Inner but not outer membrane leaflets control the transition from glycosylphosphatidylinositol-anchored influenza hemagglutinin-induced hemifusion to full fusion

Journal of Cell Biology

Volumn 136, Issue 5, 1997, Pages 995-1005

  Melikyan, Grigory B ^a   Brener, Sofya A ^a   Ok, Dong C ^a   Cohen, Fredric S ^a  

^a RUSH MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIOLEOYLPHOSPHATIDYLCHOLINE; DIOLEOYLPHOSPHATIDYLETHANOLAMINE; GLYCOSYLPHOSPHATIDYLINOSITOL; HEMAGGLUTININ; LIPID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLSERINE;

ANIMAL CELL; ARTICLE; CELL FUSION; CHO CELL; CONTROLLED STUDY; ERYTHROCYTE; HUMAN; HUMAN CELL; LIPID BILAYER; MEMBRANE; NONHUMAN; PRIORITY JOURNAL;

ANIMALIA;

EID: 0030899232     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.136.5.995     Document Type: Article

References (46)

1. Abidor, I.G., V.B. Arakelian, L.V. Chernomordik, Yu.A. Chizmadzhev, V.F. Pastushenko, and M.R. Tarasevich. 1979. Electrical breakdown of BLM: main experimental facts and their qualitative discussion. Bioelectrochem. Bioenerg. 6:37-52.
2. Binford, J.S., Jr., and W.H. Palm. 1994. Adsorption of surfactants by membranes: erythrocytes versus synthetic vesicles. Biophys. J. 66:2024-2028.
3. Browning, J.L., and D.L. Nelson. 1976. Amphipathic amines affect membrane excitability in Paramecium: role of bilayer couple. Proc. Natl. Acad. Sci. USA. 73:452-456.
4. Chernomordik, L.V., G.B. Melikyan, and Yu. A, Chizmadzhev. 1987. Biomembrane fusion: a new concept derived from model studies using two interacting planar lipid bilayers. Biochim. Biophys. Acta. 906:309-352.
5. 2+-, GTP- and pH-dependent fusion of biological membranes. FEBS Lett. 318:71-76.
6. Chernomordik, L.V., A.N. Chanturia, E. Suss-Toby, E. Nora, and J. Zimmerberg. 1994. An amphipathic peptide from the C-terminal region of the Human Immunodeficiency Virus envelope glycoprotein causes pore formation in membranes. J. Virol. 68:7115-7123.
7. Chernomordik, L.V., M.M. Kozlov, and J. Zimmerberg. 1995a. Lipids in biological membrane fusion. J. Membr. Biol. 146:1-14.
8. Chernomordik, L.V., E. Leikina. M.-S. Cho. and J. Zimmerberg. 1995b. Control of Baculovirus gp64-induced syncytium formation by membrane lipid composition. Virol. 69:3049-3058.
9. Chernomordik, L.V., A. Chanturia, J. Green, and J. Zimmerberg. 1995c. The hemifusion intermediate and its conversion to complete fusion: regulation by membrane composition. Biophys. J. 69:922-929.
10. Chgue, M.J., C. Schoch, and R. Blumenthal. 1991. Delay time for influenza virus hemagglutinin-induced membrane fusion depends on hemagglutinin surface density. J. Virol. 65:2402-2407.
11. 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 trimurs. J. Cell Biol. 133:559-569.
12. Deuticke, B. 1968. Transformation and restoration of biconcave shape of human erythrocytes induced by amphipathic agents and changes in ionic environment. Biochim. Biophys. Acta. 163:494-500.
13. Ellens, H., S. Doxsey, J.S. Glenn, and J.M. White. 1989. Delivery of macromolecules into cells expressing a viral membrane fusion protein. Methods Cell Biol. 31:155-176.
14. Ellens, H., J. Bentz, D. Mason, F. Zhang, and J.M. White. 1990. Fusion of influenza hemagglutinin-expressing fibroblasts with glycoprotein-bearing liposomes: role of hemagglutinin surface density. Biochemistry. 29:9697-9707.
15. Epand, R.M. 1985. Diacylglycerols. lysolecithin, or hydrocarbons markedly alter the bilayer to hexagonal phase transition temperature of phosphatidylethanolamines. Biochemistry. 24:7092-7095.
16. Epand, R.M., R.F. Epand, N. Ahmed, and R. Chen. 1991. Promotion of hexagonal phase formation and lipid mixing by fatty acids with varying degrees of unsaturation. Chem. Phys. Lipids. 57:75-80.
17. Günter-Ausborn, S., A. Praetor, and T. Stegmann. 1995. Inhibition of influenza-induced membrane fusion by lysophosphatidylcholine. J. Biol. Chem. 270:29279-29285.
18. Hope, M.J., and P.R. Cullis. 1981. The role of nonbilayer lipid structures in the fusion of human erythrocytes induced by lipid fusogens. Biochim. Biophys. Acta. 640:82-90.
19. Hornby, A.P., and P.R. Cullis. 1981. Influence of local and neutral anaesthetics on the polymorphic phase preferences of egg yolk phosphatidylethanolamine. Biochim. Biophys. Acta. 647:285-292.
