Development, trafficking, and function of memory T-cell subsets

Immunological Reviews

Volumn 211, Issue , 2006, Pages 93-103

  Lefrançois, Leo ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOPTIVE IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CELL DEATH; CELL LINEAGE; CELL MATURATION; CELL MIGRATION; CELL SURVIVAL; CELL TRANSPORT; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; COMPLEX FORMATION; HUMAN; IMMUNOPHENOTYPING; INFECTION PREVENTION; LISTERIA MONOCYTOGENES; LISTERIOSIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMORY T LYMPHOCYTE; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA VIRUS INFECTION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TISSUE DISTRIBUTION;

ANIMALS; HUMANS; IMMUNOLOGIC MEMORY; L-SELECTIN; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES;

EID: 33745079963     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.0105-2896.2006.00393.x     Document Type: Review

References (103)

1. Lipton MM Freund J. The formation of complement fixing and neutralizing antibodies after the injection of inactivated rabies virus with adjuvants. J Immunol 1950 64: 297 303.
2. Wherry EJ Blattman JN Murali-Krishna K van der MR Ahmed R. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol 2003 77: 4911 4927.
3. Fuller MJ Khanolkar A Tebo AE Zajac AJ. Maintenance, loss, and resurgence of T cell responses during acute, protracted, and chronic viral infections. J Immunol 2004 172: 4204 4214.
4. Cauley LS, et al. Virus-specific CD4+ memory T cells in nonlymphoid tissues express a highly activated phenotype. J Immunol 2002 169: 6655 6658.
5. Khanna KM Bonneau RH Kinchington PR Hendricks RL. Herpes simplex virus-specific memory CD8+ T cells are selectively activated and retained in latently infected sensory ganglia. Immunity 2003 18: 593 603.
6. Hammarlund E, et al. Duration of antiviral immunity after smallpox vaccination. Nat Med 2003 9: 1131 1137.
7. Slifka MK. Immunological memory to viral infection. Curr Opin Immunol 2004 16: 443 450.
8. Beverley PC. Kinetics and clonality of immunological memory in humans. Semin Immunol 2004 16: 315 321.
9. Zimmermann C Brduscha-Riem K Blaser C Zinkernagel RM Pircher H. Visualization, characterization, and turnover of CD8+ memory T cells in virus-infected hosts. J Exp Med 1996 183: 1367 1375.
10. Masopust D Vezys V Marzo AL Lefrançois L. Preferential localization of effector memory cells in nonlymphoid tissue. Science 2001 291: 2413 2417.
11. Curtsinger JM Lins DC Mescher MF. CD8+ memory T cells (CD44high, Ly-6C+) are more sensitive than naive cells (CD44low, Ly-6C-) to TCR/CD8 signaling in response to antigen. J Immunol 1998 160: 3236 3243.
12. Farber DL. Differential TCR signaling and the generation of memory T cells. J Immunol 1998 160: 535 539.
13. Hussain SF Anderson CF Farber DL. Differential SLP-76 expression and TCR-mediated signaling in effector and memory CD4 T cells. J Immunol 2002 168: 1557 1565.
14. Bachmann MF, et al. Developmental regulation of Lck targeting to the CD8 coreceptor controls signaling in naive and memory T cells. J Exp Med 1999 10: 1521 1530.
15. Kaech SM Hemby S Kersh E Ahmed R. Molecular and functional profiling of memory CD8 T cell differentiation. Cell 2002 111: 837 851.
16. Badovinac VP Messingham KA Jabbari A Haring JS Harty JT. Accelerated CD8+ T-cell memory and prime-boost response after dendritic-cell vaccination. Nat Med 2005 11: 748 756.
17. Williams MA Bevan MJ. Shortening the infectious period does not alter expansion of CD8 T cells but diminishes their capacity to differentiate into memory cells. J Immunol 2004 173: 6694 6702.
18. Van Stipdonk MJ Lemmens EE Schoenberger SP. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat Immunol 2001 2: 423 429.
19. Kaech SM Ahmed R. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat Immunol 2001 2: 415 422.
20. Lefrançois L Marzo A Williams K. Sustained response initiation is required for T cell clonal expansion but not for effector or memory development in vivo. J Immunol 2003 171: 2832 2839.
