IL-27R-mediated regulation of IL-17 controls the development of respiratory syncytial virus-associated pathogenesis

American Journal of Pathology

Volumn 184, Issue 6, 2014, Pages 1807-1818

  De Almeida Nagata, Denise E ^a   Demoor, Tine ^a   Ptaschinski, Catherine ^a   Ting, Hung An ^a   Jang, Sihyug ^a   Reed, Michelle ^a   Mukherjee, Sumanta ^a   Lukacs, Nicholas W ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EBI 3 PROTEIN; GAMMA INTERFERON; IMIQUIMOD; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 27; INTERLEUKIN 27 RECEPTOR; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN RECEPTOR; MUCIN 5AC; PROTEIN; PROTEIN P28; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; CHLORIDE CHANNEL; CLCA3 PROTEIN, MOUSE; CYTOKINE RECEPTOR; EBI3 PROTEIN, MOUSE; IL27 PROTEIN, MOUSE; IL27RA PROTEIN, MOUSE; INTERLEUKIN DERIVATIVE; MUC5AC PROTEIN, MOUSE; MUCOPROTEIN; STAT1 PROTEIN; STAT1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EOSINOPHIL; FLOW CYTOMETRY; GENE EXPRESSION; GOBLET CELL HYPERPLASIA; GOBLET CELL METAPLASIA; HYPERPLASIA; LUNG; LUNG HOMOGENATE; LUNG LAVAGE; LYMPH NODE; MACROPHAGE; METAPLASIA; MOUSE; MUCUS SECRETION; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RESPIRATORY SYNCYTIAL VIRUS INFECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TH1 CELL; TH17 CELL; TH2 CELL; UPREGULATION; VIROGENESIS; ANIMAL; GENETICS; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOLOGY; KNOCKOUT MOUSE; MUCUS; PATHOLOGY;

ANIMALS; CHLORIDE CHANNELS; INTERLEUKIN-17; INTERLEUKINS; MICE; MICE, KNOCKOUT; MUCIN 5AC; MUCOPROTEINS; MUCUS; RECEPTORS, CYTOKINE; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; STAT1 TRANSCRIPTION FACTOR; TH17 CELLS; TH2 CELLS;

EID: 84901049525     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2014.02.004     Document Type: Article

References (58)

1. S. Pflanz, J.C. Timans, J. Cheung, R. Rosales, H. Kanzler, J. Gilbert, L. Hibbert, T. Churakova, M. Travis, E. Vaisberg, W.M. Blumenschein, J.D. Mattson, J.L. Wagner, W. To, S. Zurawski, T.K. McClanahan, D.M. Gorman, J.F. Bazan, R. de Waal Malefyt, D. Rennick, and R.A. Kastelein IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells Immunity 16 2002 779 790
2. L. Hibbert, S. Pflanz, R. De Waal Malefyt, and R.A. Kastelein IL-27 and IFN-alpha signal via Stat1 and Stat3 and induce T-Bet and IL-12Rbeta2 in naive T cells J Interferon Cytokine Res 23 2003 513 522
3. S. Pflanz, L. Hibbert, J. Mattson, R. Rosales, E. Vaisberg, J.F. Bazan, J.H. Phillips, T.K. McClanahan, R. de Waal Malefyt, and R.A. Kastelein WSX-1 and glycoprotein 130 constitute a signal-transducing receptor for IL-27 J Immunol 172 2004 2225 2231
4. S. Lucas, N. Ghilardi, J. Li, and F.J. de Sauvage IL-27 regulates IL-12 responsiveness of naive CD4+ T cells through Stat1-dependent and -independent mechanisms Proc Natl Acad Sci U S A 100 2003 15047 15052
5. A. Takeda, S. Hamano, A. Yamanaka, T. Hanada, T. Ishibashi, T.W. Mak, A. Yoshimura, and H. Yoshida Cutting edge: role of IL-27/WSX-1 signaling for induction of T-bet through activation of STAT1 during initial Th1 commitment J Immunol 170 2003 4886 4890
