Influencing the fates of CD4 T cells on the path to memory: Lessons from influenza

Immunology and Cell Biology

Volumn 86, Issue 4, 2008, Pages 343-352

  Jelley Gibbs, Dawn M ^a   Strutt, Tara M ^a   McKinstry, K Kai ^a   Swain, Susan L ^a  

^a TRUDEAU INSTITUTE   (United States)

Author keywords

Antigen presentation; CD4 T cells; Effector; Inflammation; Influenza; Memory

Indexed keywords

GROWTH FACTOR; TOLL LIKE RECEPTOR; VIRUS ANTIGEN;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FATE; CELLULAR IMMUNITY; EFFECTOR CELL; HUMAN; HUMORAL IMMUNITY; IMMUNITY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INFLUENZA; INFLUENZA VIRUS; LYMPHOCYTE DIFFERENTIATION; MEMORY T LYMPHOCYTE; NONHUMAN; REVIEW; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; VACCINATION; VIRUS REPLICATION;

ANTIGENS, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; HUMANS; IMMUNOLOGIC MEMORY; INFLUENZA, HUMAN;

EID: 43449128845     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2008.13     Document Type: Review

References (158)

1. Moon JJ, Chu HH, Pepper M, McSorley SJ, Jameson SC, Kedl RM et al. Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 2007; 27: 203-213.
2. Stetson DB, Mohrs M, Mallet-Designe V, Teyton L, Locksley RM. Rapid expansion and IL-4 expression by Leishmania-specific naive helper T cells in vivo. Immunity 2002; 17: 191-200.
3. Whitmire JK, Benning N, Whitton JL. Precursor frequency, nonlinear proliferation, and functional maturation of virus-specific CD4+ T cells. J Immunol 2006; 176: 3028-3036.
4. Stockinger B, Bourgeois C, Kassiotis G. CD4+ memory T cells: functional differentiation and homeostasis. Immunol Rev 2006; 211: 39-48.
5. Rudolph MG, Stanfield RL, Wilson IA. How TCRs bind MHCs, peptides, and coreceptors. Annu Rev Immunol 2006; 24: 419-466.
6. Román E, Miller E, Harmsen A, Wiley J, Von Andrian UH, Huston G et al. CD4 effector T cell subsets in the response to influenza: heterogeneity, migration, and function. J Exp Med 2002; 196: 957-968.
7. Jelley-Gibbs DM, Dibble JP, Filipson S, Haynes L, Kemp RA, Swain SL. Repeated stimulation of CD4 effector T cells can limit their protective function. J Exp Med 2005; 201: 1101-1112.
8. Jelley-Gibbs DM, Brown DM, Dibble JP, Haynes L, Eaton SM, Swain SL. Unexpected prolonged presentation of influenza antigens promotes CD4T cell memory generation. J Exp Med 2005; 202: 697-706.
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. Brown DM, Dilzer AM, Meents DL, Swain SL. CD4T cell-mediated protection from lethal influenza: perforin and antibody-mediated mechanisms give a one-two punch. J Immunol 2006; 177: 2888-2898.
11. Swain SL, Agrewala JN, Brown DM, Jelley-Gibbs DM, Golech S, Huston G et al. CD4+ T-cell memory: generation and multi-faceted roles for CD4+ T cells in protective immunity to influenza. Immunol Rev 2006; 211: 8-22.
12. Shevach EM. CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2002; 2: 389-400.
13. Shevach EM. From vanilla to 28 flavors: multiple varieties of T regulatory cells. Immunity 2006; 25: 195-201.
14. Belkaid Y, Rouse BT. Natural regulatory T cells in infectious disease. Nat Immunol 2005; 6: 353-360.
15. Sakaguchi S. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 2005; 6: 345-352.
16. 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.
17. Kelso A, Troutt AB, Maraskovsky E, Gough NM, Morris L, Pech MH et al. Heterogeneity in lymphokine profiles of CD4+ and CD8+ T cells and clones activated in vivo and in vitro. Immunol Rev 1991; 123: 85-114.
18. Ansel KM, McHeyzer-Williams LJ, Ngo VN, McHeyzer-Williams MG, Cyster JG. In vivo-activated CD4T cells upregulate CXC chemokine receptor 5 and reprogram their response to lymphoid chemokines. J Exp Med 1999; 190: 1123-1134.
