Essential impact of NF-κB signaling on the H5N1 influenza A virus-induced transcriptome

Journal of Immunology

Volumn 183, Issue 8, 2009, Pages 5180-5189

  Schmolke, Mirco ^a   Viemann, Dorothee ^b   Roth, Johannes ^b   Ludwig, Stephan ^a  

^a INST OF REPRO MED OF THE UNIV   (Germany)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; TRANSCRIPTOME;

ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; ENDOTHELIUM CELL; HOST CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNE RESPONSE; INFLAMMATION; INFLUENZA VIRUS A H5N1; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

CELL LINE; ENDOTHELIAL CELLS; GENE EXPRESSION PROFILING; HUMANS; I-KAPPA B KINASE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA, HUMAN; INTERFERON-BETA; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION;

EID: 77954124395     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0804198     Document Type: Article

References (67)

1. Pollack, C. V., Jr., C. W. Kam, and Y. K. Mak. 1998. Update: isolation of avian influenza A(H5N1) viruses from human beings-Hong Kong, 1997-1998. Ann. Emerg. Med. 31: 647-649.
2. Uyeki, T. M. 2008. Global epidemiology of human infections with highly pathogenic avian influenza A (H5N1) viruses. Respirology 13(Suppl. 1): S2-S9.
3. Hsieh, Y. C., T. Z. Wu, D. P. Liu, P. L. Shao, L. Y. Chang, C. Y. Lu, C. Y. Lee, F. Y. Huang, and L. M. Huang. 2006. Influenza pandemics: past, present and future. J. Formos. Med. Assoc. 105: 1-6.
4. Cheung, C. Y., L. L. Poon, A. S. Lau, W. Luk, Y. L. Lau, K. F. Shortridge, S. Gordon, Y. Guan, and J. S. Peiris. 2002. Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? Lancet 360: 1831-1837.
5. Tran, T. H., T. L. Nguyen, T. D. Nguyen, T. S. Luong, P. M. Pham, V. C. Nguyen, T. S. Pham, C. D. Vo, T. Q. Le, T. T. Ngo, et al. 2004. Avian influenza A (H5N1) in 10 patients in Vietnam. N. Engl. J. Med. 350: 1179-1188.
6. Lee, D. C., C. Y. Cheung, A. H. Law, C. K. Mok, M. Peiris, and A. S. Lau. 2005. p38 mitogen-activated protein kinase-dependent hyperinduction of tumor necrosis factor α expression in response to avian influenza virus H5N1. J. Virol. 79: 10147-10154.
7. Danese, S., E. Dejana, and C. Fiocchi. 2007. Immune regulation by microvascular endothelial cells: directing innate and adaptive immunity, coagulation, and inflammation. J. Immunol. 178: 6017-6022.
8. Feldmann, A., M. K. Schafer, W. Garten, and H. D. Klenk. 2000. Targeted infection of endothelial cells by avian influenza virus A/FPV/Rostock/34 (H7N1) in chicken embryos. J. Virol. 74: 8018-8027.
9. Klenk, H. D. 2005. Infection of the endothelium by influenza viruses. Thromb. Haemost. 94: 262-265.
10. Claas, E. C., A. D. Osterhaus, R. van Beek, J. C. De Jong, G. F. Rimmelzwaan, D. A. Senne, S. Krauss, K. F. Shortridge, and R. G. Webster. 1998. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351: 472-477.
11. Deng, R., M. Lu, C. Korteweg, Z. Gao, M. A. McNutt, J. Ye, T. Zhang, and J. Gu. 2008. Distinctly different expression of cytokines and chemokines in the lungs of two H5N1 avian influenza patients. J. Pathol. 216: 328-336.
12. Pichlmair, A., O. Schulz, C. P. Tan, T. I. Naslund, P. Liljestrom, F. Weber, and C. Reis e Sousa. 2006. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314: 997-1001.
13. Fitzgerald, K. A., S. M. McWhirter, K. L. Faia, D. C. Rowe, E. Latz, D. T. Golenbock, A. J. Coyle, S. M. Liao, and T. Maniatis. 2003. IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4: 491-496.
14. Hiscott, J. 2007. Triggering the innate antiviral response through IRF-3 activation. J. Biol. Chem. 282: 15325-15329.
