Sendai virus targets inflammatory responses, as well as the interferon-induced antiviral state, In a multifaceted manner

Journal of Virology

Volumn 77, Issue 14, 2003, Pages 7903-7913

  Strähle, Laura ^a   Garcin, Dominique ^a   Le Mercier, Philippe ^a   Schlaak, Joerg F ^b,c   Kolakofsky, Daniel ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; INTERFERON; INTERLEUKIN 6; INTERLEUKIN 8; PROTEIN C;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CELL STIMULATION; GENE ACTIVATION; GENE TARGETING; IMMUNE RESPONSE; INFLAMMATION; MESSENGER RNA SYNTHESIS; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SENDAI VIRUS; VIRUS GENE; VIRUS GENOME; VIRUS REPLICATION;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; IMMUNITY, ACTIVE; INFLAMMATION; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; INTERFERONS; INTERLEUKIN-6; INTERLEUKIN-8; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SENDAI VIRUS; TRANSCRIPTION FACTORS; VIRAL PROTEINS;

EID: 0038421005     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.14.7903-7913.2003     Document Type: Article

References (69)

1. Bieback, K., E. Lien, I. M. Klagge, E. Avota, J. Schneider-Schaulies, W. P. Duprex, H. Wagner, C. J. Kirschning, V. ter Meulen, and S. Schneider-Schaulies. 2002. Hemagglutinin protein of wild-type measles virus activates toll-like receptor 2 signaling. J. Virol. 76:8729-8736.
2. Biron, C. A., and G. C. Sen. 2001. Interferons and other cytokines, p. 321-349. In D. M. Knipe and P. M. Howley (ed.), Fields virology. Lippincott, Williams, and Wilkins, Philadelphia, Pa.
3. Bosch, I., K. Xhaja, L. Estevez, G. Raines, H. Melichar, R. V. Warke, M. V. Fournier, F. A. Ennis, and A. L. Rothman. 2002. Increased production of interleukin-8 in primary human monocytes and in human epithelial and endothelial cell lines after dengue virus challenge. J. Virol. 76:5588-5597.
4. Cadd, T., D. Garcin, C. Tapparel, M. Itoh, M. Homma, L. Roux, J. Curran, and D. Kolakofsky. 1996. The Sendai paramyxovirus accessory C proteins inhibit viral genome amplification in a promoter-specific fashion. J. Virol. 70:5067-5074.
5. Casola, A., R. P. Garofalo, M. Jamaluddin, S. Vlahopoulos, and A. R. Brasier. 2000. Requirement of a novel upstream response element in respiratory syncytial virus-induced IL-8 gene expression. J. Immunol. 164:5944-5951.
6. Chen, Z., and R. M. Krug. 2000. Selective nuclear export of viral mRNAs in influenza-virus-infected cells. Trends Microbiol. 8:376-383.
7. Darnell, J. E. J. 1997. STATs and gene regulation. Science 277:1630-1635.
8. Delenda, C., S. Hausmann, D. Garcin, and D. Kolakofsky. 1997. Normal cellular replication of Sendai virus without the trans-frame, nonstructural V protein. Virology 228:55-62.
9. Denk, A., M. Goebeler, S. Schmid, I. Berberich, O. Ritz, D. Lindemann, S. Ludwig, and T. Wirth. 2001. Activation of NF-kappa B via the Ikappa B kinase complex is both essential and sufficient for proinflammatory gene expression in primary endothelial cells. J. Biol. Chem. 276:28451-28458.
10. 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. USA 95:15623-15628.
11. Feldmann, H., and H. D. Klenk. 1996. Marburg and Ebola viruses. Adv. Virus Res. 47:1-52.
12. Fujii, Y., K. Kiyotani, T. Yoshida, and T. Sakaguchi. 2001. Conserved and non-conserved regions in the Sendai virus genome: evolution of a gene possessing overlapping reading frames. Virus Genes 22:47-52.
13. Gao, J. L., and P. M. Murphy. 1994. Human cytomegalovirus open reading frame US28 encodes a functional beta chemokine receptor. J. Biol. Chem. 269:28539-28542.
14. Garcin, D., J. Curran, M. Itoh, and D. Kolakofsky. 2001. Longer and shorter forms of Sendai virus C proteins play different roles in modulating the cellular antiviral response. J. Virol. 75:6800-6807.
15. Garcin, D., M. Itoh, and D. Kolakofsky. 1997. A point mutation in the Sendai virus accessory C proteins attenuates virulence for mice, but not virus growth in cell culture. Virology 238:424-431.