6. C. Holscher, A. Holscher, D. Ruckerl, T. Yoshimoto, H. Yoshida, T. Mak, C. Saris, and S. Ehlers The IL-27 receptor chain WSX-1 differentially regulates antibacterial immunity and survival during experimental tuberculosis J Immunol 174 2005 3534 3544
7. H. Yoshida, S. Hamano, G. Senaldi, T. Covey, R. Faggioni, S. Mu, M. Xia, A.C. Wakeham, H. Nishina, J. Potter, C.J. Saris, and T.W. Mak WSX-1 is required for the initiation of Th1 responses and resistance to L. major infection Immunity 15 2001 569 578
8. D. Artis, A. Villarino, M. Silverman, W. He, E.M. Thornton, S. Mu, S. Summer, T.M. Covey, E. Huang, H. Yoshida, G. Koretzky, M. Goldschmidt, G.D. Wu, F. de Sauvage, H.R. Miller, C.J. Saris, P. Scott, and C.A. Hunter The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity J Immunol 173 2004 5626 5634
9. S. Hamano, K. Himeno, Y. Miyazaki, K. Ishii, A. Yamanaka, A. Takeda, M. Zhang, H. Hisaeda, T.W. Mak, A. Yoshimura, and H. Yoshida WSX-1 is required for resistance to Trypanosoma cruzi infection by regulation of proinflammatory cytokine production Immunity 19 2003 657 667
10. Y. Miyazaki, H. Inoue, M. Matsumura, K. Matsumoto, T. Nakano, M. Tsuda, S. Hamano, A. Yoshimura, and H. Yoshida Exacerbation of experimental allergic asthma by augmented Th2 responses in WSX-1-deficient mice J Immunol 175 2005 2401 2407
11. A. Yamanaka, S. Hamano, Y. Miyazaki, K. Ishii, A. Takeda, T.W. Mak, K. Himeno, A. Yoshimura, and H. Yoshida Hyperproduction of proinflammatory cytokines by WSX-1-deficient NKT cells in concanavalin A-induced hepatitis J Immunol 172 2004 3590 3596
12. T. Yoshimoto, T. Yoshimoto, K. Yasuda, J. Mizuguchi, and K. Nakanishi IL-27 suppresses Th2 cell development and Th2 cytokines production from polarized Th2 cells: a novel therapeutic way for Th2-mediated allergic inflammation J Immunol 179 2007 4415 4423
13. J. Yang, M. Yang, T.M. Htut, X. Ouyang, A. Hanidu, X. Li, R. Sellati, H. Jiang, S. Zhang, H. Li, J. Zhao, A.T. Ting, L. Mayer, J.C. Unkeless, M.E. Labadia, M. Hodge, J. Li, and H. Xiong Epstein-Barr virus-induced gene 3 negatively regulates IL-17, IL-22 and RORgamma t Eur J Immunol 38 2008 1204 1214
14. M. Batten, J. Li, S. Yi, N.M. Kljavin, D.M. Danilenko, S. Lucas, J. Lee, F.J. de Sauvage, and N. Ghilardi Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells Nat Immunol 7 2006 929 936
15. A.T. Borchers, C. Chang, M.E. Gershwin, and L.J. Gershwin Respiratory syncytial virus: a comprehensive review Clin Rev Allergy Immunol 45 2013 331 379
16. U. Schauer, S. Hoffjan, T. Rothoeft, H. Bartz, S. Konig, E. Fuchs, J. Bittscheidt, A. Kochling, and V. Stephan Severe respiratory syncytial virus infections and reduced interferon-gamma generation in vitro Clin Exp Immunol 138 2004 102 109
17. M.G. Semple, H.M. Dankert, B. Ebrahimi, J.B. Correia, J.A. Booth, J.P. Stewart, R.L. Smyth, and C.A. Hart Severe respiratory syncytial virus bronchiolitis in infants is associated with reduced airway interferon gamma and substance P PLoS One 2 2007 e1038
18. M. Wills-Karp Interleukin-13 in asthma pathogenesis Immunol Rev 202 2004 175 190
