Increased nuclear suppressor of cytokine signaling 1 in asthmatic bronchial epithelium suppresses rhinovirus induction of innate interferons

Journal of Allergy and Clinical Immunology

Volumn 136, Issue 1, 2015, Pages 177-188.e11

  Gielen, Vera ^a,b,c   Sykes, Annemarie ^a,b,c,d   Zhu, Jie ^a,b,c   Chan, Brian ^a   Macintyre, Jonathan ^a,b,c,d   Regamey, Nicolas ^e   Kieninger, Elisabeth ^e   Gupta, Atul ^a,c   Shoemark, Amelia ^a,c   Bossley, Cara ^a,c   Davies, Jane ^a,c   Saglani, Sejal ^a,c   Walker, Patrick ^f   Nicholson, Sandra E ^g,h   Dalpke, Alexander H ^f   Kon, Onn Min ^d   Bush, Andrew ^a,c   Johnston, Sebastian L ^a,b,c,d   Edwards, Michael R ^a,b,c  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d NATIONAL HEALTH SERVICE   (United Kingdom)

^e UNIVERSITY OF BERN   (Switzerland)

^f UNIVERSITY OF HEIDELBERG   (Germany)

^g WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^h UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

asthma; asthma exacerbation; atopy; cytokine; innate immunity; interferon; Rhinovirus; suppressor of cytokine signaling; TH2 inflammation

Indexed keywords

INTERFERON; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 4; MESSENGER RNA; SUPPRESSOR OF CYTOKINE SIGNALING 1; TUMOR NECROSIS FACTOR ALPHA; GAMMA INTERFERON; SOCS1 PROTEIN, HUMAN; SOCS1 PROTEIN, MOUSE; SUPPRESSOR OF CYTOKINE SIGNALING;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; BRONCHIAL EPITHELIAL CELL; BRONCHUS BIOPSY; BRONCHUS MUCOSA; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE RESPONSE; DISEASE EXACERBATION; DISEASE SEVERITY; EPITHELIUM CELL; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; INTERFERON INDUCTION; LUNG ALVEOLUS MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REPORTER GENE; RESPIRATORY TRACT ALLERGY; RHINOVIRUS INFECTION; VIRUS REPLICATION; ADOLESCENT; ADULT; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL NUCLEUS; CHILD; COMPLICATION; FEMALE; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MALE; METABOLISM; MIDDLE AGED; MUTATION; PHYSIOLOGY; PICORNAVIRUS INFECTION; PRESCHOOL CHILD; PROTEIN TRANSPORT; RESPIRATORY TRACT MUCOSA; RHINOVIRUS; UPREGULATION; VIROLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; ANIMALS; ASTHMA; CELL NUCLEUS; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; IMMUNITY, INNATE; INTERFERON-GAMMA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; MUTATION; PICORNAVIRIDAE INFECTIONS; PROTEIN TRANSPORT; RESPIRATORY MUCOSA; RHINOVIRUS; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; UP-REGULATION; VIRUS REPLICATION; YOUNG ADULT;

EID: 84949117566     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2014.11.039     Document Type: Article

References (52)

