Regulation of effector and memory T-cell functions by type I interferon

Immunology

Volumn 132, Issue 4, 2011, Pages 466-474

  Huber, Jonathan P ^a   David Farrar, J ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

CD4 CD8 T cells; Cytokine; Interferon; Memory

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CYTOKINE RELEASE; EFFECTOR CELL; HUMAN; MEMORY T LYMPHOCYTE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; REVIEW; TH17 CELL; TH2 CELL;

ANIMALS; DENDRITIC CELLS; HUMANS; IMMUNOLOGIC MEMORY; INTERFERON-ALPHA; INTERFERON-BETA; MICE; MODELS, IMMUNOLOGICAL; T-LYMPHOCYTES; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 79952515648     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2011.03412.x     Document Type: Review

References (104)

1. Isaacs A, Lindenmann J, Valentine RC. Virus interference. II. Some properties of interferon. Proc R Soc Lond B Biol Sci 1957; 147:268-73.
2. Isaacs A, Lindenmann J. Virus interference. I. The interferon. Proc R Soc Lond B Biol Sci 1957; 147:258-67.
3. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biochem 1998; 67:227-64.
4. Hardy MP, Owczarek CM, Jermiin LS, Ejdeback M, Hertzog PJ. Characterization of the type I interferon locus and identification of novel genes. Genomics 2004; 84:331-45.
5. Pestka S, Krause CD, Walter MR. Interferons, interferon-like cytokines, and their receptors. Immunol Rev 2004; 202:8-32.
6. Li X, Leung S, Kerr IM, Stark GR. Functional subdomains of STAT2 required for preassociation with the alpha interferon receptor and for signaling. Mol Cell Biol 1997; 17:2048-56.
7. Yan H, Krishnan K, Greenlund AC, Gupta S, Lim JT, Schreiber RD, Schindler CW, Krolewski JJ. Phosphorylated interferon-alpha receptor 1 subunit (IFNaR1) acts as a docking site for the latent form of the 113kDa STAT2 protein. EMBO J 1996; 15:1064-74.
8. Qureshi SA, Leung S, Kerr IM, Stark GR, Darnell JE Jr. Function of Stat2 protein in transcriptional activation by alpha interferon. Mol Cell Biol 1996; 16:288-93.
9. Doly J, Civas A, Navarro S, Uze G. Type I interferons: expression and signalization. Cell Mol Life Sci 1998; 54:1109-21.
10. De Maeyer E, De Maeyer-Guignard J. Type I interferons. Int Rev Immunol 1998; 17:53-73.
11. Naik SH, Sathe P, Park HY et al. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat Immunol 2007; 8:1217-26.
12. Liu YJ. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol 2005; 23:275-306.
13. Ito T, Amakawa R, Kaisho T et al. Interferon-alpha and interleukin-12 are induced differentially by Toll-like receptor 7 ligands in human blood dendritic cell subsets. J Exp Med 2002; 195:1507-12.
14. Iho S. Type I IFN synthesis in plasmacytoid dendritic cells. J Immunol 2003; 171:2767.
15. Cella M, Facchetti F, Lanzavecchia A, Colonna M. Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent TH1 polarization. Nat Immunol 2000; 1:305-10.
16. Krug A, Veeraswamy R, Pekosz A, Kanagawa O, Unanue ER, Colonna M, Cella M. Interferon-producing cells fail to induce proliferation of naive T cells but can promote expansion and T helper 1 differentiation of antigen-experienced unpolarized T cells. J Exp Med 2003; 197:899-906.
17. + T cells through IL-12 produced by Listeria-induced macrophages. Science 1993; 260:547-9.
18. + T cells from alpha beta TCR transgenic mice: IL-12 substitution for macrophages to stimulate IFN-gamma production is IFN-gamma-dependent. Int Immunol 1993; 5:1119-28.
19. + T cells. J Immunol 1995; 154:5071-9.