19. J. Schwarze, G. Cieslewicz, A. Joetham, T. Ikemura, E. Hamelmann, and E.W. Gelfand CD8 T cells are essential in the development of respiratory syncytial virus-induced lung eosinophilia and airway hyperresponsiveness J Immunol 162 1999 4207 4211
20. S. Mukherjee, D.M. Lindell, A.A. Berlin, S.B. Morris, T.P. Shanley, M.B. Hershenson, and N.W. Lukacs IL-17-induced pulmonary pathogenesis during respiratory viral infection and exacerbation of allergic disease Am J Pathol 179 2011 248 258
21. K.L. Stokes, M.H. Chi, K. Sakamoto, D.C. Newcomb, M.G. Currier, M.M. Huckabee, S. Lee, K. Goleniewska, C. Pretto, J.V. Williams, A. Hotard, T.P. Sherrill, R.S. Peebles Jr., and M.L. Moore Differential pathogenesis of respiratory syncytial virus clinical isolates in BALB/c mice J Virol 85 2011 5782 5793
22. B.D. Rudd, J.J. Smit, R.A. Flavell, L. Alexopoulou, M.A. Schaller, A. Gruber, A.A. Berlin, and N.W. Lukacs Deletion of TLR3 alters the pulmonary immune environment and mucus production during respiratory syncytial virus infection J Immunol 176 2006 1937 1942
23. J.L. McKimm-Breschkin A simplified plaque assay for respiratory syncytial virus: direct visualization of plaques without immunostaining J Virol Methods 120 2004 113 117
24. T. Demoor, B.C. Petersen, S. Morris, S. Mukherjee, C. Ptaschinski, D.E. De Almeida Nagata, T. Kawai, T. Ito, S. Akira, S.L. Kunkel, M.A. Schaller, and N.W. Lukacs IPS-1 signaling has a nonredundant role in mediating antiviral responses and the clearance of respiratory syncytial virus J Immunol 189 2012 5942 5953
25. N.W. Lukacs, J.J. Smit, S. Mukherjee, S.B. Morris, G. Nunez, and D.M. Lindell Respiratory virus-induced TLR7 activation controls IL-17-associated increased mucus via IL-23 regulation J Immunol 185 2010 2231 2239
26. M. Jankowski, P. Kopinski, and A. Goc Interleukin-27: biological properties and clinical application Arch Immunol Ther Exp (Warsz) 58 2010 417 425
27. J. Bystrom, N. Al-Adhoubi, M. Al-Bogami, A.S. Jawad, and R.A. Mageed Th17 lymphocytes in respiratory syncytial virus infection Viruses 5 2013 777 791
28. S. Mukherjee, R.M. Allen, N.W. Lukacs, S.L. Kunkel, and W.F. Carson 4th STAT3-mediated IL-17 production by postseptic T cells exacerbates viral immunopathology of the lung Shock 38 2012 515 523
29. D.C. Fitzgerald, B. Ciric, T. Touil, H. Harle, J. Grammatikopolou, J. Das Sarma, B. Gran, G.X. Zhang, and A. Rostami Suppressive effect of IL-27 on encephalitogenic Th17 cells and the effector phase of experimental autoimmune encephalomyelitis J Immunol 179 2007 3268 3275
30. C. Neufert, C. Becker, S. Wirtz, M.C. Fantini, B. Weigmann, P.R. Galle, and M.F. Neurath IL-27 controls the development of inducible regulatory T cells and Th17 cells via differential effects on STAT1 Eur J Immunol 37 2007 1809 1816
31. J.S. Stumhofer, A. Laurence, E.H. Wilson, E. Huang, C.M. Tato, L.M. Johnson, A.V. Villarino, Q. Huang, A. Yoshimura, D. Sehy, C.J. Saris, J.J. O'Shea, L. Hennighausen, M. Ernst, and C.A. Hunter Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system Nat Immunol 7 2006 937 945
32. M. Batten, N.M. Kljavin, J. Li, M.J. Walter, F.J. de Sauvage, and N. Ghilardi Cutting edge: IL-27 is a potent inducer of IL-10 but not FoxP3 in murine T cells J Immunol 180 2008 2752 2756
