Control of CD4+ T-cell memory by cytokines and costimulators

Immunological Reviews

Volumn 211, Issue , 2006, Pages 23-38

  Dooms, Hans ^a   Abbas, Abul K ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CYTOKINE; INTERLEUKIN 2; INTERLEUKIN 7;

ADOPTIVE TRANSFER; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CELL CYCLE; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CELL MATURATION; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR IMMUNITY; DENDRITIC CELL; HOMEOSTASIS; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOSTIMULATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE SUBPOPULATION; MEMORY CELL; MEMORY T LYMPHOCYTE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUALITATIVE ANALYSIS; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGENS, CD28; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; HUMANS; IMMUNOLOGIC MEMORY; INTERLEUKIN-2; INTERLEUKIN-7; MICE;

EID: 33745062839     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.0105-2896.2006.00387.x     Document Type: Review

References (105)

1. 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.
2. Gourley TS Wherry EJ Masopust D Ahmed R. Generation and maintenance of immunological memory. Semin Immunol 2004 16: 323 333.
3. Eichelberger M Allan W Zijlstra M Jaenisch R Doherty PC. Clearance of influenza virus respiratory infection in mice lacking class I major histocompatibility complex-restricted CD8+ T cells. J Exp Med 1991 174: 875 880.
4. Zhong W Roberts AD Woodland DL. Antibody-independent antiviral function of memory CD4+ T cells in vivo requires regulatory signals from CD8+ effector T cells. J Immunol 2001 167: 1379 1386.
5. Sun JC Bevan MJ. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 2003 300: 339 342.
6. Janssen EM Lemmens EE Wolfe T Christen U von Herrath MG Schoenberger SP. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 2003 421: 852 856.
7. Sun JC Williams MA Bevan MJ. CD4+ T cells are required for the maintenance, not programming, of memory CD8+ T cells after acute infection. Nat Immunol 2004 5: 927 933.
8. Radbruch A Thiel A. Cell therapy for autoimmune diseases: does it have a future? Ann Rheum Dis 2004 63 ( Suppl ii96 ii101.
9. Chen Y Heeger PS Valujskikh A. In vivo helper functions of alloreactive memory CD4+ T cells remain intact despite donor-specific transfusion and anti-CD40 ligand therapy. J Immunol 2004 172: 5456 5466.
10. Li Q, et al. Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 2005 434: 1148 1152.
11. Mattapallil JJ Douek DC Hill B Nishimura Y Martin M Roederer M. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 2005 434: 1093 1097.
12. Swain SL. Generation and in vivo persistence of polarized Th1 and Th2 memory cells. Immunity 1994 1: 543 552.
13. McHeyzer-Williams MG Altman JD Davis MM. Tracking antigen-specific helper T cell responses. Curr Opin Immunol 1996 8: 278 284.
14. Rees W, et al. An inverse relationship between T cell receptor affinity and antigen dose during CD4(+) T cell responses in vivo and in vitro. Proc Natl Acad Sci USA 1999 96: 9781 9786.
15. Arnold PY, et al. Reliable generation and use of MHC class II:gamma2aFc multimers for the identification of antigen-specific CD4(+) T cells. J Immunol Methods 2002 271: 137 151.
16. 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.
17. Mallet-Designe VI Stratmann T Homann D Carbone F Oldstone MB Teyton L. Detection of low-avidity CD4+ T cells using recombinant artificial APC: following the antiovalbumin immune response. J Immunol 2003 170: 123 131.
18. Corbin GA Harty JT. Duration of infection and antigen display have minimal influence on the kinetics of the CD4+ T cell response to Listeria monocytogenes infection. J Immunol 2004 173: 5679 5687.
19. London CA Perez VL Abbas AK. Functional characteristics and survival requirements of memory CD4+ T lymphocytes in vivo. J Immunol 1999 162: 766 773.
20. Grayson JM Zajac AJ Altman JD Ahmed R. Cutting edge: increased expression of Bcl-2 in antigen-specific memory CD8+ T cells. J Immunol 2000 164: 3950 3954.
21. London CA Lodge MP Abbas AK. Functional responses and costimulator dependence of memory CD4+ T cells. J Immunol 2000 164: 265 272.
