Role of membranotropic sequences from herpes simplex virus type I glycoproteins B and H in the fusion process(555 views) Galdiero S, Falanga A, Vitiello G, Vitiello M, Pedone C, D'Errico G, Galdiero M
Department of Biological Sciences, Division of Biostructures - University of Naples Federico II, Via Mezzocannone 16, 80134, Napoli, Italy.
Centro Interuniversitario, Ricerca sui Peptidi Bioattivi - University of Naples Federico II, Via Mezzocannone 16, 80134 Napoli, Italy
Istituto di Biostrutture, Bioimmagini - CNR, Via Mezzocannone 16, 80134 Napoli, Italy
Department of Chemistry, University of Naples Federico II, CSGI - Monte Sant'Angelo, 80126 Napoli, Italy
Consorzio per lo Studio dei Sistemi a Grande Interfase, CSGI - Monte Sant'Angelo, 80126 Napoli, Italy
Department of Experimental Medicine - II University of Naples, Via De Crecchio 7, 80138 Napoli, Italy
References: Lins, L., Decaffmeyer, M., Thomas, A., Brasseur, R., Relationships between the orientation and the structural properties of peptides and their membrane interactions (2008) Biochim. Biophys. Acta, 1778, pp. 1537-154
Killian, J.A., Nyholm, T.K.M., Peptides in lipid bilayers: the power of simple models (2006) Curr. Opin. Struct. Biol., 16, pp. 473-479
White, S.H., Wimley, W.C., Hydrophobic interactions of peptides with membrane interfaces (1998) Biochim. Biophys. Acta, 1376, pp. 339-352
Martens, S., McMahon, H.T., Mechanisms of membrane fusion: disparate players and common principles (2008) Nat. Rev., Mol. Cell Biol., 9, pp. 543-556
Weissenhorn, W., Hinz, A., Gaudin, Y., Virus membrane fusion (2007) FEBS Lett., 581, pp. 2150-2155
Rey, F.A., Molecular gymnastics at the herpesvirus surface (2006) EMBO Rep., 7, pp. 1000-1005
Farnsworth, A., Wisner, T.W., Webb, M., Roller, R., Cohen, G., Eisenberg, R., Johnson, D.C., Herpes simplex virus glycoproteins gB and gH function in fusion between the virion envelope and the outer nuclear membrane (2007) Proc. Natl. Acad. Sci. U. S. A., 104, pp. 10187-10192
White, J.M., Delos, S.E., Brecher, M., Schornberg, K., Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme (2008) Crit. Rev. Biochem. Mol. Biol., 43, pp. 189-219
Heldwein, E.E., Lou, H., Bender, F.C., Cohen, G.H., Eisenberg, R.J., Harrison, S.C., Crystal structure of glycoprotein B from herpes simplex virus 1 (2006) Science, 313, pp. 217-220
Subramanian, R.P., Geraghty, R.J., Herpes simplex virus type 1 mediates fusion through a hemifusion intermediate by sequential activity of glycoproteins D, H, L, and B (2007) Proc. Natl. Acad. Sci. U. S. A., 104, pp. 2903-2908
Galdiero, S., Falanga, A., Vitiello, M., Browne, H., Pedone, C., Galdiero, M., Fusogenic domains in herpes simplex virus type 1 glycoprotein H (2005) J. Biol. Chem., 280, pp. 28632-28643
Galdiero, S., Vitiello, M., D'Isanto, M., Falanga, A., Cantisani, M., Browne, H., Pedone, C., Galdiero, M., The identification and characterisation of fusogenic domains in herpesvirus glycoprotein B molecules (2008) ChemBioChem, 9, pp. 758-767
Blondelle, S.E., Lohner, K., Aguilar, M., Lipid-induced conformation and lipid-binding properties of cytolytic and antimicrobial peptides: determination and biological specificity (1999) Biochim. Biophys. Acta, 1462, pp. 89-108
Bechinger, B., Biophysical investigations of membrane perturbations by polypeptides using solid-state NMR spectroscopy (2000) Mol. Membr. Biol., 17, pp. 135-142
