Immunoregulatory effects of interferon-β in suppression of Th17 cells

Journal of Interferon and Cytokine Research

Volumn 34, Issue 5, 2014, Pages 330-341

  Pennell, Leesa M ^a,b   Fish, Eleanor N ^a,b  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CD28 ANTIGEN; CD3 ANTIBODY; CD3 ANTIGEN; CELL SURFACE RECEPTOR; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CXCR4; INTERFERON REGULATORY FACTOR 4; INTERLEUKIN 17; INTERLEUKIN 23 RECEPTOR; INTERLEUKIN 6 RECEPTOR; PROTEIN KINASE ZAP 70; T LYMPHOCYTE RECEPTOR; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; GENE EXPRESSION PROFILING; IMMUNOREGULATION; LYMPH NODE; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SPLEEN CELL; T LYMPHOCYTE ACTIVATION; TH17 CELL; ANIMAL; CYTOLOGY; DEFICIENCY; IMMUNOLOGY;

ANIMALS; INTERFERON-BETA; MICE; PHENOTYPE; TH17 CELLS;

EID: 84900328459     PISSN: 10799907     EISSN: 15577465     Source Type: Journal    
DOI: 10.1089/jir.2013.0088     Document Type: Article

References (64)

1. Au-Yeung BB, Deindl S, Hsu LY, Palacios EH, Levin SE, Kuriyan J, Weiss A. 2009. The structure, regulation, and function of ZAP-70. Immunol Rev 228(1):41-57.
2. Axtell RC, de Jong BA, Boniface K, van der Voort LF, Bhat R, De Sarno P, Naves R, Han M, Zhong F, Castellanos JG, Mair R, Christakos A, Kolkowitz I, Katz L, Killestein J, Polman CH, de Waal Malefyt R, Steinman L, Raman C. 2010. T helper type 1 and 17 cells determine efficacy of interferon-beta in multiple sclerosis and experimental encephalomyelitis. Nat Med 16(4):406-412.
3. Bettelli E, Carrier Y, Gao W, Korn T, Storm TB, Oukka M, Weiner HL, Kuchroo VK. 2006. Reciprocal developmental pathways for the generation of pathogenic effector Th17 and regulatory T cells. Nature 441(7090):235-238.
4. Borden EC, Sen GC, Uze G, Silverman RH, Ransohoff RM, Foster GR, Stark GR. 2007. Interferons at age 50: current and future impact on biomedicine. Nat Rev Drug Disc 6:975-990.
5. Brustle A, Heink S, Huber M, Rosenplanter C, Stadelmann C, Yu P, Arpaia E, Mak TW, Kamradt T, Lohoff M. 2007. The development of inflammatory T(H)-17 cells requires interferon regulatory factor 4. Nat Immunol 8(9):958-996.
6. Chen M, Chen G, Deng S, Liu X, Hutton GJ, Hong J. 2012. IFN-b induces the proliferation of CD4 + CD25 + FoxP3 + regulatory T cells through upregulation of GITRL on dendritic cells in the treatment of multiple sclerosis. J Neuroimmunol 242(1-2): 39-46.
7. Chen M, Chen G, Nie H, Zhang X, Niu X, Zang YCQ, Skinner SM, Zhang JZ, Killian JM, Hong J. 2009. Regulatory effects of IFN-b on production of osteopontin and IL-17 by CD4+ T cells in MS. Eur J Immunol 39(9):2525-2536.
8. Chen Z, Laurence A, Kanno Y, Pacher-Zavisin M, Zhu BM, Tato C, Yoshimura A, Hennighausen L, O'Shea JJ. 2006. Selective regulatory function of Socs3 in the formation of IL-17-secreting T cells. Proc Natl Acad Sci USA 103(21):8137-8142.
9. Codarri L, Gyü lvészi G, Tosevski V, Hesske L, Fontana A, Magenant L, Suter T, Becher B. 2011. RORgt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat Immunol 12(6):560-567.
10. Deonarain R, Verma A, Porter AC, Gewert DR, Platanias LC, Fish EN. 2003. Critical roles for IFN-beta in lymphoid development, myelopoiesis, and tumor development: links to tumor necrosis factor alpha. Proc Natl Acad Sci USA 100(23):13453-13458.
11. De Weerd SJ, Samarajiwa SA, Hertzog PJ. 2007. Type I interferon receptors:biochemistry and biological functions. J Biol Chem 282(28):20053-20057.
