Lambda interferon is the predominant interferon induced by influenza A virus infection in vivo

Journal of Virology

Volumn 84, Issue 21, 2010, Pages 11515-11522

  Jewell, Nancy A ^a,f   Cline, Troy ^a,g   Mertz, Sara E ^a   Smirnov, Sergey V ^b   Flaño, Emilio ^a,c   Schindler, Christian ^e   Grieves, Jessica L ^a,d   Durbin, Russell K ^a   Kotenko, Sergei V ^b   Durbin, Joan E ^a,c  

^a THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d OHIO STATE UNIVERSITY   (United States)

^e Och Spine at New York Presbyterian Hospitals   (United States)

^f LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^g ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; INTERFERON; INTERFERON RECEPTOR; LAMBDA INTERFERON; STAT1 PROTEIN; STAT2 PROTEIN; UNCLASSIFIED DRUG; ALPHA BETA INTERFERON RECEPTOR; CYTOKINE; INTERFERON-LAMBDA PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CYTOKINE PRODUCTION; EPITHELIUM CELL; IMMUNE RESPONSE; IN VIVO STUDY; INFLUENZA; INFLUENZA VIRUS A; MOUSE; NONHUMAN; PRIORITY JOURNAL; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; DEFICIENCY; GENETICS; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; ORTHOMYXOVIRUS INFECTION; TRANSCRIPTION INITIATION;

ANIMALIA; INFLUENZA A VIRUS; MURINAE; MUS; ORTHOMYXOVIRIDAE;

ANIMALS; CYTOKINES; EPITHELIAL CELLS; HUMANS; INFLUENZA A VIRUS; INTERFERONS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTOR, INTERFERON ALPHA-BETA; TRANSCRIPTIONAL ACTIVATION;

EID: 77957966273     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01703-09     Document Type: Article

References (59)