22. Malek TR Bayer AL. Tolerance, not immunity, crucially depends on IL-2. Nat Rev Immunol 2004 4: 665 674.
23. Gillis S Ferm MM Ou W Smith KA. T cell growth factor: parameters of production and a quantitative microassay for activity. J Immunol 1978 120: 2027 2032.
24. Mier JW Gallo RC. Purification and some characteristics of human T-cell growth factor from phytohemagglutinin-stimulated lymphocyte-conditioned media. Proc Natl Acad Sci USA 1980 77: 6134 6138.
25. Smith KA. Interleukin-2: inception, impact, and implications. Science 1988 240: 1169 1176.
26. Dooms H Kahn E Knoechel B Abbas AK. IL-2 induces a competitive survival advantage in T lymphocytes. J Immunol 2004 172: 5973 5979.
27. Lantz O Grandjean I Matzinger P Di Santo JP. Gamma chain required for naive CD4+ T cell survival but not for antigen proliferation. Nat Immunol 2000 1: 54 58.
28. Cho BK Rao VP Ge Q Eisen HN Chen J. Homeostasis-stimulated proliferation drives naive T cells to differentiate directly into memory T cells. J Exp Med 2000 192: 549 556.
29. Goldrath AW Bogatzki LY Bevan MJ. Naive T cells transiently acquire a memory-like phenotype during homeostasis-driven proliferation. J Exp Med 2000 192: 557 564.
30. Min B Yamane H Hu-Li J Paul WE. Spontaneous and homeostatic proliferation of CD4 T cells are regulated by different mechanisms. J Immunol 2005 174: 6039 6044.
31. Goldrath AW Luckey CJ Park R Benoist C Mathis D. The molecular program induced in T cells undergoing homeostatic proliferation. Proc Natl Acad Sci USA 2004 101: 16885 16890.
32. Kundig TM Schorle H Bachmann MF Hengartner H Zinkernagel RM Horak I. Immune responses in interleukin-2-deficient mice. Science 1993 262: 1059 1061.
33. Li XC, et al. IL-2 and IL-4 double knockout mice reject islet allografts: a role for novel T cell growth factors in allograft rejection. J Immunol 1998 161: 890 896.
34. Su HC, et al. CD4+ and CD8+ T cell interactions in IFN-gamma and IL-4 responses to viral infections: requirements for IL-2. J Immunol 1998 160: 5007 5017.
35. 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.
36. Malek TR Yu A Vincek V Scibelli P Kong L. CD4 regulatory T cells prevent lethal autoimmunity in IL-2Rbeta-deficient mice. Implications for the nonredundant function of IL-2. Immunity 2002 17: 167 178.
37. 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 2003 170: 236 242.
38. Khoruts A Mondino A Pape KA Reiner SL Jenkins MK. A natural immunological adjuvant enhances T cell clonal expansion through a CD28-dependent, interleukin (IL) -2-independent mechanism. J Exp Med 1998 187: 225 236.
39. Leung DT Morefield S Willerford DM. Regulation of lymphoid homeostasis by IL-2 receptor signals in vivo. J Immunol 2000 164: 3527 3534.
40. Witte PL Frantsve LM Hergott M Rahbe SM. Cytokine production and heterogeneity of primary stromal cells that support B lymphopoiesis. Eur J Immunol 1993 23: 1809 1817.
41. Lodolce JP, et al. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 1998 9: 669 676.
42. 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.
43. 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.
44. 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.
45. Schluns KS Kieper WC Jameson SC Lefrancois L. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat Immunol 2000 1: 426 432.
46. Ku CC Murakami M Sakamoto A Kappler J Marrack P. Control of homeostasis of CD8+ memory T cells by opposing cytokines. Science 2000 288: 675 678.
47. 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.
48. 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.
49. Huster KM, 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 2004 101: 5610 5615.
50. Geginat J Sallusto F Lanzavecchia A. Cytokine-driven proliferation and differentiation of human naive, central memory, and effector memory CD4(+) T cells. J Exp Med 2001 194: 1711 1719.
51. 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.
52. 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.
53. Opferman JT Letai A Beard C Sorcinelli MD Ong CC Korsmeyer SJ. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 2003 426: 671 676.
54. Murali-Krishna K Lau LL Sambhara S Lemonnier F Altman J Ahmed R. Persistence of memory CD8 T cells in MHC class I-deficient mice. Science 1999 286: 1377 1381.