12. Dikopoulos N, Bertoletti A, Kroger A, Hauser H, Schirmbeck R, Reimann J. 2005. Type I IFN negatively regulates CD8 + T cell responses through IL-10-producing CD4+ T regulatory 1 cells. J Immunol 174(1):99-109.
13. El-Behi M, Ciric B, Dai H, Yan Y, Cullimore M, Safavi F, Zhang G, Dittel BN, Rostami A. 2011. The encephalogenicity of T(H)17 cells is dependent on IL-1 and IL-23-induced production of the cytokine GM-CSF. Nat Immunol 12(6):568-575.
14. Esendagli G, Kurne AT, Sayat G, Kilic AK, Guc D, Karabudak R. 2013. Evaluation of Th17-related cytokines and receptors in multiple sclerosis patients under interferon b-1 therapy. J Neuroimmunol 255(1-2):81-84.
15. Essers MAG, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, Trumpp A. 2009. IFNalpha activates dormant haemoatopoietic stem cells in vivo. Nature 458(7240):904-908.
16. Fenner JE, Starr R, Cornish AL, Zhang JG, Metcalf D, Schreiber RD, Sheehan K, Hilton DJ, Alexander WS, Hertzog PJ. 2006. Suppressor of cytokine signaling 1 regulates the immune response to infection by a unique inhibition of type I interferon receptor activity. Nat Immunol 7(1):33-39.
17. Fitzgerald DC, Fonseca-Kelly Z, Cullimore ML, Safabakhsh P, Saris CJM, Zhang G-X, Rostami A. 2013. Independent and interdependent immunoregulatory effects of IL-27, IFN-b, and IL-10 in the suppression of human Th17 cells and murine experimental autoimmune encephalomyelitis. J Immunol 190(7):3225-3234.
18. Fleetwood AJ, Dinh H, Cook AD, Hertzog PJ, Hamilton JA. 2009. GM-CSF and M-CSF-dependent macrophage phenotypes display differential dependence on type I interferon signaling. J Leukoc Biol 86(2):411-421.
19. Galligan CL, Pennell LM, Murooka TT, Baig E, Majchrzak-Kita B, Rahbar R, Fish EN. 2010. Interferon-b is a key regu;ator of pro-inflammatory events in experimental autoimmune encephalomyelitis. Mult Scler 16(12):1458-1473.
20. Garcin G, Bordat Y, Chuchana P, Monneron D, LawHKW, Piehler J, Uzé G. 2013. Differential activity of type I interferon subtypes for dendritic cell differentiation. PLoS One 8(3):e58465.
21. Gonzalez-Navajas JM, Lee J, David M, Raz E. 2012. Immunomodulatory functions of type I interferons. Nat Rev Immunol 12(2):125-135.
22. Gough DJ, Messina NL, Clarke CJP, Johnstone RW, Levy DE. 2012. Constitutive type I interferon modulates homeostatic balance through tonic signaling. Immunity 36(2):166-174.
23. Gough DJ, Messina NL, Hii L, Gould JA, Sabapathy K, Robertson APS, Trapani JA, Levy DE, Hertzog PJ, Clarke CJP, Johnstone RW. 2010. Functional crosstalk between type I and II interferon through the regulated expression of STAT1. PLoS Biol 8(4):e1000361.
24. Graeler M, Shankar G, Goetzl EJ. 2002. Suppression of T cell chemotaxis by sphingosine 1-phosphate. J Immunol 169(8):4084-4087.
25. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT. 2005. Interleukin 17-producing CD4 + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6(11):1123-1132.
26. Huber JP, Ramos HJ, Gill MA, Farrar JD. 2010. Type I IFN reverses human Th2 commitment and stability by suppressing GATA3. J Immunol 185(2):8134-8817.
27. Huber M, Brustle A, Reinhard K, Guralnik A, Walter G, Mahiny A, von Low E, Lohoff M. 2008. IRF4 is essential for IL-21- mediated induction, amplification, and stabilization of the Th17 phenotype. Proc Natl Acad Sci USA 105(52):20846-20851.
28. Hwang SY, Hertzog PJ, Holland KA, Sumarsono SH, Tymms MJ, Hamilton JA, Whitty G, Bertoncello I, Kola I. 1995. A null mutation in the gene encoding a type I interferon receptor component eliminates antiproliferative and antiviral responses to interferons alpha and beat and alters macrophage responses. Proc Natl Acad Sci USA 92(24):11284-11288.
