Chicken interferon alpha pretreatment reduces virus replication of pandemic H1N1 and H5N9 avian influenza viruses in lung cell cultures from different avian species

Virology Journal

Darrell R Kapczynski²  Hanchun Yang¹  Haijun Jiang² 

[1] Key Laboratory of Zoonosis of Ministry of Agriculture, College of Veterinary Medicine and State Key Laboratory of Agrobiotechnology, China Agricultural University, Beijing, People's Republic of China;Exotic and Emerging Avian Disease Unit, Southeast Poultry Research Laboratory, Agricultural Research Service, USDA, 934 College Station Road, Athens, GA, 30605, USA

关键词: turkey;    duck;    chicken;    interferon;    avian influenza;   

Others  :  1156050
DOI  :  10.1186/1743-422X-8-447

 received in 2011-04-27, accepted in 2011-09-22,  发布年份 2011

【 摘 要 】

Background

Type I interferons, including interferon alpha (IFN-α), represent one of the first lines of innate immune defense against influenza virus infection. Following natural infection of chickens with avian influenza virus (AIV), transcription of IFN-α is quickly up regulated along with multiple other immune-related genes. Chicken IFN-α up regulates a number of important anti-viral response genes and has been demonstrated to be an important cytokine to establish anti-viral immunity. However, the mechanisms by which interferon inhibit virus replication in avian species remains unknown as does the biological activity of chicken interferon in other avian species.

Methods

In these studies, we assessed the protective potential of exogenous chicken IFN-α applied to chicken, duck, and turkey primary lung cell cultures prior to infection with the pandemic H1N1 virus (A/turkey/Virginia/SEP-4/2009) and an established avian H5N9 virus (A/turkey/Wisconsin/1968). Growth kinetics and induction of select immune response genes, including IFN-α and myxovirus-resistance gene I (Mx), as well as proinflammatory cytokines (IL-1β and IL-6), were measured in response to chicken IFN-α and viral infection over time.

Results

Results demonstrate that pretreatment with chicken IFN-α before AIV infection significantly reduced virus replication in both chicken-and turkey-origin lung cells and to a lesser degree the duck-origin cells. Virus growth was reduced by approximately 200-fold in chicken and turkey cells and 30-fold in duck cells after 48 hours of incubation. Interferon treatment also significantly decreased the interferon and proinflammatory response during viral infection. In general, infection with the H1N1 virus resulted in an attenuated interferon and proinflammatory response in these cell lines, compared to the H5N9 virus.

Conclusions

Taken together, these studies show that chicken IFN-α reduces virus replication, lower host innate immune response following infection, and is biologically active in other avian species.

