. T cell fitness determined by signal strength. Nat Immunol 4 (2003) 355-360
36. Lanzavecchia A., and Sallusto F. Progressive differentiation and selection of the fittest in the immune response. Nat Rev Immunol 2 (2002) 982-987
37. Jacob J., and Baltimore D. Modelling T-cell memory by genetic marking of memory T cells in vivo. Nature 399 (1999) 593-597
38. Busch D.H., Kerksiek K.M., and Pamer E.G. Differing roles of inflammation and antigen in T cell proliferation and memory generation. J Immunol 164 (2000) 4063-4070
39. Kaech S.M., and Wherry E.J. Heterogeneity and cell-fate decisions in effector and memory CD8(+) T cell differentiation during viral infection. Immunity 27 (2007) 393-405
40. Bird J.J., Brown D.R., Mullen A.C., Moskowitz N.H., Mahowald M.A., Sider J.R., et al. Helper T cell differentiation is controlled by the cell cycle. Immunity 9 (1998) 229-237
41. Yeh J.H., Sidhu S.S., and Chan A.C. Regulation of a late phase of T cell polarity and effector functions by Crtam. Cell 132 (2008) 846-859
42. Baron V., Bouneaud C., Cumano A., Lim A., Arstila T.P., Kourilsky P., et al. The repertoires of circulating human CD8(+) central and effector memory T cell subsets are largely distinct. Immunity 18 (2003) 193-204
43. Bouneaud C., Garcia Z., Kourilsky P., and Pannetier C. Lineage relationships, homeostasis, and recall capacities of central- and effector-memory CD8 T cells in vivo. J Exp Med 201 (2005) 579-590
44. Catron D.M., Rusch L.K., Hataye J., Itano A.A., and Jenkins M.K. CD4+ T cells that enter the draining lymph nodes after antigen injection participate in the primary response and become central-memory cells. J Exp Med 203 (2006) 1045-1054
45. D'Souza W.N., and Hedrick S.M. Cutting edge: latecomer CD8 T cells are imprinted with a unique differentiation program. J Immunol 177 (2006) 777-781
46. Badovinac V.P., Haring J.S., and Harty J.T. Initial T cell receptor transgenic cell precursor frequency dictates critical aspects of the CD8(+) T cell response to infection. Immunity 26 (2007) 827-841
47. Hataye J., Moon J.J., Khoruts A., Reilly C., and Jenkins M.K. Naive and memory CD4+ T cell survival controlled by clonal abundance. Science 312 (2006) 114-116
48. Marzo A.L., Klonowski K.D., Le Bon A., Borrow P., Tough D.F., and Lefrancois L. Initial T cell frequency dictates memory CD8+ T cell lineage commitment. Nat Immunol 6 (2005) 793-799
49. Ernst B., Lee D.S., Chang J.M., Sprent J., and Surh C.D. The peptide ligands mediating positive selection in the thymus control T cell survival and homeostatic proliferation in the periphery. Immunity 11 (1999) 173-181
50. Nesic D., and Vukmanovic S. MHC class I is required for peripheral accumulation of CD8+ thymic emigrants. J Immunol 160 (1998) 3705-3712
51. Goldrath A.W., Bogatzki L.Y., and Bevan M.J. Naive T cells transiently acquire a memory-like phenotype during homeostasis-driven proliferation. J Exp Med 192 (2000) 557-564
52. Hamilton S.E., Wolkers M.C., Schoenberger S.P., and Jameson S.C. The generation of protective memory-like CD8+ T cells during homeostatic proliferation requires CD4+ T cells. Nat Immunol 7 (2006) 475-481
53. Kieper W.C., and Jameson S.C. Homeostatic expansion and phenotypic conversion of naive T cells in response to self peptide/MHC ligands. Proc Natl Acad Sci USA 96 (1999) 13306-13311
54. Murali-Krishna K., Lau L.L., Sambhara S., Lemonnier F., Altman J., and Ahmed R. Persistence of memory CD8 T cells in MHC class I-deficient mice. Science 286 (1999) 1377-1381
55. Murali-Krishna K., and Ahmed R. Cutting edge: naive T cells masquerading as memory cells. J Immunol 165 (2000) 1733-1737
56. Dustin M.L., and Chan A.C. Signaling takes shape in the immune system. Cell 103 (2000) 283-294
57. Chang J.T., Palanivel V.R., Kinjyo I., Schambach F., Intlekofer A.M., Banerjee A., et al. Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 315 (2007) 1687-1691
58. Bousso P., and Robey E. Dynamics of CD8+ T cell priming by dendritic cells in intact lymph nodes. Nat Immunol 4 (2003) 579-585
59. Mescher M.F., Curtsinger J.M., Agarwal P., Casey K.A., Gerner M., Hammerbeck C.D., et al. Signals required for programming effector and memory development by CD8+ T cells. Immunol Rev 211 (2006) 81-92
60. Stemberger C., Huster K.M., Koffler M., Anderl F., Schiemann M., Wagner H., et al. A single naive CD8(+) T cell precursor can develop into diverse effector and memory subsets. Immunity 27 (2007) 985-997
61. Tough D.F., and Sprent J. Turnover of naive- and memory-phenotype T cells. J Exp Med 179 (1994) 1127-1135
62. Surh C.D., Boyman O., Purton J.F., and Sprent J. Homeostasis of memory T cells. Immunol Rev 211 (2006) 154-163