55. Swain SL Hu H Huston G. Class II-independent generation of CD4 memory T cells from effectors. Science 1999 286: 1381 1383.
56. 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.
57. 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.
58. Waldmann TA. The multi-subunit interleukin-2 receptor. Annu Rev Biochem 1989 58: 875 911.
59. Malek TR Yu A Scibelli P Lichtenheld MG Codias EK. Broad programming by IL-2 receptor signaling for extended growth to multiple cytokines and functional maturation of antigen-activated T cells. J Immunol 2001 166: 1675 1683.
60. Gett AV Sallusto F Lanzavecchia A Geginat J. T cell fitness determined by signal strength. Nat Immunol 2003 4: 355 360.
61. Opferman JT Ober BT Ashton-Rickardt PG. Linear differentiation of cytotoxic effectors into memory T lymphocytes. Science 1999 283: 1745 1748.
62. Turner JM. IL-2-dependent induction of G1 cyclins in primary T cells is not blocked by rapamycin or cyclosporin A. Int Immunol 1993 5: 1199 1209.
63. Nourse J, et al. Interleukin-2-mediated elimination of the p27Kip1 cyclin-dependent kinase inhibitor prevented by rapamycin. Nature 1994 372: 570 573.
64. Brennan P Babbage JW Burgering BM Groner B Reif K Cantrell DA. Phosphatidylinositol 3-kinase couples the interleukin-2 receptor to the cell cycle regulator E2F. Immunity 1997 7: 679 689.
65. Moriggl R, et al. Stat5 is required for IL-2-induced cell cycle progression of peripheral T cells. Immunity 1999 10: 249 259.
66. Schorle H Holtschke T Hunig T Schimpl A Horak I. Development and function of T cells in mice rendered interleukin-2 deficient by gene targeting. Nature 1991 352: 621 624.
67. Van Parijs L Biuckians A Ibragimov A Alt FW Willerford DM Abbas AK. Functional responses and apoptosis of CD25 (IL-2R alpha)-deficient T cells expressing a transgenic antigen receptor. J Immunol 1997 158: 3738 3745.
68. Gillis S Gillis AE Henney CS. Monoclonal antibody directed against interleukin 2. I. Inhibition of T lymphocyte mitogenesis and the in vitro differentiation of alloreactive cytolytic T cells. J Exp Med 1981 154: 983 988.
69. Malek TR Ortega G Jakway JP Chan C Shevach EM. The murine IL 2 receptor. II. Monoclonal anti-IL 2 receptor antibodies as specific inhibitors of T cell function in vitro. J Immunol 1984 133: 1976 1982.
70. Jelley-Gibbs DM Lepak NM Yen M Swain SL. Two distinct stages in the transition from naive CD4 T cells to effectors, early antigen-dependent and late cytokine-driven expansion and differentiation. J Immunol 2000 165: 5017 5026.
71. Duke RC Cohen JJ. IL-2 addiction: withdrawal of growth factor activates a suicide program in dependent T cells. Lymphokine Res 1986 5: 289 299.
72. Akbar AN, et al. Interleukin-2 receptor common gamma-chain signaling cytokines regulate activated T cell apoptosis in response to growth factor withdrawal: selective induction of anti-apoptotic (bcl-2, bcl-xL) but not pro-apoptotic (bax, bcl-xS) gene expression. Eur J Immunol 1996 26: 294 299.
73. 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.
74. Cote-Sierra J, et al. Interleukin 2 plays a central role in Th2 differentiation. Proc Natl Acad Sci USA 2004 101: 3880 3885.
75. Yamane H Zhu J Paul WE. Independent roles for IL-2 and GATA-3 in stimulating naive CD4+ T cells to generate a Th2-inducing cytokine environment. J Exp Med 2005 202: 793 804.
76. Saparov A, et al. Interleukin-2 expression by a subpopulation of primary T cells is linked to enhanced memory/effector function. Immunity 1999 11: 271 280.
77. Hurez V, et al. Restricted clonal expression of IL-2 by naive T cells reflects differential dynamic interactions with dendritic cells. J Exp Med 2003 198: 123 132.
78. Sadlack B Merz H Schorle H Schimpl A Feller AC Horak I. Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell 1993 75: 253 261.
79. Willerford DM Chen J Ferry JA Davidson L Ma A Alt FW. Interleukin-2 receptor alpha chain regulates the size and content of the peripheral lymphoid compartment. Immunity 1995 3: 521 530.
80. Lenardo MJ. Interleukin-2 programs mouse alpha beta T lymphocytes for apoptosis. Nature 1991 353: 858 861.
81. Refaeli Y Van Parijs L London CA Tschopp J Abbas AK. Biochemical mechanisms of IL-2-regulated Fas-mediated T cell apoptosis. Immunity 1998 8: 615 623.