20. Bacon CM, McVicar DW, Ortaldo JR, Rees RC, O'Shea JJ, Johnston JA. Interleukin 12 (IL-12) induces tyrosine phosphorylation of JAK2 and TYK2: differential use of Janus family tyrosine kinases by IL-2 and IL-12. J Exp Med 1995; 181:399-404.
21. Bacon CM, Petricoin EF 3rd, Ortaldo JR, Rees RC, Larner AC, Johnston JA, O'Shea JJ. Interleukin 12 induces tyrosine phosphorylation and activation of STAT4 in human lymphocytes. Proc Natl Acad Sci U S A 1995; 92:7307-11.
22. Jacobson NG, Szabo SJ, Weber-Nordt RM, Zhong Z, Schreiber RD, Darnell JE Jr, Murphy KM. Interleukin 12 signaling in T helper type 1 (Th1) cells involves tyrosine phosphorylation of signal transducer and activator of transcription (Stat)3 and Stat4. J Exp Med 1995; 181:1755-62.
23. Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, Glimcher LH. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 2000; 100:655-69.
24. Szabo SJ, Sullivan BM, Stemmann C, Satoskar AR, Sleckman BP, Glimcher LH. Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 2002; 295:338-42.
25. + T cells. J Immunol 2009; 183:7743-51.
26. Ramos HJ, Davis AM, George TC, Farrar JD. IFN-alpha is not sufficient to drive Th1 development due to lack of stable T-bet expression. J Immunol 2007; 179:3792-803.
27. Thieu VT, Yu Q, Chang HC, Yeh N, Nguyen ET, Sehra S, Kaplan MH. Signal transducer and activator of transcription 4 is required for the transcription factor T-bet to promote T helper 1 cell-fate determination. Immunity 2008; 29:679-90.
28. Szabo SJ, Dighe AS, Gubler U, Murphy KM. Regulation of the interleukin (IL)-12R beta 2 subunit expression in developing T helper 1 (Th1) and Th2 cells. J Exp Med 1997; 185:817-24.
29. + T cells. Nat Immunol 2002; 3:549-57.
30. Cho SS, Bacon CM, Sudarshan C, Rees RC, Finbloom D, Pine R, O'Shea JJ. Activation of STAT4 by IL-12 and IFN-alpha: evidence for the involvement of ligand-induced tyrosine and serine phosphorylation. J Immunol 1996; 157:4781-9.
31. Rogge L, D'Ambrosio D, Biffi M, Penna G, Minetti LJ, Presky DH, Adorini L, Sinigaglia F. The role of Stat4 in species-specific regulation of Th cell development by type I IFNs. J Immunol 1998; 161:6567-74.
32. Farrar JD, Smith JD, Murphy TL, Murphy KM. Recruitment of Stat4 to the human interferon-alpha/beta receptor requires activated Stat2. J Biol Chem 2000; 275:2693-7.
33. Berenson LS, Farrar JD, Murphy TL, Murphy KM. Frontline: absence of functional STAT4 activation despite detectable tyrosine phosphorylation induced by murine IFN-alpha. Eur J Immunol 2004; 34:2365-74.
34. Farrar JD, Smith JD, Murphy TL, Leung S, Stark GR, Murphy KM. Selective loss of type I interferon-induced STAT4 activation caused by a minisatellite insertion in mouse Stat2. Nat Immunol 2000; 1:65-9.
35. Farrar JD, Murphy KM. Type I interferons and T helper development. Immunol Today 2000; 21:484-9.
36. + T cells expressing a chimeric murine/human Stat2 gene. J Immunol 2005; 174:294-301.
37. Ota N, Brett TJ, Murphy TL, Fremont DH, Murphy KM. N-domain-dependent nonphosphorylated STAT4 dimers required for cytokine-driven activation. Nat Immunol 2004; 5:208-15.
38. Murphy TL, Geissal ED, Farrar JD, Murphy KM. Role of the Stat4 N domain in receptor proximal tyrosine phosphorylation. Mol Cell Biol 2000; 20:7121-31.
