Probing the early temporal and spatial interaction of the sindbis virus capsid and E2 proteins with reverse genetics

Journal of Virology

Volumn 86, Issue 22, 2012, Pages 12372-12383

  Snyder, Jonathan E ^a   Berrios, Christian J ^a,c   Edwards, Thomas J ^a   Jose, Joyce ^a   Perera, Rushika ^a   Kuhna, Richard J ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; ENVELOPE PROTEIN; GLYCOPROTEIN E2; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BUDDING; CELL AGGREGATION; CELL VACUOLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOPLASM; ESCHERICHIA COLI; GENE EXPRESSION SYSTEM; IN VITRO STUDY; MAMMAL CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; REVERSE GENETICS; SINDBIS VIRUS; VIRUS CAPSID; VIRUS INFECTION; VIRUS NUCLEOCAPSID; VIRUS PARTICLE; VIRUS RELEASE;

AMINO ACID MOTIFS; ANIMALS; CAPSID; CELL LINE; CRICETINAE; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; MICROSCOPY, ELECTRON; MUTATION; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; SINDBIS VIRUS; VIRAL ENVELOPE PROTEINS;

ESCHERICHIA COLI; MAMMALIA; MIRIDAE; SINDBIS VIRUS;

EID: 84869112226     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01220-12     Document Type: Article

References (53)