82. Bathe OF Dalyot-Herman N Malek TR. IL-2 during in vitro priming promotes subsequent engraftment and successful adoptive tumor immunotherapy by persistent memory phenotypic CD8(+) T cells. J Immunol 2001 167: 4511 4517.
83. Cheng LE Greenberg PD. Selective delivery of augmented IL-2 receptor signals to responding CD8+ T cells increases the size of the acute antiviral response and of the resulting memory T cell pool. J Immunol 2002 169: 4990 4997.
84. Chang J Choi SY Jin HT Sung YC Braciale TJ. Improved effector activity and memory CD8 T cell development by IL-2 expression during experimental respiratory syncytial virus infection. J Immunol 2004 172: 503 508.
85. Dai Z Konieczny BT Lakkis FG. The dual role of IL-2 in the generation and maintenance of CD8+ memory T cells. J Immunol 2000 165: 3031 3036.
86. Blattman JN Grayson JM Wherry EJ Kaech SM Smith KA Ahmed R. Therapeutic use of IL-2 to enhance antiviral T-cell responses in vivo. Nat Med 2003 9: 540 547.
87. Foussat A, et al. Effects of exogenous IL-2 administration on the homeostasis of CD4+ T lymphocytes. J Clin Immunol 2004 24: 503 514.
88. Alpdogan O van den Brink MR. IL-7 and IL-15: therapeutic cytokines for immunodeficiency. Trends Immunol 2005 26: 56 64.
89. Melchionda F Fry TJ Milliron MJ McKirdy MA Tagaya Y Mackall CL. Adjuvant IL-7 or IL-15 overcomes immunodominance and improves survival of the CD8+ memory cell pool. J Clin Invest 2005 115: 1177 1187.
90. Salomon B Bluestone JA. Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation. Annu Rev Immunol 2001 19: 225 252.
91. Mittrucker HW Kursar M Kohler A Hurwitz R Kaufmann SH. Role of CD28 for the generation and expansion of antigen-specific CD8(+) T lymphocytes during infection with Listeria monocytogenes. J Immunol 2001 167: 5620 5627.
92. Suresh M, et al. Role of CD28-B7 interactions in generation and maintenance of CD8 T cell memory. J Immunol 2001 167: 5565 5573.
93. Villegas EN Elloso MM Reichmann G Peach R Hunter CA. Role of CD28 in the generation of effector and memory responses required for resistance to Toxoplasma gondii. J Immunol 1999 163: 3344 3353.
94. Lucas PJ Negishi I Nakayama K Fields LE Loh DY. Naive CD28-deficient T cells can initiate but not sustain an in vitro antigen-specific immune response. J Immunol 1995 154: 5757 5768.
95. Sperling AI Auger JA Ehst BD Rulifson IC Thompson CB Bluestone JA. CD28/B7 interactions deliver a unique signal to naive T cells that regulates cell survival but not early proliferation. J Immunol 1996 157: 3909 3917.
96. Kundig TM, et al. Duration of TCR stimulation determines costimulatory requirement of T cells. Immunity 1996 5: 41 52.
97. Rulifson IC Sperling AI Fields PE Fitch FW Bluestone JA. CD28 costimulation promotes the production of Th2 cytokines. J Immunol 1997 158: 658 665.
98. Howland KC Ausubel LJ London CA Abbas AK. The roles of CD28 and CD40 ligand in T cell activation and tolerance. J Immunol 2000 164: 4465 4470.
99. Whitmire JK Ahmed R. Costimulation in antiviral immunity: differential requirements for CD4(+) and CD8(+) T cell responses. Curr Opin Immunol 2000 12: 448 455.
100. Borrow P, et al. CD40L-deficient mice show deficits in antiviral immunity and have an impaired memory CD8+ CTL response. J Exp Med 1996 183: 2129 2142.
101. Calderhead DM Buhlmann JE van den Eertwegh AJ Claassen E Noelle RJ Fell HP. Cloning of mouse Ox40: a T cell activation marker that may mediate T-B cell interactions. J Immunol 1993 151: 5261 5271.
102. al-Shamkhani A Birkeland ML Puklavec M Brown MH James W Barclay AN. OX40 is differentially expressed on activated rat and mouse T cells and is the sole receptor for the OX40 ligand. Eur J Immunol 1996 26: 1695 1699.
103. Rogers PR Song J Gramaglia I Killeen N Croft M. OX40 promotes Bcl-xL and Bcl-2 expression and is essential for long-term survival of CD4 T cells. Immunity 2001 15: 445 455.
104. Gramaglia I Jember A Pippig SD Weinberg AD Killeen N Croft M. The OX40 costimulatory receptor determines the development of CD4 memory by regulating primary clonal expansion. J Immunol 2000 165: 3043 3050.
105. Salek-Ardakani S, et al. OX40 (CD134) controls memory T helper 2 cells that drive lung inflammation. J Exp Med 2003 198: 315 324.