Role of sindbis virus capsid protein region II in nucleocapsid core assembly and encapsidation of genomic RNA

Journal of Virology

Volumn 82, Issue 9, 2008, Pages 4461-4470

  Warrier, Ranjit ^a   Linger, Benjamin R ^b,c   Golden, Barbara L ^b   Kuhn, Richard J ^a  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CAPSID PROTEIN; GENOMIC RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; SINDBIS VIRUS; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS CORE; VIRUS NUCLEOCAPSID;

AMINO ACID SEQUENCE; CAPSID PROTEINS; GENOME, VIRAL; MUTATION; NUCLEOCAPSID; RNA, VIRAL; SINDBIS VIRUS; VIRUS ASSEMBLY;

ALPHAVIRUS; MIRIDAE; RNA VIRUSES; SINDBIS VIRUS;

EID: 42449146575     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01936-07     Document Type: Article

References (41)

1. Aliperti, G., and M. J. Schlesinger. 1978. Evidence for an autoprotease activity of Sindbis virus capsid protein. Virology 90:366-369.
2. Burge, B. W., and E. R. Pfefferkorn. 1966. Phenotypic mixing between group A arboviruses. Nature 210:1397-1399.
3. Cheng, R. H., R. J. Kuhn, N. H. Olson, M. G. Rossmann, H. K. Choi, T. J. Smith, and T. S. Baker. 1995. Nucleocapsid and glycoprotein organization in an enveloped virus. Cell 80:621-630.
4. Choi, H.-K., S. Lee, Y.-P. Zhang, B. R. McKinney, G. Wengler, M. G. Rossmann, and R. J. Kuhn. 1996. Structural analysis of Sindbis virus capsid mutants involving assembly and catalysis. J. Mol. Biol. 262:151-167.
5. Coombs, K., B. Brown, and D. T. Brown. 1984. Evidence for a change in capsid morphology during Sindbis virus envelopment. Virus Res. 1:297-302.
6. Coombs, K., and D. T. Brown. 1987. Topological organization of Sindbis virus capsid protein in isolated nucleocapsids. Virus Res. 7:131-149.
7. Forsell, K., G. Griffiths, and H. Garoff. 1996. Preformed cytoplasmic nucleocapsids are not necessary for alphavirus budding. EMBO J. 15:6495-6505.
8. Forsell, K., L. Xing, T. Kozlovska, R. H. Cheng, and H. Garoff. 2000. Membrane proteins organize a symmetrical virus. EMBO J. 19:5081-5091.
9. Geigenmüller-Gnirke, U., H. Nitschko, and S. Schlesinger. 1993. Deletion analysis of the capsid protein of Sindbis virus: identification of the RNA binding region. J. Virol. 67:1620-1626.
10. Hong, E. M., R. Perera, and R. J. Kuhn. 2006. Alphavirus capsid protein helix 1 controls a checkpoint in nucleocapsid core assembly. J. Virol. 80: 8848-8855.
11. Kuhn, R. J., Z. Hong, and J. H. Strauss. 1990. Mutagenesis of the 3′ nontranslated region of Sindbis virus RNA. J. Virol. 64:1465-1476.
12. Kuhn, R. J., H. G. M. Niesters, Z. Hong, and J. H. Strauss. 1991. Infectious RNA transcripts from Ross River virus cDNA clones and the construction and characterization of defined chimeras with Sindbis virus. Virology 182:430-441.
13. Lee, S., K. E. Owen, H. K. Choi, H. Lee, G. Lu, G. Wengler, D. T. Brown, M. G. Rossmann, and R. J. Kuhn. 1996. Identification of a protein binding site on the surface of the alphavirus nucleocapsid and its implication in virus assembly. Structure 4:531-541.
14. Linger, B. R., L. Kunovska, R. J. Kuhn, and B. L. Golden. 2004. Sindbis virus nucleocapsid assembly: RNA folding promotes capsid protein dimerization. RNA 10:128-138.
15. Lopez, S., J. S. Yao, R. J. Kuhn, E. G. Strauss, and J. H. Strauss. 1994. Nucleocapsid-glycoprotein interactions required for assembly of alphaviruses. J. Virol. 68:1316-1323.
16. Mancini, E. J., M. Clarke, B. E. Gowen, T. Rutten, and S. D. Fuller. 2000. Cryo-electron microscopy reveals the functional organization of an enveloped virus, Semliki Forest virus. Mol. Cell 5:255-266.
17. Milligan, J. F., D. R. Groebe, G. W. Witherell, and O. C. Uhlenbeck. 1987. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res. 15:8783-8798.
18. Mossessova, E., and C. D. Lima. 2000. Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol. Cell 5:865-876.
19. Mukhopadhyay, S., W. Zhang, S. Gabler, P. R. Chipman, E. G. Strauss, J. H. Strauss, T. S. Baker, R. J. Kuhn, and M. G. Rossmann. 2006. Mapping the structure and function of the E1 and E2 glycoproteins in alphaviruses. Structure 14:63-73.
20. Nicola, A. V., W. Chen, and A. Helenius. 1999. Co-translational folding of an alphavirus capsid protein in the cytosol of living cells. Nat. Cell Biol. 1:341-345.
