1887

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Volume 89, Issue 5

The C, V and W proteins of Nipah virus inhibit minigenome replication Free

Abstract

Nipah virus (NiV) is a recently emergent, highly pathogenic, zoonotic paramyxovirus of the genus . Like the phosphoprotein (P) gene of other paramyxoviruses, the P gene of NiV is predicted to encode three additional proteins, C, V and W. When the C, V and W proteins of NiV were tested for their ability to inhibit expression of the chloramphenicol acetyltransferase (CAT) reporter gene in plasmid-based, minigenome replication assays, each protein inhibited CAT expression in a dose-dependent manner. The C, V and W proteins of NiV also inhibited expression of CAT from a measles virus (MV) minigenome, but not from a human parainfluenzavirus 3 (hPIV3) minigenome. Interestingly, the C and V proteins of MV, which have previously been shown to inhibit MV minigenome replication, also inhibited NiV minigenome replication; however, they were not able to inhibit hPIV3 minigenome replication. In contrast, the C protein of hPIV3 inhibited minigenome replication of hPIV3, NiV and MV. Although there is very limited amino acid sequence similarity between the C, V and W proteins within the paramyxoviruses, the heterotypic inhibition of replication suggests that these proteins may share functional properties.

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2008-05-01
2024-04-25
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References

