CD4+ memory T cells: Functional differentiation and homeostasis

Immunological Reviews

Volumn 211, Issue , 2006, Pages 39-48

  Stockinger, Brigitta ^a   Bourgeois, Christine ^a   Kassiotis, George ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE;

ANTIGEN EXPRESSION; APOPTOSIS; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL DIVISION; CELL HETEROGENEITY; CELL INTERACTION; CELL PROLIFERATION; CELL SURVIVAL; CYTOKINE RELEASE; DOWN REGULATION; GENETIC TRANSCRIPTION; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; LYMPHOCYTE FUNCTION; MEMORY T LYMPHOCYTE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; HOMEOSTASIS; HUMANS; IMMUNOLOGIC MEMORY; MICE;

EID: 33745086257     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.0105-2896.2006.00381.x     Document Type: Review

References (99)

1. Stoll S Delon J Brotz TM Germain RN. Dynamic imaging of T cell-dendritic cell interactions in lymph nodes. Science 2002 296: 1873 1876.
2. Celli S Garcia Z Bousso P. CD4 T cells integrate signals delivered during successive DC encounters in vivo. J Exp Med 2005 202: 1271 1278.
3. Lanzavecchia A Sallusto F. Progressive differentiation and selection of the fittest in the immune response. Nat Rev Immunol 2002 2: 982 987.
4. 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.
5. Obst R van Santen HM Mathis D Benoist C. Antigen persistence is required throughout the expansion phase of a CD4(+) T cell response. J Exp Med 2005 201: 1555 1565.
6. 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.
7. Tew JG Kosco MH Burton GF Szakal AK. Follicular dendritic cells as accessory cells. Immunol Rev 1990 17: 185 211.
8. Gray D Kosco M Stockinger B. Novel pathways of antigen presentation for the maintenance of memory. Int Immunol 1991 3: 141 148.
9. Seder RA Ahmed R. Similarities and differences in CD4+ and CD8+ effector and memory T cell generation. Nat Immunol 2003 4: 835 842.
10. Foulds KE Zenewicz LA Shedlock DJ Jiang J Troy AE Shen H. Cutting edge: CD4 and CD8 T cells are intrinsically different in their proliferative responses. J Immunol 2002 168: 1528 1532.
11. Srinivasan A Foley J McSorley SJ. Massive number of antigen-specific CD4 T cells during vaccination with live attenuated Salmonella causes interclonal competition. J Immunol 2004 172: 6884 6893.
12. Whitmire JK Ahmed R. Costimulation in antiviral immunity: differential requirements for CD4(+) and CD8(+) T cell responses. Curr Opin Immunol 2000 12: 448 455.
13. Hess J Ladel C Miko D Kaufmann SH. Salmonella typhimurium aroA-infection in gene-targeted immunodeficient mice: major role of CD4+ TCR-alpha beta cells and IFN-gamma in bacterial clearance independent of intracellular location. J Immunol 1996 156: 3321 3326.
14. Chao CC Jensen R Dailey MO. Mechanisms of 1-selectin regulation by activated T cells. J Immunol 1997 159: 1686 1694.
15. Wherry EJ, et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 2003 4: 225 234.
16. 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.
17. Kassiotis G Stockinger B. Anatomical heterogeneity of memory CD4+ T cells due to reversible adaptation to the microenvironment. J Immunol 2004 173: 7292 7298.
18. Steeber DA Green NE Sato S Tedder TF. Lymphocyte migration in L-selectin-deficient mice. Altered subset migration and aging of the immune system. J Immunol 1996 157: 1096 1106.
19. Zhang X, et al. Unequal death in T helper cell (Th)1 and Th2 effectors: Th1, but not Th2, effectors undergo rapid Fas/FasL-mediated apoptosis. J Exp Med 1997 185: 1837 1849.
20. Wu CY, et al. Distinct lineages of T(H)1 cells have differential capacities for memory cell generation in vivo. Nat Immunol 2002 3: 852 858.
21. Stetson DB, et al. Constitutive cytokine mRNAs mark natural killer (NK) and NK T cells poised for rapid effector function. J Exp Med 2003 198: 1069 1076.
