Type-III interferon, not type-I, is the predominant interferon induced by respiratory viruses in nasal epithelial cells

Virus Research

Volumn 160, Issue 1-2, 2011, Pages 360-366

  Okabayashi, Tamaki ^a   Kojima, Takashi ^a   Masaki, Tomoyuki ^a   Yokota, Shin ichi ^a   Imaizumi, Tadaatsu ^b   Tsutsumi, Hiroyuki ^a   Himi, Tetsuo ^a   Fujii, Nobuhiro ^a   Sawada, Norimasa ^a  

^a SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b HIROSAKI UNIVERSITY   (Japan)

Author keywords

Human nasal epithelial cells; Interferon lambda; Respiratory virus

Indexed keywords

ALPHA2 INTERFERON; BETA INTERFERON; INTERFERON; INTERFERON TYPE III; MELANOMA DIFFERENTIATION ASSOCIATED PROTEIN 5; MESSENGER RNA; PATTERN RECOGNITION RECEPTOR; RANTES; RETINOIC ACID INDUCIBLE PROTEIN I; SMALL INTERFERING RNA; TELOMERASE REVERSE TRANSCRIPTASE; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL STRAIN; CELL STRAIN A 549; CELL STRAIN HEP 2; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; INNATE IMMUNITY; MEASLES VIRUS; MUCOSAL IMMUNITY; MUMPS VIRUS; NONHUMAN; NOSE MUCOSA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; VIRAL RESPIRATORY TRACT INFECTION; VIRUS IMMUNITY; VIRUS REPLICATION; VIRUS TITRATION; WESTERN BLOTTING;

CELLS, CULTURED; EPITHELIAL CELLS; HUMANS; INTERFERON-ALPHA; INTERFERON-BETA; INTERLEUKINS; MEASLES VIRUS; MUMPS VIRUS; RESPIRATORY MUCOSA; RESPIRATORY SYNCYTIAL VIRUSES;

MEASLES VIRUS; MUMPS VIRUS; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

EID: 80052181676     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2011.07.011     Document Type: Article

References (39)