33. A.O. Hall, D.P. Beiting, C. Tato, B. John, G. Oldenhove, C.G. Lombana, G.H. Pritchard, J.S. Silver, N. Bouladoux, J.S. Stumhofer, T.H. Harris, J. Grainger, E.D. Wojno, S. Wagage, D.S. Roos, P. Scott, L.A. Turka, S. Cherry, S.L. Reiner, D. Cua, Y. Belkaid, M.M. Elloso, and C.A. Hunter The cytokines interleukin 27 and interferon-gamma promote distinct Treg cell populations required to limit infection-induced pathology Immunity 37 2012 511 523
34. E.D. Wojno, N. Hosken, J.S. Stumhofer, A.C. O'Hara, E. Mauldin, Q. Fang, L.A. Turka, S.D. Levin, and C.A. Hunter A role for IL-27 in limiting T regulatory cell populations J Immunol 187 2011 266 273
35. Y. Carrier, M.J. Whitters, J.S. Miyashiro, T.P. LaBranche, H.E. Ramon, S.E. Benoit, M.S. Ryan, S.P. Keegan, H. Guay, J. Douhan, M. Collins, K. Dunussi-Joannopoulos, and Q.G. Medley Enhanced GITR/GITRL interactions augment IL-27 expression and induce IL-10-producing Tr-1 like cells Eur J Immunol 42 2012 1393 1404
36. D.C. Newcomb, M.G. Boswell, T.P. Sherrill, V.V. Polosukhin, K.L. Boyd, K. Goleniewska, S.L. Brody, J.K. Kolls, K.B. Adler, and R.S. Peebles Jr. IL-17A induces signal transducers and activators of transcription-6-independent airway mucous cell metaplasia Am J Respir Cell Mol Biol 48 2013 711 716
37. P.A. Gonzalez, C.E. Prado, E.D. Leiva, L.J. Carreno, S.M. Bueno, C.A. Riedel, and A.M. Kalergis Respiratory syncytial virus impairs T cell activation by preventing synapse assembly with dendritic cells Proc Natl Acad Sci U S A 105 2008 14999 15004
38. B. Voges, S. Vallbracht, G. Zimmer, S. Bossow, W.J. Neubert, K. Richter, E. Hobeika, G. Herrler, and S. Ehl Recombinant Sendai virus induces T cell immunity against respiratory syncytial virus that is protective in the absence of antibodies Cell Immunol 247 2007 85 94
39. R. Zeng, H. Zhang, Y. Hai, Y. Cui, L. Wei, N. Li, J. Liu, C. Li, and Y. Liu Interleukin-27 inhibits vaccine-enhanced pulmonary disease following respiratory syncytial virus infection by regulating cellular memory responses J Virol 86 2012 4505 4517
40. J.S. Stumhofer, and C.A. Hunter Advances in understanding the anti-inflammatory properties of IL-27 Immunol Lett 117 2008 123 130
41. L.M. Haynes, D.D. Moore, E.A. Kurt-Jones, R.W. Finberg, L.J. Anderson, and R.A. Tripp Involvement of toll-like receptor 4 in innate immunity to respiratory syncytial virus J Virol 75 2001 10730 10737
42. S. Shibata, Y. Tada, Y. Asano, K. Yanaba, M. Sugaya, T. Kadono, N. Kanda, S. Watanabe, and S. Sato IL-27 activates Th1-mediated responses in imiquimod-induced psoriasis-like skin lesions J Invest Dermatol 133 2013 479 488
43. S. Wang, Y. Miyazaki, Y. Shinozaki, and H. Yoshida Augmentation of antigen-presenting and Th1-promoting functions of dendritic cells by WSX-1(IL-27R) deficiency J Immunol 179 2007 6421 6428
44. T. Owaki, M. Asakawa, S. Kamiya, K. Takeda, F. Fukai, J. Mizuguchi, and T. Yoshimoto IL-27 suppresses CD28-mediated [correction of medicated] IL-2 production through suppressor of cytokine signaling 3 J Immunol 176 2006 2773 2780
