Artículo

Carneiro, F.A.; Lapido-Loureiro, P.A.; Cordo, S.M.; Stauffer, F.; Weissmüller, G.; Bianconi, M.L.; Juliano, M.A.; Juliano, L.; Bisch, P.M.; Da Poian, A.T. "Probing the interaction between vesicular stomatitis virus and phosphatidylserine" (2006) European Biophysics Journal. 35(2):145-154
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The entry of enveloped animal viruses into their host cells always depends on membrane fusion triggered by conformational changes in viral envelope glycoproteins. Vesicular stomatitis virus (VSV) infection is mediated by virus spike glycoprotein G, which induces membrane fusion between the viral envelope and the endosomal membrane at the acidic environment of this compartment. In this work, we evaluated VSV interactions with membranes of different phospholipid compositions, at neutral and acidic pH, using atomic force microscopy (AFM) operating in the force spectroscopy mode, isothermal calorimetry (ITC) and molecular dynamics simulation. We found that the binding forces differed dramatically depending on the membrane phospholipid composition, revealing a high specificity of G protein binding to membranes containing phosphatidylserine (PS). In a previous work, we showed that the sequence corresponding amino acid 145-164 of VSV G protein was as efficient as the virus in catalyzing membrane fusion at pH 6.0. Here, we used this sequence to explore VSV-PS interaction using ITC. We found that peptide binding to membranes was exothermic, suggesting the participation of electrostatic interactions. Peptide-membrane interaction at pH 7.5 was shown to be specific to PS and dependent on the presence of His residues in the fusion peptide. The application of the simplified continuum Gouy-Chapman theory to our system predicted a pH of 5.0 at membrane surface, suggesting that the His residues should be protonated when located close to the membrane. Molecular dynamics simulations suggested that the peptide interacts with the lipid bilayer through its N-terminal residues, especially Val145 and His148. © EBSA 2005.

Registro:

Documento: Artículo
Título:Probing the interaction between vesicular stomatitis virus and phosphatidylserine
Autor:Carneiro, F.A.; Lapido-Loureiro, P.A.; Cordo, S.M.; Stauffer, F.; Weissmüller, G.; Bianconi, M.L.; Juliano, M.A.; Juliano, L.; Bisch, P.M.; Da Poian, A.T.
Filiación:Instituto de Bioquìmica Médica, Universidade Federal do Rio de Janeiro, Rio de Janeiro, 21941-590, Brazil
Laboratório de Física Biológica, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21949-900, Brazil
Laboratorio de Virología, Departamento de Quimica Biológica, Universidad de Buenos Aires, Buenos Aires, Argentina
Departamento de Biofísica, Escola Paulista de Medicina, UNIFESP, Rua Trêsde Maio, 100, São Paulo, 04044-020, Brazil
Palabras clave:phosphatidylserine; acidity; article; atomic force microscopy; chemical interaction; controlled study; membrane fusion; membrane transport; molecular dynamics; molecular probe; nonhuman; peptide synthesis; pH measurement; prediction; spectrometry; theoretical study; Vesicular stomatitis virus; Amino Acids; Animals; Calorimetry; Cell Line; Cell Membrane; Computer Simulation; Electrostatics; Histidine; Hydrogen-Ion Concentration; Liposomes; Membrane Glycoproteins; Microscopy, Atomic Force; Phosphatidylserines; Protein Binding; Thermodynamics; Valine; Vesicular stomatitis-Indiana virus; Viral Envelope Proteins; Viral Fusion Proteins; Animalia; Vesicular stomatitis virus
Año:2006
Volumen:35
Número:2
Página de inicio:145
Página de fin:154
DOI: http://dx.doi.org/10.1007/s00249-005-0012-z
Título revista:European Biophysics Journal
Título revista abreviado:Eur. Biophys. J.
ISSN:01757571
CODEN:EBJOE
CAS:Amino Acids; G protein, vesicular stomatitis virus; Histidine, 71-00-1; Liposomes; Membrane Glycoproteins; Phosphatidylserines; Valine, 7004-03-7; Viral Envelope Proteins; Viral Fusion Proteins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_01757571_v35_n2_p145_Carneiro