21. Hou S Hyland L Ryan KW Portner A Doherty PC. Virus specific CD8+ T-cell memory determined by clonal burst size. Nature 1994 369: 652 654.
22. Curtsinger JM Johnson CM Mescher MF. CD8 T cell clonal expansion and development of effector function require prolonged exposure to antigen, costimulation, and signal 3 cytokine. J Immunol 2003 171: 5165 5171.
23. Edelson BT Unanue ER. MyD88-dependent but Toll-like receptor 2-independent innate immunity to Listeria: no role for either in macrophage listericidal activity. J Immunol 2002 169: 3869 3875.
24. Feng H, et al. Listeria-infected myeloid dendritic cells produce IFN-β, priming T cell activation. J Immunol 2005 175: 421 432.
25. Muraille E, et al. Distinct in vivo dendritic cell activation by live versus killed Listeria monocytogenes. Eur J Immunol 2005 35: 1463 1471.
26. Bousso P Robey E. Dynamics of CD8(+) T cell priming by dendritic cells in intact lymph nodes. Nat Immunol 2003 4: 579 585.
27. Mempel TR Henrickson SE von Andrian UH. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 2004 427: 154 159.
28. Cahalan MD Parker I. Close encounters of the first and second kind: T-DC and T-B interactions in the lymph node. Semin Immunol 2005 17: 442 451.
29. Schluns KS Kieper WC Jameson SC Lefrançois L. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat Immunol 2000 1: 426 432.
30. Schluns KS Williams K Ma A Zheng XX Lefrançois L. Cutting edge: requirement for IL-15 in the generation of primary and memory antigen-specific CD8 T cells. J Immunol 2002 168: 4827 4831.
31. Schluns KS Lefrancois L. Cytokine control of memory T-cell development and survival. Nat Rev Immunol 2003 3: 269 279.
32. Klonowski KD Lefrancois L. The CD8 memory T cell subsystem: integration of homeostatic signaling during migration. Semin Immunol 2005 17: 219 229.
33. Yajima T, et al. IL-15 regulates CD8+ T cell contraction during primary infection. J Immunol 2006 176: 507 515.
34. Sprent J Tough DF. T cell death and memory. Science 2001 293: 245 248.
35. Gett AV Sallusto F Lanzavecchia A Geginat J. T cell fitness determined by signal strength. Nat Immunol 2003 4: 355 360.
36. Grayson JM Zajac AJA Ahmed R. Increased expression of Bcl-2 in antigen-specific memory CD8+ T cells. J Immunol 2000 164: 3950 3954.
37. Marrack P Kappler J. Control of T cell viability. Annu Rev Immunol 2004 22: 765 787.
38. Mitchell TC, et al. Immunological adjuvants promote activated T cell survival via induction of Bcl-3. Nat Immunol 2001 2: 397 402.
39. Valenzuela JO Hammerbeck CD Mescher MF. Cutting edge: Bcl-3 up-regulation by signal 3 cytokine (IL-12) prolongs survival of antigen-activated CD8 T cells. J Immunol 2005 174: 600 604.
40. Hildeman DA, et al. Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. Immunity 2002 16: 759 767.
41. 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 2003 100: 14175 14180.
42. Sudo T, et al. Expression and function of the interleukin 7 receptor in murine lymphocytes. Proc Natl Acad Sci USA 1993 90: 9125 9129.
43. Maraskovsky E, et al. Impaired survival and proliferation in IL-7 receptor-deficient peripheral T cells. J Immunol 1996 157: 5315 5323.
44. Kaech SM Tan JT Wherry EJ Konieczny BT Surh CD Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol 2003 4: 1191 1198.
45. Badovinac VP Porter BB Harty JT. CD8+ T cell contraction is controlled by early inflammation. Nat Immunol 2004 5: 809 817.
46. Lacombe MH Hardy MP Rooney J Labrecque N. IL-7 receptor expression levels do not identify CD8+ memory T lymphocyte precursors following peptide immunization. J Immunol 2005 175: 4400 4407.
47. Seddon B Tomlinson P Zamoyska R. Interleukin 7 and T cell receptor signals regulate homeostasis of CD4 memory cells. Nat Immunol 2003 4: 680 686.
48. Goldrath AW, et al. Cytokine requirements for acute and basal homeostatic proliferation of naive and memory CD8+ T cells. J Exp Med 2002 195: 1515 1522.