Shai, Y., Mechanism of the binding, insertion and destabilization of phopsholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides (1999) Biochim. Biophys. Acta, 1462, pp. 55-70
Bechinger, B., The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy (1999) Biochim. Biophys. Acta, 1462, pp. 157-182
Cooper, M.A., Optical biosensors in drug discovery (2002) Nat. Rev. Drug. Discov., 1, pp. 515-528
Mozsolits, H., Thomas, W.G., Aguilar, M.I., Surface plasmon resonance spectroscopy in the study of membrane-mediated cell signalling (2003) J. Pept. Sci., 9, pp. 77-89
Besenicar, M., Macek, P., Lakey, J.H., Anderluh, G., Surface plasmon resonance in protein-membrane interactions (2006) Chem. Phys. Lipids, 141, pp. 169-178
Heyse, S., Stora, T., Schmid, E., Lakey, J.H., Vogel, H., Emerging techniques for investigating molecular interactions at lipid membranes (1998) Biochim. Biophys. Acta, 1376, pp. 319-338
Mozsolits, H., Wirth, H.J., Werkmeister, J., Aguilar, M.I., Analysis of antimicrobial peptide interactions with hybrid bilayer membrane systems using surface plasmon resonance (2001) Biochim. Biophys. Acta, 1512, pp. 64-76
Wang, W., Smith, D.K., Moulding, K., Chen, H.M., The dependence of membrane permeability by the antibacterial peptide cecropin B and its analogues, CB-1 and CB-3, on liposomes of different composition (1998) J. Biol. Chem., 273, pp. 27438-27448
Mozsolits, H., Aguilar, M.I., Surface plasmon resonance spectroscopy: an emerging tool for the study of peptide-membrane interactions (2002) Biopolymers, 66, pp. 3-18
Papo, N., Shai, Y., Exploring peptide membrane interaction using surface plasmon resonance: differentiation between pore formation versus membrane disruption by lytic peptides (2003) Biochemistry, 42, pp. 458-466
Ladokhin, A.S., White, S.H., Detergent-like permeabilization of anionic lipid vesicles by melittin (2001) Biochim. Biophys. Acta, 1514, pp. 253-260
Marsh, D., Horvath, L.I., Structure, dynamics and composition of the lipid-protein interface. Perspectives from spinlabelling (1998) Biochim. Biophys. Acta, 1376, pp. 267-296
Marsh, D., Pali, T., The protein-lipid interface: perspectives from magnetic resonance and crystal structures (2004) Biochim. Biophys. Acta, 1666, pp. 118-141
Gordon, L.M., Curtain, C.C., Zhong, Y.C., Kirkpatrick, A., Mobley, P.W., Waring, A.J., The amino-terminal peptide of HIV-1 glycoprotein 41 interacts with human erythrocyte membranes: peptide conformation, orientation and aggregation (1992) Biochim. Biophys. Acta, 1139, pp. 257-274
Curtain, C., Separovic, F., Nielsen, K., Craik, D., Zhong, Y., Kirkpatrick, A., The interactions of the N-terminal fusogenic peptide of HIV-1 gp41 with neutral phospholipids (1999) Eur. Biophys. J., 28, pp. 427-436
Hope, M.J., Bally, M.B., Webb, G., Cullis, P.R., Production of large unilamellar vesicles by a rapid extrusion procedure. Characterization of size distribution, trapped volume and ability to maintain a membrane potential (1985) Biochim. Biophys. Acta, Biomembr., 812, pp. 55-65
Gazit, E., Lee, W.J., Brey, P.T., Shai, Y., Mode of action of the antibacterial cecropin B2: a spectrofluorometric study (1994) Biochemistry, 33, pp. 10681-10692
Struck, D.K., Hoekstra, D., Pagano, R.E., Use of resonance energy transfer to monitor membrane fusion (1981) Biochemistry, 20, pp. 4093-4099