Referencias:

  • Berendsen, H.J.C., Postma, J.P.M., Dinola, A., Haak, J.R., Molecular dynamics with coupling to an external bath (1984) J Chem Phys, 81, pp. 3684-3690
  • Berendsen, H.J.C., Grigera, J.R., Straatsma, T.P., The missing term in effective pair potentials (1987) J Phys Chem, 91, pp. 6269-6271
  • Boström, M., Williams, D.R.M., Ninham, B.W., Specific ion effects: Role of salt and buffer in protonation of cytochrome c (2004) Eur Phys J, 13, pp. 239-245
  • Carneiro, F.A., Ferradosa, A.S., Da Poian, A.T., Low pH-induced conformational changes in vesicular stomatitis virus glycoprotein involve dramatic structure reorganization (2001) J Biol Chem, 276, pp. 62-67
  • Carneiro, F.A., Bianconi, M.L., Weissmuller, G., Stauffer, F., Da Poian, A.T., Membrane recognition by vesicular stomatitis virus involves enthalpy-driven protein-lipid interactions (2002) J Virol, 76, pp. 3756-3764
  • Carneiro, F.A., Stauffer, F., Lima, C.S., Juliano, M.A., Juliano, L., Da Poian, A.T., Membrane fusion induced by vesicular stomatitis virus depends on histidine protonation (2003) J Biol Chem, 278, pp. 13789-13794
  • Cevc, G., Membrane electrostatics (1990) Biochim Biophys Acta, 1031 (3), pp. 311-382
  • Chandrasekhar, I., Kastenholz, M., Lins, R.D., Oostenbrink, C., Schuler, L.D., Tieleman, D.P., Van Gunsteren, W.F., A consistent potential energy parameter set for lipids: Dipalmitoylphosphatidylcholine as a benchmark of the GROMOS96 45 A3 force field (2003) Eur Biophys J, 32, pp. 62-67
  • Cleverley, P.Z., Lenard, J., The transmembrane domain in viral fusion: Essential role for a conserved glycine residue in vesicular stomatitis virus G protein (1998) Proc Natl Acad Sci, 95, pp. 3425-3430. , USA
  • Coil, D.A., Miller, A.D., Phosphatidylserine is not the cell surface receptor for vesicular stomatitis virus (2004) J Virol, 78, pp. 10920-10926
  • Coll, J.M., Synthetic peptids from the heptad repeats of the glicoproteins of rabies, vesicular stomatitis and fish rhabdoviruses bind phosphatidylserine (1997) Arch Virol, 142, pp. 2089-2097
  • Crimmins, D.L., Mehard, W.B., Schlesinger, S., Physical properties of a soluble form of the glycoprotein of vesicular stomatitis virus at neutral and acidic pH (1983) Biochemistry, 22, pp. 5790-5796
  • Da Poian, A.T., Gomes, A.M.O., Oliveira, R.J.N., Silva, J.L., Migration of vesicular stomatitis virus glycoprotein to the nucleus of infected cells (1996) Proc Natl Acad Sci, 93, pp. 8268-8273. , USA
  • Da Poian, A.T., Gomes, A.M.O., Coelho-Sampaio, T., Kinetics of intracellular viral disassembly probed by bodipy fluorescence dequenching (1998) J Virol Meth, 70, pp. 45-58
  • Darden, T., York, D., Pedersen, L., Particle Mesh Ewald: An Nlog (N) method for Ewald sums in large systems (1993) J Chem Phys, 98, pp. 10089-10092
  • Durrer, P., Gaudin, Y., Ruigrok, R.W., Graf, R., Brunner, J., Photolabeling identifies a putative fusion domain in the envelope glycoprotein of rabies and vesicular stomatitis viruses (1995) J Biol Chem, 270, pp. 17575-17581
  • Eckert, D.M., Kim, P.S., Mechanisms of viral membrane fusion and its inhibition (2001) Annu Rev Biochem, 70, pp. 777-810
  • Eidelman, O., Schlegel, R., Tralka, T.S., Blumenthal, R., pH-dependent fusion induced by vesicular stomatitis virus glycoprotein reconstituted into phospholipid vesicles (1984) J Biol Chem, 259, pp. 4622-4628
  • Estepa, A., Coll, J.M., Pepscan mapping and fusion related properties of the major phosphatidylserine-binding domain of the glycoprotein of viral hemorragic septicemia virus, a salmonid rhabdovirus (1996) Virology, 216, pp. 60-70
  • Florin, E.L., Moy, V.T., Gaub, H.E., Adhesion forces between individual ligand-receptor pairs (1994) Science, 264, pp. 415-417
  • Fredericksen, B., Whitt, M.A., Vesicular stomatitis virus glycoprotein mutations that affect membrane fusion activity and abolish virus infectivity (1995) J Virol, 69, pp. 1435-1443
  • Gergely, C., Voegel, J.-C., Schaaf, P., Senger, B., Maaloum, M., Hörber, J.K.H., Hermmerlé, J., Unbinding process of adsorbed proteins under external stress studied by atomic force microscopy spectroscopy (2000) Proc Natl Acad Sci, 97, pp. 10802-10807. , USA