16. Garcin, D., P. Latorre, and D. Kolakofsky. 1999. Sendai virus C proteins counteract the interferon-mediated induction of an antiviral state. J. Virol. 73:6559-6565.
17. Garcin, D., J. B. Marq, S. Goodbourn, and D. Kolakofsky. 2003. The amino-terminal extensions of the longer Sendai virus C proteins modulate pY701-Stat1 and bulk Stat1 levels independently of interferon signaling. J. Virol. 77:2321-2329.
18. Garcin, D., J. B. Marq, L. Strahle, P. Le Mercier, and D. Kolakofsky. 2002. All four Sendai virus C proteins bind Stat1, but only the larger forms also induce its mono-ubiquitination and degradation. Virology 295:256-265.
19. Garcin, D., T. Pelet, P. Calain, L. Roux, J. Curran, and D. Kolakofsky. 1995. A highly recombinogenic system for the recovery of infectious Sendai paramyxovirus from cDNA: generation of a novel copy-back nondefective interfering virus. EMBO J. 14:6087-6094.
20. Garcin, D., G. Taylor, K. Tanebayashi, R. Compans, and D. Kolakofsky. 1998. The short Sendai virus leader region controls induction of programmed cell death. Virology 243:340-353.
21. Garofalo, R., M. Sabry, M. Jamaluddin, R. K. Yu, A. Casola, P. L. Ogra, and A. R. Brasier. 1996. Transcriptional activation of the interleukin-8 gene by respiratory syncytial virus infection in alveolar epithelial cells: nuclear translocation of the RelA transcription factor as a mechanism producing airway mucosal inflammation. J. Virol. 70:8773-8781.
22. Geiss, G., G. Jin, J. Guo, R. Bumgarner, M. G. Katze, and G. C. Sen. 2001. A comprehensive view of regulation of gene expression by double-stranded RNA-mediated cell signaling. J. Biol. Chem. 276:30178-30182.
23. Genin, P., M. Algarte, P. Roof, R. Lin, and J. Hiscott. 2000. Regulation of RANTES chemokine gene expression requires cooperativity between NF-kappa B and IFN-regulatory factor transcription factors. J. Immunol. 164: 5352-5361.
24. Goodbourn, S., L. Didcock, and R. E. Randall. 2000. Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 81:2341-2364.
25. Hasan, M. K., A. Kato, M. Muranaka, R. Yamaguchi, Y. Sakai, I. Hatano, M. Tashiro, and Y. Nagai. 2000. Versatility of the accessory C proteins of Sendai virus: contribution to virus assembly as an additional role. J. Virol. 74:5619-5628.
26. He, B., R. G. Paterson, N. Stock, J. E. Durbin, R. K. Durbin, S. Goodbourn, R. E. Randall, and R. A. Lamb. 2002. Recovery of paramyxovirus simian virus 5 with a V protein lacking the conserved cysteine-rich domain: the multifunctional V protein blocks both interferon-beta induction and interferon signaling. Virology 303:15-32.
27. Hobert, M. E., K. A. Sands, R. J. Mrsny, and J. L. Madara. 2002. Cdc42 and Rac1 regulate late events in Salmonella typhimurium-induced interleukin-8 secretion from polarized epithelial cells. J. Biol. Chem. 277: 51025-51032.
28. Iseni, F., D. Garcin, M. Nishio, N. Kedersha, P. Anderson, and D. Kolakofsky. 2002. Sendai virus trailer RNA binds TIAR, a cellular protein involved in virus-induced apoptosis. EMBO J. 21:5141-5150.
29. Ishida, N., and M. Homma. 1978. Sendai virus. Adv. Virus Res. 23:349-383.
30. Israel, A. 2000. The IKK complex: an integrator of all signals that activate NF-kappaB? Trends Cell Biol. 10:129-133.
31. Itoh, M., Y. Isegawa, H. Hotta, and M. Homma. 1997. Isolation of an avirulent mutant of Sendai virus with two amino acid mutations from a highly virulent field strain through adaptation to LLC-MK2 cells. J. Gen Virol. 78:3207-3215.
32. Jacobs, B. L., and J. O. Langland. 1996. When two strands are better than one: the mediators and modulators of the cellular responses to double-stranded RNA. Virology 219:339-349.
33. Karin, M., and Y. Ben Neriah. 2000. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu. Rev. Immunol. 18:621-663.
34. Kato, A., K. Kiyotani, K. Sakai, T. Yoshida, and Y. Nagai. 1997. The paramyxovirus, Sendai virus, V protein encodes a luxury function required for viral pathogenesis. EMBO J. 16:578-685.
