Charged residues are involved in membrane fusion mediated by a hydrophilic peptide located in vesicular stomatitis virus G protein

Molecular Membrane Biology

Volumn 23, Issue 5, 2006, Pages 396-406

  Carneiro, Fabiana A ^a   Vandenbussche, Guy ^b   Juliano, Maria A ^c   Juliano, Luiz ^c   Ruysschaert, Jean Marie ^b   Da Poian, Andrea T ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Dicyclohexylcarbodiimide; Fusion peptide; Hydrophobicity; Membrane fusion; Vesicular stomatitis virus

Indexed keywords

ASPARTIC ACID; DICYCLOHEXYLCARBODIIMIDE; GLUTAMIC ACID; HISTIDINE; MUTANT PROTEIN; PEPTIDE DERIVATIVE; THROMBOSPONDIN;

ACIDITY; ARTICLE; CONTROLLED STUDY; ELECTRICITY; HYDROPHILICITY; HYDROPHOBICITY; MEMBRANE FUSION; NONHUMAN; OLIGOMERIZATION; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; VESICULAR STOMATITIS VIRUS;

AMINO ACID SEQUENCE; ASPARTIC ACID; DICYCLOHEXYLCARBODIIMIDE; GLUTAMIC ACID; HYDROPHOBICITY; MEMBRANE FUSION; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDES; VESICULAR STOMATITIS-INDIANA VIRUS; VIRAL ENVELOPE PROTEINS;

ANIMALIA; VESICULAR STOMATITIS VIRUS;

EID: 33750313676     PISSN: 09687688     EISSN: 14645203     Source Type: Journal    
DOI: 10.1080/09687860600780892     Document Type: Article

References (44)