1. Ank, N., M. B. Iversen, C. Bartholdy, P. Staeheli, R. Hartmann, U. B. Jensen, F. Dagnaes-Hansen, A. R. Thomsen, Z. Chen, H. Haugen, K. Klucher, and S. R. Paludan. 2008. An important role for type III interferon (IFN-lambda/ IL-28) in TLR-induced antiviral activity. J. Immunol. 180:2474-2485.
2. Ank, N., H. West, C. Bartholdy, K. Eriksson, A. R. Thomsen, and S. R. Paludan. 2006. Lambda interferon (IFN-λ), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J. Virol. 80:4501-4509.
3. Berghall, H., J. Siren, D. Sarkar, I. Julkunen, P. B. Fisher, R. Vainionpaa, and S. Matikainen. 2006. The interferon-inducible RNA helicase, mda-5, is involved in measles virus-induced expression of antiviral cytokines. Microbes Infect. 8:2138-2144.
4. Bourmakina, S. V., and A. Garcia-Sastre. 2003. Reverse genetics studies on the filamentous morphology of influenza A virus. J. Gen. Virol. 84:517-527.
5. Bustamante, J., S. Boisson-Dupuis, E. Jouanguy, C. Picard, A. Puel, L. Abel, and J. L. Casanova. 2008. Novel primary immunodeficiencies revealed by the investigation of paediatric infectious diseases. Curr. Opin. Immunol. 20:39-48.
6. Chi, B., H. L. Dickensheets, K. M. Spann, M. A. Alston, C. Luongo, L. Dumoutier, J. Huang, J. C. Renauld, S. V. Kotenko, M. Roederer, J. A. Beeler, R. P. Donnelly, P. L. Collins, and R. L. Rabin. 2006. Alpha and lambda interferon together mediate suppression of CD4 T cells induced by respiratory syncytial virus. J. Virol. 80:5032-5040.
7. Contoli, M., S. D. Message, V. Laza-Stanca, M. R. Edwards, P. A. Wark, N. W. Bartlett, T. Kebadze, P. Mallia, L. A. Stanciu, H. L. Parker, L. Slater, A. Lewis-Antes, O. M. Kon, S. T. Holgate, D. E. Davies, S. V. Kotenko, A. Papi, and S. L. Johnston. 2006. Role of deficient type III interferon-lambda production in asthma exacerbations. Nat. Med. 12:1023-1026.
8. Curtsinger, J. M., J. O. Valenzuela, P. Agarwal, D. Lins, and M. F. Mescher. 2005. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J. Immunol. 174:4465-4469.
9. Daly, K., P. Nguyen, D. L. Woodland, and M. A. Blackman. 1995. Immunodominance of major histocompatibility complex class I-restricted influenza virus epitopes can be influenced by the T-cell receptor repertoire. J. Virol. 69:7416-7422.
10. Darnell, J. E., Jr. 1997. STATs and gene regulation. Science 277:1630-1635.
11. Der, S. D., A. Zhou, B. R. Williams, and R. H. Silverman. 1998. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl. Acad. Sci. U. S. A. 95:15623-15628.
12. Dittmann, J., S. Stertz, D. Grimm, J. Steel, A. Garcia-Sastre, O. Haller, and G. Kochs. 2008. Influenza A virus strains differ in sensitivity to the antiviral action of Mx-GTPase. J. Virol. 82:3624-3631. (Pubitemid 351429938)
13. Doyle, S. E., H. Schreckhise, K. Khuu-Duong, K. Henderson, R. Rosler, H. Storey, L. Yao, H. Liu, F. Barahmand-pour, P. Sivakumar, C. Chan, C. Birks, D. Foster, C. H. Clegg, P. Wietzke-Braun, S. Mihm, and K. M. Klucher. 2006. Interleukin-29 uses a type 1 interferon-like program to promote antiviral responses in human hepatocytes. Hepatology 44:896-906.
14. Dumoutier, L., A. Tounsi, T. Michiels, C. Sommereyns, S. V. Kotenko, and J. C. Renauld. 2004. Role of the interleukin (IL)-28 receptor tyrosine residues for antiviral and antiproliferative activity of IL-29/interferon-lambda 1: similarities with type I interferon signaling. J. Biol. Chem. 279:32269-32274.
15. Durbin, J., R. Hackenmiller, M. C. Simon, and D. E. Levy. 1996. Targeted disruption of the STAT1 gene results in compromised innate immunity to viral disease. Cell 84:443-450.
16. Reference deleted.
17. Flandorfer, A., A. Garcia-Sastre, C. F. Basler, and P. Palese. 2003. Chimeric influenza A viruses with a functional influenza B virus neuraminidase or hemagglutinin. J. Virol. 77:9116-9123.
18. Garcia-Sastre, A., and C. A. Biron. 2006. Type 1 interferons and the virus-host relationship: a lesson in detente. Science 312:879-882.
19. Garcia-Sastre, A., R. K. Durbin, H. Zheng, P. Palese, R. Gertner, D. E. Levy, and J. E. Durbin. 1998. The role of interferon in influenza virus tissue tropism. J. Virol. 72:8550-8558.
20. Gil, M. P., R. Salomon, J. Louten, and C. A. Biron. 2006. Modulation of STAT1 protein levels: a mechanism shaping CD8 T-cell responses in vivo. Blood 107:987-993.