1. Alam R., York J., Boyars M., Stafford S., Grant J.A., Lee J., Forsythe P., Sim T., Ida N. Increased MCP-1, RANTES, and MIP-1alpha in bronchoalveolar lavage fluid of allergic asthmatic patients. Am. J. Respir. Crit. Care Med. 1996, 153:1398-1404.
2. Ank N., Iversen M.B., Bartholdy C., Staeheli P., Hartmann R., Jensen U.B., Dagnaes-Hansen F., Thomsen A.R., Chen Z., Haugen H., Klucher K., Paludan S.R. An important role for type III interferon (IFN-lambda/IL-28) in TLR-induced antiviral activity. J. Immunol. 2008, 180:2474-2485.
3. Becker S., Soukup J., Yankaskas J.R. Respiratory syncytial virus infection of human primary nasal and bronchial epithelial cell cultures and bronchoalveolar macrophages. Am. J. Respir. Cell Mol. Biol. 1992, 6:369-374.
4. Brand S., Beigel F., Olszak T., Zitzmann K., Eichhorst S.T., Otte J.M., Diebold J., Diepolder H., Adler B., Auernhammer C.J., Goke B., Dambacher J. IL-28A and IL-29 mediate antiproliferative and antiviral signals in intestinal epithelial cells and murine CMV infection increases colonic IL-28A expression. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 289:G960-G968.
5. Chi B., Dickensheets H.L., Spann K.M., Alston M.A., Luongo C., Dumoutier L., Huang J., Renauld J.C., Kotenko S.V., Roederer M., Beeler J.A., Donnelly R.P., Collins P.L., Rabin R.L. Alpha and lambda interferon together mediate suppression of CD4T cells induced by respiratory syncytial virus. J. Virol. 2006, 80:5032-5040.
6. Contoli M., Message S.D., Laza-Stanca V., Edwards M.R., Wark P.A., Bartlett N.W., Kebadze T., Mallia P., Stanciu L.A., Parker H.L., Slater L., Lewis-Antes A., Kon O.M., Holgate S.T., Davies D.E., Kotenko S.V., Papi A., Johnston S.L. Role of deficient type III interferon-lambda production in asthma exacerbations. Nat. Med. 2006, 12:1023-1026.
7. Fujii N., Kimura K., Murakami T., Indoh T., Ishida S., Fujinaga K., Oguma K. Suppression of interferon-induced oligo-2',5'-adenylate synthetase induction in persistent infection. J. Gen. Virol. 1990, 71(Pt 12):3071-3074.
8. Gitlin L., Barchet W., Gilfillan S., Cella M., Beutler B., Flavell R.A., Diamond M.S., Colonna M. Essential role of MDA-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:8459-8464.
9. Gonzalo J.A., Lloyd C.M., Wen D., Albar J.P., Wells T.N., Proudfoot A., Martinez A.C., Dorf M., Bjerke T., Coyle A.J., Gutierrez-Ramos J.C. The coordinated action of CC chemokines in the lung orchestrates allergic inflammation and airway hyperresponsiveness. J. Exp. Med. 1998, 188:157-167.
10. Groskreutz D.J., Monick M.M., Powers L.S., Yarovinsky T.O., Look D.C., Hunninghake G.W. Respiratory syncytial virus induces TLR3 protein and protein kinase R, leading to increased double-stranded RNA responsiveness in airway epithelial cells. J. Immunol. 2006, 176:1733-1740.
11. Imaizumi T., Aratani S., Nakajima T., Carlson M., Matsumiya T., Tanji K., Ookawa K., Yoshida H., Tsuchida S., McIntyre T.M., Prescott S.M., Zimmerman G.A., Satoh K. Retinoic acid-inducible gene-I is induced in endothelial cells by LPS and regulates expression of COX-2. Biochem. Biophys. Res. Commun. 2002, 292:274-279.
12. Indoh T., Shirakawa S., Kubota T., Yashiki T., Isogai E., Fujii N. Augmentation of interferon production after cell-differentiation of U937 cells by TPA. Microbiol. Immunol. 1996, 40:675-679.
13. Jewell N.A., Cline T., Mertz S.E., Smirnov S.V., Flano E., Schindler C., Grieves J.L., Durbin R.K., Kotenko S.V., Durbin J.E. Lambda interferon is the predominant interferon induced by influenza A virus infection in vivo. J. Virol. 2010, 84:11515-11522.
14. Khaitov M.R., Laza-Stanca V., Edwards M.R., Walton R.P., Rohde G., Contoli M., Papi A., Stanciu L.A., Kotenko S.V., Johnston S.L. Respiratory virus induction of alpha-, beta- and lambda-interferons in bronchial epithelial cells and peripheral blood mononuclear cells. Allergy 2009, 64:375-386.
15. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., Uematsu S., Jung A., Kawai T., Ishii K.J., Yamaguchi O., Otsu K., Tsujimura T., Koh C.S., Reis e Sousa C., Matsuura Y., Fujita T., Akira S. Differential role of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006, 4:101-105.
16. Kotenko S.V., Gallagher G., Baurin V.V., Lewis-Antes A., Shen M., Shah N.K., Langer J.A., Sheikh F., Dickensheets H., Donnelly R.P. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol. 2003, 4:69-77.
17. Kubota T., Yokosawa N., Yokota S., Fujii N. Association of mumps virus V protein with RACK1 results in dissociation of STAT-1 from the alpha interferon receptor complex. J. Virol. 2002, 76:12676-12682.
18. Kurose M., Kojima T., Koizumi J., Kamekura R., Ninomiya T., Murata M., Ichimiya S., Osanai M., Chiba H., Himi T., Sawada N. Induction of claudins in passaged hTERT-transfected human nasal epithelial cells with an extended life span. Cell Tissue Res. 2007, 330:63-74.
