The alphavirus E3 glycoprotein functions in a clade-specific manner

Journal of Virology

Volumn 86, Issue 24, 2012, Pages 13609-13620

  Snyder, Anthony J ^a   Mukhopadhyay, Suchetana ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN E3; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ALPHA VIRUS; ARTICLE; CLADISTICS; CONTROLLED STUDY; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVERTANT; SPIKE; TRANSMISSION ELECTRON MICROSCOPY; VIRUS GENOME; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS STRAIN; WILD TYPE;

ALPHAVIRUS; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL LINE; CRICETINAE; DNA PRIMERS; GLYCOPROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL PROTEINS;

ALPHAVIRUS;

EID: 84870667470     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01805-12     Document Type: Article

References (55)

1. Akahata W, Nabel GJ. 2012. A specific domain of the Chikungunya virus E2 protein regulates particle formation in human cells: implications for alphavirus vaccine design. J. Virol. 86:8879-8883.
2. Bonatti S, Blobel G. 1979. Absence of a cleavable signal sequence in Sindbis virus glycoprotein PE2. J. Biol. Chem. 254:12261-12264.
3. 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.
4. Byrnes AP, Griffin DE. 1998. Binding of Sindbis virus to cell surface heparan sulfate. J. Virol. 72:7349-7356.
5. Cheng RH, et al. 1995. Nucleocapsid and glycoprotein organization in an enveloped virus. Cell 80:621-630.
6. de Curtis I, Simons K. 1988. Dissection of Semliki Forest virus glycoprotein delivery from the trans-Golgi network to the cell surface in permeabilized BHK cells. Proc. Natl. Acad. Sci. U. S. A. 85:8052-8056.
7. Elshuber S, Allison SL, Heinz FX, Mandl CW. 2003. Cleavage of protein prM is necessary for infection of BHK-21 cells by tick-borne encephalitis virus. J. Gen. Virol. 84:183-191.
8. Firth AE, Chung BY, Fleeton MN, Atkins JF. 2008. Discovery of frameshifting in alphavirus 6K resolves a 20-year enigma. Virol. J. 5:108.
9. Forrester NL, et al. 2012. Genome-scale phylogeny of the alphavirus genus suggests a marine origin. J. Virol. 86:2729-2738.
10. Gahmberg CG, Utermann G, Simons K. 1972. The membrane proteins of Semliki Forest virus have a hydrophobic part attached to the viral membrane. FEBS Lett. 28:179-182.
11. 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.
12. Garoff H, Simons K, Renkonen O. 1974. Isolation and characterization of the membrane proteins of Semliki Forest virus. Virology 61:493-504.
13. Goujon M, et al. 2010. A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res. 38:W695-W699. doi:10.1093/nar/gkq313.
14. Guirakhoo F, Bolin RA, Roehrig JT. 1992. The Murray Valley encephalitis virus prM protein confers acid resistance to virus particles and alters the expression of epitopes within the R2 domain of E glycoprotein. Virology 191:921-931.
15. Guirakhoo F, Heinz FX, Mandl CW, Holzmann H, Kunz C. 1991. Fusion activity of flaviviruses: comparison of mature and immature (prM-containing) tick-borne encephalitis virions. J. Gen. Virol. 72(Pt 6): 1323-1329.
16. Harrison SC. 2008. Viral membrane fusion. Nat. Struct. Mol. Biol. 15: 690-698.
17. Jain SK, DeCandido S, Kielian M. 1991. Processing of the p62 envelope
18. 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.
19. Kuhn RJ, Niesters HG, Hong Z, Strauss JH. 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.
20. Larkin MA, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
21. Li L, Jose J, Xiang Y, Kuhn RJ, Rossmann MG. 2010. Structural changes of envelope proteins during alphavirus fusion. Nature 468:705-708.
22. Li L, et al. 2008. The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 319:1830-1834.
23. Liljestrom 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.
24. Liljestrom P, Lusa S, Huylebroeck D, Garoff H. 1991. In vitro mutagenesis of a full-length cDNA clone of Semliki Forest virus: the small 6,000-molecular-weight membrane protein modulates virus release. J. Virol. 65: 4107-4113.
25. Lobigs M, Wahlberg JM, Garoff H. 1990. Spike protein oligomerization control of Semliki Forest virus fusion. J. Virol. 64:5214-5218.
26. Lobigs M, Zhao HX, Garoff H. 1990. Function of Semliki Forest virus E3 peptide in virus assembly: replacement of E3 with an artificial signal peptide abolishes spike heterodimerization and surface expression of E1. J. Virol. 64:4346-4355.
