Phosphorylation of bluetongue virus nonstructural protein 2 is essential for formation of viral inclusion bodies

Journal of Virology

Volumn 79, Issue 15, 2005, Pages 10023-10031

  Modrof, Jens ^a   Lymperopoulos, Kostas ^a   Roy, Polly ^a,b  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE; RNA; SERINE; SINGLE STRANDED RNA; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; VIRUS NONSTRUCTURAL PROTEIN 2; VIRUS PROTEIN;

ARTICLE; BINDING SITE; BLUETONGUE ORBIVIRUS; CELLULAR DISTRIBUTION; CYTOPLASM; GENE MAPPING; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; VIRUS ASSEMBLY; VIRUS INCLUSION; VIRUS MORPHOLOGY; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; BLUETONGUE VIRUS; CASEIN KINASE II; CELL LINE; HUMANS; INCLUSION BODIES; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; SEQUENCE ALIGNMENT; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

BLUETONGUE VIRUS;

EID: 22544470304     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.15.10023-10031.2005     Document Type: Article

References (48)

1. Afrikanova, I., M. C. Miozzo, S. Giambiagi, and O. Burrone. 1996. Phosphorylation generates different forms of rotavirus NSP5. J. Gen. Virol. 77:2059-2065.
2. Becker, M. M., T. R. Peters, and T. S. Dermody. 2003. Reovirus sigma NS and mu NS proteins form cytoplasmic inclusion structures in the absence of viral infection. J. Virol. 77:5948-5963.
3. Blom, N., S. Gammeltoft, and S. Brunak. 1999. Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294:1351-1362.
4. Boussif, O., F. Lezoualc'h, M. A. Zanta, M. D. Mergny, D. Scherman, B. Demeneix, and J. P. Behr. 1995. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl. Acad. Sci. USA 92:7297-7301.
5. Boyce, M., J. Wehrfritz, R. Noad, and P. Roy. 2004. Purified recombinant bluetongue virus VP1 exhibits RNA replicase activity. J. Virol. 78:3994-4002.
6. Broering, T. J., J. S. Parker, P. L. Joyce, J. Kim, and M. L. Nibert. 2002. Mammalian reovirus nonstructural protein microNS forms large inclusions and colocalizes with reovirus microtubule-associated protein micro2 in transfected cells. J. Virol. 76:8285-8297.
7. Brookes, S. M., A. D. Hyatt, and B. T. Eaton. 1993. Characterization of virus inclusion bodies in bluetongue virus infected cells. J. Gen. Virol. 74:525-530.
8. Butan, C., H. Van Der Zandt, and P. A. Tucker. 2004. Structure and assembly of the RNA binding domain of bluetongue virus non-structural protein 2. J. Biol. Chem. 279:37613-37621.
9. Das, S. C., and A. K. Pattnaik. 2004. Phosphorylation of vesicular stomatitis virus phosphoprotein P is indispensable for virus growth. J. Virol. 78:6420-6430.
10. Devaney, M. A., J. Kendall, and M. J. Grubman. 1988. Characterization of a non-structural phosphoprotein of two orbiviruses. Virus Res. 11:151-164.
11. Eaton, B. T., A. D. Hyatt, and J. R. White. 1987. Association of bluetongue virus with the cytoskeleton. Virology 157:107-116.
12. Eichwald, C., F. Vascotto, E. Fabbretti, and O. Burrone. 2002. Rotavirus NSP5: mapping phosphorylation sites and kinase activation and viroplasm localization domains. J. Virol. 76:3461-3470.
13. Evans, M. J., C. M. Rice, and S. P. Goff. 2004. Phosphorylation of hepatitis C virus nonstructural protein 5A modulates its protein interactions and viral RNA replication. Proc. Natl. Acad. Sci. USA 101:13038-13043.
14. Fabbretti, E., I. Afrikanova, F. Vascotto, and O. R. Burrone. 1999. Two non-structural rotavirus proteins, NSP2 and NSP5, form viroplasm-like structures in vivo. J. Gen. Virol. 80:333-339.
15. Fillmore, G. C., H. Lin, and J. K.-K. Li. 2002. Localization of the single-stranded RNA-binding domains of bluetongue virus nonstructural protein NS2. J. Virol. 76:499-506.
16. Fukusho, A., Y. Yu, S. Yamaguchi, and P. Roy. 1989. Completion of the sequence of bluetongue virus serotype 10 by the characterization of a structural protein, VP6, and a non-structural protein, NS2. J. Gen. Virol. 70:1677-1689.
17. Gajardo, R., P. Vende, D. Poncet, and J. Cohen. 1997. Two proline residues are essential in the calcium-binding activity of rotavirus VP7 outer capsid protein. J. Virol. 71:2211-2216.
18. Gao, Y., and J. Lenard. 1995. Multimerization and transcriptional activation of the phosphoprotein (P) of vesicular stomatitis virus by casein kinase-II. EMBO J. 14:1240-1247.
19. Green, P. L., M. T. Yip, Y. Xie, and I. S. Chen. 1992. Phosphorylation regulates RNA binding by the human T-cell leukemia virus Rex protein. J. Virol. 66:4325-4330.
20. Harlow, E., and D. P. Lane. 1999. Using antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
21. Hassan, S. H., C. Wirblich, M. Forzan, and P. Roy. 2001. Expression and functional characterization of bluetongue virus VP5 protein: role in cellular permeabilization. J. Virol. 75:8356-8367.
22. Hemonnot, B., C. Cartier, B. Gay, S. Rebuffat, M. Bardy, C. Devaux, V. Boyer, and L. Briant. 2004. The host cell MAP kinase ERK-2 regulates viral assembly and release by phosphorylating the p6gag protein of HIV-1. J. Biol. Chem. 279:32426-32434.