19. Breitfeld D, Ohl L, Kremmer E, Ellwart J, Sallusto F, Lipp M et al. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J Exp Med 2000; 192: 1545-1552.
20. Schaerli P, Willimann K, Lang AB, Lipp M, Loetscher P, Moser B. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J Exp Med 2000; 192: 1553-1562.
21. Kim CH, Rott LS, Clark-Lewis I, Campbell DJ, Wu L, Butcher EC. Subspecialization of CXCR5+ T cells: B helper activity is focused in a germinal center-localized subset of CXCR5+ T cells. J Exp Med 2001; 193: 1373-1381.
22. Vinuesa CG, Cook MC, Angelucci C, Athanasopoulos V, Rui L, Hill KM et al. A RING-type ubiquitin ligase family member required to repress follicular helper T cells and autoimmunity. Nature 2005; 435: 452-458.
23. Wynn TA. T(H)-17: a giant step from T(H)1 and T(H)2. Nat Immunol 2005; 6: 1069-1070.
24. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P et al. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 2001; 194: 519-527.
25. Liang SC, Long AJ, Bennett F, Whitters MJ, Karim R, Collins M et al. An IL-17F/A heterodimer protein is produced by mouse Th17 cells and induces airway neutrophil recruitment. J Immunol 2007; 179: 7791-7799.
26. Hsu HC, Yang P, Wang J, Wu Q, Myers R, Chen J et al. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat Immunol 2008; 9: 166-175.
27. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005; 201: 233-240.
28. Murphy CA, Langrish CL, Chen Y, Blumenschein W, McClanahan T, Kastelein RA et al. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 2003; 198: 1951-1957.
29. Khader SA, Bell GK, Pearl JE, Fountain JJ, Rangel-Moreno J, Cilley GE et al. IL-23 and IL-17 in the establishment of protective pulmonary CD4(+) T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 2007; 8: 369-377.
30. McGeachy MJ, Bak-Jensen KS, Chen Y, Tato CM, Blumenschein W, McClanahan T et al. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat Immunol 2007; 8: 1390-1397.
31. Swain SL, Bradley LM, Croft M, Tonkonogy S, Atkins G, Weinberg AD et al. Helper T-cell subsets: phenotype, function and the role of lymphokines in regulating their development. Immunol Rev 1991; 123: 115-144.
32. Seder RA, Paul WE. Acquisition of lymphokine-producing phenotype by CD4+ T cells. Annu Rev Immunol 1994; 12: 635-673.
33. Ansel KM, Lee DU, Rao A. An epigenetic view of helper T cell differentiation. Nat Immunol 2003; 4: 616-623.
34. Fitzpatrick DR, Shirley KM, McDonald LE, Bielefeldt-Ohmann H, Kay GF, Kelso A. Distinct methylation of the interferon gamma (IFN-gamma) and interleukin 3 (IL-3) genes in newly activated primary CD8+ T lymphocytes: regional IFN-gamma promoter demethylation and mRNA expression are heritable in CD44(high)CD8+ T cells. J Exp Med 1998; 188: 103-117.
35. Fields PE, Lee GR, Kim ST, Bartsevich VV, Flavell RA. Th2-specific chromatin remodeling and enhancer activity in the Th2 cytokine locus control region. Immunity 2004; 21: 865-876.
36. Schoenborn JR, Dorschner MO, Sekimata M, Santer DM, Shnyreva M, Fitzpatrick DR et al. Comprehensive epigenetic profiling identifies multiple distal regulatory elements directing transcription of the gene encoding interferon-gamma. Nat Immunol 2007; 8: 732-742.
37. Akimzhanov AM, Yang XO, Dong C. Chromatin remodeling of interleukin-17 (IL-17)-IL-17F cytokine gene locus during inflammatory helper T cell differentiation. J Biol Chem 2007; 282: 5969-5972.
38. Floess S, Freyer J, Siewert C, Baron U, Olek S, Polansky J et al. Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol 2007; 5: e38.
39. Mucida D, Park Y, Kim G, Turovskaya O, Scott I, Kronenberg M et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 2007; 317: 256-260.
40. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM 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.