49. Li J Huston G Swain SL. IL-7 promotes the transition of CD4 effectors to persistent memory cells. J Exp Med 2003 198: 1807 1815.
50. Kondrack RM Harbertson J Tan JT McBreen ME Surh CD Bradley LM. Interleukin 7 regulates the survival and generation of memory CD4 cells. J Exp Med 2003 198: 1797 1806.
51. Mosmann TR Coffman RL. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol 1989 7: 145 173.
52. Swain SL. Generation and in vivo persistence of polarized Th1 and Th2 memory cells. Immunity 1994 1: 543 552.
53. Boursalian TE Bottomly K. Stability of naive and memory phenotypes on resting CD4 T cells in vivo. J Immunol 1999 163: 9 16.
54. Sallusto F Lenig D Forster R Lipp M Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999 401: 708 712.
55. Warnock RA Askari S Butcher EC von Andrian UH. Molecular mechanisms of lymphocyte homing to peripheral lymph nodes. J Exp Med 1998 187: 205 216.
56. Parretta E Cassese G Barba P Santoni A Guardiola J Di Rosa F. CD8 cell division maintaining cytotoxic memory occurs predominantly in the bone marrow. J Immunol 2005 174: 7654 7664.
57. Mazo IB, et al. Bone marrow is a major reservoir and site of recruitment for central memory CD8+ T cells. Immunity 2005 22: 259 270.
58. Becker TC Coley SM Wherry EJ Ahmed R. Bone marrow is a preferred site for homeostatic proliferation of memory CD8 T cells. J Immunol 2005 174: 1269 1273.
59. Di Rosa F Pabst R. The bone marrow: a nest for migratory memory T cells. Trends Immunol 2005 26: 360 366.
60. Sallusto F Geginat J Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 2004 22: 745 763.
61. Baars PA, et al. Properties of murine (CD8+) CD27- T cells. Eur J Immunol 2005 35: 3131 3141.
62. Baron V, et al. The repertoires of circulating human CD8(+) central and effector memory T cell subsets are largely distinct. Immunity 2003 18: 193 204.
63. Wherry EJ, et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 2003 4: 225 234.
64. Marzo AL Klonowski KD Le Bon A Borrow P Tough DF Lefrancois L. Initial T cell frequency dictates memory CD8+ T cell lineage commitment. Nat Immunol 2005 6: 793 799.
65. Yoshida R, et al. Molecular cloning of a novel human CC chemokine EBI1-ligand chemokine that is a specific functional ligand for EBI1, CCR7. J Biol Chem 1997 272: 13803 13809.
66. Potsch C Vohringer D Pircher H. Distinct migration patterns of naive and effector CD8 T cells in the spleen: correlation with CCR7 receptor expression and chemokine reactivity. Eur J Immunol 1999 29: 3562 3570.
67. Sallusto F, et al. Switch in chemokine receptor expression upon TCR stimulation reveals novel homing potential for recently activated T cells. Eur J Immunol 1999 29: 2037 2045.
68. Gallatin WM Weissman IL Butcher EC. A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature 1983 304: 30 34.
69. Jalkanen S Reichert RA Gallatin WM Bargatze RF Weissman IL Butcher EC. Homing receptors and the control of lymphocyte migration. Immunol Rev 1986 91: 39 60.
70. Jung TM Gallatin WM Weissman IL Dailey MO. Down-regulation of homing receptors after T cell activation. J Immunol 1988 141: 4110 4117.
71. Jung TM Dailey MO. Reversibility of loss of homing receptor expression following activation. Adv Exp Med Biol 1988 237: 519 524.
72. Jung TM Dailey MO. Rapid modulation of homing receptors (gp90MEL-14) induced by activators of protein kinase C. Receptor shedding due to accelerated proteolytic cleavage at the cell surface. J Immunol 1990 144: 3130 3136.
73. Chao CC Jensen R Dailey MO. Mechanisms of L-selectin regulation by activated T cells. J Immunol 1997 159: 1686 1694.
74. Venturi GM, et al. Leukocyte migration is regulated by L-selectin endoproteolytic release. Immunity 2003 19: 713 724.
75. Smalley DM Ley K. L-selectin: mechanisms and physiological significance of ectodomain cleavage. J Cell Mol Med 2005 9: 255 266.
76. Campbell DJ Kim CH Butcher EC. Chemokines in the systemic organization of immunity. Immunol Rev 2003 195: 58 71.