21. Gilliet, M., A. Boonstra, C. Paturel, S. Antonenko, X. L. Xu, G. Trinchieri, A. O'Garra, and Y. J. Liu. 2002. The development of murine plasmacytoid dendritic cell precursors is differentially regulated by FLT3-ligand and granulocyte/ macrophage colony-stimulating factor. J. Exp. Med. 195:953-958.
22. Haller, O., P. Staeheli, and G. Kochs. 2009. Protective role of interferon-indeed Mx GTPases against influenza viruses. Rev. Sci. Tech. 28:219-231.
23. Hiscott, J. 2007. Triggering the innate antiviral response through IRF-3 activation. J. Biol. Chem. 282:15325-15329.
24. Honda, K., S. Sakaguchi, C. Nakajima, A. Watanabe, H. Yanai, M. Matsumoto, T. Ohteki, T. Kaisho, A. Takaoka, S. Akira, T. Seya, and T. Taniguchi. 2003. Selective contribution of IFN-alpha-beta signaling to the maturation of dendritic cells induced by double-stranded RNA or viral infection. Proc. Natl. Acad. Sci. U. S. A. 100:10872-10877.
25. Jewell, N. A., N. Vaghefi, S. E. Mertz, P. Akter, R. S. Peebles, Jr., L. O. Bakaletz, R. K. Durbin, E. Flano, and J. E. Durbin. 2007. Differential type I interferon induction by respiratory syncytial virus and influenza A virus in vivo. J. Virol. 81:9790-9800.
26. Johnson, T. R., S. E. Mertz, N. Gitiban, S. Hammond, R. Legallo, R. K. Durbin, and J. E. Durbin. 2005. Role for innate IFNs in determining respiratory syncytial virus immunopathology. J. Immunol. 174:7234-7241.
27. Kato, H., S. Sato, M. Yoneyama, M. Yamamoto, S. Uematsu, K. Matsui, T. Tsujimura, K. Takeda, T. Fujita, O. Takeuchi, and S. Akira. 2005. Cell type-specific involvement of RIG-I in antiviral response. Immunity 23:19-28.
28. Kolumam, G. A., S. Thomas, L. J. Thompson, J. Sprent, and K. Murali- Krishna. 2005. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J. Exp. Med. 202:637-650.
29. Kotenko, S. V., G. Gallagher, V. V. Baurin, A. Lewis-Antes, M. Shen, N. K. Shah, J. A. Langer, F. Sheikh, H. Dickensheets, and R. P. Donnelly. 2003. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol. 4:69-77.
30. Kotenko, S. V., and J. A. Langer. 2004. Full house: 12 receptors for 27 cytokines. Int. Immunopharmacol. 4:593-608.
31. Lasfar, A., A. Lewis-Antes, S. V. Smirnov, S. Anantha, W. Abushahba, B. Tian, K. Reuhl, H. Dickensheets, F. Sheikh, R. P. Donnelly, E. Raveche, and S. V. Kotenko. 2006. Characterization of the mouse IFN-lambda ligand-receptor system: IFN-lambdas exhibit antitumor activity against B16 melanoma. Cancer Res. 66:4468-4477.
32. Lindenmann, J. 1982. From interference to interferon: a brief historical introduction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 299:3-6.
33. Loo, Y.-M., J. Fornek, N. Crochet, G. Bajwa, O. Perwitasari, L. Martinez- Sobrido, S. Akira, M. A. Gill, A. García-Sastre, M. G. Katze, and M. Gale, Jr. 2008. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 82:335-345.
34. Marcello, T., A. Grakoui, G. Barba-Spaeth, E. S. Machlin, S. V. Kotenko, M. R. MacDonald, and C. M. Rice. 2006. Interferons alpha and lambda inhibit hepatitis C virus replication with distinct signal transduction and gene regulation kinetics. Gastroenterology 131:1887-1898.
35. Marie, I., J. E. Durbin, and D. E. Levy. 1998. Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J. 17:6660-6669.
36. Martinez-Sobrido, L., N. Gitiban, A. Fernandez-Sesma, J. Cros, S. E. Mertz, N. A. Jewell, S. Hammond, E. Flano, R. K. Durbin, A. Garcia-Sastre, and J. E. Durbin. 2006. Protection against respiratory syncytial virus by a recombinant Newcastle disease virus vector. J. Virol. 80:1130-1139.
37. Matikainen, S., J. Siren, J. Tissari, V. Veckman, J. Pirhonen, M. Severa, Q. Sun, R. Lin, S. Meri, G. Uze, J. Hiscott, and I. Julkunen. 2006. Tumor necrosis factor alpha enhances influenza A virus-induced expression of antiviral cytokines by activating RIG-I gene expression. J. Virol. 80:3515-3522.
38. Mordstein, M., G. Kochs, L. Dumoutier, J. C. Renauld, S. R. Paludan, K. Klucher, and P. Staeheli. 2008. Interferon-lambda contributes to innate immunity of mice against influenza A virus but not against hepatotropic viruses. PLoS Pathog. 4:e1000151.
39. Muller, U., U. Steinhoff, L. F. L. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional roles of type I and type II interferons in antiviral defense. Science 264:1818-1821.
