The amino-terminal extensions of the longer Sendai virus C proteins modulate pY701-Stat1 and bulk Stat1 levels independently of interferon signaling

Journal of Virology

Volumn 77, Issue 4, 2003, Pages 2321-2329

  Garcin, Dominique ^a   Marq, Jean Baptiste ^a   Goodbourn, Stephen ^b   Kolakofsky, Daniel ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; STAT PROTEIN; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL MUTANT; CONTROLLED STUDY; NONHUMAN; PARAMYXOVIRUS; PRIORITY JOURNAL; PROTEIN INTERACTION; SENDAI VIRUS; VIRUS INFECTION;

ANIMALS; CELL LINE; DNA-BINDING PROTEINS; HUMANS; INTERFERONS; MICE; SENDAI VIRUS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; STRUCTURE-ACTIVITY RELATIONSHIP; TRANS-ACTIVATORS; TRANSFECTION; TUMOR CELLS, CULTURED; VIRAL PROTEINS;

EID: 0037320240     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.4.2321-2329.2003     Document Type: Article

References (55)

1. Bontron, S., C. Ucla, B. Mach, and V. Steimle. 1997. Efficient repression of endogenous major histocompatibility complex class II expression through dominant negative CIITA mutants isolated by a functional selection strategy. Mol. Cell. Biol. 17:4249-4258.
2. Buchholz, U. J., S. Finke, and K. K. Conzelmann. 1999. Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J. Virol. 73:251-259.
3. 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.
4. Chang, Y. E., and L. A. Laimins. 2000. Microarray analysis identifies interferon-inducible genes and Stat-1 as major transcriptional targets of human papillomavirus type 31. J. Virol. 74:4174-4182.
5. Chatterjee-Kishore, M., A. F. van Den, and G. R. Stark. 2000. Adenovirus E1A down-regulates LMP2 transcription by interfering with the binding of stat1 to IRF1. J. Biol. Chem. 275:20406-20411.
6. Chatterjee-Kishore, M., K. L. Wright, J. P. Ting, and G. R. Stark. 2000. How Stat1 mediates constitutive gene expression: a complex of unphosphorylated Stat1 and IRF1 supports transcription of the LMP2 gene. EMBO J. 19:4111-4122.
7. Costa-Pereira, A. P., S. Tininini, B. Strobl, T. Alonzi, J. F. Schlaak, H. Is'harc, I. Gesualdo, S. J. Newman, I. M. Kerr, and V. Poli. 2002. Mutational switch of an IL-6 response to an interferon-gamma-like response. Proc. Natl. Acad. Sci. USA 99:8043-8047.
8. Curran, J., and D. Kolakofsky. 1988. Ribosomal initiation from an ACG codon in the Sendai virus P/C mRNA. EMBO J. 7:245-251.
9. Curran, J., J.-B. Marq, and D. Kolakofsky. 1992. The Sendai virus nonstructural C proteins specifically inhibit viral mRNA synthesis. Virology 189:647-656.
10. Darnell, J. E. J. 1997. STATs and gene regulation. Science JID-0404511 277:1630-1635.
11. 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.
12. Didcock, L., D. F. Young, S. Goodbourn, and R. E. Randall. 1999. Sendai virus and simian virus 5 block activation of interferon-responsive genes: importance for virus pathogenesis. J. Virol. JID-0113724 73:3125-3133.
13. Didcock, L., D. F. Young, S. Goodbourn, and R. E. Randall. 1999. The V protein of simian virus 5 inhibits interferon signalling by targeting STAT1 for proteasome-mediated degradation. J. Virol. JID-0113724 73:9928-9933.
14. Fambrough, D., K. McClure, A. Kazlauskas, and E. S. Lander. 1999. Diverse signaling pathways activated by growth factor receptors induce broadly overlapping, rather than independent, sets of genes. Cell 97:727-741.
15. 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.
16. 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.
17. 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.
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. 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.
21. Gil, M. P., E. Bohn, A. K. O'Guin, C. V. Ramana, B. Levine, G. R. Stark, H. W. Virgin, and R. D. Schreiber. 2001. Biologic consequences of Stat1-independent IFN signaling. Proc. Natl. Acad. Sci. USA 98:6680-6685.
22. Giorgi, C., B. M. Blumberg, and D. Kolakofsky. 1983. Sendai virus contains overlapping genes expressed from a single mRNA. Cell 35:829-836.
23. Gotoh, B., K. Takeuchi, T. Komatsu, J. Yokoo, Y. Kimura, A. Kurotani, A. Kato, and Y. Nagai. 1999. Knockout of the Sendai virus C gene eliminates the viral ability to prevent the interferon-alpha/beta-mediated responses. FEBS Lett. 459:205-210.
24. Hardwick, J. M. 2001. Apoptosis in viral pathogenesis. Cell Death Differ. 8:109-110.
25. Haspel, R. L., and J. E. Darnell, Jr. 1999. A nuclear protein tyrosine phosphatase is required for the inactivation of Stat1. Proc. Natl. Acad. Sci. USA 96:10188-10193.
26. a. He, B., R. G. Paterson, N. Stock, J. E. Durbin, R. 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-β induction and interferon signalling. Virology 303:15-32.
