A key interaction between the alphavirus envelope proteins responsible for initial dimer dissociation during fusion

Journal of Virology

Volumn 87, Issue 7, 2013, Pages 3774-3781

  Fields, Whitney ^a   Kielian, Margaret ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMINO ACID; ASPARTIC ACID; GLYCOPROTEIN E1; GLYCOPROTEIN E2; HETERODIMER; HISTIDINE; HYBRID PROTEIN; LYSINE; METHIONINE; SERINE;

ALPHA VIRUS; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; EXOCYTOSIS; IMMATURE VIRUS; MATURE VIRUS; NONHUMAN; PH MEASUREMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TRANSPORT; REGULATORY MECHANISM;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; DIMERIZATION; FLUORESCENT ANTIBODY TECHNIQUE; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; MEMBRANE GLYCOPROTEINS; MUTAGENESIS; SEMLIKI FOREST VIRUS; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

ALPHAVIRUS; SEMLIKI FOREST VIRUS;

EID: 84875486890     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03310-12     Document Type: Article

References (47)

1. Kuhn RJ. 2007. Togaviridae: the viruses and their replication, p 1001- 1022. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed, vol 1. Lippincott, Williams and Wilkins, Philadelphia, PA.
2. Enserink M. 2007. Infectious diseases. Chikungunya: no longer a third world disease. Science 318:1860 -1861.
3. Schwartz O, Albert ML. 2010. Biology and pathogenesis of Chikungunya virus. Nat. Rev. Microbiol. 8:491-500.
4. Mancini EJ, Clarke M, Gowen BE, Rutten T, Fuller SD. 2000. Cryoelectron microscopy reveals the functional organization of an enveloped virus, Semliki forest virus. Mol. Cell 5:255-266.
5. Mukhopadhyay S, Zhang W, Gabler S, Chipman PR, Strauss EG, Strauss JH, Baker TS, Kuhn RJ, Rossmann MG. 2006. Mapping the structure and function of the E1 and E2 glycoproteins in alphaviruses. Structure 14:63-73.
6. Lescar J, Roussel A, Wien MW, Navaza J, Fuller SD, Wengler G, Rey FA. 2001. The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105:137-148.
7. Roussel A, Lescar J, Vaney M-C, Wengler G, Wengler G, Rey FA. 2006. Structure and interactions at the viral surface of the envelope protein E1 of Semliki Forest virus. Structure 14:75- 86.
8. Li L, Jose J, Xiang Y, Kuhn RJ, Rossmann MG. 2010. Structural changes of envelope proteins during alphavirus fusion. Nature 468:705-708.
9. Voss JE, Vaney MC, Duquerroy S, Vonrhein C, Girard-Blanc C, Crublet E, Thompson A, Bricogne G, Rey FA. 2010. Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography. Nature 468:709 -712.
10. Helenius A, Kartenbeck J, Simons K, Fries E. 1980. On the entry of Semliki Forest virus into BHK-21 cells. J. Cell Biol. 84:404-420.
11. Kielian M, Chanel-Vos C, Liao M. 2010. Alphavirus entry and membrane fusion. Viruses 2:796-825.
12. Gibbons DL, Vaney M-C, Roussel A, Vigouroux A, Reilly B, Lepault J, Kielian M, Rey FA. 2004. Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 427:320-325.
13. Zhang X, Fugere M, Day R, Kielian M. 2003. Furin processing and proteolytic activation of Semliki Forest virus. J. Virol. 77:2981-2989.
14. Sjöberg M, Lindqvist B, Garoff H. 2011. Activation of the alphavirus spike protein is suppressed by bound E3. J. Virol. 85:5644 -5650.
15. White J, Helenius A. 1980. pH-dependent fusion between the Semliki Forest virus membrane and liposomes. Proc. Natl. Acad. Sci. U. S. A. 77:3273-3277.
16. Salminen A, Wahlberg JM, Lobigs M, Liljeström 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.
17. Smit JM, Klimstra WB, Ryman KD, Bittman R, Johnston RE, Wilschut J. 2001. PE2 cleavage mutants of Sindbis virus: correlation between viral infectivity and pH-dependent membrane fusion activation of the spike heterodimer. J. Virol. 75:11196 -11204.
18. Wahlberg JM, Boere WAM, Garoff H. 1989. The heterodimeric association between the membrane proteins of Semliki Forest virus changes its sensitivity to low pH during virus maturation. J. Virol. 63:4991- 4997.
19. 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.
20. Gordon VM, Klimpel KR, Arora N, Henderson MA, Leppla SH. 1995. Proteolytic activation of bacterial toxins by eukaryotic cells is performed by furin and by additional cellular proteases. Infect. Immun. 63:82- 87.
