Characterization of pH-sensitive molecular switches that trigger the structural transition of vesicular stomatitis virus glycoprotein from the postfusion state toward the prefusion state

Journal of Virology

Volumn 88, Issue 22, 2014, Pages 13396-13409

  Ferlin, Anna ^a   Raux, Hélène ^a   Baquero, Eduard ^a   Lepault, Jean ^a   Gaudin, Yves ^a  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; VIRUS GLYCOPROTEIN; G PROTEIN, VESICULAR STOMATITIS VIRUS; MEMBRANE PROTEIN; MUTANT PROTEIN; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; EMBRYO; GLYCOPROTEIN GENE; GOLGI COMPLEX; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PH MEASUREMENT; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN TRANSPORT; VESICULAR STOMATITIS; VESICULAR STOMATITIS VIRUS; VIRUS GENOME; VIRUS MUTATION; VIRUS RECOMBINANT; ANIMAL; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; DNA MUTATIONAL ANALYSIS; DRUG EFFECTS; GENETICS; PH; PHYSIOLOGY; PROTEIN CONFORMATION; VESICULOVIRUS; VIRUS ENTRY; X RAY CRYSTALLOGRAPHY;

ANIMALS; CELL LINE; CRYSTALLOGRAPHY, X-RAY; DNA MUTATIONAL ANALYSIS; HUMANS; HYDROGEN-ION CONCENTRATION; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; MUTANT PROTEINS; PROTEIN CONFORMATION; VESICULOVIRUS; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EID: 84908388229     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01962-14     Document Type: Article

References (41)

