Nipah virus V and W proteins have a common STAT1-binding domain yet inhibit STAT1 activation from the cytoplasmic and nuclear compartments, respectively

Journal of Virology

Volumn 78, Issue 11, 2004, Pages 5633-5641

  Shaw, Megan L ^a   García Sastre, Adolfo ^a   Palese, Peter ^a   Basler, Christopher F ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; COMPLEMENTARY DNA; GREEN FLUORESCENT PROTEIN; NIPAH VIRUS V PROTEIN; NIPAH VIRUS W PROTEIN; STAT1 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL NUCLEUS; CYTOPLASM; GENE EXPRESSION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NIPAH VIRUS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; REPORTER GENE; VIRUS CELL INTERACTION; VIRUS VIRULENCE;

ANIMALS; BINDING SITES; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; CYTOPLASM; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; INTERFERONS; NIPAH VIRUS; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS; VERO CELLS; VIRAL PROTEINS;

EID: 2442661542     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.11.5633-5641.2004     Document Type: Article

References (61)

1. Andrejeva, J., E. Poole, D. F. Young, S. Goodbourn, and R. E. Randall. 2002. The p127 subunit (DDB1) of the UV-DNA damage repair binding protein is essential for the targeted degradation of STAT1 by the V protein of the paramyxovirus simian virus 5. J. Virol. 76:11379-11386.
2. Basler, C. F., A. Mikulasova, L. Martinez-Sobrido, J. Paragas, E. Muhlberger, M. Bray, H. D. Klenk, P. Palese, and A. Garcia-Sastre. 2003. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 77:7945-7956.
3. Basler, C. F., A. H. Reid, J. K. Dybing, T. A. Janczewski, T. G. Fanning, H. Zheng, M. Salvatore, M. L. Perdue, D. E. Swayne, A. Garcia-Sastre, P. Palese, and J. K. Taubenberger. 2001. Sequence of the 1918 pandemic influenza virus nonstructural gene (NS) segment and characterization of recombinant viruses bearing the 1918 NS genes. Proc. Natl. Acad. Sci. USA 98:2746-2751.
4. Basler, C. F., X. Wang, E. Muhlberger, V. Volchkov, J. Paragas, H. D. Klenk, A. Garcia-Sastre, and P. Palese. 2000. The Ebola virus VP35 protein functions as a type I IFN antagonist. Proc. Natl. Acad. Sci. USA 97:12289-12294.
5. Bossert, B., and K. K. Conzelmann. 2002. Respiratory syncytial virus (RSV) nonstructural (NS) proteins as host range determinants: a chimeric bovine RSV with NS genes from human RSV is attenuated in interferon-competent bovine cells. J. Virol. 76:4287-4293.
6. Bridgen, A., F. Weber, J. K. Fazakerley, and R. M. Elliott. 2001. Bunyamwera bunyavirus nonstructural protein NSs is a nonessential gene product that contributes to viral pathogenesis. Proc. Natl. Acad. Sci. USA 98:664-669.
7. Chua, K. B., W. J. Bellini, P. A. Rota, B. H. Harcourt, A. Tamin, S. K. Lam, T. G. Ksiazek, P. E. Rollin, S. R. Zaki, W. Shieh, C. S. Goldsmith, D. J. Gubler, J. T. Roehrig, B. Eaton, A. R. Gould, J. Olson, H. Field, P. Daniels, A. E. Ling, C. J. Peters, L. J. Anderson, and B. W. Mahy. 2000. Nipah virus: a recently emergent deadly paramyxovirus. Science 288:1432-1435.
8. Chua, K. B., C. L. Koh, P. S. Hooi, K. F. Wee, J. H. Khong, B. H. Chua, Y. P. Chan, M. E. Lim, and S. K. Lam. 2002. Isolation of Nipah virus from Malaysian Island flying-foxes. Microbes Infect. 4:145-151.
9. Curran, J., R. Boeck, and D. Kolakofsky. 1991. The Sendai virus P gene expresses both an essential protein and an inhibitor of RNA synthesis by shuffling modules via mRNA editing. EMBO J. 10:3079-3085.
10. Curran, J., J. B. Marq, and D. Kolakofsky. 1995. An N-terminal domain of the Sendai paramyxovirus P protein acts as a chaperone for the NP protein during the nascent chain assembly step of genome replication. J. Virol. 69:849-855.
11. Darnell, J. E., Jr. 1997. STATs and gene regulation. Science 277:1630-1635.
12. Didcock, L., D. F. Young, S. Goodbourn, and R. E. Randall. 1999. The V protein of simian virus 5 inhibits interferon signaling by targeting STAT1 for proteasome-mediated degradation. J. Virol. 73:9928-9933.
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. Garcia-Sastre, A. 2001. Inhibition of interferon-mediated antiviral responses by influenza A viruses and other negative-strand RNA viruses. Virology 279:375-384.