77. Lefrançois L Masopust D. T cell immunity in lymphoid and non-lymphoid tissues. Curr Opin Immunol 2002 14: 503 508.
78. Masopust D, et al. Activated primary and memory CD8 T cells migrate to nonlymphoid tissues regardless of site of activation or tissue of origin. J Immunol 2004 172: 4875 4882.
79. Bunster E Meyer RK. An improved method of parabiosis. Anat Rec 1933 57: 339 343.
80. Donskoy E Goldschneider I. Thymocytopoiesis is maintained by blood-borne precursors throughout postnatal life. A study in parabiotic mice. J Immunol 1992 148: 1604 1612.
81. Klonowski KD Williams KJ Marzo AL Blair DA Lingenheld EG Lefrancois L. Dynamics of blood-borne CD8 memory T cell migration in vivo. Immunity 2004 20: 551 562.
82. Mackay CR Marston WL Dudler L. Naive and memory T cells show distinct pathways of lymphocyte recirculation. J Exp Med 1990 171: 801 817.
83. Mackay CR Andrew DP Briskin M Ringler DJ Butcher EC. Phenotype, and migration properties of three major subsets of tissue homing T cells in sheep. Eur J Immunol 1996 26: 2433 2439.
84. Bromley SK Thomas SY Luster AD. Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics. Nat Immunol 2005 6: 895 901.
85. Debes GF, et al. Chemokine receptor CCR7 required for T lymphocyte exit from peripheral tissues. Nat Immunol 2005 6: 889 894.
86. Forster R, et al. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 1999 99: 23 33.
87. MartIn-Fontecha A, et al. Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J Exp Med 2003 198: 615 621.
88. Randolph GJ Angeli V Swartz MA. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol 2005 5: 617 628.
89. Unsoeld H Pircher H. Complex memory T-cell phenotypes revealed by coexpression of CD62L and CCR7. J Virol 2005 79: 4510 4513.
90. Kim SK Schluns KS Lefrançois L. Induction and visualization of mucosal memory CD8 T cells following systemic virus infection. J Immunol 1999 163: 4125 4132.
91. Jelley-Gibbs DM Brown DM Dibble JP Haynes L Eaton SM Swain SL. Unexpected prolonged presentation of influenza antigens promotes CD4 T cell memory generation. J Exp Med 2005 202: 697 706.
92. Dubois S Mariner J Waldmann TA Tagaya Y. IL-15Ralpha recycles and presents IL-15 In trans to neighboring cells. Immunity 2002 17: 537 547.
93. Becker TC, et al. Interleukin 15 is required for proliferative renewal of virus-specific memory CD8 T cells. J Exp Med 2002 195: 1541 1548.
94. Burkett PR, et al. IL-15Ralpha expression on CD8+ T cells is dispensable for T cell memory. Proc Natl Acad Sci USA 2003 100: 4724 4729.
95. Koka R, et al. Interleukin (IL)-15R[alpha]-deficient natural killer cells survive in normal but not IL-15R[alpha]-deficient mice. J Exp Med 2003 197: 977 984.
96. Schluns KS Klonowski KD Lefrançois L. Trans-regulation of memory CD8 T cell proliferation by IL-15Rα+ bone marrow-derived cells. Blood 2004 103: 988 994.
97. Sandau MM Schluns KS Lefrancois L Jameson SC. Cutting edge: transpresentation of IL-15 by bone marrow-derived cells necessitates expression of IL-15 and IL-15R alpha by the same cells. J Immunol 2004 173: 6537 6541.
98. Woodland DL. Jump-starting the immune system: prime-boosting comes of age. Trends Immunol 2004 25: 98 104.
99. Zaph C Uzonna J Beverley SM Scott P. Central memory T cells mediate long-term immunity to Leishmania major in the absence of persistent parasites. Nat Med 2004 10: 1104 1110.
100. Roberts AD Ely KH Woodland DL. Differential contributions of central and effector memory T cells to recall responses. J Exp Med 2005 202: 123 133.
101. An LL Rodriguez F Harkins S Zhang J Whitton JL. Quantitative and qualitative analyses of the immune responses induced by a multivalent minigene DNA vaccine. Vaccine 2000 18: 2132 2141.
102. Flajnik MF Du PL. Evolution of innate and adaptive immunity: can we draw a line? Trends Immunol 2004 25: 640 644.
103. Zell T Khoruts A Ingulli E Bonnevier JL Mueller DL Jenkins MK. Single-cell analysis of signal transduction in CD4 T cells stimulated by antigen in vivo. Proc Natl Acad Sci USA 2001 98: 10805 10810.