Rhinovirus inhibits IL-17A and the downstream immune responses in allergic asthma

Mucosal Immunology

Volumn 9, Issue 5, 2016, Pages 1183-1192

  Graser, A ^a   Ekici, A B ^a   Sopel, N ^a   Melichar, V O ^a   Zimmermann, T ^a   Papadopoulos, N G ^b   Taka, S ^b   Ferrazzi, F ^a   Vuorinen, T ^c   Finotto, S ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b UNIVERSITY OF ATHENS   (Greece)

^c UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; 2',5' OLIGOADENYLATE SYNTHETASE 1; BETA INTERFERON; INTERLEUKIN 17; MESSENGER RNA; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG; IL17A PROTEIN, HUMAN; OAS1 PROTEIN, HUMAN; OVALBUMIN; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR TBX21;

A549 CELL LINE; ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MALE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; RHINOVIRUS INFECTION; TH17 CELL; UPPER RESPIRATORY TRACT INFECTION; VIRAL CLEARANCE; A-549 CELL LINE; ANIMAL; ASTHMA; CLINICAL TRIAL; DRUG HYPERSENSITIVITY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; PICORNAVIRUS INFECTION; PRESCHOOL CHILD; PRIMARY CELL CULTURE; RHINOVIRUS; SIGNAL TRANSDUCTION; VIROLOGY;

2',5'-OLIGOADENYLATE SYNTHETASE; A549 CELLS; ANIMALS; ASTHMA; CD4-POSITIVE T-LYMPHOCYTES; CHILD; CHILD, PRESCHOOL; DRUG HYPERSENSITIVITY; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INTERFERON-BETA; INTERLEUKIN-17; LUNG; MALE; MICE; MICE, KNOCKOUT; OVALBUMIN; PICORNAVIRIDAE INFECTIONS; PRIMARY CELL CULTURE; RHINOVIRUS; RNA, MESSENGER; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS;

EID: 84982311226     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2015.130     Document Type: Article

References (63)

