Oligomerization of Fusogenic Peptides Promotes Membrane Fusion by Enhancing Membrane Destabilization

Biophysical Journal

Volumn 86, Issue 1 I, 2004, Pages 272-284

  Lau, Wai Leung ^a   Ege, David S ^a,b   Lear, James D ^a   Hammer, Daniel A ^a,b   DeGrado, William F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COILED COIL X31 PEPTIDE; FUSOGENIC PEPTIDE; HEMAGGLUTININ; HEMAGGLUTININ FUSION PEPTIDE; HYBRID PROTEIN; LIPOSOME; MONOMER; PEPTIDE; PHOSPHOLIPID; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CIRCULAR DICHROISM; COILED COIL DOMAIN; GEOMETRY; INFLUENZA VIRUS; LIPID BILAYER; MEMBRANE DESTABILIZATION; MEMBRANE FUSION; MEMBRANE STABILIZATION; MEMBRANE VESICLE; OLIGOMERIZATION; PHOSPHOLIPID BILAYER; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN INTERACTION; TRIPLE HELIX; VIRUS;

INFLUENZA VIRUS; RNA VIRUSES;

EID: 0346057944     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(04)74103-X     Document Type: Article

References (68)

1. Angelova, M. I., and D. S. Dimitrov. 1986. Liposome electroformation. Faraday Discuss. 81:303-311.
2. Angelova, M. I., S. Soleau, P. Meleard, J. F. Faucon, and P. Bothorel. 1992. Preparation of giant vesicles by external AC electric fields. Kinetics and applications. Prog. Colloid Polym. Sci. 89:127-131.
3. Bentz, J. 2000. Minimal aggregation size and minimal fusion unit for the first fusion pore of influenza hemagglutinin mediated membrane fusion. Biophys. J. 78:227-245.
4. Blumenthal, R., D. P. Sarkar, D. E. Howard, and S. J. Morris. 1996. Dilation of the influenza hemagglutinin fusion pore revealed by the kinetics of individual cell-cell fusion events. J. Cell Biol. 135:63-71.
5. Boice, J. A., G. R. Dieckmann, W. F. DeGrado, and R. Fairman. 1996. Thermodynamic analysis of a designed three-stranded coiled coil. Biochemistry. 35:14480-14485.
6. Brunger, A. T. 2001. Structure of proteins involved in synaptic vesicle fusion in neurons. Annu. Rev. Biophys. Biomol. Struct. 30:157-171.
7. Bullough, P. A., F. M. Hughson, J. J. Skehel, and D. C. Wiley. 1994. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature. 371:37-43.
8. Chakrabartty, A., J. A. Schellman, and R. L. Baldwin. 1991. Large difference in the helix propensities of alanine and glycine. Nature. 351:586-588.
9. Chatelier, R., and A. P. Minton. 1996. Adsorption of globular proteins on locally planar surfaces: Models for the effect of excluded surface area and aggregation of adsorbed protein on adsorption equilibria. Biophys. J. 71:2367-2374.
10. Chernomordik, L. V., G. B. Melikyan, and Y. A. Chizmadzhev. 1987. Biomembrane fusion - a new concept derived from model studies using 2 interacting planar lipid bilayers. Biochim. Biophys. Acta. 906:309-352.
11. Cohen, F. S., and G. B. Melikyan. 2001. Implications of a fusion peptide structure. Nat. Struct. Biol., 8:653-655.
12. Danieli, T., S. L. Pelletier, Y. I. Henis, and J. M. White. 1996. Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers. J. Cell Biol. 133:559-569.
13. Delahunty, M. D., I. Rhee, E. O. Freed, and J. S. Bonifacino. 1996. Mutational analysis of the fusion peptide of the human immunodeficiency virus type 1: identification of critical glycine residues. Virology. 218:94-102.