Kalb, E., Frey, S., Tamm, L.K., Formation of supported planar bilayers by fusion of vesicles to supported phopsholipid monolayers (1992) Biochim. Biophys. Acta, 1103, pp. 307-316
Morton, T.A., Myszka, D.G., Chaiken, I.M., Interpreting complex binding kinetics from optical biosensors: a comparison of linear analysis, the integrated rate equation and numerical integration (1995) Anal. Biochem., 227, pp. 176-185
Bolen, E.J., Holloway, P.W., Quenching of tryptophan fluorescence by brominated phospholipids (1990) Biochemistry, 29, pp. 9638-9643
De Kroon, A.I., Soekarjo, M.W., De Gier, J., De Kruijff, B., The role of charge and hydrophobicity in peptide-lipid interaction: a comparative study based on tryptophan fluorescence measurements combined with the use of aqueous and hydrophobic quenchers (1990) Biochemistry, 29, pp. 8229-8240
D'Errico, G., D'Ursi, A.M., Marsh, D., Interaction of a peptide derived from glycoprotein gp36 of Feline Immunodeficiency Virus and its lipoylated analogue with phospholipid membranes (2008) Biochemistry, 47, pp. 5317-5327
Akkarawongsa, R., Pocaro, N.E., Case, G., Kolb, A.W., Brandt, C.R., Multiple peptides homologous to herpes simplex virus type 1 glycoprotein B inhibit viral infection (2009) Antimicrob. Agents Chemother., 53, pp. 987-996
Habermann, E., Jentsch, J., Sequence analysis of melittin from tryptic and peptic degradation products (1967) Hoppe-Seyler Z. Physiol. Chem., 348, pp. 37-50
Rafalski, M., Lear, J., DeGrado, W., Phospholipid interactions of synthetic peptides representing the N-terminus of HIV gp41 (1990) Biochemistry, 29, pp. 7917-7922
Amon, M.A., Ali, M., Bender, V., Hall, K., Aguilar, M.I., Aldrich-Wright, J., Manolis, N., Kinetic and conformational properties of a novel T-cell antigen receptor transmembrane peptide in model membranes (2008) J. Pept. Sci., 14, pp. 714-724
Lee, T.H., Mozsolits, H., Aguilar, M.I., Measurements of the affinity of melittin for zwitterionic and anionic membranes using immobilized lipid biosensors (2001) J. Pept. Res., 58, pp. 464-476
Niemz, A., Tirrell, D.A., Self-association and membrane-binding behaviour of melittin containing trifluoroleucine (2001) J. Am. Chem. Soc., 123, pp. 7407-7413
D'Errico, G., Vitiello, G., D'Ursi, A.M., Marsh, D., Interaction of short modified peptides deriving from glycoprotein gp36 of feline immunodeficiency virus with phospholipid membranes (2009) Eur. Biophys. J., 38, pp. 873-882
R. Spadaccini, G. D'Errico, V. D'Alessio, E. Notomista, A. Bianchi, M. Merola, D. Picone, Structural characterization of the transmembrane proximal region of the hepatitis C virus E1 glycoprotein, Biochim. Biophys. Acta (2009). Published on the web doi:10.1016/j.bbamem.2009.10.018Sankaram, M.B., Marsh, D., Protein-lipid interactions with peripheral membrane proteins (1993) New Comprehensive Biochemistry: Protein-Lipid Interactions, pp. 127-162. , Watts A. (Ed), Elsevier, Amsterdam 25
Marsh, D., Protein modulation of lipids and vice versa in membranes (2008) Biochim. Biophys. Acta, 1778, pp. 1545-1575
Ramakrishnan, M., Jensen, P.H., Marsh, D., α:-synuclein association with phosphatidylglycerol probed by lipid spin labels (2003) Biochemistry, 42, pp. 12919-12926
Swamy, M.J., Marsh, D., Spin-label electron paramagnetic resonance studies on the interaction of avidin with dimyristoyl-phosphatidylglycerol membranes (2001) Biochim. Biophys. Acta, 1513, pp. 122-130