1. Albertini A, Bressanelli S, Lepault J, Gaudin Y. 2011. Structure and working of viral fusion machinery. Curr. Top. Membr. 68:49-80. http://dx.doi.org/10.1016/B978-0-12-385891-7.00003-9.
2. Harrison SC. 2008. Viral membrane fusion. Nat. Struct. Mol. Biol. 15: 690-698. http://dx.doi.org/10.1038/nsmb.1456.
3. Li Y, Modis Y. 2014. A novel membrane fusion protein family in Flaviviridae? Trends Microbiol. 22:176-182. http://dx.doi.org/10.1016/j.tim.2014.01.008.
4. Gaudin Y. 2000. Reversibility in fusion protein conformational changes. The intriguing case of rhabdovirus-induced membrane fusion. Subcell. Biochem. 34:379-408. http://dx.doi.org/10.1007/0-306-46824-7_10.
5. Anderson RG, Orci L. 1988. A view of acidic intracellular compartments. J. Cell Biol. 106:539-543. http://dx.doi.org/10.1083/jcb.106.3.539.
6. Sugrue RJ, Bahadur G, Zambon MC, Hall-Smith M, Douglas AR, Hay AJ. 1990. Specific structural alteration of the influenza haemagglutinin by amantadine. EMBO J. 9:3469-3476.
7. Pinto LH, Holsinger LJ, Lamb RA. 1992. Influenza virus M2 protein has ion channel activity. Cell 69:517-528. http://dx.doi.org/10.1016/0092-8674(92)90452-I.
8. Stieneke-Grober A, Vey M, Angliker H, Shaw E, Thomas G, Roberts C, Klenk HD, Garten W. 1992. Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J. 11:2407-2414.
9. Skehel JJ, Wiley DC. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531-569. http://dx.doi.org/10.1146/annurev.biochem.69.1.531.
10. Heinz FX, Stiasny K, Puschner-Auer G, Holzmann H, Allison SL, Mandl CW, Kunz C. 1994. Structural changes and functional control of the tick-borne encephalitis virus glycoprotein E by the heterodimeric association with protein prM. Virology 198:109-117. http://dx.doi.org/10.1006/viro.1994.1013.
11. Lobigs M, Garoff H. 1990. Fusion function of the Semliki Forest virus spike is activated by proteolytic cleavage of the envelope glycoprotein precursor p62. J. Virol. 64:1233-1240.
12. Rose JK, Whitt MA. 2001. Rhabdoviridae: the viruses and their replication, p 1221-1224. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
13. Albertini AAV, Baquero E, Ferlin A, Gaudin Y. 2012. Molecular and cellular aspects of rhabdovirus entry. Viruses 4:117-139. http://dx.doi.org/10.3390/v4010117.
14. Doms RW, Keller DS, Helenius A, Balch WE. 1987. Role for adenosine triphosphate in regulating the assembly and transport of vesicular stomatitis virus G protein trimers. J. Cell Biol. 105:1957-1969. http://dx.doi.org/10.1083/jcb.105.5.1957.
15. Gaudin Y, Ruigrok RW, Knossow M, Flamand A. 1993. Low-pH conformational changes of rabies virus glycoprotein and their role in membrane fusion. J. Virol. 67:1365-1372.
16. Libersou S, Albertini AA, Ouldali M, Maury V, Maheu C, Raux H, de Haas F, Roche S, Gaudin Y, Lepault J. 2010. Distinct structural rearrangements of the VSV glycoprotein drive membrane fusion. J. Cell Biol. 191:199-210. http://dx.doi.org/10.1083/jcb.201006116.
17. Albertini AA, Merigoux C, Libersou S, Madiona K, Bressanelli S, Roche S, Lepault J, Melki R, Vachette P, Gaudin Y. 2012. Characterization of monomeric intermediates during VSV glycoprotein structural transition. PLoS Pathog. 8:e1002556. http://dx.doi.org/10.1371/journal.ppat.1002556.
18. Roche S, Gaudin Y. 2002. Characterization of the equilibrium between the native and fusion-inactive conformation of rabies virus glycoprotein indicates that the fusion complex is made of several trimers. Virology 297:128-135. http://dx.doi.org/10.1006/viro.2002.1429.
19. Gaudin Y, Tuffereau C, Durrer P, Flamand A, Ruigrok RW. 1995. Biological function of the low-pH, fusion-inactive conformation of rabies virus glycoprotein (G): G is transported in a fusion-inactive state-like conformation. J. Virol. 69:5528-5534.
20. Roche S, Rey FA, Gaudin Y, Bressanelli S. 2007. Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G. Science 315: 843-848. http://dx.doi.org/10.1126/science.1135710.
21. Roche S, Bressanelli S, Rey FA, Gaudin Y. 2006. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313:187-191. http://dx.doi.org/10.1126/science.1127683.
22. Sun X, Belouzard S, Whittaker GR. 2008. Molecular architecture of the bipartite fusion loops of vesicular stomatitis virus glycoprotein G, a class III viral fusion protein. J. Biol. Chem. 283:6418-6427. http://dx.doi.org/10.1074/jbc.M708955200.