22. Hu H Huston G Duso D Lepak N Roman E Swain SL. CD4(+) T cell effectors can become memory cells with high efficiency and without further division. Nat Immunol 2001 2: 705 710.
23. Harrington LE, et al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005 6: 1123 1132.
24. Park H, et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005 6: 1133 1141.
25. Cua DJ, et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003 421: 744 748.
26. Kolls JK Linden A. Interleukin-17 family members and inflammation. Immunity 2004 21: 467 476.
27. Langrish CL, et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005 201: 233 240.
28. Nakae S Saijo S Horai R Sudo K Mori S Iwakura Y. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc Natl Acad Sci USA 2003 10: 5986 5990.
29. Veldhoen M Hocking RJ Atkins CJ Locksley RM Stockinger B. TGF beta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006 24: 179 189.
30. Aggarwal S Ghilardi N Xie MH de Sauvage FJ Gurney AL. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 2003 278: 1910 1914.
31. Fontenot JD Rudensky AY. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol 2005 6: 331 337.
32. Nishimura E Sakihama T Setoguchi R Tanaka K Sakaguchi S. Induction of antigen-specific immunologic tolerance by in vivo and in vitro antigen-specific expansion of naturally arising Foxp3+CD25+CD4+ regulatory T cells. Int Immunol 2004 16: 1189 1201.
33. Klein L Khazaie K von Boehmer H. In vivo dynamics of antigen-specific regulatory T cells not predicted from behavior in vitro. Proc Natl Acad Sci USA 2003 10: 8886 8891.
34. Walker LS Chodos A Eggena M Dooms H Abbas AK. Antigen-dependent proliferation of CD4+ CD25+ regulatory T cells in vivo. J Exp Med 2003 198: 249 258.
35. Huehn J, et al. Developmental stage, phenotype, and migration distinguish naive- and effector/memory-like CD4+ regulatory T cells. J Exp Med 2004 19: 303 313.
36. Stockinger B Kassiotis G Bourgeois C. CD4 T-cell memory. Semin Immunol 2004 16: 295 303.
37. 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.
38. 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.
39. 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.
40. Xue HH, et al. IL-2 negatively regulates IL-7 receptor alpha chain expression in activated T lymphocytes. Proc Natl Acad Sci USA 2002 9: 13759 13764.
41. 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.
42. Roman E, et al. CD4 effector T cell subsets in the response to influenza: heterogeneity, migration, and function. J Exp Med 2002 196: 957 968.
43. Garcia S DiSanto J Stockinger B. Following the development of a CD4 T cell response in vivo: from activation to memory formation. Immunity 1999 1: 163 171.
44. 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.
45. Cavanagh LL, et al. Activation of bone marrow-resident memory T cells by circulating, antigen-bearing dendritic cells. Nat Immunol 2005 6: 1029 1037.
46. Berg LP James MJ Alvarez-Iglesias M Glennie S Lechler RI Marelli-Berg FM. Functional consequences of noncognate interactions between CD4+ memory T lymphocytes and the endothelium. J Immunol 2002 168: 3227 3234.
47. Lee DU Agarwal S Rao A. Th2 lineage commitment and efficient IL-4 production involves extended demethylation of the IL-4 gene. Immunity 2002 16: 649 660.
48. Grogan JL Mohrs M Harmon B Lacy DA Sedat JW Locksley RM. Early transcription and silencing of cytokine genes underlie polarization of T helper cell subsets. Immunity 2001 14: 205 215.
49. Murphy E, et al. Reversibility of T helper 1 and 2 populations is lost after long-term stimulation. J Exp Med 1996 183: 901 913.
50. Ahmadzadeh M Farber DL. Functional plasticity of an antigen-specific memory CD4 T cell population. Proc Natl Acad Sci USA 2002 9: 11802 11807.