39. Tyler DR, Persky ME, Matthews LA, Chan S, Farrar JD. Pre-assembly of STAT4 with the human IFN-alpha/beta receptor-2 subunit is mediated by the STAT4 N-domain. Mol Immunol 2007; 44:1864-72.
40. Athie-Morales V, Smits HH, Cantrell DA, Hilkens CM. Sustained IL-12 signaling is required for Th1 development. J Immunol 2004; 172:61-9.
41. Berenson LS, Gavrieli M, Farrar JD, Murphy TL, Murphy KM. Distinct characteristics of murine STAT4 activation in response to IL-12 and IFN-{alpha}. J Immunol 2006; 177:5195-203.
42. + T cells via a cytokine relay network. J Immunol 2008; 180:6923-32.
43. Havenar-Daughton C, Kolumam GA, Murali-Krishna K. Cutting edge: the direct action of type I IFN on CD4 T cells is critical for sustaining clonal expansion in response to a viral but not a bacterial infection. J Immunol 2006; 176:3315-9.
44. Way SS, Havenar-Daughton C, Kolumam GA, Orgun NN, Murali-Krishna K. IL-12 and type-I IFN synergize for IFN-gamma production by CD4 T cells, whereas neither are required for IFN-gamma production by CD8 T cells after Listeria monocytogenes infection. J Immunol 2007; 178:4498-505.
45. Schijns VE, Haagmans BL, Wierda CM, Kruithof B, Heijnen IA, Alber G, Horzinek MC. Mice lacking IL-12 develop polarized Th1 cells during viral infection. J Immunol 1998; 160:3958-64.
46. Sareneva T, Julkunen I, Matikainen S. IFN-alpha and IL-12 induce IL-18 receptor gene expression in human NK and T cells. J Immunol 2000; 165:1933-8.
47. Matikainen S, Paananen A, Miettinen M, Kurimoto M, Timonen T, Julkunen I, Sareneva T. IFN-alpha and IL-18 synergistically enhance IFN-gamma production in human NK cells: differential regulation of Stat4 activation and IFN-gamma gene expression by IFN-alpha and IL-12. Eur J Immunol 2001; 31:2236-45.
48. Strengell M, Julkunen I, Matikainen S. IFN-alpha regulates IL-21 and IL-21R expression in human NK and T cells. J Leukoc Biol 2004; 76:416-22.
49. Strengell M, Matikainen S, Siren J, Lehtonen A, Foster D, Julkunen I, Sareneva T. IL-21 in synergy with IL-15 or IL-18 enhances IFN-gamma production in human NK and T cells. J Immunol 2003; 170:5464-9.
50. Strengell M, Sareneva T, Foster D, Julkunen I, Matikainen S. IL-21 up-regulates the expression of genes associated with innate immunity and Th1 response. J Immunol 2002; 169:3600-5.
51. Marrack P, Kappler J, Mitchell T. Type I interferons keep activated T cells alive. J Exp Med 1999; 189:521-30.
52. 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; 401:708-12.
53. + central memory T cells. J Immunol 2008; 181:8204-8.
54. Ziegler SF. The role of thymic stromal lymphopoietin (TSLP) in allergic disorders. Curr Opin Immunol 2010; 22:795-9.
55. Paul WE, Zhu J. How are T(H)2-type immune responses initiated and amplified? Nat Rev Immunol 2010; 10:225-35.
56. Murphy KM, Ouyang W, Farrar JD, Yang J, Ranganath S, Asnagli H, Afkarian M, Murphy TL. Signaling and transcription in T helper development. Annu Rev Immunol 2000; 18:451-94.
57. Ouyang W, Ranganath SH, Weindel K, Bhattacharya D, Murphy TL, Sha WC, Murphy KM. Inhibition of Th1 development mediated by GATA-3 through an IL-4-independent mechanism. Immunity 1998; 9:745-55.