15. Garcia-Sastre, A., A. Egorov, D. Matassov, S. Brandt, D. E. Levy, J. E. Durbin, P. Palese, and T. Muster. 1998. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252:324-330.
16. 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.
17. 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.
18. 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.
19. 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.
20. Garcin, D., J. B. Marq, L. Strahle, P. le Mercier, and D. Kolakofsky. 2002. All four Sendai virus C proteins bind Statl, but only the larger forms also induce its mono-ubiquitination and degradation. Virology 295:256-265.
21. Goh, K. J., C. T. Tan, N. K. Chew, P. S. Tan, A. Kamarulzaman, S. A. Sarji, K. T. Wong, B. J. Abdullah, K. B. Chua, and S. K. Lam. 2000. Clinical features of Nipah virus encephalitis among pig farmers in Malaysia. N. Engl. J. Med. 342:1229-1235.
22. Gotoh, B., T. Komatsu, K. Takeuchi, and J. Yokoo. 2002. Paramyxovirus strategies for evading the interferon response. Rev. Med. Virol. 12:337-357.
23. Hagmaier, K., S. Jennings, J. Buse, F. Weber, and G. Kochs. 2003. Novel gene product of Thogoto virus segment 6 codes for an interferon antagonist. J. Virol. 77:2747-2752.
24. Harcourt, B. H., A. Tamin, T. G. Ksiazek, P. E. Rollin, L. J. Anderson, W. J. Bellini, and P. A. Rota. 2000. Molecular characterization of Nipah virus, a newly emergent paramyxovirus. Virology 271:334-349.
25. 2- and COOH-terminal domains for interactions with the nucleoprotein (N) but only the COOH terminus for interactions with itself. J. Gen. Virol. 76:2863-2867.
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. Hooper, P., S. Zaki, P. Daniels, and D. Middleton. 2001. Comparative pathology of the diseases caused by Hendra and Nipah viruses. Microbes Infect. 3:315-322.
28. Huang, Z., S. Krishnamurthy, A. Panda, and S. K. Samal. 2003. Newcastle disease virus V protein is associated with viral pathogenesis and functions as an alpha interferon antagonist. J. Virol. 77:8676-8685.
29. Katze, M. G., Y. He, and M. Gale, Jr. 2002. Viruses and interferon: a fight for supremacy. Nat. Rev. Immunol. 2:675-687.
30. Kubota, T., N. Yokosawa, S. Yokota, and N. Fujii. 2001. C-terminal CYS-RICH region of mumps virus structural V protein correlates with block of interferon alpha and gamma signal transduction pathway through decrease of STAT 1-α. Biochem. Biophys. Res. Commun. 283:255-259.
31. Levy, D. E., and A. Garcia-Sastre. 2001. The virus battles: IFN induction of the antiviral state and mechanisms of viral evasion. Cytokine Growth Factor Rev. 12:143-156.
32. Mebatsion, T., S. Verstegen, L. T. De Vaan, A. Romer-Oberdorfer, and C. C. Schrier. 2001. A recombinant Newcastle disease virus with low-level V protein expression is immunogenic and lacks pathogenicity for chicken embryos. J. Virol. 75:420-428.
33. Meyer, T., K. Gavenis, and U. Vinkemeier. 2002. Cell type-specific and tyrosine phosphorylation-independent nuclear presence of STAT1 and STAT3. Exp. Cell Res. 272:45-55.
34. Muhlberger, E., M. Weik, V. E. Volchkov, H. D. Klenk, and S. Becker. 1999. Comparison of the transcription and replication strategies of Marburg virus and Ebola virus by using artificial replication systems. J. Virol. 73:2333-2342.
35. Nishio, M., M. Tsurudome, M. Ito, M. Kawano, H. Komada, and Y. Ito. 2001. High resistance of human parainfluenza type 2 virus protein-expressing cells to the antiviral and anti-cell proliferative activities of alpha/beta interferons: cysteine-rich V-specific domain is required for high resistance to the interferons. J. Virol. 75:9165-9176.
36. Niwa, H., K. Yamamura, and J. Miyazaki. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193-199.
37. Palosaari, H., J. P. Parisien, J. J. Rodriguez, C. M. Ulane, and C. M. Horvath. 2003. STAT protein interference and suppression of cytokine signal transduction by measles virus V protein. J. Virol. 77:7635-7644.
38. Parisien, J. P., J. F. Lau, and C. M. Horvath. 2002. STAT2 acts as a host range determinant for species-specific paramyxovirus interferon antagonism and simian virus 5 replication. J. Virol. 76:6435-6441.