【 授权许可】

   
2011 Jiang et al; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Webby RJ, Webster RG: Are we ready for pandemic influenza? Science 2003, 302:1519-1522.
• [2]Akey BL: Low-pathogenicity H7N2 avian influenza outbreak in Virgnia during 2002. Avian Dis 2003, 47:1099-1103.
• [3]Isaacs A, Lindenmann J: Virus interference. I. The interferon. Proc R Soc Lond B Biol Sci 1957, 147:258-267.
• [4]Schultz U, Kock J, Schlicht HJ, Staeheli P: Recombinant duck interferon: a new reagent for studying the mode of interferon action against hepatitis B virus. Virology 1995, 212:641-649.
• [5]Bertram EM, Jilbert AR, Kotlarski I: An homologous in vitro assay to detect lymphokines released by PHA-activated duck peripheral blood lymphocytes and spleen cells. Vet Immunol Immunopathol 1997, 56:163-174.
• [6]Suresh M, Karaca K, Foster D, Sharma JM: Molecular and functional characterization of turkey interferon. J Virol 1995, 69:8159-8163.
• [7]Ziegler RE, Joklik WK: Effect of interferon on multiplication of avian sarcoma virus B77 in duck embryo fibroblasts. J Interferon Res 1981, 1:521-538.
• [8]Garcia-Sastre A: Inhibition of interferon-mediated antiviral responses by influenza A viruses and other negative-strand RNA viruses. Virology 2001, 279:375-384.
• [9]Sarmento L, Pantin-Jackwood M, Kapczynski DR, Swayne DE, Afonso CL: Immediate early responses of avian tracheal epithelial cells to infection with highly pathogenic avian influenza virus. Dev Biol (Basel) 2008, 132:175-183.
• [10]Daviet S, Van Borm S, Habyarimana A, Ahanda ML, Morin V, Oudin A, Van Den Berg T, Zoorob R: Induction of Mx and PKR failed to protect chickens from H5N1 infection. Viral Immunol 2009, 22:467-472.
• [11]Schumacher B, Bernasconi D, Schultz U, Staeheli P: The chicken Mx promoter contains an ISRE motif and confers interferon inducibility to a reporter gene in chick and monkey cells. Virology 1994, 203:144-148.
• [12]Bernasconi D, Schultz U, Staeheli P: The interferon-induced Mx protein of chickens lacks antiviral activity. J Interferon Cytokine Res 1995, 15:47-53.
• [13]Ko JH, Jin HK, Asano A, Takada A, Ninomiya A, Kida H, Hokiyama H, Ohara M, Tsuzuki M, Nishibori M, et al.: Polymorphisms and the differential antiviral activity of the chicken Mx gene. Genome Res 2002, 12:595-601.
• [14]Ewald SJ, Kapczynski DR, Livant EJ, Suarez DL, Ralph J, McLeod S, Miller C: Association of Mx1 Asn631 variant alleles with reductions in morbidity, early mortality, viral shedding, and cytokine responses in chickens infected with a highly pathogenic avian influenza virus. Immunogenetics 2011, 363-375.
• [15]Bazzigher L, Schwarz A, Staeheli P: No enhanced influenza virus resistance of murine and avian cells expressing cloned duck Mx protein. Virology 1993, 195:100-112.
• [16]Dawood FS, Jain S, Finelli L, Shaw MW, Lindstrom S, Garten RJ, Gubareva LV, Xu X, Bridges CB, Uyeki TM: Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 2009, 360:2605-2615.
• [17]Dundon WG, De Benedictis P, Viale E, Capua I: Serologic evidence of pandemic (H1N1) 2009 infection in dogs, Italy. Emerg Infect Dis 2010, 16:2019-2021.
• [18]Munster VJ, de Wit E, van den Brand JM, Herfst S, Schrauwen EJ, Bestebroer TM, van de Vijver D, Boucher CA, Koopmans M, Rimmelzwaan GF, et al.: Pathogenesis and transmission of swine-origin 2009 A(H1N1) influenza virus in ferrets. Science 2009, 325:481-483.
• [19]Kapczynski DR, Gonder E, Liljebjelke K, Lippert R, Petkov D, Tilley B: Vaccine-induced protection from egg production losses in commercial turkey breeder hens following experimental challenge with a triple-reassortant H3N2 avian influenza virus. Avian Dis 2009, 53:7-15.
• [20]Choi YK, Lee JH, Erickson G, Goyal SM, Joo HS, Webster RG, Webby RJ: H3N2 influenza virus transmission from swine to turkeys, United States. Emerg Infect Dis 2004, 10:2156-2160.
• [21]Tang Y, Lee CW, Zhang Y, Senne DA, Dearth R, Byrum B, Perez DR, Suarez DL, Saif YM: Isolation and characterization of H3N2 influenza A virus from turkeys. Avian Dis 2005, 49:207-213.
• [22]Yassine HM, Al-Natour MQ, Lee CW, Saif YM: Interspecies and intraspecies transmission of triple reassortant H3N2 influenza A viruses. Virol J 2007, 4:129. BioMed Central Full Text
• [23]Honda A, Mizumoto K, Ishihama A: Minimum molecular architectures for transcription and replication of the influenza virus. Proc Natl Acad Sci USA 2002, 99:13166-13171.
• [24]Yamanaka K, Ishihama A, Nagata K: Reconstitution of influenza virus RNA-nucleoprotein complexes structurally resembling native viral ribonucleoprotein cores. J Biol Chem 1990, 265:11151-11155.