58. + cell subset with combined Th2 and Th1 cell functions. Immunity 2010; 32:116-28.
59. Ouyang W, Lohning M, Gao Z, Assenmacher M, Ranganath S, Radbruch A, Murphy KM. Stat6-independent GATA-3 autoactivation directs IL-4-independent Th2 development and commitment. Immunity 2000; 12:27-37.
60. Farrar JD, Ouyang W, Lohning M, Assenmacher M, Radbruch A, Kanagawa O, Murphy KM. An instructive component in T helper cell type 2 (Th2) development mediated by GATA-3. J Exp Med 2001; 193:643-50.
61. Zielinski RM, Lawrence WD. Interferon-alpha for the hypereosinophilic syndrome. Ann Intern Med 1990; 113:716-8.
62. + T cells. J Clin Invest 1996; 97:309-15.
63. Huber JP, Ramos HJ, Gill MA, Farrar JD. Cutting edge: type I IFN reverses human Th2 commitment and stability by suppressing GATA3. J Immunol 2010; 185:813-7.
64. Dai J, Megjugorac NJ, Gallagher GE, Yu RY, Gallagher G. IFN-lambda1 (IL-29) inhibits GATA3 expression and suppresses Th2 responses in human naive and memory T cells. Blood 2009; 113:5829-38.
65. Dumoutier L, Tounsi A, Michiels T, Sommereyns C, Kotenko SV, Renauld JC. Role of the interleukin (IL)-28 receptor tyrosine residues for antiviral and antiproliferative activity of IL-29/interferon-lambda 1: similarities with type I interferon signaling. J Biol Chem 2004; 279:32269-74.
66. Ciprandi G, De Amici M, Murdaca G, Fenoglio D, Ricciardolo F, Marseglia G, Tosca M. Serum interleukin-17 levels are related to clinical severity in allergic rhinitis. Allergy 2009; 64:1375-8.
67. + T helper cells. Cell 2006; 126:1121-33.
68. Lee YK, Mukasa R, Hatton RD, Weaver CT. Developmental plasticity of Th17 and Treg cells. Curr Opin Immunol 2009; 21:274-80.
69. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005; 6:1123-32.
70. Moschen AR, Geiger S, Krehan I, Kaser A, Tilg H. Interferon-alpha controls IL-17 expression in vitro and in vivo. Immunobiology 2008; 213:779-87.
71. Bennett JL, Stuve O. Update on inflammation, neurodegeneration, and immunoregulation in multiple sclerosis: therapeutic implications. Clin Neuropharmacol 2009; 32:121-32.
72. + T cells in MS. Eur J Immunol 2009; 39:2525-36.
73. Tversky JR, Le TV, Bieneman AP, Chichester KL, Hamilton RG, Schroeder JT. Human blood dendritic cells from allergic subjects have impaired capacity to produce interferon-alpha via Toll-like receptor 9. Clin Exp Allergy 2008; 38:781-8.
74. Bufe A, Gehlhar K, Grage-Griebenow E, Ernst M. Atopic phenotype in children is associated with decreased virus-induced interferon-alpha release. Int Arch Allergy Immunol 2002; 127:82-8.
75. Gehlhar K, Bilitewski C, Reinitz-Rademacher K, Rohde G, Bufe A. Impaired virus-induced interferon-alpha2 release in adult asthmatic patients. Clin Exp Allergy 2006; 36:331-7.
76. Gill MA, Bajwa G, George TA, Dong CC, Dougherty II, Jiang N, Gan VN, Gruchalla RS. Counterregulation between the FcepsilonRI pathway and antiviral responses in human plasmacytoid dendritic cells. J Immunol 2010; 184:5999-6006.
77. Schroeder JT, Bieneman AP, Xiao H, Chichester KL, Vasagar K, Saini S, Liu MC. TLR9- and FcepsilonRI-mediated responses oppose one another in plasmacytoid dendritic cells by down-regulating receptor expression. J Immunol 2005; 175:5724-31.