14. Durrer, P., C. Galli, S. Hoenke, C. Corti, R. Gluck, T. Vorherr, and J. Brunner. 1996. H+-induced membrane insertion of influenza virus hemagglutinin involves the HA2 amino-terminal fusion peptide but not the coiled coil region. J. Biol. Chem. 271:13417-13421.
15. Durrer, P., Y. Gaudin, R. W. H. Ruigrok, R. Graf, and J. Brunner. 1995. Photolabeling identifies a putative fusion domain in the envelope glycoprotein of rabies and vesicular stomatitis viruses. J. Biol. Chem. 87:648-652.
16. Eckert, D. M., and P. S. Kim. 2001. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70:777-810.
17. Ellens, H., J. Bentz, D. Mason, F. Zhang, and J. M. White. 1990. Fusion of influenza hemagglutinin-expressing fibroblasts with glycophorin-bearing liposomes: role of hemagglutinin surface density. Biochemistry. 29:9697-9707.
18. Epand, R. F., J. C. Macosko, C. J. Russell, Y.-K. Shin, and R. M. Epand. 1999. The ectodomain of HA2 of influenza virus promotes rapid pH dependent membrane fusion. J. Mol. Biol. 286:489-503.
19. Evans, E., and D. Needham. 1987. Physical properties of surfactant bilayer membranes: thermal transitions, elasticity, rigidity, cohesion, and colloidial interactions. J. Phys. Chem. 91:4129-4228.
20. Evans, E., and W. Rawicz. 1990. Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys. Rev. Lett. 64:2094-2097.
21. Freed, E. O., E. L. Delwart, G. L. Buchschacher, and A. T. Panganiban. 1992. A mutation in the human immunodeficiency virus type 1 transmembrane glycoprotein gp41 dominantly interferes with fusion and infectivity. Proc. Natl. Acad. Sci. USA. 89:70-74.
22. Glabe, C. G. 1985. Interaction of the sperm adhesive protein, bindin, with phospholipid vesicles. II. Bindin induces the fusion of mixed-phase vesicles that contain phosphatidylcholine and phosphatidylserine in vitro. J. Cell Biol. 100:800-806.
23. Han, X., J. H. Bushweller, D. S. Cafiso, and L. K. Tamm. 2001. Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nat. Struct. Biol. 8:715-720.
24. Harter, C., T. Bachi, G. Semenza, and J. Brunner. 1988. Hydrophobic photolabeling identifies BHA2 as the subunit mediating the interaction of bromelain-solubilized influenza virus hemagglutinin with liposomes at low pH. Biochemistry. 27:1856-1864.
25. Harter, C., P. James, T. Bachi, G. Semenza, and J. Brunner. 1989. Hyrdophobic binding of the ectodomain of influenza hemagglutinin to membranes occurs through the "fusion peptide". J. Biol. Chem. 264:6459-6464.
26. Helm, C. A., J. N. Israelachvili, and P. M. McGuiggan. 1992. Role of hydrophobic force in bilayer adhesion and fusion. Biochemistry. 31:1794-1805.
27. Hernandez, L. D., L. R. Hoffman, T. G. Wolfsberg, and J. M. White. 1996. Virus-cell and cell-cell fusion. Annu. Rev. Cell Dev. Biol. 12:627-641.
28. Israelachvili, J. N., S. Marcelja, and R. G. Horn. 1980. Physical principles of membrane organization. Q. Rev. Biophys. 13:121-200.
29. Jahn, R., and T. C. Sudhof. 1999. Membrane fusion and exocytosis. Annu. Rev. Biochem. 68:863-911.
30. Jones, J. S., and R. Risser. 1993. Cell fusion induced by the murine leukemia virus envelope glycoprotein. J. Virol. 67:67-74.
31. Kielian, M., M. R. Klimjack, S. Ghosh, and W. A. Duffus. 1996. Mechanisms of mutations inhibiting fusion and infection by Semliki Forest virus. J. Cell Biol. 134:863-872.
32. Lamb, R. A. 1993. Paramyxovirus fusion: a hypothesis for change. Virology. 197:1-11.