29. Isaacs A, Lindenmann J. 1957. Virus interference. I. The interferon. Proc R Soc Lond B Biol Sci 147:258-267.
30. Kebir H, Ifergan I, Alvarez JI, Bernard M, Poirier J, Arbour N, Duquette P, Prat A. 2009. Preferential recruitment of interferon- gamma-expressing TH17 cells in multiple sclerosis. Ann Neurol 66(3):390-402.
31. Kurtuncu M, Tuzun E, Turkoglu R, Petek-Balci B, Icoz S, Pehlivan M, Birisik O, Ulusoy C, Shugaiv E, Akman-Demir G, Eraksoy M. 2012. Effect of short term interferon-b treatment on cytokines in multiple sclerosis: Significant modulation of IL-17 and IL-23. Cytokine 59(2):400-402.
32. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, McClanahan T, Kastelein RA, Cua DJ. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 21(2):233-240.
33. Laurence A, Tato CM, Davidson TS, Kanno Y, Chen Z, Yao Z, Blank RB, Meylan F, Siegel R, Hennighausen L, Shevach EM, O'Shea JJ. 2007. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26(3):371-381.
34. Lohoff M, Mittrucker HW, Brustle A, Sommer F, Casper B, Huber M, Ferrick DA, Duncan GS, Mak TW. 2004. Enhanced TCR-induced apoptosis in interferon regulatory 4-deficient CD4( + ) Th cells. J Exp Med 200(2):247-253.
35. Mack EA, Kallal LE, Demers DA, Biron CA. 2011. Type 1 interferon induction of natural killer cell gamma interferon production for defense during lymphocytic choriomeningitis virus infection. MBio 2(4):e00169-e11.
36. McCandless EE, Piccio L, Woerner BM, Schmidt RE, Rubin JB, Cross AH, Klein RS. 2008. Pathological exptression of CXCL12 at the blood-brain barrier correlates with severity of multiple sclerosis. Am J Pathol 172(3):799-808.
37. MehlingM, Lindberg R, Raulf F, Kuhle J, Hess C, Kappos L, Brinkmann V. 2010. Th17 centralmemory T cells are reduced by FTY720 in patients with multiple sclerosis. Neurology 75(5):403-410.
38. Miyagi T, Pilar Gil M, Wang X, Louten J, Chu W, Biron CA. 2007. High basal STAT4 balanced by STAT1 induction to control type 1 interferon effects in natural killer cells. J Exp Med 204(10):2383-2396.
39. Montoya M, Schiavoni G, Mattei F, Gresser I, Belardelli F, Borrow P, Tough DF. 2002. Type I interferons produced by dendritic cells promote their phenotypic and functional activation. Blood 99(9):3263-3271.
40. Moschen AR, Geiger S, Krehan I, Kaser A, Tilg H. 2008. Interferon- alpha controls IL-17 expression in vitro and in vivo. Immunobiol 213(9-10):779-787.
41. Mossmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. 1986. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 136(7):2348-2357.
42. Muller U, Steinhoff U, Reis LF, Hemmi S, Pavlovic J, Zinkernagel RM, Aguet M. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264(5167):1918-1921.
43. Mus AMC, Cornelissen F, Asmawidjaja PS, van Hamburg JP, Boon L, Hendricks RW, Lubberts E. 2010. Interleukin-23 promotoes Th17 differentiation by inhibiting T-bet and FoxP3 and is required for elevation of interleukin-22, but not interleukin- 21, in autoimmune experimental arthritis. Arthritis Rheum 62(4):1043-1050.
44. Ng D, Gommerman JL. 2013. The regulation of immune responses by DC derived Type I IFN. Front Immunol 4:1-8.
45. Nguyen KB, Salazar-Mather TP, Dalod MY, Van Deusen JB, Wei X, Liew FY, Caligiuri MA, Durbin JE, Biron CA. 2002. Coordinated and distinct roles for IFN-alpha beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J Immunol 169(8):4279-4287.