1. Edwards, M.R., Bartlett, N.W., Hussell, T., Openshaw, P., & Johnston, S.L. The microbiology of asthma. Nat. Rev. Microbiol. 10, 459-471 (2012
2. Fuchs, R., & Blaas, D. Productive entry pathways of human rhinoviruses. Adv. Virol. 2012, 826301 (2012
3. Johnston, S.L., et al. Community study of role of viral infections in exacerbations of asthma in 9-11 year old children. BMJ 310, 1225-1229 (1995
4. Nicholson, K.G., Kent, J., & Ireland, D.C. Respiratory viruses and exacerbations of asthma in adults. BMJ 307, 982-986 (1993
5. Winther, B. Rhinovirus infections in the upper airway. Proc. Am. Thorac. Soc. 8, 79-89 (2011
6. Subauste, M.C., Jacoby, D.B., Richards, S.M., & Proud, D. Infection of a human respiratory epithelial cell line with rhinovirus. Induction of cytokine release and modulation of susceptibility to infection by cytokine exposure. J. Clin. Invest. 96, 549-557 (1995
7. Deszcz, L., Gaudernak, E., Kuechler, E., & Seipelt, J. Apoptotic events induced by human rhinovirus infection. J. Gen. Virol. 86, 1379-1389 (2005
8. Hadfield, A.T., et al. The refined structure of human rhinovirus 16 at 2.15A resolution: implications for the viral life cycle. Structure 5, 427-441 (1997
9. Kapikian, A.Z., Almeida, J.D., & Stott, E.J. Immune electron microscopy of rhinoviruses. J. Virol. 10, 142-146 (1972
10. Newcomb, D.C., et al. Human rhinovirus 1B exposure induces phosphatidylinositol 3-kinase-dependent airway inflammation in mice. Am. J. Respir. Crit. Care Med 177, 1111-1121 (2008
11. Savolainen, C., Mulders, M.N., & Hovi, T. Phylogenetic analysis of rhinovirus isolates collected during successive epidemic seasons. Virus Res. 85, 41-46 (2002
12. Reppert, S., Zinser, E., Holzinger, C., Sandrock, L., Koch, S., & Finotto, S. NFATc1 deficiency in Tcells protects mice from experimental autoimmune encephalomyelitis. Eur. J. Immunol. 45, 1426-1440 (2015
13. Aujla, S.J., & Alcorn, J.F. T(H)17 cells in asthma and inflammation. Biochim. Biophys. Acta 1810, 1066-1079 (2011
14. Schnyder-Candrian, S., et al. Interleukin-17 is a negative regulator of established allergic asthma. J. Exp. Med. 203, 2715-2725 (2006
15. Murdoch, J.R., & Lloyd, C.M. Resolution of allergic airway inflammation and airway hyperreactivity is mediated by IL-17-producing {gamma}{delta}T cells. Am. J. Respir. Crit. Care Med. 182, 464-476 (2010
16. Hirota, K., Ahlfors, H., Duarte, J.H., & Stockinger, B. Regulation and function of innate and adaptive interleukin-17-producing cells.EMBORep. 13, 113-120 (2012
17. Hirota, K., et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 12, 255-263 (2011
18. Van De Veerdonk, F.L., Gresnigt, M.S., Kullberg, B.J., Van Der Meer, J.W., Joosten, L.A., & Netea, M.G. Th17 responses and host defense against microorganisms: an overview. BMB Rep. 42, 776-787 (2009
19. Kumar, S., Mitnik, C., Valente, G., & Floyd-Smith, G. Expansion and molecular evolution of the interferon-induced 2-5 oligoadenylate synthetase gene family. Mol. Biol. Evol. 17, 738-750 (2000
20. Sadler, A.J., & Williams, B.R. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 8, 559-568 (2008
21. Courtney, S.C., Di, H., Stockman, B.M., Liu, H., Scherbik, S.V., & Brinton, M.A. Identification of novel host cell binding partners of Oas1b, the protein conferring resistance to flavivirus-induced disease in mice. J. Virol. 86, 7953-7963 (2012
22. Miossec, P., & Kolls, J.K. Targeting IL-17 and TH17 cells in chronic inflammation. Nat. Rev. Drug Discov. 11, 763-776 (2012
23. Busse, W.W., et al. Randomized, double-blind, placebo-controlled study of brodalumab, a human anti-IL-17 receptor monoclonal antibody, in moderate to severe asthma. Am. J. Respir. Crit. Care Med. 188, 1294-1302 (2013
24. Szabo, S.J., Kim, S.T., Costa, G.L., Zhang, X., Fathman, C.G., & Glimcher, L.H. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100, 655-669 (2000
25. Reppert, S., et al. A role for T-bet-mediated tumour immune surveillance in anti-IL-17A treatment of lung cancer. Nat. Commun. 2, 600 (2011
26. Finotto, S., et al. Asthmatic changes in mice lacking T-bet are mediated by IL-13. Int. Immunol. 17, 993-1007 (2005
27. Klein Wolterink, R.G., et al. Pulmonary innate lymphoid cells are major producers of IL-5 and IL-13 in murine models of allergic asthma. Eur. J. Immunol. 42, 1106-1116 (2012
28. Abraham, S.N., & St John, A.L. Mast cell-orchestrated immunity to pathogens. Nat. Rev. Immunol. 10, 440-452 (2010
29. Segal, A.W. How neutrophils kill microbes. Annu. Rev. Immunol. 23, 197-223 (2005
30. Dottorini, T., et al. Serum IgE reactivity profiling in an asthma affected cohort. PloS One 6, e22319 (2011
31. Dorsey, M.J., Tae, H.J., Sollenberger, K.G., Mascarenhas, N.T., Johansen, L.M.& Taparowsky, E.J. B-ATF: a novel human bZIP protein that associates with members of the AP-1 transcription factor family. Oncogene 11, 2255-2265 (1995
32. Ubel, C., et al. The activating protein 1 transcription factor basic leucine zipper transcription factor, ATF-like (BATF), regulates lymphocyte-and mast cell-driven immune responses in the setting of allergic asthma. J. Allergy Clin. Immunol. 133, 198-206. e191-199 (2014
33. Andreev, K., Graser, A., Maier, A., Mousset, S., & Finotto, S. Therapeutical measures to control airway tolerance in asthma and lung cancer. Front. Immunol. 3, 216 (2012