• [25]Baudin F, Bach C, Cusack S, Ruigrok RW: Structure of influenza virus RNP. I. Influenza virus nucleoprotein melts secondary structure in panhandle RNA and exposes the bases to the solvent. Embo J 1994, 13:3158-3165.
• [26]Garcia MA, Gil J, Ventoso I, Guerra S, Domingo E, Rivas C, Esteban M: Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol Mol Biol Rev 2006, 70:1032-1060.
• [27]Ronni T, Matikainen S, Sareneva T, Melen K, Pirhonen J, Keskinen P, Julkunen I: Regulation of IFN-alpha/beta, MxA, 2',5'-oligoadenylate synthetase, and HLA gene expression in influenza A-infected human lung epithelial cells. J Immunol 1997, 158:2363-2374.
• [28]Meng S, Yang L, Xu C, Qin Z, Xu H, Wang Y, Sun L, Liu W: Recombinant Chicken Interferon-alpha Inhibits H9N2 Avian Influenza Virus Replication In Vivo by Oral Administration. J Interferon Cytokine Res 2011.
• [29]Plachy J, Weining KC, Kremmer E, Puehler F, Hala K, Kaspers B, Staeheli P: Protective effects of type I and type II interferons toward Rous sarcoma virus-induced tumors in chickens. Virology 1999, 256:85-91.
• [30]Kimble B, Nieto GR, Perez DR: Characterization of influenza virus sialic acid receptors in minor poultry species. Virol J 2010, 7:365. BioMed Central Full Text
• [31]Pillai SP, Lee CW: Species and age related differences in the type and distribution of influenza virus receptors in different tissues of chickens, ducks and turkeys. Virol J 2010, 7:5. BioMed Central Full Text
• [32]Tumpey TM, Kapczynski DR, Swayne DE: Comparative susceptibility of chickens and turkeys to avian influenza A H7N2 virus infection and protective efficacy of a commercial avian influenza H7N2 virus vaccine. Avian Dis 2004, 48:167-176.
• [33]Spackman E, Gelb J, Preskenis LA, Ladman BS, Pope CR, Pantin-Jackwood MJ, McKinley ET: The pathogenesis of low pathogenicity H7 avian influenza viruses in chickens, ducks and turkeys. Virol J 2010, 7:331. BioMed Central Full Text
• [34]Pillai SP, Pantin-Jackwood M, Yassine HM, Saif YM, Lee CW: The high susceptibility of turkeys to influenza viruses of different origins implies their importance as potential intermediate hosts. Avian Dis 2010, 54:522-526.
• [35]Zeng H, Pappas C, Katz JM, Tumpey TM: The 2009 pandemic H1N1 and triple-reassortant swine H1N1 influenza viruses replicate efficiently but elicit an attenuated inflammatory response in polarized human bronchial epithelial cells. J Virol 2011, 85:686-696.
• [36]Osterlund P, Pirhonen J, Ikonen N, Ronkko E, Strengell M, Makela SM, Broman M, Hamming OJ, Hartmann R, Ziegler T, Julkunen I: Pandemic H1N1 2009 influenza A virus induces weak cytokine responses in human macrophages and dendritic cells and is highly sensitive to the antiviral actions of interferons. J Virol 2010, 84:1414-1422.
• [37]de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC, et al.: Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 2006, 12:1203-1207.
• [38]Degen WG, Smith J, Simmelink B, Glass EJ, Burt DW, Schijns VE: Molecular immunophenotyping of lungs and spleens in naive and vaccinated chickens early after pulmonary avian influenza A (H9N2) virus infection. Vaccine 2006, 24:6096-6109.
• [39]Lavrentieva IN, Medvedeva TE, Golubev DB: Characterization of the reproduction of influenza A epidemic viruses in cell cultures. Acta Virol 1986, 30:137-142.
• [40]Seo SH, Webster RG: Cross-reactive, cell-mediated immunity and protection of chickens from lethal H5N1 influenza virus infection in Hong Kong poultry markets. J Virol 2001, 75:2516-2525.
• [41]Reed LJ, Muench H: A simple method for estimating fifty percent endpoints. American Journal of Hygiene 1938, 27:493-497.
• [42]Wasilenko JL, Lee CW, Sarmento L, Spackman E, Kapczynski DR, Suarez DL, Pantin-Jackwood MJ: NP, PB1, and PB2 viral genes contribute to altered replication of H5N1 avian influenza viruses in chickens. J Virol 2008, 82:4544-4553.
• [43]Kapczynski DR, Kogut MH: Measurement of avian cytokines with real-time RT-PCR following infection with the avian influenza virus. Methods Mol Biol 2008, 436:127-134.
• [44]Mayne RK, Powell F, Else RW, Kaiser P, Hocking PM: Foot pad dermatitis in growing turkeys is associated with cytokine and cellular changes indicative of an inflammatory immune response. Avian Pathol 2007, 36:453-459.
• [45]Adams SC, Xing Z, Li J, Cardona CJ: Immune-related gene expression in response to H11N9 low pathogenic avian influenza virus infection in chicken and Pekin duck peripheral blood mononuclear cells. Mol Immunol 2009, 46:1744-1749.
• [46]Morrison TB, Weis JJ, Wittwer CT: Quantification of low-copy transcripts by continuous SYBR Green I monitoring during amplification. Biotechniques 1998, 24:954-958. 960, 962