41. Mangan PR, Harrington LE, O'Quinn DB, Helms WS, Bullard DC, Elson CO et al. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006; 441: 231-234.
42. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441: 235-238.
43. Weber SE, Harbertson J, Godebu E, Mros GA, Padrick RC, Carson BD et al. Adaptive islet-specific regulatory CD4T cells control autoimmune diabetes and mediate the disappearance of pathogenic Th1 cells in vivo. J Immunol 2006; 176: 4730-4739.
44. Pasare C, Medzhitov R. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 2003; 299: 1033-1036.
45. Pulendran B, Palucka K, Banchereau J. Sensing pathogens and tuning immune responses. Science 2001; 293: 253-256.
46. Ottenhoff TH, Bevan MJ. Host-pathogen interactions. Curr Opin Immunol 2004; 16: 439-442.
47. Moser M, Murphy KM. Dendritic cell regulation of TH1-TH2 development. Nat Immunol 2000; 1: 199-205.
48. Vella AT, Mitchell T, Groth B, Linsley PS, Green JM, Thompson CB et al. CD28 engagement and proinflammatory cytokines contribute to T cell expansion and long-term survival in vivo. J Immunol 1997; 158: 4714-4720.
49. Sepulveda H, Cerwenka A, Morgan T, Dutton RW. CD28, IL-2-independent costimulatory pathways for CD8T lymphocyte activation. J Immunol 1999; 163: 1133-1142.
50. Croft M. Co-stimulatory members of the TNFR family: keys to effective T-cell immunity? Nat Rev Immunol 2003; 3: 609-620.
51. Banerjee D, Liou HC, Sen R. c-Rel-dependent priming of naive T cells by inflammatory cytokines. Immunity 2005; 23: 445-458.
52. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007; 449: 819-826.
53. Akira S, Takeda K, Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2001; 2: 675-680.
54. Garcia-Sastre A, Biron CA. Type 1 interferons and the virus-host relationship: a lesson in detente. Science 2006; 312: 879-882.
55. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H et al. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 2005; 6: 981-988.
56. Rivera A, Ro G, Van Epps HL, Simpson T, Leiner I, Sant'Angelo DB et al. Innate immune activation and CD4+ T cell priming during respiratory fungal infection. Immunity 2006; 25: 665-675.
57. Pulendran B, Ahmed R. Translating innate immunity into immunological memory: implications for vaccine development. Cell 2006; 124: 849-863.
58. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ et al. Immunobiology of dendritic cells. Annu Rev Immunol 2000; 18: 767-811.
59. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392: 245-252.
60. Loré K, Betts MR, Brenchley JM, Kuruppu J, Khojasteh S, Perfetto S et al. Toll-like receptor ligands modulate dendritic cells to augment cytomegalovirus- and HIV-1-specific T cell responses. J Immunol 2003; 171: 4320-4328.
61. van Duin D, Medzhitov R, Shaw AC. Triggering TLR signaling in vaccination. Trends Immunol 2006; 27: 49-55.
62. Agrawal S, Agrawal A, Doughty B, Gerwitz A, Blenis J, Van Dyke T et al. Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos. J Immunol 2003; 171: 4984-4989.
63. Barr TA, Brown S, Ryan G, Zhao J, Gray D. TLR-mediated stimulation of APC: distinct cytokine responses of B cells and dendritic cells. Eur J Immunol 2007; 37: 3040-3053.
64. Pulendran B. Modulating vaccine responses with dendritic cells and Toll-like receptors. Immunol Rev 2004; 199: 227-250.
65. Tritel M, Stoddard AM, Flynn BJ, Darrah PA, Wu CY, Wille U et al. Prime-boost vaccination with HIV-1 Gag protein and cytosine phosphate guanosine oligodeoxynucleotide, followed by adenovirus, induces sustained and robust humoral and cellular immune responses. J Immunol 2003; 171: 2538-2547.
66. Davis HL, Weeratna R, Waldschmidt TJ, Tygrett L, Schorr J, Krieg AM. CpG DNA is a potent enhancer of specific immunity in mice immunized with recombinant hepatitis B surface antigen. J Immunol 1998; 160: 870-876.
