Gut microbiota modulates type I interferon and antibody-mediated immune responses in chickens infected with influenza virus subtype H9N2

Beneficial Microbes

Volumn 9, Issue 3, 2018, Pages 417-427

  Yitbarek, A ^a   Alkie, T ^a   Taha Abdelaziz, K ^a,c   Astill, J ^a   Rodriguez Lecompte, J C ^b   Parkinson, J ^d,e   Nagy, E ^a   Sharif, S ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF PRINCE EDWARD ISLAND   (Canada)

^c Beni Suef University   (Egypt)

^d UNIVERSITY OF TORONTO   (Canada)

^e HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

Author keywords

Antibiotic depletion; Germ free chickens; Gut lung axis

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; IMMUNOGLOBULIN G ANTIBODY; MESSENGER RNA; IMMUNOGLOBULIN G; INTERFERON; VIRUS ANTIBODY;

ACTINOBACTERIA; ALPHAPROTEOBACTERIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BACTEROIDETES; CHICKEN; CONTROLLED STUDY; ENTEROCOCCUS; FIRMICUTES; GAMMAPROTEOBACTERIA; HEMAGGLUTINATION INHIBITION TEST; INFLUENZA A VIRUS (H9N2); INTESTINE FLORA; NONHUMAN; VIRUS REPLICATION; VIRUS SHEDDING; ADAPTIVE IMMUNITY; ANIMAL; AVIAN INFLUENZA; BLOOD; CLOACA; GENE EXPRESSION PROFILING; IMMUNOLOGY; INNATE IMMUNITY; LUNG; OROPHARYNX; PATHOLOGY; SERUM; VIROLOGY;

ADAPTIVE IMMUNITY; ANIMALS; ANTIBODIES, VIRAL; CHICKENS; CLOACA; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION PROFILING; HEMAGGLUTINATION INHIBITION TESTS; IMMUNITY, INNATE; IMMUNOGLOBULIN G; INFLUENZA A VIRUS, H9N2 SUBTYPE; INFLUENZA IN BIRDS; INTERFERON TYPE I; LUNG; OROPHARYNX; SERUM; VIRUS SHEDDING;

EID: 85046762415     PISSN: 18762883     EISSN: 18762891     Source Type: Journal    
DOI: 10.3920/BM2017.0088     Document Type: Article

References (49)