15. Sharma, S., B. R. tenOever, N. Grandvaux, G. P. Zhou, R. Lin, and J. Hiscott. 2003. Triggering the interferon antiviral response through an IKK-related pathway. Science 300: 1148-1151.
16. DiDonato, J. A., M. Hayakawa, D. M. Rothwarf, E. Zandi, and M. Karin. 1997. A cytokine-responsive IκB kinase that activates the transcription factor NF-κB. Nature 388: 548-554.
17. Panne, D., T. Maniatis, and S. C. Harrison. 2007. An atomic model of the interferon-β enhanceosome. Cell 129: 1111-1123.
18. Wathelet, M. G., C. H. Lin, B. S. Parekh, L. V. Ronco, P. M. Howley, and T. Maniatis. 1998. Virus infection induces the assembly of coordinately activated transcription factors on the IFN-β enhancer in vivo. Mol. Cell 1: 507-518.
19. Imaizumi, T., M. Hatakeyama, K. Yamashita, A. Ishikawa, H. Yoshida, K. Satoh, K. Taima, F. Mori, and K. Wakabayashi. 2005. Double-stranded RNA induces the synthesis of retinoic acid-inducible gene-I in vascular endothelial cells. Endothelium 12: 133-137.
20. Levy, D. E., I. Marie, E. Smith, and A. Prakash. 2002. Enhancement and diversification of IFN induction by IRF-7-mediated positive feedback. J. Interferon Cytokine Res. 22: 87-93.
21. Rebouillat, D., and A. G. Hovanessian. 1999. The human 2′,5′-oligoadenylate synthetase family: interferon-induced proteins with unique enzymatic properties. J. Interferon Cytokine Res. 19: 295-308.
22. Takaoka, A., and H. Yanai. 2006. Interferon signalling network in innate defence. Cell Microbiol. 8: 907-922.
23. Turan, K., M. Mibayashi, K. Sugiyama, S. Saito, A. Numajiri, and K. Nagata. 2004. Nuclear MxA proteins form a complex with influenza virus NP and inhibit the transcription of the engineered influenza virus genome. Nucleic Acids Res. 32: 643-652.
24. Kim, T. K., and T. Maniatis. 1997. The mechanism of transcriptional synergy of an in vitro assembled interferon-β enhanceosome. Mol. Cell 1: 119-129.
25. Wang, X., S. Hussain, E. J. Wang, X. Wang, M. O. Li, A. Garcia-Sastre, and A. A. Beg. 2007. Lack of essential role of NF-κB p50, RelA, and cRel subunits in virus-induced type 1 IFN expression. J. Immunol. 178: 6770-6776.
26. Wei, L., M. R. Sandbulte, P. G. Thomas, R. J. Webby, R. Homayouni, and L. M. Pfeffer. 2006. NFκB negatively regulates interferon-induced gene expression and anti-influenza activity. J. Biol. Chem. 281: 11678-11684.
27. Hiscott, J. 2007. Convergence of the NF-κB and IRF pathways in the regulation of the innate antiviral response. Cytokine Growth Factor Rev. 18: 483-490.
28. Denk, A., M. Goebeler, S. Schmid, I. Berberich, O. Ritz, D. Lindemann, S. Ludwig, and T. Wirth. 2001. Activation of NF-κB via the IκB kinase complex is both essential and sufficient for proinflammatory gene expression in primary endothelial cells. J. Biol. Chem. 276: 28451-28458.
29. Viemann, D., M. Goebeler, S. Schmid, K. Klimmek, C. Sorg, S. Ludwig, and J. Roth. 2004. Transcriptional profiling of IKK2/NF-κB- and p38 MAP kinase-dependent gene expression in TNF-α-stimulated primary human endothelial cells. Blood 103: 3365-3373.
30. Viemann, D., M. Schmidt, K. Tenbrock, S. Schmid, V. Muller, K. Klimmek, S. Ludwig, J. Roth, and M. Goebeler. 2007. The contact allergen nickel triggers a unique inflammatory and proangiogenic gene expression pattern via activation of NF-κB and hypoxia-inducible factor-1α. J. Immunol. 178: 3198-3207. (Pubitemid 46333202)
31. Wurzer, W. J., C. Ehrhardt, S. Pleschka, F. Berberich-Siebelt, T. Wolff, H. Walczak, O. Planz, and S. Ludwig. 2004. NF-κB-dependent induction of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and Fas/FasL is crucial for efficient influenza virus propagation. J. Biol. Chem. 279: 30931-30937.
