Gene expression analysis of host innate immune responses during lethal H5N1 infection in ferrets

Journal of Virology

Volumn 82, Issue 22, 2008, Pages 11308-11317

  Cameron, Cheryl M ^a,b,c   Cameron, Mark J ^a,b,c   Bermejo Martin, Jesus F ^d   Ran, Longsi ^b   Xu, Luoling ^b   Turner, Patricia V ^e   Ran, Ran ^b   Danesh, Ali ^a,b,c   Fang, Yuan ^a,b,c   Chan, Pak Kei M ^a,b,c   Mytle, Nutan ^f   Sullivan, Timothy J ^g   Collins, Tassie L ^g   Johnson, Michael G ^g   Medina, Julio C ^g   Rowe, Thomas ^a,b,c   Kelvin, David J ^a,b,c  

^a SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF VALLADOLID   (Spain)

^e UNIVERSITY OF GUELPH   (Canada)

^f SOUTHERN RESEARCH INSTITUTE   (United States)

^g AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMG 487; ANTIVIRUS AGENT; CHEMOKINE RECEPTOR CXCR3; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFECT; DRUG RESPONSE; FERRET; GENE EXPRESSION; INFLUENZA; INFLUENZA VIRUS A H5N1; INFLUENZA VIRUS A H5N2; INNATE IMMUNITY; LUNG INFECTION; MALE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BIOSYNTHESIS; COMPARATIVE STUDY; DRUG ANTAGONISM; GENE EXPRESSION PROFILING; HUMAN; IMMUNOLOGY; INFLUENZA VIRUS A H3N2; LUNG; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; PHYSIOLOGY; SURVIVAL; VIROLOGY;

AVIAN INFLUENZA VIRUS; MUSTELA; ORTHOMYXOVIRIDAE;

ANIMALS; CHEMOKINE CXCL10; FERRETS; GENE EXPRESSION PROFILING; HUMANS; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; LUNG; MALE; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTORS, CXCR3; SURVIVAL ANALYSIS;

EID: 55549130267     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00691-08     Document Type: Article

References (44)