21. O'Rourke, K., L. E. Perryman, and T. C. McGuire. 1988. Antiviral, antiglycoprotein and neutralizing antibodies in foals with equine infectious anaemia virus. J. Gen. Virol. 69:667-674.
22. Owen, K. E., and R. J. Kuhn. 1996. Identification of a region in the Sindbis virus nucleocapsid protein that is involved in specificity of RNA encapsidation. J. Virol. 70:2757-2763.
23. Paredes, A. M., D. T. Brown, R. Rothnagel, W. Chiu, R. J. Schoepp, R. E. Johnston, and B. V. Prasad. 1993. Three-dimensional structure of a membrane-containing virus. Proc. Natl. Acad. Sci. USA 90:9095-9099.
24. Pastorino, B., M. Bessaud, M. Grandadam, S. Murri, H. J. Tolou, and C. N. Peyrefitte. 2005. Development of a TaqMan RT-PCR assay without RNA extraction step for the detection and quantification of African Chikungunya viruses. J. Virol. Methods 124:65-71.
25. Perera, R., K. E. Owen, T. L. Tellinghuisen, A. E. Gorbalenya, and R. J. Kuhn. 2001. Alphavirus nucleocapsid protein contains a putative coiled coil alpha-helix important for core assembly. J. Virol. 75:1-10.
26. Rümenapf, T., D. T. Brown, E. G. Strauss, M. König, R. Rameriz-Mitchel, and J. H. Strauss. 1995. Aura alphavirus subgenomic RNA is packaged into virions of two sizes. J. Virol. 69:1741-1746.
27. Rümenapf, T., E. G. Strauss, and J. H. Strauss. 1994. Subgenomic mRNA of Aura alphavirus is packaged into virions. J. Virol. 68:56-62.
28. Schuffenecker, I., I. Iteman, A. Michault, S. Murri, L. Frangeul, M. C. Vaney, R. Lavenir, N. Pardigon, J. M. Reynes, F. Pettinelli, L. Biscornet, L. Diancourt, S. Michel, S. Duquerroy, G. Guigon, M. P. Frenkiel, A. C. Brehin, N. Cubito, P. Despres, F. Kunst, F. A. Rey, H. Zeller, and S. Brisse. 2006. Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med. 3:e263.
29. Singh, I., and A. Helenius. 1992. Role of ribosomes in Semliki Forest virus nucleocapsid uncoating. J. Virol. 66:7049-7058.
30. Skoging-Nyberg, U., and P. Liljestrom. 2001. M-X-I motif of Semliki Forest virus capsid protein affects nucleocapsid assembly. J. Virol. 75:4625-4632.
31. Strauss, J. H., and E. G. Strauss. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58:491-562.
32. Tellinghuisen, T. L., A. E. Hamburger, B. R. Fisher, R. Ostendorp, and R. J. Kuhn. 1999. In vitro assembly of alphavirus cores by using nucleocapsid protein expressed in Escherichia coli. J. Virol. 73:5309-5319.
33. Tellinghuisen, T. L., and R. J. Kuhn. 2000, Nucleic acid-dependent cross-linking of the nucleocapsid protein of Sindbis virus. J. Virol. 74:4302-4309.
34. Tellinghuisen, T. L., R. Perera, and R. J. Kuhn. 2001. Genetic engineering: principles and methods, vol. 23. Genetic and biochemical studies on the assembly of an enveloped virus, p. 83-112. Plenum Press, New York, NY.
35. Tellinghuisen, T. L., R. Perera, and R. J. Kuhn. 2001. In vitro assembly of Sindbis virus core-like particles from cross-linked dimers of truncated and mutant capsid proteins. J. Virol. 75:2810-2817.
36. Weiss, B., U. Geigenmüller-Gnirke, and S. Schlesinger. 1994. Interactions between Sindbis virus RNAs and a 68 amino acid derivative of the viral capsid protein further defines the capsid binding site. Nucleic Acids Res. 22:780-786.
37. Weiss, B., H. Nitschko, I. Ghattas, R. Wright, and S. Schlesinger. 1989. Evidence for specificity in the encapsidation of Sindbis virus RNAs. J. Virol. 63:5310-5318.
38. Wengler, G., G. Wengler, U. Boege, and K. Wahn. 1984. Establishment and analysis of a system which allows assembly and disassembly of alphavirus core-like particles under physiological condition in vitro. Virology 132:401-412.
39. Wengler, G., D. Würkner, and G. Wengler. 1992. Identification of a sequence element in the alphavirus core protein which mediates interaction of cores with ribosomes and the disassembly of cores. Virology 191:880-888.
40. Zavadova, Z., J. Zavada, and R. Weiss. 1977. Unilateral phenotypic mixing of envelope antigens between togaviruses and vesicular stomatitis virus or avian RNA tumour virus. J. Gen. Virol. 37:557-567.
41. Zhang, W., S. Mukhopadhyay, S. V. Pletnev, T. S. Baker, R. J. Kuhn, and M. G. Rossmann. 2002. Placement of the structural proteins in Sindbis virus. J. Virol. 76:11645-11658.