78. Ozaki K, Spolski R, Feng CG et al. A critical role for IL-21 in regulating immunoglobulin production. Science 2002; 298:1630-4.
79. Shang XZ, Ma KY, Radewonuk J, Li J, Song XY, Griswold DE, Emmell E, Li L. IgE isotype switch and IgE production are enhanced in IL-21-deficient but not IFN-gamma-deficient mice in a Th2-biased response. Cell Immunol 2006; 241:66-74.
80. Hiromura Y, Kishida T, Nakano H, Hama T, Imanishi J, Hisa Y, Mazda O. IL-21 administration into the nostril alleviates murine allergic rhinitis. J Immunol 2007; 179:7157-65.
81. Finkelman FD, Svetic A, Gresser I, Snapper C, Holmes J, Trotta PP, Katona IM, Gause WC. Regulation by interferon alpha of immunoglobulin isotype selection and lymphokine production in mice. J Exp Med 1991; 174:1179-88.
82. Pene J, Rousset F, Briere F et al. IgE production by normal human lymphocytes is induced by interleukin 4 and suppressed by interferons gamma and alpha and prostaglandin E2. Proc Natl Acad Sci U S A 1988; 85:6880-4.
83. + T cells. J Exp Med 1999; 189:1355-60.
84. 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; 171:5165-71.
85. Curtsinger JM, Lins DC, Mescher MF. Signal 3 determines tolerance versus full activation of naive CD8 T cells: dissociating proliferation and development of effector function. J Exp Med 2003; 197:1141-51.
86. Curtsinger JM, Valenzuela JO, Agarwal P, Lins D, Mescher MF. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J Immunol 2005; 174:4465-9.
87. + T cells. Immunol Rev 2006; 211:81-92.
88. + T cells. J Immunol 2003; 170:5018-26.
89. Mattei F, Schiavoni G, Belardelli F, Tough DF. IL-15 is expressed by dendritic cells in response to type I IFN, double-stranded RNA, or lipopolysaccharide and promotes dendritic cell activation. J Immunol 2001; 167:1179-87.
90. + T cell turnover in vivo by IL-12, IL-18, and IFN-gamma. J Immunol 2001; 166:6007-11.
91. + T cells stimulated by virus-induced type I interferon. Nat Immunol 2003; 4:1009-15.
92. + T cell response during cross-priming. J Immunol 2006; 176:4682-9.
93. Sun S, Zhang X, Tough DF, Sprent J. Type I interferon-mediated stimulation of T cells by CpG DNA. J Exp Med 1998; 188:2335-42.
94. Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med 2005; 202:637-50.
95. + T-cell immunity is unaffected by the absence of type I interferon signaling. Infect Immun 2010; 78:3154-9.
96. Pearce EL, Shen H. Generation of CD8 T cell memory is regulated by IL-12. J Immunol 2007; 179:2074-81.
97. + T cell fate coupled by T-bet and eomesodermin. Nat Immunol 2005; 6:1236-44.
98. + T cell differentiation. J Immunol 2006; 177:7515-9.
99. Cui W, Joshi NS, Jiang A, Kaech SM. Effects of signal 3 during CD8 T cell priming: bystander production of IL-12 enhances effector T cell expansion but promotes terminal differentiation. Vaccine 2009; 27:2177-87.
100. + T cell fates via the graded expression of T-bet transcription factor. Immunity 2007; 27:281-95.
101. Xiao Z, Casey KA, Jameson SC, Curtsinger JM, Mescher MF. Programming for CD8 T cell memory development requires IL-12 or type I IFN. J Immunol 2009; 182:2786-94.
102. + effector versus central memory T-cell fates. Blood 2009; 113:5516-25.
103. + T cells. Eur J Immunol 2010; 40:3389-402.
104. + T cells in the lung airways during respiratory virus challenge. Immunity 2010; 33:96-105.