Phosphorylation of Rubella virus capsid regulates its RNA binding activity and virus replication

Journal of Virology

Volumn 77, Issue 3, 2003, Pages 1764-1771

  Law, Lok Man J ^a   Everitt, Jason C ^a   Beatch, Martin D ^a   Holmes, Charles F B ^a   Hobman, Tom C ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN E; PHOSPHOPROTEIN PHOSPHATASE 1; STRUCTURAL PROTEIN; VIRUS GLYCOPROTEIN;

ARTICLE; BINDING AFFINITY; DEPHOSPHORYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ISOLATION; PROTEIN PHOSPHORYLATION; PROTEIN RNA BINDING; RNA BINDING; RUBELLA VIRUS; TOGAVIRUS; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS NUCLEOCAPSID; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS TITRATION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CAPSID; CELL LINE; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; RNA, VIRAL; RUBELLA VIRUS; VIRUS ASSEMBLY; VIRUS REPLICATION;

EID: 0037302253     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.3.1764-1771.2003     Document Type: Article

References (47)

1. Agostinis, P., J. Goris, L. A. Pinna, F. Marchiori, J. W. Perich, H. E. Meyer, and W. Merlevede. 1990. Synthetic peptides as model substrates for the study of the specificity of the polycation-stimulated protein phosphatases. Eur. J. Biochem. 189:235-241.
2. Andersson, S., D. L. Davis, H. Dahlback, H. Jornvall, and D. W. Russell. 1989. Cloning, structure, and expression of the mitochondrial cytochrome P-450 sterol 26-hydroxylase, a bile acid biosynthetic enzyme. J. Biol. Chem. 264:8222-8229.
3. Andjelkovic, M., D. R. Alessi, R. Meier, A. Fernandez, N. J. Lamb, M. Frech, P. Cron, P. Cohen, J. M. Lucocq, and B. A. Hemmings. 1997. Role of translocation in the activation and function of protein kinase B. J. Biol. Chem. 272:31515-31524.
4. Atabekov, J. G., N. P. Rodionova, O. V. Karpova, S. V. Kozlovsky, V. K. Novikov, and M. V. Arkhipenko. 2001. Translational activation of encapsidated potato virus X RNA by coat protein phosphorylation. Virology 286:466-474.
5. Beatch, M. D., and T. C. Hobman. 2000. Rubella virus capsid associates with host cell protein p32 and localizes to mitochondria. J. Virol. 74:5569-5576.
6. Cohen, P. T. 1997. Novel protein serine/threonine phosphatases: variety is the spice of life. Trends Biochem. Sci. 22:245-251.
7. Donella-Deana, A., M. H. Krinks, M. Ruzzene, C. Klee, and L. A. Pinna. 1994. Dephosphorylation of phosphopeptides by calcineurin (protein phosphatase 2B). Eur. J. Biochem. 219:109-117.
8. Duncan, R., A. Esmaili, L. J. Law, S. Bertholet, C. Hough, T. C. Hobman, and H. L. Nakhasi. 2000. Rubella virus capsid protein induces apoptosis in transfected RK13 cells. Virology 275:20-29.
9. 2-terminal domain of the Semliki Forest virus capsid protein. J. Virol. 69:1556-1563.
10. Frey, T. K. 1994. Molecular biology of rubella virus. Adv. Virus Res. 44:69-160.
11. Garbutt, M., L. J. Law, H. Chan, and T. C. Hobman. 1999. Role of rubella virus glycoprotein domains in assembly of virus-like particles. J. Virol. 73:3524-3533.
12. Gazina, E. V., J. E. Fielding, B. Lin, and D. A. Anderson. 2000. Core protein phosphorylation modulates pregenomic RNA encapsidation to different extents in human and duck hepatitis B viruses. J. Virol. 74:4721-4728.
13. Helenius, A., and M. Marsh. 1982. Endocytosis of enveloped animal viruses. Ciba Found. Symp. 92:59-76.
14. Hinman, A. R., B. S. Hersh, and C. A. de Quadros. 1998. Rational use of rubella vaccine for prevention of congenital rubella syndrome in the Americas. Rev. Panam. Salud Publica 4:156-160.
15. Hobman, T. C. 2002. Rubella, p. 2849-2852. In T. E. Creighton (ed.), Wiley encyclopedia of molecular medicine. John Wiley & Sons, Inc., New York, N.Y.
16. Hobman, T. C., M. L. Lundstrom, and S. Gillam. 1990. Processing and transport of rubella virus structural proteins in COS cells. Virology 178:122-133.
17. Hobman, T. C., L. Woodward, and M. G. Farquhar. 1993. The rubella virus E2 and E1 spike glycoproteins are targeted to the Golgi complex. J. Cell Biol. 121:269-281.
18. 2-terminal targeting motifs direct dual specificity A-kinase-anchoring protein 1 (D-AKAP1) to either mitochondria or endoplasmic reticulum. J. Cell Biol. 145:951-959.
19. Hubbard, M. J., and P. Cohen. 1993. On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci. 18:172-177.
20. Ivanov, K. I., P. Puustinen, A. Merits, M. Saarma, and K. Makinen. 2001. Phosphorylation down-regulates the RNA binding function of the coat protein of potato virus A. J. Biol. Chem. 276:13530-13540.