45. A.V. Villarino, J.S. Stumhofer, C.J. Saris, R.A. Kastelein, F.J. de Sauvage, and C.A. Hunter IL-27 limits IL-2 production during Th1 differentiation J Immunol 176 2006 237 247
46. T. Yoshimura, A. Takeda, S. Hamano, Y. Miyazaki, I. Kinjyo, T. Ishibashi, A. Yoshimura, and H. Yoshida Two-sided roles of IL-27: induction of Th1 differentiation on naive CD4+ T cells versus suppression of proinflammatory cytokine production including IL-23-induced IL-17 on activated CD4+ T cells partially through STAT3-dependent mechanism J Immunol 177 2006 5377 5385
47. K. Hashimoto, J.E. Durbin, W. Zhou, R.D. Collins, S.B. Ho, J.K. Kolls, P.J. Dubin, J.R. Sheller, K. Goleniewska, J.F. O'Neal, S.J. Olson, D. Mitchell, B.S. Graham, and R.S. Peebles Jr. Respiratory syncytial virus infection in the absence of STAT 1 results in airway dysfunction, airway mucus, and augmented IL-17 levels J Allergy Clin Immunol 116 2005 550 557
48. N.W. Lukacs, K.K. Tekkanat, A. Berlin, C.M. Hogaboam, A. Miller, H. Evanoff, P. Lincoln, and H. Maassab Respiratory syncytial virus predisposes mice to augmented allergic airway responses via IL-13-mediated mechanisms J Immunol 167 2001 1060 1065
49. Q. Chen, N. Ghilardi, H. Wang, T. Baker, M.H. Xie, A. Gurney, I.S. Grewal, and F.J. de Sauvage Development of Th1-type immune responses requires the type I cytokine receptor TCCR Nature 407 2000 916 920
50. H. Hoshino, M. Laan, M. Sjostrand, J. Lotvall, B.E. Skoogh, and A. Linden Increased elastase and myeloperoxidase activity associated with neutrophil recruitment by IL-17 in airways in vivo J Allergy Clin Immunol 105 2000 143 149
51. M. Laan, Z.H. Cui, H. Hoshino, J. Lotvall, M. Sjostrand, D.C. Gruenert, B.E. Skoogh, and A. Linden Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways J Immunol 162 1999 2347 2352
52. P. Ye, F.H. Rodriguez, S. Kanaly, K.L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, J.E. Shellito, G.J. Bagby, S. Nelson, K. Charrier, J.J. Peschon, and J.K. Kolls Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense J Exp Med 194 2001 519 527
53. K. Hashimoto, B.S. Graham, S.B. Ho, K.B. Adler, R.D. Collins, S.J. Olson, W. Zhou, T. Suzutani, P.W. Jones, K. Goleniewska, J.F. O'Neal, and R.S. Peebles Jr. Respiratory syncytial virus in allergic lung inflammation increases Muc5ac and gob-5 Am J Respir Crit Care Med 170 2004 306 312
54. S. Nakae, Y. Komiyama, A. Nambu, K. Sudo, M. Iwase, I. Homma, K. Sekikawa, M. Asano, and Y. Iwakura Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses Immunity 17 2002 375 387
55. M.A. Antonysamy, W.C. Fanslow, F. Fu, W. Li, S. Qian, A.B. Troutt, and A.W. Thomson Evidence for a role of IL-17 in organ allograft rejection: IL-17 promotes the functional differentiation of dendritic cell progenitors J Immunol 162 1999 577 584
56. J. Liu, X. Guan, and X. Ma Regulation of IL-27 p28 gene expression in macrophages through MyD88- and interferon-gamma-mediated pathways J Exp Med 204 2007 141 152
57. S.L. Gaffen Structure and signalling in the IL-17 receptor family Nat Rev Immunol 9 2009 556 567
58. R. Schwandner, K. Yamaguchi, and Z. Cao Requirement of tumor necrosis factor receptor-associated factor (TRAF)6 in interleukin 17 signal transduction J Exp Med 191 2000 1233 1240