1. Abt, M.C., Osborne, L.C., Monticelli, L.A., Doering, T.A., Alenghat, T., Sonnenberg, G.F., Paley, M.A., Antenus, M., Williams, K.L., Erikson, J., Wherry, E.J. and Artis, D., 2012. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 37: 158-170.
2. Alexander, D.J., 2007. An overview of the epidemiology of avian influenza. Vaccine 25: 5637-5644.
3. Bano, S., Naeem, K. and Malik, S., 2003. Evaluation of pathogenic potential of avian influenza virus serotype H9N2 in chickens. Avian Diseases 47: 817-822.
4. Barjesteh, N., Shojadoost, B., Brisbin, J.T., Emam, M., Hodgins, D.C., Nagy, é. and Sharif, S., 2015. Reduction of avian influenza virus shedding by administration of Toll-like receptor ligands to chickens. Vaccine 33: 4843-4849.
5. Brisbin, J.T., Gong, J., Lusty, C.A., Sabour, P., Sanei, B., Han, Y., Shewen, P.E. and Sharif, S., 2008. Influence of in-feed virginiamycin on the systemic and mucosal antibody response of chickens. Poultry Science 87: 1995-1999.
6. Clarke, T.B., 2014. Early innate immunity to bacterial infection in the lung is regulated systemically by the commensal microbiota via nod-like receptor ligands. Infection and Immunity 82: 4596-4606.
7. Cornelissen, J.B.W.J., Post, J., Peeters, B., Vervelde, L. and Rebel, J.M.J., 2012. Differential innate responses of chickens and ducks to low-pathogenic avian influenza. Avian Pathology 41: 519-529.
8. Daugan, M., Murira, A., Mindt, B.C., Germain, A., Tarrab, E., Lapierre, P., Fritz, J.H. and Lamarre, A., 2016. Type I interferon impairs specific antibody responses early during establishment of LCMV infection. Frontiers in Immunology 7: 564.
9. Dolowy, W.C. and Muldoon, R.L., 1964. Studies of germfree animals I. response of mice to infection with influenza A virus. Experimental Biology and Medicine 116: 365-371.
10. Dunkley, K.D., Dunkley, C.S., Njongmeta, N.L., Callaway, T.R., Hume, M.E., Kubena, L.F., Nisbet, D.J. and Ricke, S.C., 2007. Comparison of in vitro fermentation and molecular microbial profiles of high-fiber feed substrates incubated with chicken cecal inocula. Poultry Science 86: 801-810.
11. Fagundes, C.T., Amaral, F.A., Vieira, A.T., Soares, A.C., Pinho, V., Nicoli, J.R., Vieira, L.Q., Teixeira, M.M. and Souza, D.G., 2012. Transient TLR activation restores inflammatory response and ability to control pulmonary bacterial infection in germfree mice. Journal of Immunology 188: 1411-1420.
12. Frey, A., Di Canzio, J. and Zurakowski, D., 1998. A statistically defined endpoint titer determination method for immunoassays. Journal of Immunological Methods 221: 35-41.
13. Ganal, S.C., Sanos, S.L., Kallfass, C., Oberle, K., Johner, C., Kirschning, C., Lienenklaus, S., Weiss, S., Staeheli, P., Aichele, P. and Diefenbach, A., 2012. Priming of natural killer cells by nonmucosal mononuclear phagocytes requires instructive signals from commensal microbiota. Immunity 37: 171-186.
14. Haghighi, H.R., Gong, J., Gyles, C.L., Hayes, M.A., Sanei, B., Parvizi, P., Gisavi, H., Chambers, J.R. and Sharif, S., 2005. Modulation of antibody-mediated immune response by probiotics in chickens. Clinical and Diagnostic Laboratory Immunology 12: 1387-1392.
15. Haghighi, H.R., Gong, J., Gyles, C.L., Hayes, M.A., Zhou, H., Sanei, B., Chambers, J.R. and Sharif, S., 2006. Probiotics stimulate production of natural antibodies in chickens. Clinical and Vaccine Immunology 13: 975-980.
16. Ichinohe, T., Pang, I.K., Kumamoto, Y., Peaper, D.R., Ho, J.H., Murray, T.S. and Iwasaki, A., 2011. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proceedings of the National Academy of Sciences of the USA 108: 5354-5359.