35. King, P., and S. Goodbourn. 1994. The beta-interferon promoter responds to priming through multiple independent regulatory elements. J. Biol. Chem. 269:30609-30615.
36. Kurt-Jones, E. A., L. Popova, L. Kwinn, L. M. Haynes, L. P. Jones, R. A. Tripp, E. E. Walsh, M. W. Freeman, D. T. Golenbock, L. J. Anderson, and R. W. Finberg. 2000. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1:398-401.
37. Latorre, P., T. Cadd, M. Itoh, J. Curran, and D. Kolakofsky. 1998. The various Sendai virus C proteins are not functionally equivalent and exert both positive and negative effects on viral RNA accumulation during the course of infection. J. Virol. 72:5984-5993.
38. Le Mercier, P., D. Garcin, S. Hausmann, and D. Kolakofsky. 2002. Ambisense Sendai viruses are inherently unstable but are useful to study viral RNA synthesis. J. Virol. 76:5492-5502.
39. Lillemeier, B. F., M. Koster, and I. M. Kerr. 2001. STAT1 from the cell membrane to the DNA. EMBO J. 20:2508-2517.
40. Lin, R., C. Heylbroeck, P. Genin, P. M. Pitha, and J. Hiscott. 1999. Essential role of interferon regulatory factor 3 in direct activation of RANTES chemokine transcription. Mol. Cell. Biol. 19:959-966.
41. Lin, R., C. Heylbroeck, P. M. Pitha, and J. Hiscott. 1998. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol. Cell. Biol. 18:2986-2996.
42. Liu, C., Y. Okruzhnov, H. Li, and J. Nicholas. 2001. Human herpesvirus 8 (HHV-8)-encoded cytokines induce expression of and autocrine signaling by vascular endothelial growth factor (VEGF) in HHV-8-infected primary-effusion lymphoma cell lines and mediate VEGF-independent antiapoptotic effects. J. Virol. 75:10933-10940.
43. Lutfalla, G., S. J. Holland, E. Cinato, D. Monneron, J. Reboul, N. C. Rogers, J. M. Smith, G. R. Stark, K. Gardiner, K. E. Mogensen, et al. 1995. Mutant U5A cells are complemented by an interferon-alpha beta receptor subunit generated by alternative processing of a new member of a cytokine receptor gene cluster. EMBO J. 14:5100-5108.
44. Mastronarde, J. G., B. He, M. M. Monick, N. Mukaida, K. Matsushima, and G. W. Hunninghake. 1996. Induction of interleukin (IL)-8 gene expression by respiratory syncytial virus involves activation of nuclear factor (NF)-kappa B and NF-IL-6. J. Infect. Dis. 174:262-267.
45. Muller, M., C. Laxton, J. Briscoe, C. Schindler, T. Improta, J. E. Darnell, Jr., G. R. Stark, and I. M. Kerr. 1993. Complementation of a mutant cell line: central role of the 91 kDa polypeptide of ISGF3 in the interferon-alpha and -gamma signal transduction pathways. EMBO J. 12:4221-4228.
46. Ott, M., J. L. Lovett, L. Mueller, and E. Verdin. 1998. Superinduction of IL-8 in T cells by HIV-1 Tat protein is mediated through NF-kappaB factors. J. Immunol. 160:2872-2880.
47. Palangat, M., and R. Landick. 2001. Roles of RNA:DNA hybrid stability, RNA structure, and active site conformation in pausing by human RNA polymerase II. J. Mol. Biol. 311:265-282.
48. Pellegrini, S., J. John, M. Shearer, I. M. Kerr, and G. R. Stark. 1989. Use of a selectable marker regulated by alpha interferon to obtain mutations in the signaling pathway. Mol. Cell. Biol. 9:4605-4612.
49. Polyak, S. J., K. S. A. Khabar, D. M. Paschal, H. J. Ezelle, G. Duverlie, G. N. Barber, D. E. Levy, N. Mukaida, and D. R. Gretch. 2001. Hepatitis C virus nonstructural 5A protein induces interleukin-8, leading to partial inhibition of the interferon-induced antiviral response. J. Virol. 75:6095-6106.
50. Poole, E., B. He, R. A. Lamb, R. E. Randall, and S. Goodbourn. 2002. The V proteins of simian virus 5 and other paramyxoviruses inhibit induction of interferon-beta. Virology 303:33-46.