1. Abele, R., and R. Tampe. 2004. The ABCs of immunology: structure and function of TAP, the transporter associated with antigen processing. Physiology (Bethesda) 19:216-224.
2. Baras, B., K. J. Stittelaar, J. H. Simon, R. J. Thoolen, S. P. Mossman, F. H. Pistoor, G. van Amerongen, M. A. Wettendorff, E. Hanon, and A. D. Osterhaus. 2008. Cross-protection against lethal H5N1 challenge in ferrets with an adjuvanted pandemic influenza vaccine. PLoS One 3:e1401.
3. Baskin, C. R., A. Garcia-Sastre, T. M. Tumpey, H. Bielefeldt-Ohmann, V. S. Carter, E. Nistal-Villan, and M. G. Katze. 2004. Integration of clinical data, pathology, and cDNA microarrays in influenza virus-infected pigtailed macaques (Macaca nemestrina). J. Virol. 78:10420-10432.
4. Beebe, D. P., R. D. Schreiber, and N. R. Cooper. 1983. Neutralization of influenza virus by normal human sera: mechanisms involving antibody and complement. J. Immunol. 130:1317-1322.
5. Bjornson, A. B., M. A. Mellencamp, and G. M. Schiff. 1991. Complement is activated in the upper respiratory tract during influenza virus infection. Am. Rev. Respir. Dis. 143:1062-1066.
6. Cameron, M. J., J. F. Bermejo-Martin, A. Danesh, M. P. Muller, and D. J. Kelvin. 2008. Human immunopathogenesis of severe acute respiratory syndrome (SARS). Virus Res. 133:13-19.
7. Cameron, M. J., L. Ran, L. Xu, A. Danesh, J. F. Bermejo-Martin, C. M. Cameron, M. P. Muller, W. L. Gold, S. E. Richardson, S. M. Poutanen, B. M. Willey, M. E. Devries, Y. Fang, C. Seneviratne, S. E. Bosinger, D. Persad, P. Wilkinson, L. D. Greller, R. Somogyi, A. Humar, S. Keshavjee, M. Louie, M. B. Loeb, J. Brunton, A. J. McGeer, and D. J. Kelvin. 2007. Interferon-mediated immunopathological events are associated with atypical innate and adaptive immune responses in patients with severe acute respiratory syndrome. J. Virol. 81:8692-8706.
8. Chan, M. C., C. Y. Cheung, W. H. Chui, S. W. Tsao, J. M. Nicholls, Y. O. Chan, R. W. Chan, H. T. Long, L. L. Poon, Y. Guan, and J. S. Peiris. 2005. Proinflammatory cytokine responses induced by influenza A (H5N1) viruses in primary human alveolar and bronchial epithelial cells. Respir. Res. 6:135.
9. Cicardi, M., L. Zingale, A. Zanichelli, E. Pappalardo, and B. Cicardi. 2005. C1 inhibitor: molecular and clinical aspects. Springer Semin. Immunopathol. 27:286-298.
10. Deblandre, G. A., O. P. Marinx, S. S. Evans, S. Majjaj, O. Leo, D. Caput, G. A. Huez, and M. G. Wathelet. 1995. Expression cloning of an interferon-inducible 17-kDa membrane protein implicated in the control of cell growth. J. Biol. Chem. 270:23860-23866.
11. de Jong, M. D., C. P. Simmons, T. T. Thanh, V. M. Hien, G. J. Smith, T. N. Chau, D. M. Hoang, N. V. Chau, T. H. Khanh, V. C. Dong, P. T. Qui, B. V. Cam, D. Q. Ha, Y. Guan, J. S. Peiris, N. T. Chinh, T. T. Hien, and J. Farrar. 2006. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 12:1203-1207.
12. de Veer, M. J., M. Holko, M. Frevel, E. Walker, S. Der, J. M. Paranjape, R. H. Silverman, and B. R. Williams. 2001. Functional classification of interferon-stimulated genes identified using microarrays. J. Leukoc. Biol. 69:912-920.
13. Frederiksen, P. D., S. Thiel, C. B. Larsen, and J. C. Jensenius. 2005. M-ficolin, an innate immune defence molecule, binds patterns of acetyl groups and activates complement. Scand. J. Immunol. 62:462-473.
14. Ghai, R., P. Waters, L. T. Roumenina, M. Gadjeva, M. S. Kojouharova, K. B. Reid, R. B. Sim, and U. Kishore. 2007. C1q and its growing family. Immunobiology 212:253-266.