33. Lear, J. D., and W. F. DeGrado. 1987. Membrane binding and conformational properties of peptides representing the NH2 terminus of influenza HA-2. J. Biol. Chem. 262:6500-6505.
34. LeDuc, D. L., Y.-K. Shin, R. F. Epand, and R. M. Epand. 2000. Factors determining vesicular lipid mixing induced by shortened constructs of influenza hemagglutinin. Biochemistry. 39:2733-2739.
35. Longo, M., A. J. Waring, and D. A. Hammer. 1997. Interaction of the influenza hemagglutinin fusion peptide with lipid bilayers: area expansion and permeation. Biophys. J. 73:1430-1439.
36. Markovic, I., H. Pulyaeva, A. Sokoloff, and L. V. Chernomordik. 1998. Membrane fusion mediated by baculovirus gp64 involves assembly of stable gp64 trimers into multiprotein aggregates. J. Cell Biol. 143:1155-1166.
37. McIntosh, T. J., S. Advani, R. E. Burton, D. V. Zhelev, D. Needham, and S. A. Simon. 1995. Experimental tests for protrusion and undulation pressures in phospholipid bilayers. Biochemistry. 34:8520-8532.
38. Minton, A. P. 1999. Adsorption of globular proteins on locally planar surfaces. II. Models for the effect of multiple adsorbate conformations on adsorption equilibria and kinetics. Biophys. J. 76:176-187.
39. Ogihara, N. L., M. S. Weiss, W. F. DeGrado, and D. Eisenberg. 1997. The crystal structure of the designed trimeric coiled coil coil-VaLd: Implications for engineering crystals and supramolecular assemblies. Protein Sci. 6:80-88.
40. Olbrich, K., W. Rawicz, D. Needham, and E. Evans. 2000. Water permeability and mechanical strength of polyunsaturated lipid bilayers. Biophys. J. 79:321-327.
41. Pak, C. C., M. Krumbiegel, R. Blumenthal, and Y. Raviv. 1994. Detection of influenza hemagglutinin interaction with biological membranes by photosensitized activation of [125-I]iodonaphthylazide. J. Biol. Chem. 269:14614-14619.
42. Parente, R. A., S. Nir, and F. C. Szoka, Jr. 1990. Mechanisms of leakage of phospholipid vesicle contents induced by the peptide GALA. Biochemistry. 29:8720-8728.
43. Pecheur, E. I., J. Sainte-Marie, A. Bienvenue, and D. Hoekstra. 1999. Lipid headgroup spacing and peptide penetration, but not peptide oligomerization, modulate peptide-induced fusion. Biochemistry. 38:364-373.
44. Primakoff, P., H. Hyatt, and J. Tredick-Kline. 1987. Identification and purification of a sperm surface protein with a potential role in a sperm-egg membrane fusion. J. Cell Biol. 104:141-149.
45. Rafalski, M., A. Oritz, A. Rockwell, L. van Ginkel, J. D. Lear, W. F. DeGrado, and J. Wilschut. 1991. Membrane fusion activity of the influenza virus hemagglutinin: interaction of HA2 N-terminal peptides with phospholipid vesicles. Biochemistry. 30:10211-10220.
46. Rand, P. R., and V. A. Parsegian. 1986. Mimicry and mechanism in phospholipid models of membrane fusion. Annu. Rev. Physiol. 48:201-212.
47. Rapaport, D., R. Peled, S. Nir, and Y. Shai. 1996. Reversible surface aggregation in pore formation by pardaxin. Biophys. J. 70:2502-2512.
48. Rapaport, D., and Y. Shai. 1994. Interaction of fluorescently labeled analogues of the amino-terminal fusion peptide of sendai virus with phospholipid membranes. J. Biol. Chem. 269:15124-15131.
49. Rawicz, W., K. C. Olbrich, T. McIntosh, D. Needham, and E. Evans. 2000. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys. J. 79:328-339.