32. Olschlager, V., S. Pleschka, T. Fischer, H. J. Rziha, W. Wurzer, L. Stitz, U. R. Rapp, S. Ludwig, and O. Planz. 2004. Lung-specific expression of active Raf kinase results in increased mortality of influenza A virus-infected mice. Oncogene 23: 6639-6646.
33. Ehrhardt, C., M. Schmolke, A. Matzke, A. Knoblauch, C. Will, V. Wixler, and S. Ludwig. 2006. Polyethyleneimine, a cost-effective transfection reagent. Signal Transduction 6: 179-184.
34. Ehrhardt, C., T. Wolff, S. Pleschka, O. Planz, W. Beermann, J. G. Bode, M. Schmolke, and S. Ludwig. 2007. Influenza A virus NS1 protein activates the PI3K/Akt pathway to mediate antiapoptotic signaling responses. J. Virol. 81: 3058-3067.
35. T) method. Methods 25: 402-408.
36. Alter, O., P. O. Brown, and D. Botstein. 2000. Singular value decomposition for genome-wide expression data processing and modeling. Proc. Natl. Acad. Sci. USA 97: 10101-10106.
37. Haverty, P. M., M. C. Frith, and Z. Weng. 2004. CARRIE web service: automated transcriptional regulatory network inference and interactive analysis. Nucleic Acids Res. 32: W213-216.
38. Katze, M. G., and R. M. Krug. 1984. Metabolism and expression of RNA polymerase II transcripts in influenza virus-infected cells. Mol. Cell. Biol. 4: 2198-2206. (Pubitemid 15209994)
39. Qiu, Y., and R. M. Krug. 1994. The influenza virus NS1 protein is a poly(A)-binding protein that inhibits nuclear export of mRNAs containing poly(A). J. Virol. 68: 2425-2432. (Pubitemid 24091922)
40. Barkett, M., and T. D. Gilmore. 1999. Control of apoptosis by Rel/NF-κB transcription factors. Oncogene 18: 6910-6924.
41. DeMeester, S. L., Y. Qiu, T. G. Buchman, R. S. Hotchkiss, K. Dunnigan, I. E. Karl, and J. P. Cobb. 1998. Nitric oxide inhibits stress-induced endothelial cell apoptosis. Crit. Care Med. 26: 1500-1509.
42. Mazur, I., W. J. Wurzer, C. Ehrhardt, S. Pleschka, P. Puthavathana, T. Silberzahn, T. Wolff, O. Planz, and S. Ludwig. 2007. Acetylsalicylic acid (ASA) blocks influenza virus propagation via its NF-κB-inhibiting activity. Cell Microbiol. 9: 1683-1694.
43. de Haan, J. R., R. Wehrens, S. Bauerschmidt, E. Piek, R. C. van Schaik, and L. M. Buydens. 2007. Interpretation of ANOVA models for microarray data using PCA. Bioinformatics 23: 184-190.
44. Spackman, E., D. A. Senne, T. J. Myers, L. L. Bulaga, L. P. Garber, M. L. Perdue, K. Lohman, L. T. Daum, and D. L. Suarez. 2002. Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. J. Clin. Microbiol. 40: 3256-3260.
45. Hu, X., S. D. Chakravarty, and L. B. Ivashkiv. 2008. Regulation of interferon and Toll-like receptor signaling during macrophage activation by opposing feedforward and feedback inhibition mechanisms. Immunol. Rev. 226: 41-56.
46. Malmgaard, L. 2004. Induction and regulation of IFNs during viral infections. J. Interferon Cytokine Res. 24: 439-454. (Pubitemid 39120592)
47. Sato, M., N. Hata, M. Asagiri, T. Nakaya, T. Taniguchi, and N. Tanaka. 1998. Positive feedback regulation of type I IFN genes by the IFN-inducible transcription factor IRF-7. FEBS Lett. 441: 106-110.
48. 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. USA 104: 12479-12481.
49. Sumikoshi, M., K. Hashimoto, Y. Kawasaki, H. Sakuma, T. Suzutani, H. Suzuki, and M. Hosoya. 2008. Human influenza virus infection and apoptosis induction in human vascular endothelial cells. J. Med. Virol. 80: 1072-1078.
50. Rimmelzwaan, G. F., D. van Riel, M. Baars, T. M. Bestebroer, G. van Amerongen, R. A. Fouchier, A. D. Osterhaus, and T. Kuiken. 2006. Influenza A virus (H5N1) infection in cats causes systemic disease with potential novel routes of virus spread within and between hosts. Am. J. Pathol. 168: 176-183, quiz 364.