Davis, J.H., Clair, J.J., Juhasz, J., Phase equilibria in DOPC/DPPC-d62/cholesterol mixtures (2009) Biophys. J., 96, pp. 521-539
Hubbell, W., McConnell, H.M., Molecular motion in spin-labelled phospholipids and membranes (1971) J. Am. Chem. Soc., 93, pp. 314-326
Gordon, L.M., Sauerheber, R.D., Studies on spin-labelled egg lecithin dispersions (1977) Biochim. Biophys. Acta, 466, pp. 34-43
Lange, A., Marsh, D., Wassmer, K.H., Meier, P., Kothe, G., Electron spin resonance study of phospholipid membranes employing a comprehensive line-shape model (1985) Biochemistry, 24, pp. 4383-4392
Moser, M., Marsh, D., Meier, P., Wassmer, K.H., Kothe, G., Chain configuration and flexibility gradient in phospholipid membranes. Comparison between spin-label electron spin resonance and deuteron nuclear magnetic resonance, and identification of new conformations (1989) Biophys. J., 55, pp. 111-123
Rama Krishna, Y.V.S., Marsh, D., Spin label ESR and 31P-NMR studies of the cubic and inverted hexagonal phases of dimyristoylphosphatidylcholine/myristic acid (1:2, mol/mol) mixtures (1990) Biochim. Biophys. Acta, 1024, pp. 89-94
Kleinschmidt, J.H., Mahaney, J.E., Thomas, D.D., Marsh, D., Interaction of bee venom melittin with zwitterionic and negatively charged phospholipid bilayers: a spin-label electron spin resonance study (1997) Biophys. J., 72, pp. 767-778
Gianni, T., Martelli, P.L., Casadio, R., Campadelli-Fiume, G., The ectodomain of herpes simplex virus glycoprotein H contains a membrane α-helix with attributes of an internal fusion peptide, positionally conserved in the Herpesviridae family (2005) J. Virol., 79, pp. 2931-2940
Tu, Y., Kim, J., A fusogenic segment of glycoprotein H from her simplex virus enhances transfection efficiency of cationic liposomes (2008) J. Gene Med., 10, pp. 646-654
DeGrado, W.F., Lear, J.D., Conformationally constrained alpha-helical peptide models for protein ion channels (1990) Biopolymers, 29, pp. 205-213
Parente, R.A., Nadasdi, L., Subbarao, N.K., Szoka, F.C., Association of a pH-sensitive peptide with membrane vesicles: role of amino acid sequence (1990) Biochemistry, 29, pp. 8713-8719
Lear, J.D., DeGrado, W.F., Membrane binding and conformational properties of peptides representing the NH2 terminus of influenza HA-2 (1987) J. Biol. Chem., 262, pp. 6500-6505
Roche, S., Bressanelli, S., Rey, F.A., Gaudin, Y., Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G (2006) Science, 313, pp. 187-191
Roche, S., Rey, F.A., Gaudin, Y., Bressanelli, S., Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G (2007) Science, 315, pp. 843-848
Killian, J. A., Nyholm, T. K. M., Peptides in lipid bilayers: the power of simple models (2006) Curr. Opin. Struct. Biol., 16, pp. 473-479
White, S. H., Wimley, W. C., Hydrophobic interactions of peptides with membrane interfaces (1998) Biochim. Biophys. Acta, 1376, pp. 339-352
Rey, F. A., Molecular gymnastics at the herpesvirus surface (2006) EMBO Rep., 7, pp. 1000-1005
White, J. M., Delos, S. E., Brecher, M., Schornberg, K., Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme (2008) Crit. Rev. Biochem. Mol. Biol., 43, pp. 189-219
Heldwein, E. E., Lou, H., Bender, F. C., Cohen, G. H., Eisenberg, R. J., Harrison, S. C., Crystal structure of glycoprotein B from herpes simplex virus 1 (2006) Science, 313, pp. 217-220