27. Lopez S, Yao JS, Kuhn RJ, Strauss EG, Strauss JH. 1994. Nucleocapsidglycoprotein interactions required for assembly of alphaviruses. J. Virol. 68:1316-1323.
28. Lorenz IC, Allison SL, Heinz FX, Helenius A. 2002. Folding and dimerization of tick-borne encephalitis virus envelope proteins prM and E in the endoplasmic reticulum. J. Virol. 76:5480-5491.
29. Lustig S, et al. 1988. Molecular basis of Sindbis virus neurovirulence in mice. J. Virol. 62:2329-2336.
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. Mulvey M, Brown DT. 1996. Assembly of the Sindbis virus spike protein complex. Virology 219:125-132.
32. Omar A, Koblet H. 1988. Semliki Forest virus particles containing only the E1 envelope glycoprotein are infectious and can induce cell-cell fusion. Virology 166:17-23.
33. Owen KE, Kuhn RJ. 1996. Identification of a region in the Sindbis virus nucleocapsid protein that is involved in specificity of RNA encapsidation. J. Virol. 70:2757-2763.
34. Parrott MM, et al. 2009. Role of conserved cysteines in the alphavirus E3 protein. J. Virol. 83:2584-2591.
35. Rice CM, Bell JR, Hunkapiller MW, Strauss EG, Strauss JH. 1982. Isolation and characterization of the hydrophobic COOH-terminal domains of the Sindbis virion glycoproteins. J. Mol. Biol. 154:355-378.
36. Rumenapf T, Strauss EG, Strauss JH. 1994. Subgenomic mRNA of Aura alphavirus is packaged into virions. J. Virol. 68:56-62.
37. Salminen A, Wahlberg JM, Lobigs M, Liljestrom P, Garoff H. 1992. Membrane fusion process of Semliki Forest virus. II. Cleavage-dependent reorganization of the spike protein complex controls virus entry. J. Cell Biol. 116:349-357.
38. Sjoberg M, Lindqvist B, Garoff H. 2011. Activation of the alphavirus spike protein is suppressed by bound E3. J. Virol. 85:5644-5650.
39. Smith TJ, et al. 1995. Putative receptor binding sites on alphaviruses as visualized by cryoelectron microscopy. Proc. Natl. Acad. Sci. U. S. A. 92: 10648-10652.
40. Snyder AJ, Sokoloski KJ, Mukhopadhyay S. 2012. Mutating conserved cysteines in the alphavirus e2 glycoprotein causes virus-specific assembly defects. J. Virol. 86:3100-3111.
41. Sokoloski KJ, et al. 2012. Sindbis virus infectivity improves during the course of infection in both mammalian and mosquito cells. Virus Res. 167:26-33.
42. Stadler K, Allison SL, Schalich J, Heinz FX. 1997. Proteolytic activation of tick-borne encephalitis virus by furin. J. Virol. 71:8475-8481.
43. Strauss JH, Strauss EG. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58:491-562.
44. von Bonsdorff CH, Harrison SC. 1978. Hexagonal glycoprotein arrays from Sindbis virus membranes. J. Virol. 28:578-583.
45. Voss JE, et al. 2010. Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography. Nature 468:709-712.
46. Wahlberg JM, Boere WA, Garoff H. 1989. The heterodimeric association E3 Chimeric Alphaviruses between the membrane proteins of Semliki Forest virus changes its sensitivity to low pH during virus maturation. J. Virol. 63:4991-4997.
47. Wahlberg JM, Garoff H. 1992. Membrane fusion process of Semliki Forest virus. I. Low pH-induced rearrangement in spike protein quaternary structure precedes virus penetration into cells. J. Cell Biol. 116:339-348.
48. Woycechowsky KJ, Wittrup KD, Raines RT. 1999. A small-molecule catalyst of protein folding in vitro and in vivo. Chem. Biol. 6:871-879.
49. Zhang R, et al. 2011. 4.4 Å cryo-EM structure of an enveloped alphavirus Venezuelan equine encephalitis virus. EMBO J. 30:3854-3863.
50. Zhang RM, Snyder GH. 1989. Dependence of formation of small disulfide loops in two-cysteine peptides on the number and types of intervening amino acids. J. Biol. Chem. 264:18472-18479.
51. Zhang X, Fugere M, Day R, Kielian M. 2003. Furin processing and proteolytic activation of Semliki Forest virus. J. Virol. 77:2981-2989.
52. Zhang X, Kielian M. 2004. Mutations that promote furin-independent growth of Semliki Forest virus affect p62-E1 interactions and membrane fusion. Virology 327:287-296.
53. Zhang Y, et al. 2003. Structures of immature flavivirus particles. EMBO J. 22:2604-2613.
54. Zhang Y, et al. 2004. Conformational changes of the flavivirus E glycoprotein. Structure 12:1607-1618.
55. Zybert IA, van der Ende-Metselaar H, Wilschut J, Smit JM. 2008. Functional importance of dengue virus maturation: infectious properties of immature virions. J. Gen. Virol. 89:3047-3051.