21. Kann, M., and W. H. Gerlich. 1994. Effect of core protein phosphorylation by protein kinase C on encapsidation of RNA within core particles of hepatitis B virus. J. Virol. 68:7993-8000.
22. Kosmopoulou, I., G. Koliakos, C. Haitoglou, D. Christodoulou, A. Dimitriadou, and A. Trakatellis. 1994. Rat liver endoplasmic reticulum protein kinases. Int. J. Biochem. 26:403-414.
23. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
24. Lan, Y. T., J. Li, W. Liao, and J. Ou. 1999. Roles of the three major phosphorylation sites of hepatitis B virus core protein in viral replication. Virology 259:342-348.
25. Law, L. M., R. Duncan, A. Esmaili, H. L. Nakhasi, and T. C. Hobman. 2001. Rubella virus E2 signal peptide is required for perinuclear localization of capsid protein and virus assembly. J. Virol. 75:1978-1983.
26. Li, G. P., M. W. La Starza, W. R. Hardy, J. H. Strauss, and C. M. Rice. 1990. Phosphorylation of Sindbis virus nsP3 in vivo and in vitro. Virology 179:416-427.
27. Liu, Z., D. Yang, Z. Qiu, K.-T. Lim, P. Chong, and S. Gillam. 1996. Identification of domains in rubella virus genomic RNA and capsid protein necessary for specific interaction. J. Virol. 70:2184-2190.
28. Maroto, B., J. C. Ramirez, and J. M. Almendral. 2000. Phosphorylation status of the parvovirus minute virus of mice particle: mapping and biological relevance of the major phosphorylation sites. J. Virol. 74:10892-10902.
29. Marr, L. D., A. Sanchez, and T. K. Frey. 1991. Efficient in vitro translation and processing of the rubella virus structural proteins in the presence of microsomes. Virology 180:400-405.
30. McCready, T. L., B. F. Islam, F. J. Schmitz, H. A. Luu, J. F. Dawson, and C. F. Holmes. 2000. Inhibition of protein phosphatase-1 by clavosines A and B. Novel members of the calyculin family of toxins. J. Biol. Chem. 275:4192-4198.
31. Mizushima, S., and S. Nagata. 1990. pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 18:5322.
32. Mochly-Rosen, D. 1995. Localization of protein kinases by anchoring proteins: a theme in signal transduction. Science 268:247-251.
33. 2-C-E2-E1-COOH. J. Virol. 51:354-358.
34. Oker-Blom, C., N. Kalkkinen, L. Kaariainen, and R. F. Pettersson. 1983. Rubella virus contains one capsid protein and three envelope glycoproteins, E1, E2a, and E2b. J. Virol. 46:964-973.
35. Pawson, T., and J. D. Scott. 1997. Signaling through scaffold, anchoring, and adaptor proteins. Science 278:2075-2080.
36. Peranen, J. 1991. Localization and phosphorylation of Semliki Forest virus non-structural protein nsP3 expressed in COS cells from a cloned cDNA. J. Gen. Virol. 72:195-199.
37. Peters, C., P. D. Andrews, M. J. Stark, S. Cesaro-Tadic, A. Glatz, A. Podtelejnikov, M. Mann, and A. Mayer. 1999. Control of the terminal step of intracellular membrane fusion by protein phosphatase 1. Science 285:1084-1087.
38. Schmidt, M. F. 1982. Acylation of viral spike glycoproteins: a feature of enveloped RNA viruses. Virology 116:327-338.
39. Sefton, B. M. 1975. Virus-dependent glycosylation. J. Virol. 17:85-93.
40. Semerikov, V. V., I. N. Lavrentyeva, V. F. Popov, M. A. Fletcher, and M. E. Kolotov. 2000. Rubella in the Russian federation: epidemiological features and control measures to prevent the congenital rubella syndrome. Epidemiol. Infect. 125:359-366.
41. Simons, K., H. Garoff, and A. Helenius. 1982. How an animal virus gets into and out of its host cell. Sci. Am. 246:58-66.
42. Suomalainen, M., H. Garoff, and M. D. Baron. 1990. The E2 signal sequence of Rubella virus remains part of the capsid protein and confers membrane association in vitro. J. Virol. 64:5500-5509.
43. Waxham, M. N., and J. S. Wolinsky. 1985. A model of the structural organization of rubella virus virions. J. Infect. Dis. 7:S133-S139.
44. Wolinsky, J. 1996. Rubella, p. 899-929. In B. N. Fields et al. (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
45. Wu, X., X. Gong, H. Foley, M. Schnell, and Z. Fu. 2002. Both viral transcription and replication are reduced when the rabies virus nucleoprotein is not phosphorylated. J. Virol. 76:4153-4161.
46. Yao, J., and S. Gillam. 1999. Mutational analysis, using a full-length rubella virus cDNA clone, of rubella virus E1 transmembrane and cytoplasmic domains required for virus release. J. Virol. 73:4622-4630.
47. Yu, M., and J. Summers. 1994. Phosphorylation of the duck hepatitis B virus capsid protein associated with conformational changes in the C terminus. J. Virol. 68:2965-2969.