Subramanian, R. P., Geraghty, R. J., Herpes simplex virus type 1 mediates fusion through a hemifusion intermediate by sequential activity of glycoproteins D, H, L, and B (2007) Proc. Natl. Acad. Sci. U. S. A., 104, pp. 2903-2908
Blondelle, S. E., Lohner, K., Aguilar, M., Lipid-induced conformation and lipid-binding properties of cytolytic and antimicrobial peptides: determination and biological specificity (1999) Biochim. Biophys. Acta, 1462, pp. 89-108
Cooper, M. A., Optical biosensors in drug discovery (2002) Nat. Rev. Drug. Discov., 1, pp. 515-528
Ladokhin, A. S., White, S. H., Detergent-like permeabilization of anionic lipid vesicles by melittin (2001) Biochim. Biophys. Acta, 1514, pp. 253-260
Gordon, L. M., Curtain, C. C., Zhong, Y. C., Kirkpatrick, A., Mobley, P. W., Waring, A. J., The amino-terminal peptide of HIV-1 glycoprotein 41 interacts with human erythrocyte membranes: peptide conformation, orientation and aggregation (1992) Biochim. Biophys. Acta, 1139, pp. 257-274
Hope, M. J., Bally, M. B., Webb, G., Cullis, P. R., Production of large unilamellar vesicles by a rapid extrusion procedure. Characterization of size distribution, trapped volume and ability to maintain a membrane potential (1985) Biochim. Biophys. Acta, Biomembr., 812, pp. 55-65
Gazit, E., Lee, W. J., Brey, P. T., Shai, Y., Mode of action of the antibacterial cecropin B2: a spectrofluorometric study (1994) Biochemistry, 33, pp. 10681-10692
Struck, D. K., Hoekstra, D., Pagano, R. E., Use of resonance energy transfer to monitor membrane fusion (1981) Biochemistry, 20, pp. 4093-4099
Morton, T. A., Myszka, D. G., Chaiken, I. M., Interpreting complex binding kinetics from optical biosensors: a comparison of linear analysis, the integrated rate equation and numerical integration (1995) Anal. Biochem., 227, pp. 176-185
Bolen, E. J., Holloway, P. W., Quenching of tryptophan fluorescence by brominated phospholipids (1990) Biochemistry, 29, pp. 9638-9643
De Kroon, A. I., Soekarjo, M. W., De Gier, J., De Kruijff, B., The role of charge and hydrophobicity in peptide-lipid interaction: a comparative study based on tryptophan fluorescence measurements combined with the use of aqueous and hydrophobic quenchers (1990) Biochemistry, 29, pp. 8229-8240
Amon, M. A., Ali, M., Bender, V., Hall, K., Aguilar, M. I., Aldrich-Wright, J., Manolis, N., Kinetic and conformational properties of a novel T-cell antigen receptor transmembrane peptide in model membranes (2008) J. Pept. Sci., 14, pp. 714-724
Lee, T. H., Mozsolits, H., Aguilar, M. I., Measurements of the affinity of melittin for zwitterionic and anionic membranes using immobilized lipid biosensors (2001) J. Pept. Res., 58, pp. 464-476
Swamy, M. J., Marsh, D., Spin-label electron paramagnetic resonance studies on the interaction of avidin with dimyristoyl-phosphatidylglycerol membranes (2001) Biochim. Biophys. Acta, 1513, pp. 122-130
Davis, J. H., Clair, J. J., Juhasz, J., Phase equilibria in DOPC/DPPC-d62/cholesterol mixtures (2009) Biophys. J., 96, pp. 521-539
Gordon, L. M., Sauerheber, R. D., Studies on spin-labelled egg lecithin dispersions (1977) Biochim. Biophys. Acta, 466, pp. 34-43
Rama Krishna, Y. V. S., Marsh, D., Spin label ESR and 31P-NMR studies of the cubic and inverted hexagonal phases of dimyristoylphosphatidylcholine/myristic acid (1: 2, mol/mol) mixtures (1990) Biochim. Biophys. Acta, 1024, pp. 89-94