19. Liu P., Jamaluddin M., Li K., Garofalo R.P., Casola A., Brasier A.R. Retinoic acid-inducible gene I mediates early antiviral response and Toll-like receptor 3 expression in respiratory syncytial virus-infected airway epithelial cells. J. Virol. 2007, 81:1401-1411.
20. Miller D.M., Klucher K.M., Freeman J.A., Hausman D.F., Fontana D., Williams D.E. Interferon lambda as a potential new therapeutic for hepatitis C. Ann. N. Y. Acad. Sci. 2009, 1182:80-87.
21. Monick M.M., Yarovinsky T.O., Powers L.S., Butler N.S., Carter A.B., Gudmundsson G., Hunninghake G.W. Respiratory syncytial virus up-regulates TLR4 and sensitizes airway epithelial cells to endotoxin. J. Biol. Chem. 2003, 278:53035-53044.
22. Mordstein M., Kochs G., Dumoutier L., Renauld J.C., Paludan S.R., Klucher K., Staeheli P. Interferon-lambda contributes to innate immunity of mice against influenza A virus but not against hepatotropic viruses. PLoS Pathog. 2008, 4:e1000151.
23. Mordstein M., Neugebauer E., Ditt V., Jessen B., Rieger T., Falcone V., Sorgeloos F., Ehl S., Mayer D., Kochs G., Schwemmle M., Gunther S., Drosten C., Michiels T., Staeheli P. Lambda interferon renders epithelial cells of the respiratory and gastrointestinal tracts resistant to viral infections. J. Virol. 2010, 84:5670-5677.
24. Ohkuni T., Kojima T., Ogasawara N., Masaki T., Ninomiya T., Kikuchi S., Go M., Takano K., Himi T., Sawada N. Expression and localization of tricellulin in human nasal epithelial cells in vivo and in vitro. Med. Mol. Morphol. 2009, 42:204-211.
25. Okabayashi T., Kariwa H., Yokota S., Iki S., Indoh T., Yokosawa N., Takashima I., Tsutsumi H., Fujii N. Cytokine regulation in SARS coronavirus infection compared to other respiratory virus infections. J. Med. Virol. 2006, 78:417-424.
26. Onoguchi K., Yoneyama M., Takemura A., Akira S., Taniguchi T., Namiki H., Fujita T. Viral infections activate types I and III interferon genes through a common mechanism. J. Biol. Chem. 2007, 282:7576-7581.
27. Osterlund P.I., Pietila T.E., Veckman V., Kotenko S.V., Julkunen I. IFN regulatory factor family members differentially regulate the expression of type III IFN (IFN-lambda) genes. J. Immunol. 2007, 179:3434-3442.
28. Robek M.D., Boyd B.S., Chisari F.V. Lambda interferon inhibits hepatitis B and C virus replication. J. Virol. 2005, 79:3851-3854.
29. Scagnolari C., Midulla F., Pierangeli A., Moretti C., Bonci E., Berardi R., De Angelis D., Selvaggi C., Di Marco P., Girardi E., Antonelli G. Gene expression of nucleic acid-sensing pattern recognition receptors in children hospitalized for respiratory syncytial virus-associated acute bronchiolitis. Clin. Vaccine Immunol. 2009, 16:816-823.
30. Schroder M., Bowie A.G. TLR3 in antiviral immunity: key player or bystander?. Trends Immunol. 2005, 26:462-468.
31. Sheppard P., Kindsvogel W., Xu W., Henderson K., Schlutsmeyer S., Whitmore T.E., Kuestner R., Garrigues U., Birks C., Roraback J., Ostrander C., Dong D., Shin J., Presnell S., Fox B., Haldeman B., Cooper E., Taft D., Gilbert T., Grant F.J., Tackett M., Krivan W., McKnight G., Clegg C., Foster D., Klucher K.M. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat. Immunol. 2003, 4:63-68.
32. Sommereyns C., Paul S., Staeheli P., Michiels T. IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog. 2008, 4:e1000017.
33. Spann K.M., Tran K.C., Chi B., Rabin R.L., Collins P.L. Suppression of the induction of alpha, beta, and lambda interferons by the NS1 and NS2 proteins of human respiratory syncytial virus in human epithelial cells and macrophages [corrected]. J. Virol. 2004, 78:4363-4369.
34. Thomson S.J., Goh F.G., Banks H., Krausgruber T., Kotenko S.V., Foxwell B.M., Udalova I.A. The role of transposable elements in the regulation of IFN-lambda1 gene expression. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:11564-11569.
35. Venge J., Lampinen M., Hakansson L., Rak S., Venge P. Identification of IL-5 and RANTES as the major eosinophil chemoattractants in the asthmatic lung. J. Allergy Clin. Immunol. 1996, 97:1110-1115.
36. Yokosawa N., Yokota S., Kubota T., Fujii N. C-terminal region of STAT-1alpha is not necessary for its ubiquitination and degradation caused by mumps virus V protein. J. Virol. 2002, 76:12683-12690.
37. Yokota S., Okabayashi T., Yokosawa N., Fujii N. Growth arrest of epithelial cells during measles virus infection is caused by upregulation of interferon regulatory factor 1. J. Virol. 2004, 78:4591-4598.
38. Yokota S., Saito H., Kubota T., Yokosawa N., Amano K., Fujii N. Measles virus suppresses interferon-alpha signaling pathway: suppression of Jak1 phosphorylation and association of viral accessory proteins, C and V, with interferon-alpha receptor complex. Virology 2003, 306:135-146.
39. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 2004, 5:730-737.