51. Yamashita M, et al. Interleukin (IL)-4-independent maintenance of histone modification of the IL-4 gene loci in memory Th2 cells. J Biol Chem 2004 279: 39454 39464.
52. Martins GA Hutchins AS Reiner SL. Transcriptional activators of helper T cell fate are required for establishment but not maintenance of signature cytokine expression. J Immunol 2005 175: 5981 5985.
53. Pai SY Truitt ML Ho IC. GATA-3 deficiency abrogates the development and maintenance of T helper type 2 cells. Proc Natl Acad Sci USA 2004 101: 1993 1998.
54. Zhu J, et al. Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses. Nat Immunol 2004 5: 1157 1165.
55. Mohrs K Wakil AE Killeen N Locksley RM Mohrs M. A two-step process for cytokine production revealed by IL-4 dual-reporter mice. Immunity 2005 23: 419 429.
56. Homann D Teyton L Oldstone MB. Differential regulation of antiviral T-cell immunity results in stable CD8+ but declining CD4+ T-cell memory. Nat Med 2001 7: 913 919.
57. De Boer RJ Homann D Perelson AS. Different dynamics of CD4+ and CD8+ T cell responses during and after acute lymphocytic choriomeningitis virus infection. J Immunol 2003 171: 3928 3935.
58. Whitmire JK Asano MS Murali-Krishna K Suresh M Ahmed R. Long-term CD4 Th1 and Th2 memory following acute lymphocytic choriomeningitis virus infection. J Virol 1998 72: 8281 8288.
59. Topham DJ Doherty PC. Longitudinal analysis of the acute Sendai virus-specific CD4+ T cell response and memory. J Immunol 1998 161: 4530 4535.
60. Varga SM Welsh RM. Stability of virus-specific CD4+ T cell frequencies from acute infection into long term memory. J Immunol 1998 161: 367 374.
61. Sierra B, et al. Long-term memory cellular immune response to dengue virus after a natural primary infection. Int J Infect Dis 2002 6: 125 128.
62. Hammarlund E, et al. Duration of antiviral immunity after smallpox vaccination. Nat Med 2003 9: 1131 1137.
63. Amara RR Nigam P Sharma S Liu J Bostik V. Long-lived poxvirus immunity, robust CD4 help, and better persistence of CD4 than CD8 T cells. J Virol 2004 78: 3811 3816.
64. Doherty PC Topham DJ Tripp RA. Establishment and persistence of virus-specific CD4+ and CD8+ T cell memory. Immunol Rev 1996 150: 23 44.
65. Beverley PC Maini MK. Differences in the regulation of CD4 and CD8 T-cell clones during immune responses. Philos Trans R Soc Lond B Biol Sci 2000 35: 401 406.
66. Hasenkrug KJ Brooks DM Dittmer U. Critical role for CD4(+) T cells in controlling retrovirus replication and spread in persistently infected mice. J Virol 1998 72: 6559 6564.
67. Hasenkrug KJ Dittmer U. The role of CD4 and CD8 T cells in recovery and protection from retroviral infection: lessons from the Friend virus model. Virology 2000 272: 244 249.
68. Grakoui A, et al. HCV persistence and immune evasion in the absence of memory T cell help. Science 2003 302: 659 662.
69. Hebeis BJ, et al. Activation of virus-specific memory B cells in the absence of T cell help. J Exp Med 2004 19: 593 602.
70. Ochsenbein AF Pinschewer DD Sierro S Horvath E Hengartner H Zinkernagel RM. Protective long-term antibody memory by antigen-driven and T help-dependent differentiation of long-lived memory B cells to short-lived plasma cells independent of secondary lymphoid organs. Proc Natl Acad Sci USA 2000 97: 13263 13268.
71. Zinkernagel RM. On differences between immunity and immunological memory. Curr Opin Immunol 2002 14: 523 536.
72. Recher M, et al. Deliberate removal of T cell help improves virus-neutralizing antibody production. Nat Immunol 2004 5: 934 942.
73. Chattopadhyay PK Yu J Roederer M. A live-cell assay to detect antigen-specific CD4(+) T cells with diverse cytokine profiles. Nat Med 2005 1: 1113 1117.