1. P.M. O'Byrne, S. Pedersen, C.J. Lamm, W.C. Tan, and W.W. Busse Severe exacerbations and decline in lung function in asthma Am J Respir Crit Care Med 179 2009 19 24
2. S.L. Johnston, P.K. Pattemore, G. Sanderson, S. Smith, F. Lampe, L. Josephs, and et al. Community study of role of viral infections in exacerbations of asthma in 9-11 year old children BMJ 310 1995 1225 1229
3. N.W. Johnston, S.L. Johnston, J.M. Duncan, J.M. Greene, T. Kebadze, P.K. Keith, and et al. The September epidemic of asthma exacerbations in children: a search for etiology J Allergy Clin Immunol 115 2005 132 138
4. J.M. Corne, C. Marshall, S. Smith, J. Schreiber, G. Sanderson, S.T. Holgate, and et al. Frequency, severity, and duration of rhinovirus infections in asthmatic and non-asthmatic individuals: a longitudinal cohort study Lancet 359 2002 831 834
5. S.D. Message, V. Laza-Stanca, P. Mallia, H.L. Parker, J. Zhu, T. Kebadze, and et al. Rhinovirus-induced lower respiratory illness is increased in asthma and related to virus load and Th1/2 cytokine and IL-10 production Proc Natl Acad Sci U S A 105 2008 13562 13567
6. P.A. Wark, S.L. Johnston, F. Bucchieri, R. Powell, S. Puddicombe, V. Laza-Stanca, and et al. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus J Exp Med 201 2005 937 947
7. M. Contoli, S.D. Message, V. Laza-Stanca, M.R. Edwards, P.A. Wark, N.W. Bartlett, and et al. Role of deficient type III interferon-lambda production in asthma exacerbations Nat Med 12 2006 1023 1026
8. K. Gehlhar, C. Bilitewski, K. Reinitz-Rademacher, G. Rohde, and A. Bufe Impaired virus-induced interferon-alpha2 release in adult asthmatic patients Clin Exp Allergy 36 2006 331 337
9. M.A. Gill, G. Bajwa, T.A. George, C.C. Dong, I.I. Dougherty, N. Jiang, and et al. Counterregulation between the FcepsilonRI pathway and antiviral responses in human plasmacytoid dendritic cells J Immunol 184 2010 5999 6006
10. K. Iikura, T. Katsunuma, S. Saika, S. Saito, S. Ichinohe, H. Ida, and et al. Peripheral blood mononuclear cells from patients with bronchial asthma show impaired innate immune responses to rhinovirus in vitro Int Arch Allergy Immunol 155 suppl 1 2011 27 33
11. S. Baraldo, M. Contoli, E. Bazzan, G. Turato, A. Padovani, B. Marku, and et al. Deficient antiviral immune responses in childhood: distinct roles of atopy and asthma J Allergy Clin Immunol 130 2012 1307 1314
12. S.R. Durrani, D.J. Montville, A.S. Pratt, S. Sahu, M.K. Devries, V. Rajamanickam, and et al. Innate immune responses to rhinovirus are reduced by the high-affinity IgE receptor in allergic asthmatic children J Allergy Clin Immunol 130 2012 489 495
13. A. Sykes, M.R. Edwards, J. Macintyre, A. Del Rosario, E. Bakhsoliani, M.B. Trujillo-Torralbo, and et al. Rhinovirus 16-induced IFN-α and IFN-β are deficient in bronchoalveolar lavage cells in asthmatic patients J Allergy Clin Immunol 129 2012 1506 1514.e6
14. M.R. Edwards, N. Regamey, M. Vareille, E. Kieninger, A. Gupta, A. Shoemark, and et al. Impaired innate interferon induction in severe therapy resistant atopic asthmatic children Mucosal Immunol 6 2012 797 806
15. A. Sykes, J. Macintyre, M.R. Edwards, A. Del Rosario, J. Haas, V. Gielen, and et al. Rhinovirus-induced interferon production is not deficient in well controlled asthma Thorax 69 2014 240 246
16. B.J. Thomas, M. Lindsay, H. Dagher, N.J. Freezer, D. Li, R. Ghildyal, and et al. Transforming growth factor-beta enhances rhinovirus infection by diminishing early innate responses Am J Respir Cell Mol Biol 41 2009 339 347
17. N. Bedke, D. Sammut, B. Green, V. Kehagia, P. Dennison, G. Jenkins, and et al. Transforming growth factor-Beta promotes rhinovirus replication in bronchial epithelial cells by suppressing the innate immune response PLoS One 7 2012 e44580
18. T. Naka, H. Tsutsui, M. Fujimoto, Y. Kawazoe, H. Kohzaki, Y. Morita, and et al. SOCS-1/SSI-1-deficient NKT cells participate in severe hepatitis through dysregulated cross-talk inhibition of IFN-gamma and IL-4 signaling in vivo Immunity 14 2001 535 545