1. Akahata W, et al. 2010. A virus-like particle vaccine for epidemic Chikungunya virus protects nonhuman primates against infection. Nat. Med.16:334-338.
2. Bonatti S, Migliaccio G, Blobel G, Walter P. 1984. Role of signal recognition particle in the membrane assembly of Sindbis viral glycoproteins. Eur. J. Biochem. 140:499-502.
3. Byrnes AP, Griffin DE. 1998. Binding of Sindbis virus to cell surface heparan sulfate. J. Virol. 72:7349-7356.
4. Cheng RH, et al. 1995. Nucleocapsid and glycoprotein organization in an enveloped virus. Cell 80:621-630.
5. Choi HK, et al. 1991. Structure of Sindbis virus core protein reveals a chymotrypsin-like serine proteinase and the organization of the virion. Nature 354:37-43.
6. Cristea IM, et al. 2010. Host factors associated with the Sindbis virus RNA-dependent RNA polymerase: role for G3BP1 and G3BP2 in virus replication. J. Virol. 84:6720-6732.
7. Dokland T. 1999. Scaffolding proteins and their role in viral assembly. Cell. Mol. Life Sci. 56:580-603.
8. Elrad OM, Hagan MF. 2010. Encapsulation of a polymer by an icosahedral virus. Phys Biol. 7:045003. doi:10.1088/1478-3975/7/4/045003.
9. Forsell K, Griffiths G, Garoff H. 1996. Preformed cytoplasmic nucleocapsids are not necessary for alphavirus budding. EMBO J. 15:6495-6505.
10. Frolova EI, Gorchakov R, Pereboeva L, Atasheva S, Frolov I. 2010. Functional Sindbis virus replicative complexes are formed at the plasma membrane. J. Virol. 84:11679-11695.
11. Froshauer S, Kartenbeck J, Helenius A. 1988. Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. J. Cell Biol. 107:2075-2086.
12. Fuller SD, Berriman JA, Butcher SJ, Gowen BE. 1995. Low pH induces swiveling of the glycoprotein heterodimers in the Semliki Forest virus spike complex. Cell 81:715-725.
13. Gaedigk-Nitschko K, Schlesinger MJ. 1991. Site-directed mutations in Sindbis virus E2 glycoprotein's cytoplasmic domain and the 6K protein lead to similar defects in virus assembly and budding. Virology 183:206-214.
14. Garoff H, Frischauf AM, Simons K, Lehrach H, Delius H. 1980. Nucleotide sequence of cdna coding for Semliki Forest virus membrane glycoproteins. Nature 288:236-241.
15. Garoff H, Simons K. 1974. Location of the spike glycoproteins in the Semliki Forest virus membrane. Proc. Natl. Acad. Sci. U. S. A. 71:3988-3992.
16. Garoff H, Sjoberg M, Cheng RH. 2004. Budding of alphaviruses. Virus Res. 106:103-116.
17. Garoff H, Soderlund H. 1978. The amphiphilic membrane glycoproteins of Semliki Forest virus are attached to the lipid bilayer by their COOHterminal ends. J. Mol. Biol. 124:535-549.
18. Gorchakov R, Garmashova N, Frolova E, Frolov I. 2008. Different types of nsP3-containing protein complexes in Sindbis virus-infected cells. J. Virol. 82:10088-10101.
19. Griffiths G, et al. 1989. The dynamic nature of the Golgi complex. J. Cell Biol. 108:277-297.
20. Gualtieri EJ, et al. 2011. Detection of membrane protein twodimensional crystals in living cells. Biophys. J. 100:207-214.
21. Hagan MF, Elrad OM. 2010. Understanding the concentration dependence of viral capsid assembly kinetics-the origin of the lag time and identifying the critical nucleus size. Biophys. J. 98:1065-1074.
22. Jose J, et al. 2012. Interactions of the cytoplasmic domain of Sindbis virus E2 with nucleocapsid cores promote alphavirus budding. J. Virol. 86:2585-2599.
23. Kail M, et al. 1991. The cytoplasmic domain of alphavirus E2 glycoprotein contains a short linear recognition signal required for viral budding. EMBO J. 10:2343-2351.
24. Klimstra WB, Ryman KD, Johnston RE. 1998. Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J. Virol. 72:7357-7366.
25. Lee S, et al. 1996. Identification of a protein binding site on the surface of the alphavirus nucleocapsid and its implication in virus assembly. Structure 4:531-541.
26. Liljeström P, Garoff H. 1991. Internally located cleavable signal sequences direct the formation of Semliki Forest virus membrane proteins from a polyprotein precursor. J. Virol. 65:147-154.
27. Linger BR, Kunovska L, Kuhn RJ, Golden BL. 2004. Sindbis virus nucleocapsid assembly: RNA folding promotes capsid protein dimerization. RNA 10:128-138.
28. Liu N, Brown DT. 1993. Transient translocation of the cytoplasmic (endo) domain of a type I membrane glycoprotein into cellular membranes. J. Cell Biol. 120:877-883.
29. Lopez S, Yao JS, Kuhn RJ, Strauss EG, Strauss JH. 1994. Nucleocapsid-glycoprotein interactions required for assembly of alphaviruses. J. Virol. 68:1316-1323.
30. Melancon P, Garoff H. 1987. Processing of the Semliki Forest virus structural polyprotein: role of the capsid protease. J. Virol. 61:1301-1309.
31. Metsikkö K, Garoff H. 1990. Oligomers of the cytoplasmic domain of the p62/E2 membrane protein of Semliki Forest virus bind to the nucleocapsid in vitro. J. Virol. 64:4678-4683.
32. Mukhopadhyay S, Chipman PR, Hong EM, Kuhn RJ, Rossmann MG. 2002. In vitro-assembled alphavirus core-like particles maintain a structure similar to that of nucleocapsid cores in mature virus. J. Virol. 76:11128-11132.
33. Mukhopadhyay S, et al. 2006. Mapping the structure and function of the E1 and E2 glycoproteins in alphavirusesStructure 14:63-73.
34. Mulvey M, Brown DT. 1996. Assembly of the Sindbis virus spike protein complex. Virology 219:125-132.
35. Neuvonen M, et al. 2011. SH3 domain-mediated recruitment of host cell amphiphysins by alphavirus nsP3 promotes viral RNA replication. PLoS Pathog. 7:e1002383. doi:10.1371/journal.ppat.1002383.
36. Owen KE, Kuhn RJ. 1997. Alphavirus budding is dependent on the interaction between the nucleocapsid and hydrophobic amino acids on the cytoplasmic domain of the E2 envelope glycoprotein. Virology 230:187-196.
37. Schwartz M, Chen J, Lee WM, Janda M, Ahlquist P. 2004. Alternate,virus-induced membrane rearrangements support positive-strand RNA virus genome replication. Proc. Natl. Acad. Sci. U. S. A. 101:11263-11268.
38. Skoging U, Vihinen M, Nilsson L, Liljestrom P. 1996. Aromatic interactions define the binding of the alphavirus spike to its nucleocapsid. Structure 4:519-529.
39. Snyder JE, et al. 2011. Rescue of infectious particles from preassembled alphavirus nucleocapsid cores. J. Virol. 85:5773-5781.
40. Söderlund H. 1973. Kinetics of formation of the Semliki Forest virus nucleocapsid. Intervirology 1:354-361.
41. Soonsawad P, et al. 2010. Structural evidence of glycoprotein assembly in cellular membrane compartments prior to alphavirus budding. J. Virol.84:11145-11151.
42. Strauss JH, Strauss EG. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58:491-562.
43. Suomalainen M, Liljestrom P, Garoff H. 1992. Spike proteinnucleocapsid interactions drive the budding of alphaviruses. J. Virol. 66:4737-4747.
44. Tang J, et al. 2011. Molecular links between the E2 envelope glycoprotein and nucleocapsid core in Sindbis virus. J. Mol. Biol. 414:442-459.
45. Tellinghuisen TL, Hamburger AE, Fisher BR, Ostendorp R, Kuhn RJ.1999. In vitro assembly of alphavirus cores by using nucleocapsid protein expressed in Escherichia coli. J. Virol. 73:5309-5319.
46. Tellinghuisen TL, Kuhn RJ. 2000. Nucleic acid-dependent cross-linking of the nucleocapsid protein of Sindbis virus. J. Virol. 74:4302-4309.
47. Thiboutot MM, et al. 2010. Chikungunya: a potentially emerging epidemic? PLoS Negl. Trop. Dis. 4:e623. doi:10.1371/journal.pntd.0000623.
48. Tong L, Choi HK, Minor W, Rossmann MG. 1992. The structure determination of Sindbis virus core protein using isomorphous replacement and molecular replacement averaging between two crystal forms. Acta Crystallogr. A 48(Pt 4):430-442
49. von Bonsdorff CH, Harrison SC. 1978. Hexagonal glycoprotein arrays from Sindbis virus membranes. J. Virol. 28:578-583.
50. Wahlberg JM, Bron R, Wilschut J, Garoff H. 1992. Membrane fusion of Semliki Forest virus involves homotrimers of the fusion protein. J. Virol.66:7309-7318.
51. Wilkinson TA, Tellinghuisen TL, Kuhn RJ, Post CB. 2005. Association of Sindbis virus capsid protein with phospholipid membranes and the glycoprotein: implications for alphavirus assembly. Biochemistry 44:2800-281.
52. Zhang X, Fugere M, Day R, Kielian M. 2003. Furin processing and proteolytic activation of Semliki Forest virus. J. Virol. 77:2981-2989.
53. Zhao H, Lindqvist B, Garoff H, von Bonsdorff CH, Liljestrom P. 1994. A tyrosine-based motif in the cytoplasmic domain of the alphavirus envelope protein is essential for budding. EMBO J. 13:4204-4211.