63. Schluns K.S., and Lefrancois L. Cytokine control of memory T-cell development and survival. Nat Rev Immunol 3 (2003) 269-279
64. Judge A.D., Zhang X., Fujii H., Surh C.D., and Sprent J. Interleukin 15 controls both proliferation and survival of a subset of memory-phenotype CD8(+) T cells. J Exp Med 196 (2002) 935-946
65. Lodolce J.P., Boone D.L., Chai S., Swain R.E., Dassopoulos T., Trettin S., et al. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 9 (1998) 669-676
66. Tan J.T., Ernst B., Kieper W.C., LeRoy E., Sprent J., and Surh C.D. Interleukin (IL)-15 and IL-7 jointly regulate homeostatic proliferation of memory phenotype CD8+ cells but are not required for memory phenotype CD4+ cells. J Exp Med 195 (2002) 1523-1532
67. Goldrath A.W., Sivakumar P.V., Glaccum M., Kennedy M.K., Bevan M.J., Benoist C., et al. Cytokine requirements for acute and basal homeostatic proliferation of naive and memory CD8+ T cells. J Exp Med 195 (2002) 1515-1522
68. Ku C.C., Murakami M., Sakamoto A., Kappler J., and Marrack P. Control of homeostasis of CD8+ memory T cells by opposing cytokines. Science 288 (2000) 675-678
69. Sabbagh L., Snell L.M., and Watts T.H. TNF family ligands define niches for T cell memory. Trends Immunol 28 (2007) 333-339
70. Pulle G., Vidric M., and Watts T.H. IL-15-dependent induction of 4-1BB promotes antigen-independent CD8 memory T cell survival. J Immunol 176 (2006) 2739-2748
71. Cannons J.L., Bertram E.M., and Watts T.H. Cutting edge: profound defect in T cell responses in TNF receptor-associated factor 2 dominant negative mice. J Immunol 169 (2002) 2828-2831
72. Warnock R.A., Askari S., Butcher E.C., and von Andrian U.H. Molecular mechanisms of lymphocyte homing to peripheral lymph nodes. J Exp Med 187 (1998) 205-216
73. Di Rosa F., and Pabst R. The bone marrow: a nest for migratory memory T cells. Trends Immunol 26 (2005) 360-366
74. Becker T.C., Coley S.M., Wherry E.J., and Ahmed R. Bone marrow is a preferred site for homeostatic proliferation of memory CD8 T cells. J Immunol 174 (2005) 1269-1273
75. Mazo I.B., Honczarenko M., Leung H., Cavanagh L.L., Bonasio R., Weninger W., et al. Bone marrow is a major reservoir and site of recruitment for central memory CD8+ T cells. Immunity 22 (2005) 259-270
76. Sigmundsdottir H., and Butcher E.C. Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat Immunol 9 (2008) 981-987
77. Luckey C.J., Bhattacharya D., Goldrath A.W., Weissman I.L., Benoist C., and Mathis D. Memory T and memory B cells share a transcriptional program of self-renewal with long-term hematopoietic stem cells. Proc Natl Acad Sci USA 103 (2006) 3304-3309
78. Kiel M.J., Yilmaz O.H., Iwashita T., Yilmaz O.H., Terhorst C., and Morrison S.J. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121 (2005) 1109-1121
79. Romero X., Benitez D., March S., Vilella R., Miralpeix M., and Engel P. Differential expression of SAP and EAT-2-binding leukocyte cell-surface molecules CD84, CD150 (SLAM), CD229 (Ly9) and CD244 (2B4). Tissue Antigens 64 (2004) 132-144
80. Moss P., and Rickinson A. Cellular immunotherapy for viral infection after HSC transplantation. Nat Rev Immunol 5 (2005) 9-20
81. Riddell S.R., Watanabe K.S., Goodrich J.M., Li C.R., Agha M.E., and Greenberg P.D. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 257 (1992) 238-241
82. Tan R., Xu X., Ogg G.S., Hansasuta P., Dong T., Rostron T., et al. Rapid death of adoptively transferred T cells in acquired immunodeficiency syndrome. Blood 93 (1999) 1506-1510
83. Murali-Krishna K., Altman J.D., Suresh M., Sourdive D.J., Zajac A.J., Miller J.D., et al. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8 (1998) 177-187
84. Sylwester A.W., Mitchell B.L., Edgar J.B., Taormina C., Pelte C., Ruchti F., et al. Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J Exp Med 202 (2005) 673-685
85. Cobbold M., Khan N., Pourgheysari B., Tauro S., McDonald D., Osman H., et al. Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA-peptide tetramers. J Exp Med 202 (2005) 379-386
86. Feuchtinger T., Lang P., Hamprecht K., Schumm M., Greil J., Jahn G., et al. Isolation and expansion of human adenovirus-specific CD4+ and CD8+ T cells according to IFN-gamma secretion for adjuvant immunotherapy. Exp Hematol 32 (2004) 282-289
87. Feuchtinger T., Matthes-Martin S., Richard C., Lion T., Fuhrer M., Hamprecht K., et al. Safe adoptive transfer of virus-specific T-cell immunity for the treatment of systemic adenovirus infection after allogeneic stem cell transplantation. Br J Haematol 134 (2006) 64-76
88. Bannard O., Kraman M., and Fearon D.T. Secondary replicative function of CD8+ T cells that had developed an effector phenotype. Science 323 (2009) 505-509