  1. Atreya P. L., Peeples M. E., Collins P. L. 1998; The NS1 protein of human respiratory syncytial virus is a potent inhibitor of minigenome transcription and RNA replication. J Virol 72:1452–1461
     [Google Scholar]
  2. Bailey D., Chard L. S., Dash P., Barrett T., Banyard A. C. 2007; Reverse genetics for peste-des-petits-ruminants virus (PPRV): promoter and protein specificities. Virus Res 126:250–255 [CrossRef]
     [Google Scholar]
  3. Bankamp B., Kearney S. P., Liu X., Bellini W. J., Rota P. A. 2002; Activity of polymerase proteins of vaccine and wild-type measles virus strains in a minigenome replication assay. J Virol 76:7073–7081 [CrossRef]
     [Google Scholar]
  4. Bankamp B., Wilson J., Bellini W. J., Rota P. A. 2005; Identification of naturally occurring amino acid variations that affect the ability of the measles virus C protein to regulate genome replication and transcription. Virology 336:120–129 [CrossRef]
     [Google Scholar]
  5. Baron M. D., Barrett T. 2000; Rinderpest viruses lacking the C and V proteins show specific defects in growth and transcription of viral RNAs. J Virol 74:2603–2611 [CrossRef]
     [Google Scholar]
  6. Baron M. D., Shaila M. S., Barrett T. 1993; Cloning and sequence analysis of the phosphoprotein gene of rinderpest virus. J Gen Virol 74:299–304 [CrossRef]
     [Google Scholar]
  7. Brown D. D., Rima B. K., Allen I. V., Baron M. D., Banyard A. C., Barret T., Duprex W. P. 2005; Rational attenuation of a morbillivirus by modulating the activity of the RNA-dependent RNA polymerase. J Virol 79:14330–14338 [CrossRef]
     [Google Scholar]
  8. Buchholz U. J., Finke S., Conzelmann K.-K. 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
     [Google Scholar]
  9. Chua K. B., Bellini W. J., Rota P. A., Harcourt B. H., Tamin A., Lam S. K., Ksiazek T. G., Rollin P. E., Zaki S. R. other authors 2000; Nipah virus: a recently emergent deadly paramyxovirus. Science 288:1432–1435 [CrossRef]
     [Google Scholar]
  10. Curran J., Boeck R., Kolakofsky D. 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
     [Google Scholar]
  11. Curran J., Marq J. B., Kolakofsky D. 1992; The Sendai virus nonstructural C proteins specifically inhibit viral mRNA synthesis. Virology 189:647–656 [CrossRef]
     [Google Scholar]
  12. Didcock L., Young D. F., Goodbourn S., Randall R. E. 1999; The V protein of simian virus 5 inhibits interferon signaling by targeting STAT1 for proteasome-mediated degradation. J Virol 73:9928–9933
     [Google Scholar]
  13. Durbin A. P., Hall S. L., Siew J. W., Whitehead S. S., Collins P. L., Murphy B. R. 1997; Recovery of infectious human parainfluenza virus type 3 from cDNA. Virology 235:323–332 [CrossRef]
     [Google Scholar]
  14. Galinski M. S., Troy R. M., Banerjee A. K. 1992; RNA editing in the phosphoprotein gene of the human parainfluenza virus type 3. Virology 186:543–550 [CrossRef]
     [Google Scholar]
  15. Goodbourn S., Didcock L., Randall R. E. 2000; Interferons: cell signaling, immune modulation, antiviral response and virus countermeasures. J Gen Virol 81:2341–2364
     [Google Scholar]
  16. Grogan C. C., Moyer S. A. 2001; Sendai virus wild-type and mutant C proteins show a direct correlation between L polymerase binding and inhibition of viral RNA synthesis. Virology 288:96–108 [CrossRef]
     [Google Scholar]
  17. Halpin K., Bankamp B., Harcourt B. H., Bellini W. J., Rota P. A. 2004; Nipah virus conforms to the rule of six in a minigenome replication assay. J Gen Virol 85:701–707 [CrossRef]
     [Google Scholar]
  18. Harcourt B. H., Tamin A., Ksiazek T. G., Rollin P. E., Anderson L. J., Bellini W. J., Rota P. A. 2000; Molecular characterization of Nipah virus, a newly emergent paramyxovirus. Virology 271:334–349 [CrossRef]
     [Google Scholar]
  19. Harcourt B. H., Tamin A., Halpin K., Ksiazek T. G., Rollin P. E., Bellini W. J., Rota P. A. 2001; Molecular characterization of the polymerase gene and genomic termini of Nipah virus. Virology 287:192–201 [CrossRef]
     [Google Scholar]
  20. He B., Paterson G., Stock N., Durbin J. E., Durbin R. K., Goodbourn S., Randall R. E., Lamb R. A. 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 signaling. Virology 303:15–32 [CrossRef]
     [Google Scholar]
  21. Horikami S. M., Smallwood S., Moyer S. A. 1996; The Sendai virus V protein interacts with the NP protein to regulate viral genome RNA replication. Virology 222:383–390 [CrossRef]
     [Google Scholar]
  22. Hsu V. P., Hossain M. J., Parashar U. D., Ali M. M., Ksiazek T. G., Kuzmin I., Niezgoda M., Rupprecht C., Bresee J., Breiman R. F. 2004; Nipah virus reemergence, Bangadesh. Emerg Infect Dis 10:2082–2087 [CrossRef]
     [Google Scholar]
  23. Hummel K. B., Lowe L., Bellini W. J., Rota P. A. 2006; Development of quantitative gene-specific real-time RT-PCR assays for the detection of measles virus in clinical specimens. J Virol Methods 132:166–173 [CrossRef]
     [Google Scholar]
  24. Jeyaseelan K., Ma D., Armugam A. 2001; Real-time detection of gene promoter activity: quantitation of toxin gene transcription. Nucleic Acids Res 29:E58 [CrossRef]
     [Google Scholar]
  25. Kato A., Kiyotani K., Sakai Y., Yoshida T., Nagai Y. 1997a; The paramyxovirus, Sendai virus, V protein encodes a luxury function required for viral pathogenesis. EMBO J 16:578–587 [CrossRef]
     [Google Scholar]
  26. Kato A., Kiyotani K., Sakai Y., Yoshida T., Shioda T., Nagai Y. 1997b; Importance of the cysteine-rich carboxyl-terminal half of V protein for Sendai virus pathogenesis. J Virol 71:7266–7272
     [Google Scholar]
  27. Kato A., Ohnishi Y., Hishiyama M., Kohase M., Saito S., Tashiro M., Nagai Y. 2002; The amino-terminal half of Sendai virus C protein is not responsible for either counteracting the antiviral action of interferons or down-regulating viral RNA synthesis. J Virol 76:7114–7124 [CrossRef]
     [Google Scholar]