1. Hernandez LD, Hoffman LR, Wolfsberg TG, White JM. Virus-cell and cell-cell fusion. Ann Rev Cell Dev Biol 1996;12:627-661.
2. Skehel JJ, Wiley DC. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Ann Rev Biochem 2000;69:531-569.
3. Heinz FX, Allison SL. The machinery for flavivirus fusion with host cell membranes. Curr Opin Microbiol 2001;4:450-455.
4. Jardetzky TS, Lamb RA. Virology: a class act. Nature 2004;427:307-308.
5. Li Y, Drone C, Sat E, Ghosh HP. Mutational analysis of the vesicular stomatitis virus glycoprotein G for membrane fusion domains. J Virol 1993;67:4070-4077.
6. Zhang L, Ghosh HP. Characterization of the putative fusogenic domain in vesicular stomatitis virus glycoprotein G. J Virol 1994;68:2186-2193.
7. Fredericksen B, Whitt MA. Vesicular stomatitis virus glycoprotein mutations that affect membrane fusion activity and abolish virus infectivity. J Virol 1995;69:1435-1443.
8. Carneiro FA, Bianconi ML, Weissmuller G, Stauffer F, Da Poian AT. Membrane recognition by vesicular stomatitis virus involves enthalpy-driven protein-lipid interactions. J Virol 2002;76:3756-3764.
9. Carneiro FA, Stauffer F, Lima CL, Juliano MA, Juliano L, Da Poian AT. Membrane fusion induced by vesicular stomatitis virus depends on histidine protonation. J Biol Chem 2003;278:13789-13794.
10. Coll JM. Synthetic peptides from the heptad repeats of the glycoproteins of rabies, vesicular stomatitis and fish rhabdoviruses bind phosphatidylserine. Arch Virol 1997;142:2089-2097.
11. Estepa A, Coll JM. Pepscan mapping and fusion-related properties of the major phosphatidylserine-binding domain of the glycoprotein of viral hemorrhagic septicemia virus, a salmonid rhabdovirus. Virology 1996;216:60-70.
12. Coll JM. Heptad-repeat sequences in the glycoprotein of rhabdoviruses. Virus Genes 1995;10:107-114.
13. Struck DK, Hoekstra D, Pagano RE. Use of resonance energy transfer to monitor membrane fusion. Biochemistry 1981;20:4093-4099.
14. Goormaghtigh E, Raussens V, Ruysschaert J-M. Attenuated total reflection infrared spectroscopy of proteins and lipids in biological membranes. Biochim Biophys Acta 1999;1422:105-185.
15. Grimard V, Li C, Ramjeesingh M, Bear CE, Goormaghtigh E, Ruysschaert J-M. Phosphorylation-induced conformational changes of cystic fibrosis transmembrane conductance regulator monitored by attenuated total reflection-Fourier transform IR spectroscopy and fluorescence spectroscopy. J Biol Chem 2004;279:5528-5536.
16. Manciu L, Chang X-B, Buyse F, Hou YX, Gustot A, Riordan JR, Ruysschaert J-M. Intermediate structural states involved in MRP1-mediated drug transport. Role of glutathione. J Biol Chem 2003;278:3347-3356.
17. Carraway KL, Koshland DE Jr. Carbodiimide modification of proteins. Meth Enzymol 1972;25:616-623.
18. Eidelman O, Schlegel R, Tralka TS, Blumenthal R. pH-dependent fusion induced by vesicular stomatitis virus glycoprotein reconstituted into phospholipid vesicles. J Biol Chem 1984;259:4622-4628.
19. Carneiro FA, Ferradosa AS, Da Poian AT. Low pH-induced conformational changes in vesicular stomatitis virus glycoprotein involve dramatic structure reorganization. J Biol Chem 2001;276:62-67.
20. Carr CM, Chaudhry C, Kim PS. Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc Natl Acad Sci USA 1997;94:14306-14313.
21. Gaudin Y, Tuffereau C, Segretain D, Knossow M, Flamand A. Reversible conformational changes and fusion activity of rabies virus glycoprotein. J Virol 1991;65:4853-4859.
22. Pak CC, Puri A, Blumenthal R. Conformational changes and fusion activity of vesicular stomatitis virus glycoprotein: [125I]iodonaphthyl azide photolabeling studies in biological membranes. Biochemistry 1997;36:8890-8896.
23. Gaudin Y. Rabies virus-induced membrane fusion pathway. J Cell Biol 2000;150:601-611.
24. Harter C, James P, Bachi T, Semenza G, Brunner J. Hydrophobic binding of the ectodomain of influenza hemagglutinin to membranes occurs through the "fusion peptide". J Biol Chem 1989;264:6459-6464.
25. Rabenstein M, Shin Y-K. A peptide from the heptad repeat of human immunodeficiency virus gp41 shows both membrane binding and coiled-coil formation. Biochemistry 1995;34:13390-13397.
26. Adam B, Lins L, Stroobant V, Thomas A, Brasseur R. Distribution of hydrophobic residues is crucial for the fusogenic properties of the Ebola virus GP2 fusion peptide. J Virol 2004;78:2131-2136.
27. Nieva JL, Agirre A. Are fusion peptides a good model to study viral cell fusion? Biochim Biophys Acta 2003;1614:104-115.
28. Kliger Y, Aharoni A, Rapaport D, Jones P, Blumenthal R, Shai Y. Fusion peptides derived from the HIV type 1 glycoprotein 41 associate within phospholipid membranes and inhibit cell-cell Fusion. Structure-function study. J Biol Chem 1997;272:13496-13505.
29. Tatulian SA, Jones LR, Reddy LG, Stokes DL, Tamm LK. Secondary structure and orientation of phospholamban reconstituted in supported bilayers from polarized attenuated total reflection FTIR spectroscopy. Biochemistry 1995;34:4448-4456.
30. Martin I, Dubois MC, Defrise-Quertain F, Saermark T, Burny A, Brasseur R, Ruysschaert JM. Correlation between fusogenicity of synthetic modified peptides corresponding to the NH2-terminal extremity of simian immunodeficiency virus gp32 and their mode of insertion into the lipid bilayer: an infrared spectroscopy study. J Virol 1994;68:1139-1148.
31. Martin I, Schaal H, Scheid A, Ruysschaert JM. Lipid membrane fusion induced by the human immunodeficiency virus type 1 gp41 N-terminal extremity is determined by its orientation in the lipid bilayer. J Virol 1996;70:298-304.
32. Ghosh JK, Shai Y. Direct evidence that the N-terminal heptad repeat of Sendai virus fusion protein participates in membrane fusion. J Mol Biol 1999;292:531-546.
33. Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein. J Mol Biol 1982;157:105-132.
34. Lau WL, Ege DS, Lear JD, Hammer DA, DeGrado WF. Oligomerization of fusogenic peptides promotes membrane fusion by enhancing membrane destabilization. Biophys J 2004;86:272-284.
35. Yang J, Prorok M, Castellino FJ, Weliky DP. Oligomeric beta-structure of the membrane-bound HIV-1 fusion peptide formed from soluble monomers. Biophys J 2004;87:1951-1963.
36. Han X, Tamm LK. pH-dependent self-association of influenza hemagglutinin fusion peptides in lipid bilayers. J Mol Biol 2000;304:953-965.
37. Yang J, Weliky DP. Solid-state nuclear magnetic resonance evidence for parallel and antiparallel strand arrangements in the membrane-associated HIV-1 fusion peptide. Biochemistry 2003;42:11879-11890.
38. Li W, Nicol F, Szoka FC Jr. GALA: a designed synthetic pH-responsive amphipathic peptide with applications in drug and gene delivery. Adv Drug Deliv Rev 2004;56:967-985.
39. Goormaghtigh E, De Meutter J, Szoka F, Cabiaux V, Parente RA, Ruysschaert J-M. Secondary structure and orientation of the amphipathic peptide GALA in lipid structures. An infrared-spectroscopic approach. Eur J Biochem 1991;195:421-429.
40. Pecheur EI, Sainte-Marie J, Bienvenue A, Hoekstra D. Lipid headgroup spacing and peptide penetration, but not peptide oligomerization, modulate peptide-induced fusion. Biochemistry 1999;38:364-373.
41. Walker PJ, Kongsuwan K. Deduced structural model for animal rhabdovirus glycoproteins. J Gen Virol 1999;80: 1211-1220.
42. Shai Y. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim Biophys Acta 1999;1462:55-70.
43. Modis Y, Ogata S, Clements D, Harrison SC. Structure of the dengue virus envelope protein after membrane fusion. Nature 2004;427:313-319.
44. Durrer P, Gaudin Y, Ruigrok WH, Graf R, Brunner J. Photolabeling identifies a putative fusion domain in the envelope glycoprotein of rabies and vesicular stomatitis viruses. J Biol Chem 1995;270:17575-17581.