  • Hernandez, L.D., Hoffman, L.R., Wolfsberg, T.G., White, J.M., Virus-cell and cell-cell fusion (1996) Annu Rev Cell Dev Biol, 12, pp. 627-661
  • Herrmann, A., Clague, M.J., Puri, A., Morris, S.J., Blumenthal, R., Grimaldi, S., Effect of erythrocyte transbilayer phospholipid distribution on fusion with vesicular stomatitis virus (1990) Biochemistry, 29, pp. 4054-4058
  • Jass, J., Tjärnhage, T., Puu, G., From liposomes to supported, planar bilayer structures on hydrophilic and hydrophobic surfaces: An atomic force microscopy study (2000) Biophys J, 79, pp. 3153-3163
  • Li, Y., Drone, C., Sat, E., Ghosh, H.P., Mutational analysis of the vesicular stomatitis virus glycoprotein G for membrane fusion domains (1993) J Virol, 67, pp. 4070-4077
  • Lindahl, E., Hess, B., Van Der Spoel, D., GROMACS 3.0: A package for molecular simulation and trajectory analysis (2001) J Mol Mod, 7, pp. 306-317
  • Mastromarino, P., Conti, C., Goldoni, P., Hauttecoeur, B., Orsi, N., Characterization of membrane components of the erythrocyte involved in vesicular stomatitis virus attachment and fusion at acidic pH (1987) J Gen Virol, 68, pp. 2359-2369
  • Miles, E.W., Modification of histidyl residues in proteins by diethyl pyrocarbonate (1977) Meth Enzymol, 47, pp. 431-442
  • Nieva, J.L., Agirre, A., Are fusion peptides a good model to study viral cell fusion? (2003) Biochim Biophys Acta, 1614 (1), pp. 104-115
  • Odell, D., Wanas, E., Yan, J., Ghosh, H.P., Influence of membrane anchoring and cytoplasmic domains on the fusogenic activity of vesicular stomatitis virus glycoprotein G (1997) J Virol, 71, pp. 7996-8000
  • Pak, C.C., Puri, A., Blumenthal, R., Conformational changes and fusion activity of vesicular stomatitis virus glycoprotein: [125 I]iodonaphtyl azide photolabeling studies in biological membranes (1987) Biochemistry, 36, pp. 8890-8896
  • Pandit, S.A., Berkowitz, M.L., Molecular dynamics simulation of dipalmitoylphosphatidylserine bilayer with Na+ counterions (2002) Biophys J, 82, pp. 1818-1827
  • Puu, G., Gustafson, I., Planar lipid bilayers on solid supports from liposomes-factors of importance for kinetics and stability (1997) Biochim Biophys Acta, 1327, pp. 149-161
  • Puu, G., Artursson, E., Gustafson, I., Lundstro, M., Jass, J., Distribution and stability of membrane proteins in lipid membranes on solid supports (2000) Biosensors Bioelectronics, 15, pp. 31-41
  • Reviakine, I., Brisson, A., Formation of supported phospholipid bilayers from unilamellar vesicles investigated by atomic force microscopy (2000) Langmuir, 16, pp. 1806-1815
  • Ryckaert, J.P., Ciccott, G.I., Berendsen, H.J.C., Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes (1977) J Comp Phys, 23, pp. 327-341
  • Schlegel, R., Willingham, M.C., Pastan, I.H., Saturable binding sites for vesicular stomatitis virus on the surface of Vero cells (1982) J Virol, 43, pp. 871-875
  • Schlegel, R., Tralka, T.S., Willingham, M.C., Pastan, I., Inhibition of VSV binding and infectivity by phosphatidylserine: Is phosphatidylserine a VSV-binding site? (1983) Cell, 32, pp. 639-646
  • Shokralla, S., He, Y., Wanas, E., Ghosh, H.P., Mutations in a carboxy-terminal region of vesicular stomatitis virus glycoprotein G that affect membrane fusion activity (1998) Virology, 256, pp. 119-129
  • Skehel, J.J., Wiley, D.C., Receptor binding and membrane fusion in virus entry: The influenza hemagglutinin (2000) Annu Rev Biochem, 69, pp. 531-569
  • Superti, F., Seganti, L., Tsiang, H., Orsi, N., Role of phospholipids in rhabdovirus attachment to CER cells (1984) Arch Virol, 81, pp. 321-328
  • Zhang, L., Ghosh, H.P., Characterization of the putative fusogenic domain in vesicular stomatitis virus glycoprotein G (1994) J Virol, 68, pp. 2186-2193
  • Zlatanova, J., Lindsay, S.M., Leuba, S.H., Single molecule force spectroscopy in biology using the atomic force microscope (2000) Prog Biophys Mol Biol, 74, pp. 37-61