67. Rhee EG, Mendez S, Shah JA, Wu CY, Kirman JR, Turon TN et al. Vaccination with heat-killed Leishmania antigen or recombinant leishmanial protein and CpG oligodeoxynucleotides induces long-term memory CD4+ and CD8+ T cell responses and protection against Leishmania major infection. J Exp Med 2002; 195: 1565-1573.
68. Ichinohe T, Watanabe I, Ito S, Fujii H, Moriyama M, Tamura S et al. Synthetic double-stranded RNA poly(I:C) combined with mucosal vaccine protects against influenza virus infection. J Virol 2005; 79: 2910-2919.
69. Krieg AM. Toll-like receptor 9 (TLR9) agonists in the treatment of cancer. Oncogene 2008; 27: 161-167.
70. Klinman DM, Xie H, Little SF, Currie D, Ivins BE. CpG oligonucleotides improve the protective immune response induced by the anthrax vaccination of Rhesus macaques. Vaccine 2004; 22: 2881-2886.
71. Proietti E, Bracci L, Puzelli S, Di Pucchio T, Sestili P, De Vincenzi E et al. Type I IFN as a natural adjuvant for a protective immune response: lessons from the influenza vaccine model. J Immunol 2002; 169: 375-383.
72. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 2003; 3: 133-146.
73. Rochman I, Paul WE, Ben-Sasson SZ. IL-6 increases primed cell expansion and survival. J Immunol 2005; 174: 4761-4767.
74. Diehl S, Rincon M. The two faces of IL-6 on Th1/Th2 differentiation. Mol Immunol 2002; 39: 531-536.
75. Zhou L, Ivanov II, Spolski R, Min R, Shenderov K, Egawa T et al. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 2007; 8: 967-974.
76. Kuchen S, Robbins R, Sims GP, Sheng C, Phillips TM, Lipsky PE et al. Essential role of IL-21 in B cell activation, expansion, and plasma cell generation during CD4+ T cell-B cell collaboration. J Immunol 2007; 179: 5886-5896.
77. Mitchell TC, Hildeman D, Kedl RM, Teague TK, Schaefer BC, White J et al. Immunological adjuvants promote activated T cell survival via induction of Bcl-3. Nat Immunol 2001; 2: 397-402.
78. Gururajan M, Jacob J, Pulendran B. Toll-like receptor expression and responsiveness of distinct murine splenic and mucosal B-cell subsets. PLoS ONE 2007; 2: e863.
79. Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol 2004; 5: 987-995.
80. Pulendran B, Kumar P, Cutler CW, Mohamadzadeh M, Van Dyke T, Banchereau J. Lipopolysaccharides from distinct pathogens induce different classes of immune responses in vivo. J Immunol 2001; 167: 5067-5076.
81. Blander JM, Medzhitov R. Regulation of phagosome maturation by signals from toll-like receptors. Science 2004; 304: 1014-1018.
82. Blander JM, Medzhitov R. On regulation of phagosome maturation and antigen presentation. Nat Immunol 2006; 7: 1029-1035.
83. West MA, Wallin RP, Matthews SP, Svensson HG, Zaru R, Ljunggren HG et al. Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 2004; 305: 1153-1157.
84. Swain SL, Weinberg AD, English M, Huston G. IL-4 directs the development of Th2-like helper effectors. J Immunol 1990; 145: 3796-3806.
85. Swain SL, Weinberg AD, English M. CD4+ T cell subsets. Lymphokine secretion of memory cells and of effector cells that develop from precursors in vitro. J Immunol 1990; 144: 1788-1799.
86. Jenkins MK, Taylor PS, Norton SD, Urdahl KB. CD28 delivers a costimulatory signal involved in antigen-specific IL-2 production by human T cells. J Immunol 1991; 147: 2461-2466.
87. Croft M, Duncan DD, Swain SL. Response of naive antigen-specific CD4+ T cells in vitro: characteristics and antigen-presenting cell requirements. J ExpMed 1992; 176: 1431-1437.
88. Dubey C, Croft M, Swain SL. Costimulatory requirements of naive CD4+ T cells. ICAM-1 or B7-1 can costimulate naive CD4T cell activation but both are required for optimum response. J Immunol 1995; 155: 45-57.
89. Smith KA. Interleukin-2: inception, impact, and implications. Science 1988; 240: 1169-1176.
90. Rogers PR, Huston G, Swain SL. High antigen density and IL-2 are required for generation of CD4 effectors secreting Th1 rather than Th0 cytokines. J Immunol 1998; 161: 3844-3852.