40. Onoguchi, K., M. Yoneyama, A. Takemura, S. Akira, T. Taniguchi, H. Namiki, and T. Fujita. 2007. Viral infections activate types I and III interferon genes through a common mechanism. J. Biol. Chem. 282:7576-7581.
41. Osterlund, P., T. Pietila, V. Veckman, S. Kotenko, and I. Julkunen. 2007. IFN regulatory factor family members differentially regulate the expression of type III IFN (IFN-lambda) genes. J. Immunol. 179:3434-3442.
42. Osterlund, P., V. Veckman, J. Siren, K. M. Klucher, J. Hiscott, S. Matikainen, and I. Julkunen. 2005. Gene expression and antiviral activity of alpha/beta interferons and interleukin-29 in virus-infected human myeloid dendritic cells. J. Virol. 79:9608-9617. (Pubitemid 41022304)
43. Park, C., S. Li, E. Cha, and C. Schindler. 2000. Immune response in Stat2 knockout mice. Immunity 13:795-804. (Pubitemid 32041802)
44. Pestka, S., C. D. Krause, and M. R. Walter. 2004. Interferons, interferon-like cytokines, and their receptors. Immunol. Rev. 202:8-32.
45. Prakash, A., E. Smith, C. K. Lee, and D. E. Levy. 2005. Tissue-specific positive feedback requirements for production of type I interferon following virus infection. J. Biol. Chem. 280:18651-18657.
46. Price, G., A. Gaszewska-Mastarlarz, and D. Moskophidis. 2000. The role of alpha/beta and gamma interferons in development of immunity to influenza A virus in mice. J. Virol. 74:3996-4003. (Pubitemid 30214404)
47. Sato, M., H. Suemori, N. Hata, M. Asagiri, K. Ogasawara, K. Nakao, T. Nakaya, M. Katsuki, S. Noguchi, N. Tanaka, and T. Taniguchi. 2000. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13:539-548.
48. Schindler, C., and J. E. Darnell, Jr. 1995. Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu. Rev. Biochem. 64:621-651.
49. Schindler, C., D. E. Levy, and T. Decker. 2007. JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 282:20059-20063.
50. Schulman, J. L., and P. Palese. 1977. Virulence factors of influenza A viruses: WSN virus neuraminidase required for plaque production in MDBK cells. J. Virol. 24:170-176.
51. Sheppard, P., W. Kindsvogel, W. Xu, K. Henderson, S. Schlutsmeyer, T. E. Whitmore, R. Kuestner, U. Garrigues, C. Birks, J. Roraback, C. Ostrander, D. Dong, J. Shin, S. Presnell, B. Fox, B. Haldeman, E. Cooper, D. Taft, T. Gilbert, F. J. Grant, M. Tackett, W. Krivan, G. McKnight, C. Clegg, D. Foster, and K. M. Klucher. 2003. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat. Immunol. 4:63-68.
52. Siren, J., T. Imaizumi, D. Sarkar, T. Pietila, D. L. Noah, R. Lin, J. Hiscott, R. M. Krug, P. B. Fisher, I. Julkunen, and S. Matikainen. 2006. Retinoic acid inducible gene-I and mda-5 are involved in influenza A virus-induced expression of antiviral cytokines. Microbes Infect. 8:2013-2020. (Pubitemid 44311573)
53. Sommereyns, C., S. Paul, P. Staeheli, and T. Michiels. 2008. IFN-lambda (IFN-λ) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog. 4:e1000017.
54. Spann, K. M., K. C. Tran, B. Chi, R. L. Rabin, and P. L. Collins. 2004. 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. J. Virol. 78:4363-4369.
55. Reference deleted.
56. Sugiura, A., and M. Ueda. 1980. Neurovirulence of influenza virus in mice. I. Neurovirulence of recombinants between virulent and avirulent virus strains. Virology 101:440-449.
57. Wang, J., R. Oberley-Deegan, S. Wang, M. Nikrad, C. Funk, K. Hartshorn, and R. Mason. 2009. Differentiated human alveolar type II cells secrete antiviral IL-29 (IFN-λ1) in response to influenza A infection. J. Immunol. 182:1296-1304.
58. Wikenheiser, K. A., D. K. Vorbroker, W. R. Rice, J. C. Clark, C. J. Bachurski, H. K. Oie, and J. A. Whitsett. 1993. Production of immortalized distal respiratory epithelial cell lines from surfactant protein C/simian virus 40 large tumor antigen transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 90: 11029-11033.
59. Zhou, Z., O. J. Hamming, N. Ank, S. R. Paludan, A. L. Nielsen, and R. Hartmann. 2007. Type III interferon (IFN) induces a type I IFN-like response in a restricted subset of cells through signaling pathways involving both the Jak-STAT pathway and the mitogen-activated protein kinases. J. Virol. 81:7749-7758. (Pubitemid 47047861)