34. Heymann, P.W., & Kennedy, J.L. Rhinovirus-induced asthma exacerbations during childhood: the importance of understanding the atopic status of the host. J. Allergy Clin. Immunol. 130, 1315-1316 (2012
35. Fazio, S., Hasty, A.H., Carter, K.J., Murray, A.B., Price, J.O., & Linton, M.F. Leukocyte low density lipoprotein receptor (LDL-R) does not contribute to LDL clearance in vivo: bone marrow transplantation studies in the mouse. J. Lipid Res. 38, 391-400 (1997
36. Ho, Y.K., Brown, S., Bilheimer, D.W., & Goldstein, J.L. Regulation of low density lipoprotein receptor activity in freshly isolated human lymphocytes. J. Clin. Invest. 58, 1465-1474 (1976
37. Ilarraza, R., Wu, Y., Skappak, C.D., Ajamian, F., Proud, D., & Adamko, D.J. Rhinovirus has the unique ability to directly activate human T cells in vitro. J. Allergy Clin. Immunol. 131, 395-404 (2013
38. Subramaniam, S.V., Pearson, L.L., & Adunyah, S.E. Interleukin-17 induces rapid tyrosine phosphorylation and activation of raf-1 kinase in human monocytic progenitor cell line U937. Biochem. Biophys. Res. Commun. 259, 172-177 (1999
39. Subramaniam, S.V., Cooper, R.S., & Adunyah, S.E. Evidence for the involvement of JAK/STAT pathway in the signaling mechanism of interleukin-17. Biochem. Biophys. Res. Commun. 262, 14-19 (1999
40. Yao, Z., et al. Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 3, 811-821 (1995
41. Jiang, Z., Mak, T.W., Sen, G., & Li, X. Toll-like receptor 3-mediated activation of NF-kappaB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFN-beta. Proc. Natl Acad. Sci. USA 101, 3533-3538 (2004
42. Khaitov, M.R., et al. Respiratory virus induction of alpha-, beta-and lambdainterferons in bronchial epithelial cells and peripheral blood mononuclear cells. Allergy 64, 375-386 (2009
43. Sykes, A., et al. Rhinovirus 16-induced IFN-alpha and IFN-beta are deficient in bronchoalveolar lavage cells in asthmatic patients. J. Allergy Clin. Immunol. 129, 1506-1514 (2012
44. Kotla, S., Peng, T., Bumgarner, R.E., & Gustin, K.E. Attenuation of the type I interferon response in cells infected with human rhinovirus. Virology 374, 399-410 (2008
45. Edwards, M.R., et al. Impaired innate interferon induction in severe therapy resistant atopic asthmatic children. Mucosal Immunol. 6, 797-806 (2013
46. Baraldo, S., et al. Deficient antiviral immune responses in childhood: distinct roles of atopy and asthma. J. Allergy Clin. Immunol. 130, 1307-1314 (2012
47. Wang, J., & Mountz, J. IL-17 augment type IIFN-mediated antibody production in BXD2 autoimmune mouse. J. Invest. Med. 56, 430-430 (2008
48. Wang, J.H., et al. IL-17 promotes type I interferon signaling in autoimmune BXD2 mice. Arthritis Rheum. 58, S181-S181 (2008
49. Iwakura, Y., Nakae, S., Saijo, S., & Ishigame, H. The roles of IL-17A in inflammatory immune responses and host defense against pathogens. Immunol. Rev. 226, 57-79 (2008
50. Glaab, T., Taube, C., Braun, A., & Mitzner, W. Invasive and noninvasive methods for studying pulmonary function in mice. Respir. Res. 8, 63 (2007
51. Kaur, D., et al. IL-33 drives airway hyper-responsiveness through IL-13-mediated mast cell: airway smooth muscle crosstalk. Allergy 70, 556-567 (2015
52. Kondo, Y., et al. Administration of IL-33 induces airway hyperresponsiveness and goblet cell hyperplasia in the lungs in the absence of adaptive immune system. Int. Immunol. 20, 791-800 (2008
53. Stock, P., Lombardi, V., Kohlrautz, V., & Akbari, O. Induction of airway hyperreactivity by IL-25 is dependent on a subset of invariant NKT cells expressing IL-17RB. J. Immunol. 182, 5116-5122 (2009
54. Kinyanjui, M.W., Shan, J., Nakada, E.M., Qureshi, S.T., & Fixman, E.D. Dose-dependent effects of IL-17 on IL-13-induced airway inflammatory responses and airway hyperresponsiveness. J. Immunol. 190, 3859-3868 (2013
55. Vareille, M., Kieninger, E., Edwards, M.R., & Regamey, N. The airway epithelium: soldier in the fight against respiratory viruses. Clin. Microbiol. Rev. 24, 210-229 (2011
56. Peltola, V., Waris, M., Osterback, R., Susi, P., Ruuskanen, O., & Hyypia, T. Rhinovirus transmission within families with children: incidence of symptomatic and asymptomatic infections. J. Infect. Dis. 197, 382-389 (2008
57. Tuthill, T.J., et al. Mouse respiratory epithelial cells support efficient replication of human rhinovirus. J.Gen. Virol. 84, 2829-2836 (2003
58. Finotto, S., et al. Treatment of allergic airway inflammation and hyperresponsiveness by antisense-induced local blockade of GATA-3 expression. J. Exp. Med. 193, 1247-1260 (2001
59. Kraft, M., et al. Disruption of the histone acetyltransferase MYST4 leads to a Noonan syndrome-like phenotype and hyperactivated MAPK signaling in humans and mice. J. Clin. Invest. 121, 3479-3491 (2011
60. Papadopoulos, N.G., et al. Rhinoviruses infect the lower airways. J. Infect. Dis. 181, 1875-1884 (2000
61. Hornung, V., Hartmann, R., Ablasser, A., & Hopfner, K.P. OAS proteins and cGAS: unifying concepts in sensing and responding to cytosolic nucleic acids. Nat. Rev. Immunol. 14, 521-528 (2014
62. Silverman, R.H. Viral encounters with 2, 5-oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol. 81, 12720-12729 (2007
63. Zhao, L., et al. Antagonism of the interferon-induced OAS-RNase L pathway by murine coronavirus ns2 protein is required for virus replication and liver pathology. Cell Host Microbe 11, 607-616 (2012