39. Parisien, J. P., J. F. Lau, J. J. Rodriguez, B. M. Sullivan, A. Moscona, G. D. Parks, R. A. Lamb, and C. M. Horvath. 2001. The V protein of human parainfluenza virus 2 antagonizes type I interferon responses by destabilizing signal transducer and activator of transcription 2. Virology 283:230-239.
40. 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.
41. Park, M. S., A. Garcia-Sastre, J. F. Cros, C. F. Basler, and P. Palese. 2003. Newcastle disease virus V protein is a determinant of host range restriction. J. Virol. 77:9522-9532.
42. Park, M. S., M. L. Shaw, J. Munoz-Jordan, J. F. Cros, T. Nakaya, N. Bouvier, P. Palese, A. Garcia-Sastre, and C. F. Basler. 2003. Newcastle disease virus (NDV)-based assay demonstrates interferon-antagonist activity for the NDV V protein and the Nipah virus V, W, and C proteins. J. Virol. 77:1501-1511.
43. Patterson, J. B., D. Thomas, H. Lewicki, M. A. Billeter, and M. B. Oldstone. 2000. V and C proteins of measles virus function as virulence factors in vivo. Virology 267:80-89.
44. 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.
45. Rodriguez, J. J., J. P. Parisien, and C. M. Horvath. 2002. Nipah virus V protein evades alpha and gamma interferons by preventing STAT1 and STAT2 activation and nuclear accumulation. J. Virol. 76:11476-11483.
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. Schindler, C., X. Y. Fu, T. Improta, R. Aebersold, and J. E. Darnell, Jr. 1992. Proteins of transcription factor ISGF-3: one gene encodes the 91- and 84-kDa ISGF-3 proteins that are activated by interferon alpha. Proc. Natl. Acad. Sci. USA 89:7836-7839.
48. Schlender, J., B. Bossert, U. Buchholz, and K. K. Conzelmann. 2000. Bovine respiratory syncytial virus nonstructural proteins NS1 and NS2 cooperatively antagonize alpha/beta interferon-induced antiviral response. J. Virol. 74: 8234-8242.
49. 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.
50. Smallwood, S., K. W. Ryan, and S. A. Moyer. 1994. Deletion analysis defines a carboxyl-proximal region of Sendai virus P protein that binds to the polymerase L protein. Virology 202:154-163.
51. Steward, M., I. B. Vipond, N. S. Millar, and P. T. Emmerson. 1993. RNA editing in Newcastle disease virus. J. Gen. Virol. 74:2539-2547.
52. 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.
53. Tarbouriech, N., J. Curran, C. Ebel, R. W. Ruigrok, and W. P. Burmeister. 2000. On the domain structure and the polymerization state of the Sendai virus P protein. Virology 266:99-109.
54. Ulane, C. M., and C. M. Horvath. 2002. Paramyxoviruses SV5 and HPIV2 assemble STAT protein ubiquitin ligase complexes from cellular components. Virology 304:160-166.
55. Ulane, C. M., J. J. Rodriguez, J. P. Parisien, and C. M. Horvath. 2003. STAT3 ubiquitylation and degradation by mumps virus suppress cytokine and oncogene signaling. J. Virol. 77:6385-6393.
56. Wang, L., B. H. Harcourt, M. Yu, A. Tamin, P. A. Rota, W. J. Bellini, and B. T. Eaton. 2001. Molecular biology of Hendra and Nipah viruses. Microbes Infect. 3:279-287.
57. Wang, L. F., W. P. Michalski, M. Yu, L. I. Pritchard, G. Crameri, B. Shiell, and B. T. Eaton. 1998. A novel P/V/C gene in a new member of the Paramyxoviridae family, which causes lethal infection in humans, horses, and other animals. J. Virol. 72:1482-1490.
58. Weber, F., A. Bridgen, J. K. Fazakerley, H. Streitenfeld, N. Kessler, R. E. Randall, and R. M. Elliott. 2002. Bunyamwera bunyavirus nonstructural protein NSs counteracts the induction of alpha/beta interferon. J. Virol. 76:7949-7955.
59. Yokosawa, N., S. Yokota, T. Kubota, and N. Fujii. 2002. C-terminal region of STAT-1α is not necessary for its ubiquitination and degradation caused by mumps virus V protein. J. Virol. 76:12683-12690.
60. Young, D. F., N. Chatziandreou, B. He, S. Goodbourn, R. A. Lamb, and R. E. Randall. 2001. Single amino acid substitution in the V protein of simian virus 5 differentiates its ability to block interferon signaling in human and murine cells. J. Virol. 75:3363-3370.
61. Young, D. F., L. Didcock, S. Goodbourn, and R. E. Randall. 2000. Paramyxoviridae use distinct virus-specific mechanisms to circumvent the interferon response. Virology 269:383-390.