91. Jelley-Gibbs DM, Lepak NM, Yen M, Swain SL. Two distinct stages in the transition from naive CD4T cells to effectors, early antigen-dependent and late cytokine-driven expansion and differentiation. J Immunol 2000; 165: 5017-5026.
92. Haynes L, Linton PJ, Eaton SM, Tonkonogy SL, Swain SL. Interleukin 2, but not other common gamma chain-binding cytokines, can reverse the defect in generation of CD4 effector T cells from naive T cells of aged mice. J Exp Med 1999; 190: 1013-1024.
93. Lanzavecchia A, Sallusto F. Progressive differentiation and selection of the fittest in the immune response. Nat Rev Immunol 2002; 2: 982-987.
94. Swain SL, Croft M, Dubey C, Haynes L, Rogers P, Zhang X et al. From naive to memory T cells. Immunol Rev 1996; 150: 143-167.
95. Dubey C, Croft M, Swain SL. Naive and effector CD4Tcells differ in their requirements for T cell receptor versus costimulatory signals. J Immunol 1996; 157: 3280-3289.
96. McKinstry KK, Golech S, Lee WH, Huston G, Weng NP, Swain SL. Rapid default transition of CD4T cell effectors to functional memory cells. J Exp Med 2007; 204: 2199-2211.
97. Agrewala JN, Brown DM, Lepak NM, Duso D, Huston G, Swain SL. Unique ability of activated CD4+ T cells but not rested effectors to migrate to non-lymphoid sites in the absence of inflammation. J Biol Chem 2007; 282: 6106-6115.
98. Bradley LM, Duncan DD, Tonkonogy S, Swain SL. Characterization of antigen-specific CD4+ effector T cells in vivo: immunization results in a transient population of MEL-14-, CD45RB- helper cells that secretes interleukin 2 (IL-2), IL-3, IL-4, and interferon gamma. J Exp Med 1991; 174: 547-559.
99. Chackerian AA, Alt JM, Perera TV, Dascher CC, Behar SM. Dissemination of Mycobacterium tuberculosis is influenced by host factors and precedes the initiation of T-cell immunity. Infect Immun 2002; 70: 4501-4509.
100. Wolf AJ, Desvignes L, Linas B, Banaiee N, Tamura T, Takatsu K et al. Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J ExpMed 2008; 205: 105-115.
101. Itano AA, McSorley SJ, Reinhardt RL, Ehst BD, Ingulli E, Rudensky AY et al. Distinct dendritic cell populations sequentially present antigen to CD4T cells and stimulate different aspects of cell-mediated immunity. Immunity 2003; 19: 47-57.
102. Miller MJ, Hejazi AS, Wei SH, Cahalan MD, Parker I. T cell repertoire scanning is promoted by dynamic dendritic cell behavior and random T cell motility in the lymph node. Proc Natl Acad Sci USA 2004; 101: 998-1003.
103. 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.
104. Shakhar G, Lindquist RL, Skokos D, Dudziak D, Huang JH, Nussenzweig MC et al. Stable T cell-dendritic cell interactions precede the development of both tolerance and immunity in vivo. Nat Immunol 2005; 6: 707-714.
105. Henrickson SE, Mempel TR, Mazo IB, Liu B, Artyomov MN, Zheng H et al. T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation. Nat Immunol 2008; 9: 282-291.
106. Swain SL, Hu H, Huston G. Class II-independent generation of CD4 memory T cells from effectors. Science 1999; 286: 1381-1383.
107. 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.
108. 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.
109. Bradley LM, Haynes L, Swain SL. IL-7: maintaining T-cell memory and achieving homeostasis. Trends Immunol 2005; 26: 172-176.
110. Marrack P, Kappler J. Control of T cell viability. Annu Rev Immunol 2004; 22: 765-787.
111. Belz GT, Bedoui S, Kupresanin F, Carbone FR, Heath WR. Minimal activation of memory CD8+ T cell by tissue-derived dendritic cells favors the stimulation of naive CD8+ T cells. Nat Immunol 2007; 8: 1060-1066.