Kleinschmidt, J. H., Mahaney, J. E., Thomas, D. D., Marsh, D., Interaction of bee venom melittin with zwitterionic and negatively charged phospholipid bilayers: a spin-label electron spin resonance study (1997) Biophys. J., 72, pp. 767-778
DeGrado, W. F., Lear, J. D., Conformationally constrained alpha-helical peptide models for protein ion channels (1990) Biopolymers, 29, pp. 205-213
Parente, R. A., Nadasdi, L., Subbarao, N. K., Szoka, F. C., Association of a pH-sensitive peptide with membrane vesicles: role of amino acid sequence (1990) Biochemistry, 29, pp. 8713-8719
Lear, J. D., DeGrado, W. F., Membrane binding and conformational properties of peptides representing the NH2 terminus of influenza HA-2 (1987) J. Biol. Chem., 262, pp. 6500-6505
Roche, S., Rey, F. A., Gaudin, Y., Bressanelli, S., Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G (2007) Science, 315, pp. 843-848
Role of membranotropic sequences from herpes simplex virus type I glycoproteins B and H in the fusion process
The entry of enveloped viruses involves attachment followed by close apposition of the viral and plasma membranes. Then, either on the cell surface or in an endocytotic vesicle, the two membranes fuse by an energetically unfavourable process requiring the destabilisation of membrane microenvironment in order to release the viral nucleocapsid into the cytoplasm. The core fusion machinery, conserved throughout the herpesvirus family, involves glycoprotein B (gB) and the non-covalently associated complex of glycoproteins H and L (gH/gL). Both gB and gH possess several hydrophobic domains necessary for efficient induction of fusion, and synthetic peptides corresponding to these regions are able to associate to membranes and induce fusion of artificial liposomes. Here, we describe the first application of surface plasmon resonance (SPR) to the study of the interaction of viral membranotropic peptides with model membranes in order to enhance our molecular understanding of the mechanism of membrane fusion. SPR spectroscopy data are supported by tryptophan fluorescence, circular dichroism and electron spin resonance spectroscopy (ESR). We selected peptides from gB and gH and also analysed the behaviour of HIV gp41 fusion peptide and the cationic antimicrobial peptide melittin. The combined results of SPR and ESR showed a marked difference between the mode of action of the HSV peptides and the HIV fusion peptide compared to melittin, suggesting that viral-derived membrane interacting peptides all act via a similar mechanism, which is substantially different from that of the non-cell selective lytic peptide melittin. Copyright 2010 Elsevier B.V. All rights reserved.
Role of membranotropic sequences from herpes simplex virus type I glycoproteins B and H in the fusion process
Petraglia F, Singh AA, Carafa V, Nebbioso A, Conte M, Scisciola L, Valente S, Baldi A, Mandoli A, Petrizzi VB, Ingenito C, De Falco S, Cicatiello V, Apicella I, Janssen-megens EM, Kim B, Yi G, Logie C, Heath S, Ruvo M, Wierenga ATJ, Flicek P, Yaspo ML, Della Valle V, Bernard O, Tomassi S, Novellino E, Feoli A, Sbardella G, Gut I, Vellenga E, Stunnenberg HG, Mai A, Martens JHA, Altucci L * Combined HAT/EZH2 modulation leads to cancer-selective cell death(284 views) Oncotarget (ISSN: 1949-2553electronic, 1949-2553linking), 2018 May 22; 9(39): 25630-25646. Impact Factor:5.008 ViewExport to BibTeXExport to EndNote