51. Indraccolo, S., U. Pfeffer, S. Minuzzo, G. Esposito, V. Roni, S. Mandruzzato, N. Ferrari, L. Anfosso, R. Dell'Eva, D. M. Noonan, et al. 2007. Identification of genes selectively regulated by IFNs in endothelial cells. J. Immunol. 178: 1122-1135.
52. Melchjorsen, J., H. Kristiansen, R. Christiansen, J. Rintahaka, S. Matikainen, S. R. Paludan, and R. Hartmann. 2009. Differential regulation of the OASL and OAS1 genes in response to viral infections. J. Interferon Cytokine Res.
53. Geiss, G. K., M. C. An, R. E. Bumgarner, E. Hammersmark, D. Cunningham, and M. G. Katze. 2001. Global impact of influenza virus on cellular pathways is mediated by both replication-dependent and -independent events. J. Virol. 75: 4321-4331.
54. Flory, E., M. Kunz, C. Scheller, C. Jassoy, R. Stauber, U. R. Rapp, and S. Ludwig. 2000. Influenza virus-induced NF-κB-dependent gene expression is mediated by overexpression of viral proteins and involves oxidative radicals and activation of IκB kinase. J. Biol. Chem. 275: 8307-8314.
55. Pahl, H. L., and P. A. Baeuerle. 1995. Expression of influenza virus hemagglutinin activates transcription factor NF-κB. J. Virol. 69: 1480-1484.
56. 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.
57. Keeler, C. L., Jr., T. W. Bliss, M. Lavric, and M. N. Maughan. 2007. A functional genomics approach to the study of avian innate immunity. Cytogenet. Genome Res. 117: 139-145.
58. Wang, G., J. Zhang, W. Li, G. Xin, Y. Su, Y. Gao, H. Zhang, G. Lin, X. Jiao, and K. Li. 2008. Apoptosis and proinflammatory cytokine responses of primary mouse microglia and astrocytes induced by human H1N1 and avian H5N1 influenza viruses. Cell Mol. Immunol. 5: 113-120.
59. Cameron, C. M., M. J. Cameron, J. F. Bermejo-Martin, L. Ran, L. Xu, P. V. Turner, R. Ran, A. Danesh, Y. Fang, P. K. Chan, et al. 2008. Gene expression analysis of host innate immune responses during lethal H5N1 infection in ferrets. J. Virol. 82: 11308-11317.
60. Kash, J. C., C. F. Basler, A. Garcia-Sastre, V. Carter, R. Billharz, D. E. Swayne, R. M. Przygodzki, J. K. Taubenberger, M. G. Katze, and T. M. Tumpey. 2004. Global host immune response: pathogenesis and transcriptional profiling of type A influenza viruses expressing the hemagglutinin and neuraminidase genes from the 1918 pandemic virus. J. Virol. 78: 9499-9511.
61. Kobasa, D., S. M. Jones, K. Shinya, J. C. Kash, J. Copps, H. Ebihara, Y. Hatta, J. H. Kim, P. Halfmann, M. Hatta, et al. 2007. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445: 319-323.
62. Nimmerjahn, F., D. Dudziak, U. Dirmeier, G. Hobom, A. Riedel, M. Schlee, L. M. Staudt, A. Rosenwald, U. Behrends, G. W. Bornkamm, and J. Mautner. 2004. Active NF-κB signalling is a prerequisite for influenza virus infection. J. Gen. Virol. 85: 2347-2356.
63. Wurzer, W. J., O. Planz, C. Ehrhardt, M. Giner, T. Silberzahn, S. Pleschka, and S. Ludwig. 2003. Caspase 3 activation is essential for efficient influenza virus propagation. EMBO J. 22: 2717-2728.
64. Kumar, N., Z. Xin, Y. Liang, H. Ly, and Y. Liang. 2008. NF-κB signaling differentially regulates influenza viral RNA synthesis. J. Virol. 82: 9880-9889.
65. Thanos, D., and T. Maniatis. 1995. Virus induction of human IFN β gene expression requires the assembly of an enhanceosome. Cell 83: 1091-1100.
66. Grandvaux, N., M. J. Servant, B. tenOever, G. C. Sen, S. Balachandran, G. N. Barber, R. Lin, and J. Hiscott. 2002. Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J. Virol. 76: 5532-5539.
67. Schafer, S. L., R. Lin, P. A. Moore, J. Hiscott, and P. M. Pitha. 1998. Regulation of type I interferon gene expression by interferon regulatory factor-3. J. Biol. Chem. 273: 2714-2720.