Citas:

---------- APA ----------
Carneiro, F.A., Lapido-Loureiro, P.A., Cordo, S.M., Stauffer, F., Weissmüller, G., Bianconi, M.L., Juliano, M.A.,..., Da Poian, A.T. (2006) . Probing the interaction between vesicular stomatitis virus and phosphatidylserine. European Biophysics Journal, 35(2), 145-154.
http://dx.doi.org/10.1007/s00249-005-0012-z
---------- CHICAGO ----------
Carneiro, F.A., Lapido-Loureiro, P.A., Cordo, S.M., Stauffer, F., Weissmüller, G., Bianconi, M.L., et al. "Probing the interaction between vesicular stomatitis virus and phosphatidylserine" . European Biophysics Journal 35, no. 2 (2006) : 145-154.
http://dx.doi.org/10.1007/s00249-005-0012-z
---------- MLA ----------
Carneiro, F.A., Lapido-Loureiro, P.A., Cordo, S.M., Stauffer, F., Weissmüller, G., Bianconi, M.L., et al. "Probing the interaction between vesicular stomatitis virus and phosphatidylserine" . European Biophysics Journal, vol. 35, no. 2, 2006, pp. 145-154.
http://dx.doi.org/10.1007/s00249-005-0012-z
---------- VANCOUVER ----------
Carneiro, F.A., Lapido-Loureiro, P.A., Cordo, S.M., Stauffer, F., Weissmüller, G., Bianconi, M.L., et al. Probing the interaction between vesicular stomatitis virus and phosphatidylserine. Eur. Biophys. J. 2006;35(2):145-154.
http://dx.doi.org/10.1007/s00249-005-0012-z