23. Horscroft, N., and P. Roy. 2000. NTP-binding and phosphohydrolase activity associated with purified bluetongue virus non-structural protein NS2. J. Gen. Virol. 81:1961-1965.
24. Hu, C., and K. C. Gupta. 2000. Functional significance of alternate phosphorylation in Sendai virus P protein. Virology 268:517-532.
25. Huismans, H., A. A. van Dijk, and A. R. Bauskin. 1987. In vitro phosphorylation and purification of a nonstructural protein of bluetongue virus with affinity for single-stranded RNA. J. Virol. 61:3589-3595.
26. Johnson, L. N., and D. Barford. 1993. The effects of phosphorylation on the structure and function of proteins. Annu. Rev. Biophys. Biomol. Struct. 22:199-232.
27. King, L. A., and R. D. Possee (ed.). 1992. The baculovirus expression system: a laboratory guide. Chapman and Hall, London, United Kingdom.
28. Law, L., J. Everitt, M. Beatch, C. Holmes, and T. Hobman. 2003. Phosphorylation of rubella virus capsid regulates its RNA binding activity and virus replication. J. Virol. 77:1764-1771.
29. Litchfield, D. W. 2003. Protein kinase CK2: structure, regulation and role in cellular decisions of life and death. Biochem. J. 369:1-15.
30. Lymperopoulos, K., C. Wirblich, I. Brierley, and P. Roy. 2003. Sequence specificity in the interaction of bluetongue virus non-structural protein 2 (NS2) with viral RNA. J. Biol. Chem. 278:31722-31730.
31. Markotter, W., J. Theron, and L. H. Nel. 2004. Segment specific inverted repeat sequences in bluetongue virus mRNA are required for interaction with the virus non structural protein NS2. Virus Res. 105:1-9.
32. Martinez-Costas, J., G. Sutton, and P. Roy. 1998. Guanylyltranferase and RNA5-triphosphatase activities of the purified expressed VP4 protein of bluetongue virus. J. Mol. Biol. 280:859-866.
33. Meggio, F., and L. Pinna. 2003. One-thousand-and-one substrates of protein kinase CK2? FASEB J. 17:349-368.
34. Modrof, J., E. Muhlberger, H. D. Klenk, and S. Becker. 2002. Phosphorylation of VP30 impairs ebola virus transcription. J. Biol. Chem. 277:33099-33104.
35. Obenauer, J. C., L. C. Cantley, and M. B. Yaffe. 2003. Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31:3635-3641.
36. Ramadevi, N., J. N. Burroughs, P. P. C. Mertens, I. M. Jones, and P. Roy. 1998. Capping and methylation of mRNA by purified recombinant VP4 protein of bluetongue virus. Proc. Natl. Acad. Sci. USA 95:13537-13542.
37. Reddy, Y. V., Q. Ding, S. P. Lees-Miller, K. Meek, and D. A. Ramsden. 2004. Non-homologous end joining requires that the DNA-PK complex undergo an autophosphorylation-dependent rearrangement at DNA ends. J. Biol. Chem. 279:39408-39413.
38. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
39. Sarcevic, B., A. Mawson, R. T. Baker, and R. L. Sutherland. 2002. Regulation of the ubiquitin-conjugating enzyme hHR6A by CDK-mediated phosphorylation. EMBO J. 21:2009-2018.
40. Silvestri, L. S., Z. F. Taraporewala, and J. T. Patton. 2004. Rotavirus replication: plus-sense templates for double-stranded RNA synthesis are made in viroplasms. J. Virol. 78:7763-7774.
41. Stauber, N., J. Martinez-Costas, G. Sutton, K. Monastyrskaya, and P. Roy. 1997. Bluetongue virus VP6 protein binds ATP and exhibits an RNA-dependent ATPase function and a helicase activity that catalyze the unwinding of double-stranded RNA substrates. J. Virol. 71:7220-7226.
42. Taraporewala, Z., D. Chen, and J. Patton. 2001. Multimers of the bluetongue virus nonstructural protein, NS2, possess nucleotidyl phosphatase activity: similarities between NS2 and rotavirus NSP2. Virology 280:221-231.
43. Theron, J., J. M. Uitenweerde, H. Huismans, and L. H. Nel. 1994. Comparison of the expression and phosphorylation of the non-structural protein NS2 of three different orbiviruses: evidence for the involvement of an ubiquitous cellular kinase. J. Gen. Virol. 75:3401-3411.
44. Thomas, C. P., T. F. Booth, and P. Roy. 1990. Synthesis of bluetongue virus-encoded phosphoprotein and formation of inclusion bodies by recombinant baculovirus in insect cells: it binds the single-stranded RNA species. J. Gen. Virol. 71:2073-2083.
45. Uitenweerde, J. M., J. Theron, M. A. Stoltz, and H. Huismans. 1995. The multimeric nonstructural NS2 proteins of bluetongue virus, African horse-sickness virus, and epizootic hemorrhagic disease virus differ in their single-stranded RNA-binding ability. Virology 209:624-632.
46. Welch, S. K., S. E. Crawford, and M. K. Estes. 1989. Rotavirus SA11 genome segment 11 protein is a nonstructural phosphoprotein. J. Virol. 63:3974-3982.
47. Zetina, C. R. 2001. A conserved helix-unfolding motif in the naturally unfolded proteins. Proteins 44:479-483.
48. Zhao, Y., C. Thomas, C. Bremer, and P. Roy. 1994. Deletion and mutational analyses of bluetongue virus NS2 protein indicate that the amino but not the carboxy terminus of the protein is critical for RNA-protein interactions. J. Virol. 68:2179-2185.