  28. Kato A., Cortese-Grogan C., Moyer S. A., Sugahara F., Sakaguchi T., Kubota T., Otsuki N., Kohase M., Tashiro M., Nagai Y. 2004; Characterization of the amino acid residues of Sendai virus C protein that are critically involved in its interferon antagonism and RNA synthesis down-regulation. J Virol 78:7443–7454 [CrossRef]
     [Google Scholar]
  29. Komatsu T., Takeuchi K., Yokoo J., Gotoh B. 2004; C and V proteins of Sendai virus target signaling pathways leading to IRF-3 activation for the negative regulation of interferon-beta production. Virology 325:137–148 [CrossRef]
     [Google Scholar]
  30. Lamb R. A., Kolakofsky D. 2001; Paramyxoviridae : the viruses and their replication. In Fields Virology , 4th edn. pp 1305–1340Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott Williams & Wilkins;
     [Google Scholar]
  31. Lin Y., Horvath F., Aligo J. A., Wilson R., He B. 2005; The role of simian virus 5 V protein on viral RNA synthesis. Virology 338:270–280 [CrossRef]
     [Google Scholar]
  32. Luby S. P., Rahman M., Hossain M. J., Blum L. S., Husain M. M., Gurley E., Khan R., Ahmed B.-N., Rahman S. 2006; Foodborne transmission of Nipah virus, Bangladesh. Emerg Infect Dis 12:1888–1894 [CrossRef]
     [Google Scholar]
  33. Magoffin D. E., Mackenzie J. S., Wang L.-F. 2007; Genetic analysis of J-virus and Beilong virus using minireplicons. Virology 364:103–111 [CrossRef]
     [Google Scholar]
  34. Malur A. G., Hoffman M. A., Banerjee A. K. 2004; The human parainfluenza virus type 3 (HPIV 3) C protein inhibits viral transcription. Virus Res 99:199–204 [CrossRef]
     [Google Scholar]
  35. Matsuoka Y., Curran J., Pelet T., Kolakofsky D., Ray R., Compans R. W. 1991; The P gene of human parainfluenza virus type 1 encodes P and C proteins, but not a cysteine-rich V protein. J Virol 65:3406–3410
     [Google Scholar]
  36. Mayo M. A. 2002; A summary of taxonomic changes recently approved by ICTV. Arch Virol 147:1655–1656 [CrossRef]
     [Google Scholar]
  37. Nanda S. K., Baron M. D. 2006; Rinderpest virus blocks type I and type II interferon action: role of structural and nonstructural proteins. J Virol 80:7555–7568 [CrossRef]
     [Google Scholar]
  38. Ohno S., Ono N., Takeda M., Takeuchi K., Yanagi Y. 2004; Dissection of measles virus V protein in relation to its ability to block alpha/beta interferon signal transduction. J Gen Virol 85:2991–2999 [CrossRef]
     [Google Scholar]
  39. Park M. S., Shaw M. L., Muñoz-Jordan J., Cros J. F., Nakaya T., Bouvier N., Palese P., García-Sastre A., Basler C. F. 2003; Newcastle disease virus (NDV)-based assay demonstrates inerferon-antagonist activity for the NDV V protein and the Nipah virus V, W, and C proteins. J Virol 77:1501–1511 [CrossRef]
     [Google Scholar]
  40. Parks C. L., Witko S. E., Kotash C., Lin S. L., Sidhu M. S., Udem S. A. 2006; Role of V protein RNA binding in inhibition of measles virus minigenome replication. Virology 348:96–106 [CrossRef]
     [Google Scholar]
  41. Patterson J. B., Thomas D., Lewicki H., Billeter M. A., Oldstone M. B. 2000; V and C proteins of measles virus function as virulence factors in vivo . Virology 267:80–89 [CrossRef]
     [Google Scholar]
  42. Poole E., He B., Lamb R. A., Randall R. E., Goodbourn S. 2002; The V proteins of simian virus 5 and other paramyxoviruses inhibit induction of interferon- β . Virology 303:33–46 [CrossRef]
     [Google Scholar]
  43. Reutter G. L., Cortese-Grogan C., Wilson J., Moyer S. A. 2001; Mutations in the measles virus C protein that up regulate viral RNA synthesis. Virology 285:100–109 [CrossRef]
     [Google Scholar]
  44. Rodriguez J. J., Parisien J.-P., Horvath C. M. 2002; Nipah virus V protein evades alpha and gamma interferons by preventing STAT1 and STAT2 activation and nuclear accumulation. J Virol 76:11476–11483 [CrossRef]
     [Google Scholar]
  45. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
     [Google Scholar]
  46. Shaffer J. A., Bellini W. J., Rota P. A. 2003; The C protein of measles virus inhibits the type I interferon response. Virology 315:389–397 [CrossRef]
     [Google Scholar]
  47. Sidhu M. S., Chan J., Kaelin K., Spielhofer P., Radecke F., Schneider H., Masurekar M., Dowling P. C., Billeter M. A., Udem S. A. 1995; Rescue of synthetic measles virus minireplicons: measles genomic termini direct efficient expression and propagation of a reporter gene. Virology 208:800–807 [CrossRef]
     [Google Scholar]
  48. Smallwood S., Moyer S. A. 2004; The L polymerase protein of parainfluenza virus 3 forms an oligomer and can interact with the heterologous Sendai virus L, P and C proteins. Virology 318:439–450 [CrossRef]
     [Google Scholar]
  49. Svenda M., Hjertner B., Linne T., Berg M. 2002; Both the P and V proteins of the porcine rubulavirus LPMV interact with the NP protein via their respective C-terminal unique parts. Virus Res 83:31–41 [CrossRef]
     [Google Scholar]
  50. Sweetman D. A., Miskin J., Baron M. D. 2001; Rinderpest virus C and V proteins interact with the major (L) component of the viral polymerase. Virology 281:193–204 [CrossRef]
     [Google Scholar]
  51. Tapparel C., Hausmann S., Pelet T., Curran J., Kolakofsky D., Roux L. 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
     [Google Scholar]
  52. Tober C., Seufert M., Schneider H., Billeter M. A., Johnston I. C. D., Niewiesk S., ter Meulen V., Schneider-Schaulies S. 1998; Expression of measles virus V protein is associated with pathogenicity and control of viral RNA synthesis. J Virol 72:8124–8132
     [Google Scholar]
  53. Witko S. E., Kotash C., Sidhu M. S., Udem S. A., Parks C. L. 2006; Inhibition of measles virus minireplicon-encoded reporter gene expression by V protein. Virology 348:107–119 [CrossRef]
     [Google Scholar]
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The C, V and W proteins of Nipah virus inhibit minigenome replication
J. Gen. Virol. 89, 1300 (2008); https://doi.org/10.1099/vir.0.83582-0
/content/journal/jgv/10.1099/vir.0.83582-0
/content/journal/jgv/10.1099/vir.0.83582-0
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