17. Iqbal, M., Yaqub, T., Mukhtar, N., Shabbir, M.Z. and McCauley, J.W., 2013. Infectivity and transmissibility of H9N2 avian influenza virus in chickens and wild terrestrial birds. Veterinary Research 44: 100.
18. Iwasaki, A. and Pillai, P.S., 2014. Innate immunity to influenza virus infection. Nature Reviews Immunology 14: 315-328.
19. Kaiser, A., Willer, T., Sid, H., Petersen, H., Baumgärtner, W., Steinberg, P. and Rautenschlein, S., 2016. Susceptibility of primary chicken intestinal epithelial cells for low pathogenic avian influenza virus and velogenic viscerotropic Newcastle disease virus. Virus Research 225: 50-63.
20. Kane, M., Case, L.K., Kopaskie, K., Kozlova, A., MacDearmid, C., Chervonsky, A.V. and Golovkina, T.V., 2011. Successful transmission of a retrovirus depends on the commensal microbiota. Science 334: 245-249.
21. Kawashima, T., Kosaka, A., Yan, H., Guo, Z., Uchiyama, R., Fukui, R., Kaneko, D., Kumagai, Y., You, D.J., Carreras, J., Uematsu, S., Jang, M.H., Takeuchi, O., Kaisho, T., Akira, S., Miyake, K., Tsutsui, H., Saito, T., Nishimura, I. and Tsuji, N.M., 2013. Double-stranded rna of intestinal commensal but not pathogenic bacteria triggers production of protective interferon-ß. Immunity 38: 1187-1197.
22. Kim, M. and Kim, C.H., 2017. Regulation of humoral immunity by gut microbial products. Gut Microbes 8: 392-399.
23. Kuss, S.K., Best, G.T., Etheredge, C.A., Pruijssers, A.J., Frierson, J.M., Hooper, L.V., Dermody, T.S. and Pfeiffer, J.K., 2011. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 334: 249-252.
24. Ley, R.E., Lozupone, C.A., Hamady, M., Knight, R. and Gordon, J.I., 2008. Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Reviews Microbiology 6: 776.
25. Maeda, N., Nakamura, R., Hirose, Y., Murosaki, S., Yamamoto, Y., Kase, T. and Yoshikai, Y., 2009. Oral administration of heat-killed Lactobacillus plantarum L-137 enhances protection against influenza virus infection by stimulation of type I interferon production in mice. International Immunopharmacology 9: 1122-1125.
26. Mallick, A.I., Parvizi, P., Read, L.R., Nagy, é., Behboudi, S. and Sharif, S., 2011. Enhancement of immunogenicity of a virosome-based avian influenza vaccine in chickens by incorporating CpG-ODN. Vaccine 29: 1657-1665.
27. McAleer, J.P., Nguyen, N.L.H., Chen, K., Kumar, P., Ricks, D.M., Binnie, M., Armentrout, R.A., Pociask, D.A., Hein, A., Yu, A., Vikram, A., Bibby, K., Umesaki, Y., Rivera, A., Sheppard, D., Ouyang, W., Hooper, L.V. and Kolls, J.K., 2016. Pulmonary Th17 antifungal immunity is regulated by the gut microbiome. Journal of Immunology 197: 97-107.
28. McNab, F., Mayer-Barber, K., Sher, A., Wack, A. and O'Garra, A., 2015. Type I interferons in infectious disease. Nature Reviews Immunology 15: 87-103.
29. Nice, T.J., Osborne, L.C., Tomov, V.T., Artis, D., Wherry, E.J. and Virgin, H.W., 2016. Type I interferon receptor deficiency in dendritic cells facilitates systemic murine norovirus persistence despite enhanced adaptive immunity. PLoS Pathogens 12: e1005684.
30. Oh, J.Z., Ravindran, R., Chassaing, B., Carvalho, F.A., Maddur, M.S., Bower, M., Hakimpour, P., Gill, K.P., Nakaya, H.I., Yarovinsky, F., Sartor, R.B., Gewirtz, A.T. and Pulendran, B., 2014. TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity 41: 478-492.
31. Pang, I.K. and Iwasaki, A., 2012. Control of antiviral immunity by pattern recognition and the microbiome. Immunological Reviews 245: 209-226.
32. Perumbakkam, S., Hunt, H.D. and Cheng, H.H., 2014. Marek's disease virus influences the core gut microbiome of the chicken during the early and late phases of viral replication. FEMS Microbiology Ecology 90: 300-312.