51. Rochat, S., H. Komada, and D. Kolakofsky. 1992. Loss of V protein expression in human parainfluenza virus type 1 is not a recent event. Virus Res. 24:137-144.
52. Roux, P., C. Alfieri, M. Hrimech, E. A. Cohen, and J. E. Tanner. 2000. Activation of transcription factors NF-κB and NF-IL-6 by human immunodeficiency virus type 1 protein R (Vpr) induces interleukin-8 expression. J. Virol. 74:4658-4665.
53. Sakaguchi, T., K. Kiyotani, M. Sakaki, Y. Fujii, and T. Yoshida. 1994. A field isolate of Sendai virus: its high virulence to mice and genetic divergence form prototype strains. Arch. Virol. 135:159-164.
54. 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.
55. Schlaak, J. F., C. M. Hilkens, A. P. Costa-Pereira, B. Strobl, F. Aberger, A. M. Frischauf, and I. M. Kerr. 2002. Cell-type and donor-specific transcriptional responses to interferon-alpha. Use of customized gene arrays. J. Biol. Chem. 277:49428-49437.
56. Skiadopoulos, M. H., S. R. Surman, J. M. Riggs, W. R. & Elkins, M. St Claire, M. Nishio, D. Garcin, D. Kolakofsky, P. L. Collins, and B. R. Murphy. 2002. Sendai virus, a murine parainfluenza virus type 1, replicates to a level similar to human PIV1 in the upper and lower respiratory tract of African green monkeys and chimpanzees. Virology 297:153-160.
57. Stark, G. R., I. M. Kerr, B. R. Williams, R. H. Silverman, and R. D. Schreiber. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67:227-264.
58. Strieter, R. M., J. A. Belperio, and M. P. Keane. 2002. Cytokines in innate host defense in the lung. J. Clin. Invest. 109:699-705.
59. Takeuchi, K., T. Komatsu, J. Yokoo, A. Kato, T. Shioda, Y. Nagai, and B. Gotoh. 2001. Sendai virus C protein physically associates with Stat1. Genes Cells 6:545-557.
60. Taniguchi, T., K. Ogasawara, A. Takaoka, and N. Tanaka. 2001. IRF family of transcription factors as regulators of host defense. Annu. Rev. Immunol. 19:623-655.
61. Tapparel, C., S. Hausmann, T. Pelet, J. Curran, D. Kolakofsky, and L. Roux. 1997. Inhibition of Sendai virus genome replication due to promoter-increased selectivity: a possible role for the accessory C proteins. J. Virol. 71:9588-9599.
62. Wang, X.-L., M. Itoh, H. Hotta, and M. Homma. 1994. A protease activation mutant, MVCES1, as a safe and potent live vaccine derived from currently prevailing Sendai virus. J. Virol. 68:3369-3373.
63. Wang, X., M. Li, H. Zheng, T. Muster, P. Palese, A. A. Beg, and A. Garcia-Sastre. 2000. Influenza A virus NS1 protein prevents activation of NF-κB and induction of alpha/beta interferon. J. Virol. 74:11566-11573.
64. Wansley, E. K., and G. D. Parks. 2002. Naturally occurring substitutions in the P/V gene convert the noncytopathic paramyxovirus simian virus 5 into a virus that induces alpha/beta interferon synthesis and cell death. J. Virol. 76:10109-10121.
65. 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-beta enhancer in vivo. Mol. Cell 1:507-518.
66. Yamada, Y., A. Nakamura, M. Hosoda, T. Kato, T. Asano, K. Tonegawa, and M. Itoh. 2001. Cytokines in pleural liquid for diagnosis of tuberculous pleurisy. Respir. Med. 95:577-581.
67. Yeow, W. S., W. C. Au, W. J. Lowther, and P. M. Pitha. 2001. Downregulation of IRF-3 levels by ribozyme modulates the profile of IFNA subtypes expressed in infected human cells. J. Virol. 75:3021-3027.
68. Yoneyama, M., W. Suhara, Y. Fukuhara, M. Fukuda, E. Nishida, and T. Fujita. 1998. Direct triggering of the type I interferon system by virus infection: activation of a transcription factor complex containing IRF-3 and CBP/ p300. EMBO J. 17:1087-1095.
69. Zhang, Y., B. A. Luxon, A. Casola, R. P. Garofalo, M. Jamaluddin, and A. R. Brasier. 2001. Expression of respiratory syncytial virus-induced chemokine gene networks in lower airway epithelial cells revealed by cDNA microarrays. J. Virol. 75:9044-9058.