15. Govorkova, E. A., J. E. Rehg, S. Krauss, H. L. Yen, Y. Guan, M. Peiris, T. D. Nguyen, T. H. Hanh, P. Puthavathana, H. T. Long, C. Buranathai, W. Lim, R. G. Webster, and E. Hoffman. 2006. Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J. Virol. 80:6195.
16. Itoh, Y., H. Ozaki, H. Tsuchiya, K. Okamoto, R. Torii, Y. Sakoda, Y. Kawaoka, K. Ogasawara, and H. Kida. 2008. A vaccine prepared from a non-pathogenic H5N1 avian influenza virus strain confers protective immunity against highly pathogenic avian influenza virus infection in cynomolgus macaques. Vaccine 26:562-572.
17. Itsui, Y., N. Sakamoto, M. Kurosaki, N. Kanazawa, Y. Tanabe, T. Koyama, Y. Takeda, M. Nakagawa, S. Kakinuma, Y. Sekine, S. Maekawa, N. Enomoto, and M. Watanabe. 2006. Expressional screening of interferon-stimulated genes for antiviral activity against hepatitis C virus replication. J. Viral Hepat. 13:690-700.
18. Jefferson, T., D. Rivetti, A. Rivetti, M. Rudin, C. Di Pietrantonj, and V. Demicheli. 2005. Efficacy and effectiveness of influenza vaccines in elderly people: a systematic review. Lancet 366:1165-1174.
19. Johnson, M., A. R. Li, J. Liu, Z. Fu, L. Zhu, S. Miao, X. Wang, Q. Xu, A. Huang, A. Marcus, F. Xu, K. Ebsworth, E. Sablan, J. Danao, J. Kumer, D. Dairaghi, C. Lawrence, T. Sullivan, G. Tonn, T. Schall, T. Collins, and J. Medina. 2007. Discovery and optimization of a series of quinazolinone- derived antagonists of CXCR3. Bioorg. Med. Chem. Lett. 17:3339-3343.
20. Kandun, I. N., H. Wibisono, E. R. Sedyaningsih, Yusharmen, W. Hadisoedarsuno, W. Purba, H. Santoso, C. Septiawati, E. Tresnaningsih, B. Heriyanto, D. Yuwono, S. Harun, S. Soeroso, S. Giriputra, P. J. Blair, A. Jeremijenko, H. Kosasih, S. D. Putnam, G. Samaan, M. Silitonga, K. H. Chan, L. L. Poon, W. Lim, A. Klimov, S. Lindstrom, Y. Guan, R. Donis, J. Katz, N. Cox, M. Peiris, and T. M. Uyeki. 2006. Three Indonesian clusters of H5N1 virus infection in 2005. N. Engl. J. Med. 355:2186-2194.
21. Kawada, J., H. Kimura, Y. Kamachi, K. Nishikawa, M. Taniguchi, K. Nagaoka, H. Kurahashi, S. Kojima, and T. Morishima. 2006. Analysis of gene-expression profiles by oligonucleotide microarray in children with influenza. J. Gen. Virol. 87:1677-1683.
22. Kobasa, D., S. M. Jones, K. Shinya, J. C. Kash, J. Copps, H. Ebihara, Y. Hatta, J. H. Kim, P. Halfmann, M. Hatta, F. Feldmann, J. B. Alimonti, L. Fernando, Y. Li, M. G. Katze, H. Feldmann, and Y. Kawaoka. 2007. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445:319-323.
23. Kopf, M., B. Abel, A. Gallimore, M. Carroll, and M. F. Bachmann. 2002. Complement component C3 promotes T-cell priming and lung migration to control acute influenza virus infection. Nat. Med. 8:373-378.
24. Leek, J. T., E. Monsen, A. R. Dabney, and J. D. Storey. 2006. EDGE: extraction and analysis of differential gene expression. Bioinformatics 22:507-508.
25. Leonard, W. J., and J. J. O'Shea. 1998. Jaks and STATs: biological implications. Annu. Rev. Immunol. 16:293-322.
26. Liu, Y., Y. Endo, D. Iwaki, M. Nakata, M. Matsushita, I. Wada, K. Inoue, M. Munakata, and T. Fujita. 2005. Human M-ficolin is a secretory protein that activates the lectin complement pathway. J. Immunol. 175:3150-3156.
27. Liu, Y. C., J. Penninger, and M. Karin. 2005. Immunity by ubiquitylation: a reversible process of modification. Nat. Rev. Immunol. 5:941-952.
28. Muhlbauer, M., M. Fleck, C. Schutz, T. Weiss, M. Froh, C. Blank, J. Scholmerich, and C. Hellerbrand. 2006. PD-L1 is induced in hepatocytes by viral infection and by interferon-alpha and -gamma and mediates T cell apoptosis. J. Hepatol. 45:520-528.