50. Rodriguez, J. F., E. Paez, and M. Esteban. 1987. A 14,000-Mr envelope protein of Vaccinia virus is involved in cell fusion and forms covalently linked trimers. J. Virol. 61:395-404.
51. Rodriguez-Crespo, I., E. Nunez, J. Gomez-Gutierrez, B. Yelamos, J. P. Albar, D. L. Peterson, and F. Gavilanes. 1995. Phospholipid interactions of the putative fusion peptide of hepatitis B virus surface antigen S protein. J. Gen. Virol. 76:301-308.
52. Saginario, C., H.-Y. Qian, and A. Vignery. 1995. Identification of an inducible surface molecule specific to fusing macrophages. Proc. Natl. Acad. Sci. USA. 92:12210-12214.
53. Schaal, H., M. Klein, P. Ghermann, O. Adams, and A. Scheid. 1995. Requirement of N-terminal amino acid residues of gp41 for human immunodeficiency virus type 1-mediated cell fusion. J. Virol. 69:3308-3314.
54. Skehel, J., and D. C. Wiley. 1998. Coiled coils in both intracellular vesicle and viral membrane fusion. Cell. 95:871-874.
55. Skehel, J. J., and D. C. Wiley. 2000. Receptor binding and membrane fusioin in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531-569.
56. Struck, D. K., D. Hoeksra, and R. E. Pagano. 1981. Use of resonance energy transfer to monitor membrane fusion. Biochemistry. 20:4093-4099.
57. Sutton, R. B., D. Fasshauer, R. Jahn, and A. T. Brunger. 1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature. 395:347-351.
58. Talbot, J. 1997. Molecular thermodynamics of binary mixture adsorption: A scaled particle theory approach. J. Chem. Phys. 106:4696-4706.
59. Trueheart, J., and G. R. Fink. 1989. The yeast cell fusion protein FUSI is O-glycosylated and spans the plasma membrane. Proc. Natl. Acad. Sci. USA. 86:9916-9920.
60. Ulrich, A. S., W. Tichelaar, G. Forster, O. Zschornig, S. Weinkauf, and H. W. Meyer. 1999. Ultrastructural characterization of peptide-induced membrane fusion and peptide self-assembly in the lipid bilayer. Biophys. J. 77:829-841.
61. White, J. M. 1992. Membrane fusion. Science. 258:917-924.
62. Wild, C., J. W. Dubay, T. Greenwell, T. Baird, Jr., T. G. Oas, C. McDanal, E. Hunter, and T. Matthews. 1994. Propensity for a leucine zipper-like domain of human immunodeficiency virus type 1 gp41 to form oligomers correlates with a role in virus-induced fusion rather than assembly of the glycoprotein complex. Proc. Natl. Acad. Sci. USA. 91:12676-12680.
63. Wiley, D. C., and J. J. Skehel. 1987. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 56:365-394.
64. Wilson, I. A., J. J. Skehel, and D. C. Wiley. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature. 289:366-372.
65. Yagami-Hiromasa, T., T. Sato, T. Kurisaki, K. Kamijio, Y. Nabeshima, and A. Fujisawa-Sehara. 1995. A metalloportease-disintegrin participating in myoblast fusion. Nature. 377:652-656.
66. Yu, Y. G., D. S. King, and Y. K. Shin. 1994. Insertion of a coiled-coil peptide from influenza-virus hemagglutinin into membranes. Science. 266:274-276.
67. Zhelev, D. V., N. Stoicheva, P. Scherrer, and D. Needham. 2001. Interaction of synthetic HA2 Influenza fusion peptide analog with model membranes. Biophys J. 81:285-304.
68. Zuckermann, M. J., and T. Heimburg. 2001. Insertion and pore formation driven by adsorption of proteins onto lipid bilayer membrane-water interfaces. Biophys. J. 81:2458-2472.