112. Zammit DJ, Turner DL, Klonowski KD, Lefrancois L, Cauley LS. Residual antigen presentation after influenza virus infection affects CD8T cell activation and migration. Immunity 2006; 24: 439-449.
113. Jelley-Gibbs DM, Dibble JP, Brown DM, Strutt TM, McKinstry KK, Swain SL. Persistent depots of influenza antigen fail to induce a cytotoxic CD8T cell response. J Immunol 2007; 178: 7563-7570.
114. Schiemann M, Busch V, Linkemann K, Huster KM, Busch DH. Differences in maintenance of CD8+ and CD4+ bacteria-specific effector-memory T cell populations. Eur J Immunol 2003; 33: 2875-2885.
115. 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.
116. Swain SL. Generation and in vivo persistence of polarized Th1 and Th2 memory cells. Immunity 1994; 1: 543-552.
117. 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.
118. Stockinger B, Kassiotis G, Bourgeois C. CD4 T-cell memory. Semin Immunol 2004; 16: 295-303.
119. Swain SL. Regulation of the generation and maintenance of T-cell memory: a direct, default pathway from effectors to memory cells. Microbes Infect 2003; 5: 213-219.
120. Carter LL, Zhang X, Dubey C, Rogers P, Tsui L, Swain SL. Regulation of T cell subsets from naive to memory. J Immunother 1998; 21: 181-187.
121. Carter LL, Swain SL. From naive to memory. Development and regulation of CD4+ T cell responses. Immunol Res 1998; 18: 1-13.
122. Croft M, Dubey C. Accessory molecule and costimulation requirements for CD4T cell response. Crit Rev Immunol 1997; 17: 89-118.
123. Rogers PR, Dubey C, Swain SL. Qualitative changes accompany memory T cell generation: faster, more effective responses at lower doses of antigen. J Immunol 2000; 164: 2338-2346.
124. Grayson JM, Harrington LE, Lanier JG, Wherry EJ, Ahmed R. Differential sensitivity of naive and memory CD8+ T cells to apoptosis in vivo. J Immunol 2002; 169: 3760-3770.
125. McKinstry KK, Strutt TM, Swain SL. The effector to memory transition of CD4T cells. Immunol Res 2008; 40: 114-127.
126. Harbertson J, Biederman E, Bennett KE, Kondrack RM, Bradley LM. Withdrawal of stimulation may initiate the transition of effector to memory CD4 cells. J Immunol 2002; 168: 1095-1102.
127. Bradley LM, Duncan DD, Yoshimoto K, Swain SL. Memory effectors: a potent, IL-4-secreting helper T cell population that develops in vivo after restimulation with antigen. J Immunol 1993; 150: 3119-3130.
128. Bradley LM, Atkins GG, Swain SL. Long-term CD4+ memory T cells from the spleen lack MEL-14, the lymph node homing receptor. J Immunol 1992; 148: 324-331.
129. 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.
130. Wu CY, Kirman JR, Rotte MJ, Davey DF, Perfetto SP, Rhee EG et al. Distinct lineages of T(H)1 cells have differential capacities for memory cell generation in vivo. Nat Immunol 2002; 3: 852-858.
131. de Bree GJ, van Leeuwen EM, Out TA, Jansen HM, Jonkers RE, van Lier RA. Selective accumulation of differentiated CD8+ T cells specific for respiratory viruses in the human lung. J Exp Med 2005; 202: 1433-1442.
132. Wang JP, Kurt-Jones EA, Finberg RW. Innate immunity to respiratory viruses. Cell Microbiol 2007; 9: 1641-1646.
133. Cerwenka A, Morgan TM, Harmsen AG, Dutton RW. Migration kinetics and final destination of type 1 and type 2 CD8 effector cells predict protection against pulmonary virus infection. J Exp Med 1999; 189: 423-434.
134. Kaech SM, Wherry EJ, Ahmed R. Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol 2002; 2: 251-262.
135. Wang X, Mosmann T. In vivo priming of CD4T cells that produce interleukin (IL)-2 but not IL-4 or interferon (IFN)-gamma, and can subsequently differentiate into IL-4- or IFN-gamma-secreting cells. J Exp Med 2001; 194: 1069-1080.
136. Lucas M, Day CL, Wyer JR, Cunliffe SL, Loughry A, McMichael AJ et al. Ex vivo phenotype and frequency of influenza virus-specific CD4 memory T cells. J Virol 2004; 78: 7284-7287.