19. C.A. Knosp, H.P. Carroll, J. Elliott, S.P. Saunders, H.J. Nel, S. Amu, and et al. SOCS2 regulates T helper type 2 differentiation and the generation of type 2 allergic responses J Exp Med 208 2011 1523 1531
20. Y. Seki, H. Inoue, N. Nagata, K. Hayashi, S. Fukuyama, K. Matsumoto, and et al. SOCS-3 regulates onset and maintenance of T(H)2-mediated allergic responses Nat Med 9 2003 1047 1054
21. C. Lee, T.B. Kolesnik, I. Caminschi, A. Chakravorty, W. Carter, W.S. Alexander, and et al. Suppressor of cytokine signalling 1 (SOCS1) is a physiological regulator of the asthma response Clin Exp Allergy 39 2009 897 907
22. S. Fukuyama, T. Nakano, T. Matsumoto, B.G. Oliver, J.K. Burgess, A. Moriwaki, and et al. Pulmonary suppressor of cytokine signaling-1 induced by IL-13 regulates allergic asthma phenotype Am J Respir Crit Care Med 179 2009 992 998
23. C.E. Egwuagu, C.R. Yu, M. Zhang, R.M. Mahdi, S.J. Kim, and I. Gery Suppressors of cytokine signaling proteins are differentially expressed in Th1 and Th2 cells: implications for Th cell lineage commitment and maintenance J Immunol 168 2002 3181 3187
24. M. Harada, K. Nakashima, T. Hirota, M. Shimizu, S. Doi, K. Fujita, and et al. Functional polymorphism in the suppressor of cytokine signaling 1 gene associated with adult asthma Am J Respir Cell Mol Biol 36 2007 491 496
25. J.E. Fenner, R. Starr, A.L. Cornish, J.G. Zhang, D. Metcalf, R.D. Schreiber, and et al. Suppressor of cytokine signaling 1 regulates the immune response to infection by a unique inhibition of type I interferon activity Nat Immunol 7 2006 33 39
26. R.A. Piganis, N.A. De Weerd, J.A. Gould, C.W. Schindler, A. Mansell, S.E. Nicholson, and et al. Suppressor of cytokine signaling (SOCS) 1 inhibits type I interferon (IFN) signaling via the interferon alpha receptor (IFNAR1)-associated tyrosine kinase Tyk2 J Biol Chem 286 2011 33811 33818
27. G. Vlotides, A.S. Sorensen, F. Kopp, K. Zitzmann, N. Cengic, S. Brand, and et al. SOCS-1 and SOCS-3 inhibit IFN-alpha-induced expression of the antiviral proteins 2,5-OAS and MxA Biochem Biophys Res Commun 320 2004 1007 1014
28. J. Pothlichet, M. Chignard, and M. Si-Tahar Cutting edge: innate immune response triggered by influenza A virus is negatively regulated by SOCS1 and SOCS3 through a RIG-I/IFNAR1-dependent pathway J Immunol 180 2008 2034 2038
29. J. Corren, R.F. Lemanske, N.A. Hanania, P.E. Korenblat, M.V. Parsey, J.R. Arron, and et al. Lebrikizumab treatment in adults with asthma N Engl J Med 365 2011 1088 1098
30. S. Wenzel, L. Ford, D. Pearlman, S. Spector, L. Sher, F. Skobieranda, and et al. Dupilumab in persistent asthma with elevated eosinophil levels N Engl J Med 368 2013 2455 2466
31. M.R. Khaitov, V. Laza-Stanca, M.R. Edwards, R.P. Walton, G. Rohde, M. Contoli, and et al. Respiratory virus induction of alpha-, beta- and lambda-interferons in bronchial epithelial cells and peripheral blood mononuclear cells Allergy 64 2009 375 386
32. J. Strebovsky, P. Walker, R. Lang, and A.H. Dalpke Suppressor of cytokine signaling 1 (SOCS1) limits NFkappaB signaling by decreasing p65 stability within the cell nucleus FASEB J 25 2010 863 874
33. L. Uller, M. Leino, N. Bedke, D. Sammut, B. Green, L. Lau, and et al. Double-stranded RNA induces disproportionate expression of thymic stromal lymphopoietin versus interferon-beta in bronchial epithelial cells from donors with asthma Thorax 65 2010 626 632
34. N.M. Heller, S. Matsukura, S.N. Georas, M.R. Boothby, P.B. Rothman, C. Stellato, and et al. Interferon-gamma inhibits STAT6 signal transduction and gene expression in human airway epithelial cells Am J Respir Cell Mol Biol 31 2004 573 582
35. K.M. Spann, E. Baturcam, J. Schagen, C. Jones, C.P. Straub, F.M. Preston, and et al. Viral and host factors determine innate immune responses in airway epithelial cells from children with wheeze and atopy Thorax 69 2014 918 925