46. Nishihara M, Ogura H, Ueda N, Tsuruoka M, Kitabayashi C, Tsuji F, Aono H, Ishihara K, Huseby E, Betz UAK, Murakami M, Hirano T. 2007. IL-6-gp130-STAT3 in T cells directs the development of IL-17 + Th with a minimum effect on that of Treg in the steady state. Int Immunol 19(6):695-702.
47. Ouyang W, Kolls JK, Zheng Y. 2008. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28(4):454-467.
48. Paul WE, Zhu J. 2010. How are T(H)2-type immune responses initiated and amplified? Nat Rev Immunol 10(4):225-235.
49. Ramgolam VS, Sha Y, Jin J, Zhang X, Markovic-Plese S. 2009. IFN-b inhibits human Th17 cell differentiation. J Immunol 183(8):5418-5427.
50. Rivera J, Proia RL, Olivera A. 2008. The alliance of sphingosine- 1-phosphate and its receptors in immunity. Nat Rev Imm 8(10):753-763.
51. Rogge L, D'Ambrosio D, Biff M, Penna G, Minetti LJ, Presky DH, Adorini L, Sinigaglia F. 1998. The role of Stat4 in speciesspecific regul;ation of Th cell development by type I IFNs. J Immunol 161(12):6567-6574.
52. Sallusto F, Impellizzieri D, Basso C, Laroni A, Uccelli A, Lanzavecchia A, Engelhardt B. 2012. T-cell trafficking in the central nervous system. Immunol Rev 248(1):216-277.
53. Shiow LR, Rosen DB, Brdickova N, Xu Y, An J, Lanier LL, Cyster JG, Matloubian M. 2006. CD69 acts downstream of interferonalpha/ beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440(7083):540-544.
54. Singh SP, Zhang HH, Foley JF, Hedrick MN, Farber JM. 2008. Human T cells that are able to produce IL-17 express the chemokine receptor CCR6. J Immunol 180(1):214-221.
55. Swann JB, Hayakawa Y, Zerafa N, Sheehan KCF, Scott B, Schreiber RD, Hertzog P, Smyth MJ. 2007. Type I IFN contributes to NK cell homeostasis, activation, and antitumor function. J Immunol 178(12):7540-7549.
56. Thomas KE, Galligan CL, Deonarain Newman R, Fish EN, Vogel SN. 2006. Contribution of interferon-beta to the murine macrophage response to the toll-like receptor 4 agonist, lipopolysaccharide. J Biol Chem 281(41):31119-31130.
57. Trifari S, Kaplan CD, Tran EH, Crellin NK, Spits H. 2009. Identification of a human T helper cell population that as abundant production of interleukin 22 and is distinct from T(H)-17, T(H)1 and T(H)2 cells. Nat Immunol 10(8):864-871.
58. Tzartos JS, Friese MA, Craner MJ, Palace J, Newcombe J, Esiri MM, Fugger L. 2008. Interleukin17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am J Pathol 172(1):146-155.
59. Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. 2006. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24(2):179-189.
60. Veldhoen M, Uyttenhove C, van Snick J, Helmby H, Westendorf A, Buer J, Martin B, Wilhelm C, Stockinger B. 2008. Transforming growth factor-beta 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin-9-producing subset. Nat Immunol 9(12):1341-1346.
61. Wang BX, Fish EN. 2012. The yin and yang of viruses and interferons. Trends Immunol 33(4):190-197.
62. Yamazaki T, Yang XO, Chung Y, Fukunaga A, Nurieva R, Pappu B, Martin-Orozco N, Kang HS, Ma L, Panopoulos AS, Craig S, Watowich SS, Jetten AM, Tian Q, Dong C. 2008. J Immunol 181(12):8391-8401.
63. Yoo JK, Baker DP, Fish EN. 2010. Interferon-b modulates type 1 immunity during influenza virus infection. Antiviral Res 88(1):64-71.
64. Zhang L, Yuan S, Cheng G, Guo B. 2011. Type I IFN promotes IL-10 production from T cells to suppress Th17 cells and Th17- associated autoimmune inflammation. PLoS One 6(12):e28432.