137. 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.
138. Sallusto F, Mackay CR, Lanzavecchia A. The role of chemokine receptors in primary, effector, and memory immune responses. Annu Rev Immunol 2000; 18: 593-620.
139. Amyes E, McMichael AJ, Callan MF. Human CD4+ T cells are predominantly distributed among six phenotypically and functionally distinct subsets. J Immunol 2005; 175: 5765-5773.
140. Bingaman AW, Patke DS, Mane VR, Ahmadzadeh M, Ndejembi M, Bartlett ST et al. Novel phenotypes and migratory properties distinguish memory CD4T cell subsets in lymphoid and lung tissue. Eur J Immunol 2005; 35: 3173-3186.
141. Romero P, Zippelius A, Kurth I, Pittet MJ, Touvrey C, Iancu EM et al. Four functionally distinct populations of human effector - memory CD8+ T lymphocytes. J Immunol 2007; 178: 4112-4119.
142. Opferman JT, Ober BT, Ashton-Rickardt PG. Linear differentiation of cytotoxic effectors into memory T lymphocytes. Science 1999; 283: 1745-1748.
143. Löhning M, Hegazy AN, Pinschewer DD, Busse D, Lang KS, Höfer T et al. Long-lived virus-reactive memory T cells generated from purified cytokine-secreting T helper type 1 and type 2 effectors. J Exp Med 2008; 205: 53-61.
144. 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.
145. 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.
146. Badovinac VP, Porter BB, Harty JT. CD8+ T cell contraction is controlled by early inflammation. Nat Immunol 2004; 5: 809-817.
147. Kedzierska K, La Gruta NL, Turner SJ, Doherty PC. Establishment and recall of CD8+ T-cell memory in a model of localized transient infection. Immunol Rev 2006; 211: 133-145.
148. Kedzierska K, Stambas J, Jenkins MR, Keating R, Turner SJ, Doherty PC. Location rather than CD62L phenotype is critical in the early establishment of influenza-specific CD8+ T cell memory. Proc Natl Acad Sci USA 2007; 104: 9782-9787.
149. Moulton VR, Bushar ND, Leeser DB, Patke DS, Farber DL. Divergent generation of heterogeneous memory CD4T cells. J Immunol 2006; 177: 869-876.
150. Wherry EJ, Teichgräber V, Becker TC, Masopust D, Kaech SM, Antia R et al. Lineage relationship and protective immunity of memory CD8T cell subsets. Nat Immunol 2003; 4: 225-234.
151. Ahmadzadeh M, Hussain SF, Farber DL. Heterogeneity of the memory CD4T cell response: persisting effectors and resting memory T cells. J Immunol 2001; 166: 926-935.
152. 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.
153. Fazilleau N, Eisenbraun MD, Malherbe L, Ebright JN, Pogue-Caley RR, McHeyzer-Williams LJ et al. Lymphoid reservoirs of antigen-specific memory T helper cells. Nat Immunol 2007; 8: 753-761.
154. Kohlmeier JE, Miller SC, Woodland DL. Cutting edge: antigen is not required for the activation and maintenance of virus-specific memory CD8+ T cells in the lung airways. J Immunol 2007; 178: 4721-4725.
155. Topham DJ, Castrucci MR, Wingo FS, Belz GT, Doherty PC. The role of antigen in the localization of naive, acutely activated, and memory CD8(+) T cells to the lung during influenza pneumonia. J Immunol 2001; 167: 6983-6990.
156. Day EB, Zeng W, Doherty PC, Jackson DC, Kedzierska K, Turner SJ. The context of epitope presentation can influence functional quality of recalled influenza A virus-specific memory CD8+ T cells. J Immunol 2007; 179: 2187-2194.
157. Powell TJ, Strutt T, Reome J, Hollenbaugh JA, Roberts AD, Woodland DL et al. Priming with cold-adapted influenza A does not prevent infection but elicits long-lived protection against supralethal challenge with heterosubtypic virus. J Immunol 2007; 178: 1030-1038.
158. Thomas PG, Keating R, Hulse-Post DJ, Doherty PC. Cell-mediated protection in influenza infection. Emerg Infect Dis 2006; 12: 48-54.