36. A.L. Pritchard, M.L. Carroll, J.G. Burel, O.J. White, S. Phipps, and J.W. Upham Innate IFNs and plasmacytoid dendritic cells constrain Th2 cytokine responses to rhinovirus: a regulatory mechanism with relevance to asthma J Immunol 188 2012 5898 5905
37. O. Koltsida, M. Hausding, A. Stavropoulos, S. Koch, G. Tzelepis, C. Ubel, and et al. IL-28A (IFN-lambda2) modulates lung DC function to promote Th1 immune skewing and suppress allergic airway disease EMBO Mol Med 3 2011 348 361
38. U. Sriram, C. Biswas, E.M. Behrens, J.A. Dinnall, D.K. Shivers, M. Monestier, and et al. IL-4 suppresses dendritic cell response to type I interferons J Immunol 179 2007 6446 6455
39. S. Edwards, C. Jones, A.J. Leishman, B.W. Young, H. Matsui, H. Tomizawa, and et al. TLR7 Stimulation of APCs results in inhibition of IL-5 through type I IFN and notch signaling pathways in human peripheral blood mononuclear cells J Immunol 190 2013 2585 2592
40. I.D. Pavord, S. Korn, P. Howarth, E.R. Bleecker, R. Buhl, O.N. Keene, and et al. Mepolizumab for severe eosinophilic asthma (DREAM): a multicentre, double-blind, placebo-controlled trial Lancet 380 2012 651 659
41. J.B. Morjaria, A.J. Chauhan, K.S. Babu, R. Polosa, D.E. Davies, and S.T. Holgate The role of a soluble TNFalpha receptor fusion protein (etanercept) in corticosteroid refractory asthma: a double blind, randomised, placebo controlled trial Thorax 63 2008 584 591
42. S.Y. Hwang, P.J. Hertzog, K.A. Holland, S.H. Sumarsono, M.J. Tymms, J.A. Hamilton, and et al. A null mutation in the gene encoding a type I interferon receptor component eliminates antiproliferative and antiviral responses to interferons alpha and beta and alters macrophage responses Proc Natl Acad Sci U S A 92 1995 11284 11288
43. I. Marie, J.E. Durbin, and D.E. Levy Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7 EMBO J 17 1998 6660 6669
44. C. Koelsche, J. Strebovsky, A. Baetz, and A.H. Dalpke Structural and functional analysis of a nuclear localization signal in SOCS1 Mol Immunol 46 2009 2474 2480
45. A. Papi, and S.L. Johnston Rhinovirus infection induces expression of its own receptor intercellular adhesion molecule 1 (ICAM-1) via increased NF-kappaB-mediated transcription J Biol Chem 274 1999 9707 9720
46. N.W. Bartlett, R.P. Walton, M.R. Edwards, J. Aniscenko, G. Caramori, J. Zhu, and et al. Mouse models of rhinovirus-induced disease and exacerbation of allergic airway inflammation Nat Med 14 2008 199 204
47. J. Strebovsky, P. Walker, R. Lang, and A.H. Dalpke Suppressor of cytokine signaling 1 (SOCS1) limits NFkappaB signaling by decreasing p65 stability within the cell nucleus FASEB J 25 2010 863 874
48. P.I. Osterlund, T.E. Pietila, V. Veckman, S.V. Kotenko, and I. Julkunen IFN regulatory factor family members differentially regulate the expression of type III IFN (IFN-lambda) genes J Immunol 179 2007 3434 3442
49. A. Sykes, M.R. Edwards, J. Macintyre, A. Del Rosario, E. Bakhsoliani, M.B. Trujillo-Torralbo, and et al. Rhinovirus 16-induced IFN-alpha and IFN-beta are deficient in bronchoalveolar lavage cells in asthmatic patients J Allergy Clin Immunol 129 2012 1506 1514.e6
50. M.R. Edwards, N. Regamey, M. Vareille, E. Kieninger, A. Gupta, A. Shoemark, and et al. Impaired innate interferon induction in severe therapy resistant atopic asthmatic children Mucosal Immunol 6 2012 797 806
51. C. Lee, T.B. Kolesnik, I. Caminschi, A. Chakravorty, W. Carter, W.S. Alexander, and et al. Suppressor of cytokine signalling 1 (SOCS1) is a physiological regulator of the asthma response Clin Exp Allergy 39 2009 897 907
52. N.W. Bartlett, L. Slater, N. Glanville, J.J. Haas, G. Caramori, P. Casolari, and et al. Defining critical roles for NF-kappaB p65 and type I interferon in innate immunity to rhinovirus EMBO Mol Med 4 2012 1244 1260