23. Stanifer ML, Cureton DK, Whelan SP. 2011. A recombinant vesicular stomatitis virus bearing a lethal mutation in the glycoprotein gene uncovers a second site suppressor that restores fusion. J. Virol. 85:8105-8115. http://dx.doi.org/10.1128/JVI.00735-11.
24. Baquero E, Albertini AA, Vachette P, Lepault J, Bressanelli S, Gaudin Y. 2013. Intermediate conformations during viral fusion glycoprotein structural transition. Curr. Opin. Virol. 3:143-150. http://dx.doi.org/10.1016/j.coviro.2013.03.006.
25. Pasdeloup D, Poisson N, Raux H, Gaudin Y, Ruigrok RW, Blondel D. 2005. Nucleocytoplasmic shuttling of the rabies virus P protein requires a nuclear localization signal and a CRM1-dependent nuclear export signal. Virology 334:284-293. http://dx.doi.org/10.1016/j.virol.2005.02.005.
26. Matsuura Y, Tani H, Suzuki K, Kimura-Someya T, Suzuki R, Aizaki H, Ishii K, Moriishi K, Robison CS, Whitt MA, Miyamura T. 2001. Characterization of pseudotype VSV possessing HCV envelope proteins. Virology 286:263-275. http://dx.doi.org/10.1006/viro.2001.0971.
27. Tani H, Komoda Y, Matsuo E, Suzuki K, Hamamoto I, Yamashita T, Moriishi K, Fujiyama K, Kanto T, Hayashi N, Owsianka A, Patel AH, Whitt MA, Matsuura Y. 2007. Replication-competent recombinant vesicular stomatitis virus encoding hepatitis C virus envelope proteins. J. Virol. 81:8601-8612. http://dx.doi.org/10.1128/JVI.00608-07.
28. Lawson ND, Stillman EA, Whitt MA, Rose JK. 1995. Recombinant vesicular stomatitis viruses from DNA. Proc. Natl. Acad. Sci. U. S. A. 92:4477-4481. http://dx.doi.org/10.1073/pnas.92.10.4477.
29. Schnell MJ, Buonocore L, Whitt MA, Rose JK. 1996. The minimal conserved transcription stop-start signal promotes stable expression of a foreign gene in vesicular stomatitis virus. J. Virol. 70:2318-2323.
30. Hammond C, Helenius A. 1995. Quality control in the secretory pathway. Curr. Opin. Cell Biol. 7:523-529. http://dx.doi.org/10.1016/0955-0674(95)80009-3.
31. Dunphy WG, Rothman JE. 1985. Compartmental organization of the Golgi stack. Cell 42:13-21. http://dx.doi.org/10.1016/S0092-8674(85)80097-0.
32. Desmezieres E, Maillard AP, Gaudin Y, Tordo N, Perrin P. 2003. Differential stability and fusion activity of lyssavirus glycoprotein trimers. Virus Res. 91:181-187. http://dx.doi.org/10.1016/S0168-1702(02)00267-8.
33. Jeetendra E, Ghosh K, Odell D, Li J, Ghosh HP, Whitt MA. 2003. The membrane-proximal region of vesicular stomatitis virus glycoprotein G ectodomain is critical for fusion and virus infectivity. J. Virol. 77:12807-12818. http://dx.doi.org/10.1128/JVI.77.23.12807-12818.2003.
34. Nakai T, Howatson AF. 1968. The fine structure of vesicular stomatitis virus. Virology 35:268-281. http://dx.doi.org/10.1016/0042-6822(68)90267-5.
35. Brown JC, Newcomb WW, Lawrenz-Smith S. 1988. pH-dependent accumulation of the vesicular stomatitis virus glycoprotein at the ends of intact virions. Virology 167:625-629. http://dx.doi.org/10.1016/0042-6822(88)90126-2.
36. Barge A, Gaudin Y, Coulon P, Ruigrok RW. 1993. Vesicular stomatitis virusMprotein may be inside the ribonucleocapsid coil. J. Virol. 67:7246-7253.
37. Roche S, Albertini AA, Lepault J, Bressanelli S, Gaudin Y. 2008. Structures of vesicular stomatitis virus glycoprotein: membrane fusion revisited. Cell. Mol. Life Sci. 65:1716-1728. http://dx.doi.org/10.1007/s00018-008-7534-3.
38. 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. http://dx.doi.org/10.1128/JVI.02646-08.
39. Fritz R, Stiasny K, Heinz FX. 2008. Identification of specific histidines as pH sensors in flavivirus membrane fusion. J. Cell Biol. 183:353-361. http://dx.doi.org/10.1083/jcb.200806081.
40. Obiang L, Raux H, Ouldali M, Blondel D, Gaudin Y. 2012. Phenotypes of vesicular stomatitis virus mutants with mutations in the PSAP motif of the matrix protein. J. Gen. Virol. 93:857-865. http://dx.doi.org/10.1099/vir.0.039800-0.
41. Grigorov B, Rabilloud J, Lawrence P, Gerlier D. 2011. Rapid titration of measles and other viruses: optimization with determination of replication cycle length. PLoS One 6:e24135. http://dx.doi.org/10.1371/journal.pone.0024135.