27. Horikami, S. M., R. E. Hector, S. Smallwood, and S. A. Moyer. 1997. The Sendai virus C protein binds the L polymerase protein to inhibit viral RNA synthesis. Virology 235:261-270.
28. Horvath, C. M. 2000. STAT proteins and transcriptional responses to extracellular signals. Trends Biochem. Sci. JID-7610674 25:496-502.
29. Karlin, D., S. Longhi, V. Receveur, and B. Canard. 2002. The N-terminal domain of the phosphoprotein of morbilliviruses belongs to the natively unfolded class of proteins. Virology 296:251-262.
30. Kato, A., Y. Ohnishi, M. Kohase, S. Saito, M. Tashiro, and Y. Nagai. 2001. Y2, the smallest of the Sendai virus C proteins, is fully capable of both counteracting the antiviral action of interferons and inhibiting viral RNA synthesis. J. Virol. JID-0113724 75:3802-3810.
31. King, P., and S. Goodbourn. 1994. The beta-interferon promoter responds to priming through multiple independent regulatory elements. J. Biol. Chem. 269:30609-30615.
32. King, P., and S. Goodbourn. 1998. STAT1 is inactivated by a caspase. J. Biol. Chem. 273:8699-8704.
33. Komatsu, T., K. Takeuchi, J. Yokoo, and B. Gotoh. 2002. Sendai virus C protein impairs both phosphorylation and dephosphorylation processes of Stat1. FEBS Lett. 511:139-144.
34. Kurotani, A., K. Kiyotani, A. Kato, T. Shioda, Y. Sakai, K. Mizumoto, T. Yoshida, and Y. Nagai. 1998. Sendai virus C proteins are categorically non-essential gene products but silencing their expression severely impairs viral replication and pathogenesis. Genes Cells 3:111-124.
35. Lamb, R. A., B. W. J. Mahy, and P. W. Choppin. 1976. The synthesis of Sendai virus polypeptides in infected cells. Virology 69:116-131.
36. 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.
37. Latorre, P., D. Kolakofsky, and J. Curran. 1998. Sendai virus Y proteins are initiated by a ribosomal shunt. Mol. Cell. Biol. 18:5021-5031.
38. Leung, S., S. A. Qureshi, I. M. Kerr, J. E. Darnell, Jr., and G. R. Stark. 1995. Role of STAT2 in the alpha interferon signaling pathway. Mol. Cell. Biol. 15:1312-1317.
39. Lin-Marq, N., S. Bontron, O. Leupin, and M. Strubin. 2001. Hepatitis B virus X protein interferes with cell viability through interaction with the p127-kDa UV-damaged DNA-binding protein. Virology 287:266-274.
40. Lutfalla, G., S. J. Holland, E. Cinato, D. Monneron, J. Reboul, N. C. Rogers, J. M. Smith, G. R. Stark, K. Gardiner, and K. E. Mogensen. 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.
41. 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.
42. Nishio, M., D. Garcin, V. Simonet, and D. Kolakofsky. 2002. The carboxyl segment of the mumps virus v protein associates with stat proteins in vitro via a tryptophan-rich motif. Virology 300:92.
43. Parisien, J. P., J. F. Lau, J. J. Rodriguez, C. M. Ulane, and C. M. Horvath. 2002. Selective STAT protein degradation induced by paramyxoviruses requires both STAT1 and STAT2 but is independent of alpha/beta interferon signal transduction. J. Virol. 76:4190-4198.
44. 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.
45. Roulston, A., R. C. Marcellus, and P. E. Branton. 1999. Viruses and apoptosis. Annu. Rev. Microbiol. 53:577-628.
46. Saito, S., T. Ogino, N. Miyajima, A. Kato, and M. Kohase. 2002. Dephosphorylation failure of tyrosine-phosphorylated STAT1 in IFN-stimulated Sendai virus C protein-expressing cells. Virology 293:205-209.
47. 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.
48. Strobl, B., V. Arulampalam, H. Is'harc, S. J. Newman, J. F. Schlaak, D. Watling, A. P. Costa-Pereira, F. Schaper, I. Behrmann, K. C. Sheehan, R. D. Schreiber, F. Horn, P. C. Heinrich, and I. M. Kerr. 2001. A completely foreign receptor can mediate an interferon-gamma-like response. EMBO J. 20:5431-5442.
49. 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 JID-9607379 6:545-557.
50. 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.
51. Tompa, P. 2002. Intrinsically unstructured proteins. Trends Biochem. Sci. 27:527.
52. Weber, H., D. Valenzuela, G. Lujber, M. Gubler, and C. Weissmann. 1987. Single amino acid changes that render human IFN-alpha 2 biologically active on mouse cells. EMBO J. JID-8208664 6:591-598.
53. Wright, P. E., and H. J. Dyson. 1999. Intrinsically unstructured proteins: reassessing the protein structure-function paradigm. J. Mol. Biol. 293:321-331.
54. Yang, Y. L., L. F. Reis, J. Pavlovic, A. Aguzzi, R. Schafer, A. Kumar, B. R. Williams, M. Aguet, and C. Weissmann. 1995. Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J. 14:6095-6106.
55. Zhou, A., J. M. Paranjape, S. D. Der, B. R. Williams, and R. H. Silverman. 1999. Interferon action in triply deficient mice reveals the existence of alternative antiviral pathways. Virology 258:435-440.