20. Kemble, G.W., T. Danieli, and J.M. White. 1994. Lipid-anchored influenza hemagglutinin promotes hemifusion. not complete fusion. Cell. 76:383-391.
21. Kozlov, M.M., S.L. Leikin, L.V. Chernomordik, V.S. Markin, and Yu.A. Chizmadzhev. 1989. Stalk mechanism of membrane fusion. Eur. Biophys. J. 17:121-129.
22. Lieber, M.R., Y. Lange, R.S. Weinstein, and T.L. Steck. 1984. Interaction of chlorpromazine with the human erythrocyte membrane. J. Biol. Chem. 259:9225-9234.
23. MacDonald, R.I. 1986. Trifluoperazine inhibits Sendai virus-induced hemolysis. Biochim. Biophys. Acta. 856:337-347.
24. Melikyan, G.B., W.D. Niles, and F.S. Cohen. 1995a. The fusion kinetics of influenza hemagglutinin expressing cells to planar bilayer membranes is affected by HA density and host cell surface. J. Gen. Physiol. 106:783-802.
25. Melikyan, G.B., J.M. While, and F.S. Cohen. 1995b. GPI-anchored influenza hemagglutinin induces hemifusion to both red blood cell and planar bilayer membranes. J. Cell Biol. 131:679-691.
26. Morris, S.J., O.P. Sarkar, J.M. White, and R. Blumenthal. 1989. Kinetics of pH-dependent fusion between 3T3 fibroblasts expressing influenza hemagglutinin and red blood cells. J. Biol. Chem. 264:3972-3978.
27. Perrin, D.D. 1965. Dissociation Constants of Organic Bases in Aqueous Solution. Butterworths, London. 366 pp.
28. Sarkar, O.P., S.J. Morris, O. Eidelman, J. Zimmerberg, and R. Blumenthal. 1989. Initial stages of influenza hemagglutinin-inducedcell fusion monitored simultaneously by two fluorescent events: cytoplasmic continuity and lipid mixing. J. Cell Biol. 109:113-122.
29. Schoch, C. and R. Blumenthal, 1993. Role of the fusion peptide sequence in initial stage of influenza hemagglutinin-induced cell fusion. J. Biol. Chem. 268:9267-9274.
30. 11) phase, and non-lamellar phase transitions of lipids. Biochim. Biophys. Acta. 1031:1-69.
31. Seeman, P. 1972. The membrane action of anesthetics and tranquilizers. Pharmacol. Rev. 24:583-655.
32. Shangguan, T., D. Alford, and J. Bentz. 1996, Influenza virus-liposome lipid mixing is leaky and largely insensitive to the material properties of the target membrane. Biochemistry. 35:4956-4965.
33. Sheetz, M.P., and S.J. Singer. 1974. Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc. Natl. Acad. Sci. USA. 71:4457-4461.
34. Siegel, D.P. 1993. Modeling protein-induced fusion mechanisms: insight from the relative stability of lipidic structures. In Viral Fusion Mechanisms. J. Bentz. editor. CRC Press. Inc., Boca Raton, FL. 475-512.
35. Steck, T.L. 1989. Red cell shape. In Cell Shape: Determinants. Regulation, and Regulatory Role. W.D. Stein and F. Bronner, editors. Academic Press, Inc., San Diego, CA. 205-246.
36. Stegmann, T., J.M. White, and A. Helenius. 1990. Intermediates in influenza induced membrane fusion. EMBO (Eur. Mol. Biol. Organ.) J. 9:4231-4241.
37. 2+ ions on the properties of bilayer lipid membranes, Bioelectrochem. Bioenerg. 9:133-140.
38. Tien, H.Ti. 1974. Bilayer Lipid Membranes: Theory and Practice. Marcel Dekker, New York. 532 pp.
39. Tilcock, C.P.S., and P.R. Cullis. 1987. Lipid polymorphism. Ann. NY Acad. Sci. 492:88-102.
40. Tse, F.W., A. Iwata, and W. Almers. 1993. Membrane flux through the pore formed by a fusogenic viral envelope protein during cell fusion. J. Cell Biol. 121:543-552.
41. Vogel, S.S., E.A. Leikina, and L.V. Chernomordik. 1993. Lysophosphatidylcholine reversibly arrests exocytosis and viral fusion at a stage between triggering and membrane merger. J. Biol. Chem. 268:25764-25768.
42. Wharton, S.A., J.J. Skehel, and D.C. Wiley. 1986. Studies of influenza haemag-glutinin-mediated membrane fusion. Virology. 149:27-35.
43. White, J.M. 1992. Membrane fusion. Science (Wash. DC). 258:917-924.
44. Zachowski, A., and P. Durand. 1988. Biphasic nature of the binding of cationic amphipaths with artificial and biological membranes. Biochim. Biophys. Acta. 937:411-416.
45. Zimmerberg, J., M. Curran, and F.S. Cohen. 1991. A lipid/protein complex hypothesis for exocytotic fusion pore formation. Ann. NY Acad. Sci. 635:307-317.
46. Zimmerberg, J., R. Blumenthal, O.P. Sarkar, M. Curran, and S.J. Morris. 1994. Restricted movement of lipid and aqueous dyes through pores formed by influenza hemagglutinin during cell fusion. J. Cell Biol. 127:1885-1894.