21. Chanel-Vos C, Kielian M. 2004. A conserved histidine in the ij loop of the Semliki Forest virus E1 protein plays an important role in membrane fusion. J. Virol. 78:13543-13552.
22. Liljeström 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.
23. Liao M, Kielian M. 2005. Domain III from class II fusion proteins functions as a dominant-negative inhibitor of virus-membrane fusion. J. Cell Biol. 171:111-120.
24. Justman J, Klimjack MR, Kielian M. 1993. Role of spike protein conformational changes in fusion of Semliki Forest virus. J. Virol. 67:7597-7607.
25. Kielian M, Jungerwirth S, Sayad KU, DeCandido S. 1990. Biosynthesis, maturation, and acid-activation of the Semliki Forest virus fusion protein. J. Virol. 64:4614-4624.
26. Gibbons DL, Ahn A, Liao M, Hammar L, Cheng RH, Kielian M. 2004. Multistep regulation of membrane insertion of the fusion peptide of Semliki Forest virus. J. Virol. 78:3312-3318.
27. Chanel-Vos C, Kielian M. 2006. Second-site revertants of a Semliki Forest virus fusion-block mutation reveal the dynamics of a class II membrane fusion protein. J. Virol. 80:6115- 6122.
28. Zhang X, Kielian M. 2005. An interaction site of the envelope proteins of Semliki Forest virus that is preserved after proteolytic activation. Virology 337:344 -352.
29. 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.
30. Chatterjee PK, Eng CH, Kielian M. 2002. Novel mutations that control the sphingolipid and cholesterol dependence of the Semliki Forest virus fusion protein. J. Virol. 76:12712-12722.
31. Duffus WA, Levy-Mintz P, Klimjack MR, Kielian M. 1995. Mutations in the putative fusion peptide of Semliki Forest virus affect spike protein oligomerization and virus assembly. J. Virol. 69:2471-2479.
32. Levy-Mintz P, Kielian M. 1991. Mutagenesis of the putative fusion domain of the Semliki Forest virus spike protein. J. Virol. 65:4292- 4300.
33. Hubbard SC. 1988. Regulation of glycosylation. The influence of protein structure on N-linked oligosaccharide processing. J. Biol. Chem. 263: 19303-19317.
34. Neblock DS, Berg RA. 1982. Lysosomotropic agents ammonium chloride and chloroquine inhibit both the synthesis and secretion of procollagen by freshly isolated embryonic chick tendon cells. Biochem. Biophys. Res. Commun. 105:902-908.
35. Paroutis P, Touret N, Grinstein S. 2004. The pH of the secretory pathway: measurement, determinants, and regulation. Physiology (Bethesda) 19:207-215.
36. Lu YE, Eng CH, Shome SG, Kielian M. 2001. In vivo generation and characterization of a soluble form of the Semliki Forest virus fusion protein. J. Virol. 75:8329-8339.
37. Zhao H, Garoff H. 1992. Role of cell surface spikes in alphavirus budding. J. Virol. 66:7089 -7095.
38. Heidner HW, Johnston RE. 1994. The amino-terminal residue of Sindbis virus glycoprotein E2 influences virus maturation, specific infectivity for BHK cells, and virulence in mice. J. Virol. 68:8064-8070.
39. Zhang R, Hryc CF, Cong Y, Liu X, Jakana J, Gorchakov R, Baker ML, Weaver SC, Chiu W. 2011. 4.4 Å cryo-EM structure of an enveloped alphavirus Venezuelan equine encephalitis virus. EMBO J. 30:3854 -3863.
40. Zhang W, Mukhopadhyay S, Pletnev SV, Baker TS, Kuhn RJ, Rossmann MG. 2002. Placement of the structural proteins in Sindbis virus. J. Virol. 76:11645-11658.
41. Harrison SC. 2008. The pH sensor for flavivirus membrane fusion. J. Cell Biol. 183:177-179.
42. Sánchez-San Martín C, Liu CY, Kielian M. 2009. Dealing with low pH: entry and exit of alphaviruses and flaviviruses. Trends Microbiol. 17:514-521.
43. Glomb-Reinmund S, Kielian M. 1998. fus-1, a pH-shift mutant of Semliki Forest virus, acts by altering spike subunit interactions via a mutation in the E2 subunit. J. Virol. 72:4281- 4287.
44. Klimjack MR, Jeffrey S, Kielian M. 1994. Membrane and protein interactions of a soluble form of the Semliki Forest virus fusion protein. J. Virol. 68:6940-6946.
45. Qin ZL, Zheng Y, Kielian M. 2009. Role of conserved histidine residues in the low-pH dependence of the Semliki Forest virus fusion protein. J. Virol. 83:4670-4677.
46. Zheng Y, Sanchez-San Martin C, Qin ZL, Kielian M. 2011. The domain I-domain III linker plays an important role in the fusogenic conformational change of the alphavirus membrane fusion protein. J. Virol. 85: 6334-6342.
47. DeLano WL. 2002. The PyMOL user's manual. DeLano Scientific, San Carlos, CA.