29. Neville, L. F., G. Mathiak, and O. Bagasra. 1997. The immunobiology of interferon-gamma inducible protein 10 kD (IP-10): a novel, pleiotropic member of the C-X-C chemokine superfamily. Cytokine Growth Factor Rev. 8:207-219.
30. Pennings, J. L., T. G. Kimman, and R. Janssen. 2008. Identification of a common gene expression response in different lung inflammatory diseases in rodents and macaques. PLoS One 3:e2596.
31. Salomon, R., J. Franks, E. A. Govorkova, N. A. Ilyushina, H. L. Yen, D. J. Hulse-Post, J. Humberd, M. Trichet, J. E. Rehg, R. J. Webby, R. G. Webster, and E. Hoffmann. 2006. The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J. Exp. Med. 203:689-697.
32. Salomon, R., E. Hoffmann, and R. G. Webster. 2007. Inhibition of the cytokine response does not protect against lethal H5N1 influenza infection. Proc. Natl. Acad. Sci. 104:12479-12481.
33. Szretter, K. J., S. Gangappa, X. Lu, C. Smith, W. J. Shieh, S. R. Zaki, S. Sambhara, T. M. Tumpey, and J. M. Katz. 2007. Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J. Virol. 81:2736-2744.
34. Takaoka, A., and H. Yanai. 2006. Interferon signalling network in innate defence. Cell. Microbiol. 8:907-922.
35. To, K. F., P. K. Chan, K. F. Chan, W. K. Lee, W. Y. Lam, K. F. Wong, N. L. Tang, D. N. Tsang, R. Y. Sung, T. A. Buckley, J. S. Tam, and A. F. Cheng. 2001. Pathology of fatal human infection associated with avian influenza A H5N1 virus. J. Med. Virol. 63:242-246.
36. Tominaga, N., K. Ohkusu-Tsukada, H. Udono, R. Abe, T. Matsuyama, and K. Yui. 2003. Development of Th1 and not Th2 immune responses in mice lacking IFN-regulatory factor-4. Int. Immunol. 15:1-10.
37. Ungchusak, K., P. Auewarakul, S. F. Dowell, R. Kitphati, W. Auwanit, P. Puthavathana, M. Uiprasertkul, K. Boonnak, C. Pittayawonganon, N. J. Cox, S. R. Zaki, P. Thawatsupha, M. Chittaganpitch, R. Khontong, J. M. Simmerman, and S. Chunsutthiwat. 2005. Probable person-to-person transmission of avian influenza A (H5N1). N. Engl. J. Med. 352:333-340.
38. Walser, T. C., S. Rifat, X. Ma, N. Kundu, C. Ward, O. Goloubeva, M. G. Johnson, J. C. Medina, T. L. Collins, and A. M. Fulton. 2006. Antagonism of CXCR3 inhibits lung metastasis in a murine model of metastatic breast cancer. Cancer Res. 66:7701-7707.
39. Wijtmans, M., D. Verzijl, R. Leurs, I. J. de Esch, and M. J. Smit. 2008. Towards small-molecule CXCR3 ligands with clinical potential. Chem. Med. Chem. 3:861-872.
40. Writing Committee of the Second World Health Organization Consultation on Clinical Aspects of Human Infection with Avian Influenza. 2008. Update on avian influenza A (H5N1) virus infection in humans. N. Engl. J. Med. 358:261-273.
41. Yuan, W., and R. M. Krug. 2001. Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. EMBO J. 20:362-371.
42. Zangwill, K. M., J. J. Treanor, J. D. Campbell, D. L. Noah, and J. Ryea. 2008. Evaluation of the safety and immunogenicity of a booster (third) dose of inactivated subvirion H5N1 influenza vaccine in humans. J. Infect. Dis.
43. Zhang, H., Y. A. Su, P. Hu, J. Yang, B. Zheng, P. Wu, J. Peng, Y. Tang, and L. Zhang. 2006. Signature patterns revealed by microarray analyses of mice infected with influenza virus A and Streptococcus pneumoniae. Microbes. Infect. 8:2172-2185.
44. Zitzow, L. A., T. Rowe, T. Morken, W. J. Shieh, S. Zaki, and J. M. Katz. 2002. Pathogenesis of avian influenza A (H5N1) viruses in ferrets. J. Virol. 76:4420-4429.