74. Cohen GB Kaur A Johnson RP. Isolation of viable antigen-specific CD4 T cells by CD40L surface trapping. J Immunol Methods 2005 302: 103 115.
75. Frentsch M, et al. Direct access to CD4(+) T cells specific for defined antigens according to CD154 expression. Nat Med 2005 1: 1118 1124.
76. Almeida AR Borghans JA Freitas AA. T cell homeostasis: thymus regeneration and peripheral T cell restoration in mice with a reduced fraction of competent precursors. J Exp Med 2001 194: 591 599.
77. McNally JM Welsh RM. Bystander T cell activation and attrition. Curr Top Microbiol Immunol 2002 263: 29 41.
78. Okada H, et al. Extensive lymphopenia due to apoptosis of uninfected lymphocytes in acute measles patients. Arch Virol 2000 145: 905 920.
79. Tumpey TM Lu X Morken T Zaki SR Katz JM. Depletion of lymphocytes and diminished cytokine production in mice infected with a highly virulent influenza A (H5N1) virus isolated from humans. J Virol 2000 74: 6105 6116.
80. Tanchot C Rocha B. The organization of mature T-cell pools. Immunol Today 1998 19: 575 579.
81. Bourgeois C Kassiotis G Stockinger B. A major role for memory CD4 T cells in the control of lymphopenia-induced proliferation of naive CD4 T cells. J Immunol 2005 174: 5316 5323.
82. Zhang X Sun S Hwang I Tough DF Sprent J. Potent and selective stimulation of memory-phenotype CD8+ T cells in vivo by IL-15. Immunity 1998 8: 591 599.
83. Tan JT Ernst B Kieper WC LeRoy E Sprent J Surh CD. 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 2002 195: 1523 1532.
84. Kennedy MK, et al. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 2000 191: 771 780.
85. Lodolce JP, et al. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 1998 9: 669 676.
86. 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.
87. Lenz DC, et al. IL-7 regulates basal homeostatic proliferation of antiviral CD4+ T cell memory. Proc Natl Acad Sci USA 2004 101: 9357 9362.
88. Pandey A, et al. Cloning of a receptor subunit required for signaling by thymic stromal lymphopoietin. Nat Immunol 2000 1: 59 64.
89. Geiselhart LA Humphries CA Gregorio TA Mou S Subleski J Komschlies KL. IL-7 administration alters the CD4:CD8 ratio, increases T cell numbers, and increases T cell function in the absence of activation. J Immunol 2001 16: 3019 3027.
90. Seddon B Zamoyska R. TCR and IL-7 receptor signals can operate independently or synergize to promote lymphopenia-induced expansion of naive T cells. J Immunol 2002 169: 3752 3759.
91. Kieper WC, et al. Overexpression of interleukin (IL)-7 leads to IL-15-independent generation of memory phenotype CD8+ T cells. J Exp Med 2002 195: 1533 1539.
92. Kassiotis G Zamoyska R Stockinger B. Involvement of avidity for major histocompatibility complex in homeostasis of naive and memory T cells. J Exp Med 2003 197: 1007 1016.
93. Park JH, et al. Suppression of IL7Ralpha transcription by IL-7 and other prosurvival cytokines: a novel mechanism for maximizing IL-7-dependent T cell survival. Immunity 2004 21: 289 302.
94. Fontenot JD Rasmussen JP Gavin MA Rudensky AY. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat Immunol 2005 6: 1142 1151.
95. Oppmann B, et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000 13: 715 725.
96. Callard RE Stark J Yates AJ. Fratricide: a mechanism for T memory-cell homeostasis. Trends Immunol 2003 24: 370 375.
97. Polic B Kunkel D Scheffold A Rajewsky K. How alpha beta T cells deal with induced TCR alpha ablation. Proc Natl Acad Sci USA 2001 98: 8744 8749.
98. Swain SL Hu H Huston G. Class II-independent generation of CD4 memory T cells from effectors. Science 1999 286: 1381 1383.
99. Kassiotis G Garcia S Simpson E Stockinger B. Impairment of immunological memory in the absence of MHC despite survival of memory T cells. Nat Immunol 2002 3: 244 250.