33. Perumbakkam, S., Hunt, H.D. and Cheng, H.H., 2016. Differences in CD8aa and cecal microbiome community during proliferation and late cytolytic phases of Marek's disease virus infection are associated with genetic resistance to Marek's disease. FEMS Microbiology Ecology 92: 188.
34. Post, J., Burt, D.W., Cornelissen, J.B., Broks, V., Van Zoelen, D., Peeters, B. and Rebel, J.M., 2012. Systemic virus distribution and host responses in brain and intestine of chickens infected with low pathogenic or high pathogenic avian influenza virus. Virology Journal 9: 61.
35. Price, G.E., Gaszewska-Mastarlarz, A. and Moskophidis, D., 2000. The role of alpha/beta and gamma interferons in development of immunity to influenza A virus in mice. Journal of Virology 74: 3996-4003.
36. Reemers, S.S., Koerkamp, M.J.G., Holstege, F.C., Van Eden, W. and Vervelde, L., 2009. Cellular host transcriptional responses to influenza A virus in chicken tracheal organ cultures differ from responses in in vivo infected trachea. Veterinary Immunology and Immunopathology 132: 91-100.
37. Ruiz-Hernandez, R., Mwangi, W., Peroval, M., Sadeyen, J.R., Ascough, S., Balkissoon, D., Staines, K., Boyd, A., McCauley, J., Smith, A. and Butter, C., 2016. Host genetics determine susceptibility to avian influenza infection and transmission dynamics. Scientific Reports 6: 26787.
38. Samuelson, D.R., Welsh, D.A. and Shellito, J.E., 2015. Regulation of lung immunity and host defense by the intestinal microbiota. Frontiers in Microbiology 6: 1085.
39. Santhakumar, D., Rubbenstroth, D., Martinez-Sobrido, L. and Munir, M., 2017. Avian interferons and their antiviral effectors. Frontiers in Immunology 8: 49.
40. Schuijt, T.J., Lankelma, J.M., Scicluna, B.P., De Melo, F.D.S., Roelofs, J.J., De Boer, J.D., Hoogendijk, A.J., De Beer, R., De Vos, A., Belzer, C., De Vos, W.M., Van der Poll, T. and Wiersinga, W.J., 2016. The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia. Gut 65: 575-583.
41. Singh, S.M., Alkie, T.N., Nagy, é., Kulkarni, R.R., Hodgins, D.C. and Sharif, S., 2016. Delivery of an inactivated avian influenza virus vaccine adjuvanted with poly (D, L-lactic-co-glycolic acid) encapsulated CpG ODN induces protective immune responses in chickens. Vaccine 34: 4807-4813.
42. Umar, S., Guerin, J.L. and Ducatez, M.F., 2016. Low pathogenic avian influenza and coinfecting pathogens: a review of experimental infections in avian models. Avian Diseases 61: 3-15.
43. Van de Sandt, C.E., Kreijtz, J.H.C.M. and Rimmelzwaan, G.F., 2012. Evasion of influenza A viruses from innate and adaptive immune responses. Viruses 4: 1438-1476.
44. Van den Broek, M.F., Müller, U., Huang, S., Aguet, M. and Zinkernagel, R.M., 1995. Antiviral defense in mice lacking both alpha/beta and gamma interferon receptors. Journal of Virology 69: 4792-4796.
45. Wilks, J. and Golovkina, T., 2012. Influence of microbiota on viral infections. PLoS Pathogens 8: e1002681.
46. Wu, S., Jiang, Z.Y., Sun, Y.F., Yu, B., Chen, J., Dai, C.Q., Wu, X.L., Tang, X.L. and Chen, X.Y., 2013. Microbiota regulates the TLR7 signaling pathway against respiratory tract influenza A virus infection. Current Microbiology 67: 414-422.
47. Yan, N. and Chen, Z.J., 2012. Intrinsic antiviral immunity. Nature Immunology 13: 214-222.
48. Yeoman, C.J., Chia, N., Jeraldo, P., Sipos, M., Goldenfeld, N.D. and White, B.A., 2012. The microbiome of the chicken gastrointestinal tract. Animal Health Research Reviews 13: 89-99.
49. Yitbarek, A., Echeverry, H., Brady, J., Hernandez-Doria, J., Camelo-Jaimes, G., Sharif, S., Guenter, W., House, J.D. and Rodriguez-Lecompte, J.C., 2012. Innate immune response to yeast-derived carbohydrates in broiler chickens fed organic diets and challenged with Clostridium perfringens. Poultry Science 91: 1105-1112.