An early stage of membrane fusion mediated by the low pH conformation of influenza hemagglutinin depends upon membrane lipids

Journal of Cell Biology

Volumn 136, Issue 1, 1997, Pages 81-93

  Chernomordik, Leonid V ^a   Leikina, Eugenia ^a   Frolov, Vadim ^a,b   Bronk, Peter ^a   Zimmerberg, Joshua ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b FRUMKIN INSTITUTE OF PHYSICAL CHEMISTRY AND ELECTROCHEMISTRY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ; LYSOPHOSPHATIDYLCHOLINE; MEMBRANE LIPID; OLEIC ACID; UNSATURATED FATTY ACID;

ANIMAL CELL; ARTICLE; CELL FUSION; CELL STRAIN 3T3; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ERYTHROCYTE; HUMAN; HUMAN CELL; INFLUENZA VIRUS; MEMBRANE FUSION; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL;

3T3 CELLS; ANIMALS; ENDOPEPTIDASE K; ERYTHROCYTE MEMBRANE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HYDROGEN-ION CONCENTRATION; LYSOPHOSPHATIDYLCHOLINES; MEMBRANE FUSION; MEMBRANE LIPIDS; MICE; NEURAMINIDASE; OLEIC ACID; PATCH-CLAMP TECHNIQUES; PROTEIN CONFORMATION;

EID: 0031012628     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.136.1.81     Document Type: Article

References (77)

1. Alford, D., H. Ellens, and J. Bentz. 1994. Fusion of influenza virus with sialic acid-bearing target membranes. Biochemistry. 33:1977-1987.
2. Bhamidipati, S.P., and J.A. Hamilton. 1995. Interactions of lyso 1-palmitoylphosphatidylcholine with phospholipids: a 13C and 31P NMR study. Biochemistry. 34:5666-5677.
3. Broring, K., C.W. Haest, and B. Deuticke. 1989. Translocation of oleic acid across the erythrocyte membrane. Evidence for a fast process. Biochim. Biophys. Acta. 986:321-331.
4. 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 (Lond.), 371:37-43.
5. Carr, C.M., and P.S. Kim. 1993. A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell. 73:823-832.
6. Chernomordik, L.V., G.B. Melikyan, and Y.A. Chizmadzhev. 1987. Biomembrane fusion: a new concept derived from model studies using two interacting planar lipid bilayers. Biochim. Biophys. Acta. 906:309-352.
7. Chernomordik, L.V., S.S. Vogel, A. Sokoloff, H.O. Onaran, E.A. Leikina, and J. Zimmerberg. 1993. Lysolipids reversibly inhibit Ca(2+)-, GTP- and pH-dependent fusion of biological membranes. FEBS Lett. 318:71-76.
8. Chernomordik, L., A. Chanturiya, J. Green, and J. Zimmerberg. 1995a. The hemifusion intermediate and its conversion to complete fusion: regulation by membrane composition. Biophys. J. 69:922-929.
9. Chernomordik, L., M. Kozlov, and J. Zimmerberg. 1995b. Lipids in biological membrane fusion. J. Membr. Biol. 146:1-14.
10. Chernomordik, L., E. Leikina, and J. Zimmerberg. 1995c. Control of baculovirus gp64-induced syncytia formation by membrane lipid composition. J. Virol. 69:3049-3058.
11. Coorssen, J.R. 1996. Phospholipase activation and secretion: evidence that PLA2, PLC, and PLD are not essential to exocytosis. Am. J. Physiol. 270: C1153-C1163.
12. Creutz, C.E. 1981. cis-Unsaturated fatty acids induce the fusion of chromaffin granules aggregated by synexin. J. Cell Biol. 91:247-256.
13. 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.
14. Daniels, R.S., J.C. Downie, A.J. Hay, M. Knossow, J.J. Skehel, M.L. Wang, and D.C. Wiley. 1985. Fusion mutants of the influenza virus hemagglutinin glycoprotein. Cell. 40:431-439.
15. Dimitrov, D.S., and R. Blumenthal. 1994. Photoinactivation and kinetics of membrane fusion mediated by the human immunodeficiency virus type 1 envelope glycoprotein. J. Virol. 68:1956-1961.
16. Doms, R.W., A. Helenius, and J. White. 1985. Membrane fusion activity of the influenza virus hemagglutinin. The low pH-induced conformational change. J. Biol. Chem. 260:2973-2981.
17. Doxsey, S.J., J. Sambrook, A. Helenius, and J. White. 1985. An efficient method for introducing macromolecules into living cells. J. Cell Biol. 101:19-27.
18. 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. 31:155-178.
19. Epand, R.M. 1985. Diacylglycerols, lysolecithin, or hydrocarbons markedly alter the bilayer to hexagonal phase transition temperature of phosphatidylethanolamines. Biochemistry. 24:7092-7095.
20. Epand, R.M., R.F. Epand, and C.R. Lancaster. 1988. Modulation of the bilayer to hexagonal phase transition of phosphatidylethanolamines by acylglycerols. Biochim. Biophys. Acta. 945:161-166.
21. 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.
22. Fujii, T., and A. Tamura. 1984. Shape change of human erythrocytes induced by phosphatidylcholine and lysophosphatidylcholine species with various acyl chain lengths. Cell Biochem. Funct. 2:171-176.
23. Gething, M.J., R.W. Doms, D. York, and J. White. 1986. Studies on the mechanism of membrane fusion: site-specific mutagenesis of the hemagglutinin of influenza virus. J. Cell Biol. 102:11-23.
24. Glick, B.S., and J.E. Rothman. 1987. Possible role for fatty acyl-coenzyme A in intracellular protein transport. Nature (Lond.). 326:309-312.
25. Golan, D.E., S.T. Furlong, C.S. Brown, and J.P. Caulfield. 1988. Monopalmitoylphosphatidylcholine incorporation into human erythrocyte ghost membranes causes protein and lipid immobilization and cholesterol depletion. Biochemistry. 27:2661-2667.
26. Gunther-Ausborn, S., A. Praetor, and T. Stegmann. 1995. Inhibition of influenza-induced membrane fusion by lysophosphatidylcholine. J. Biol Chem270:29279-29285.
27. Gutman, O., T. Danieli, J.M. White, and Y.I. Henis. 1993. Effects of exposure to low pH on the lateral mobility of influenza hemagglutinin expressed at the cell surface: correlation between mobility inhibition and inactivation. Biochemistry. 32:101-106.
28. Hoekstra, D., T. de Boer, K. Klappe, and J. Wilschut. 1984. Fluorescence method for measuring the kinetics of fusion between biological membranes, Biochemistry. 23:5675-5681.
29. Kemble, G.W., Y.I. Henis, and J.M. White. 1993. GPI- and transmembraneanchored influenza hemagglutinin differ in structure and receptor binding activity. J. Cell Biol. 122:1253-1265.
30. Kemble, G.W., T. Danieli, and J.M. White. 1994. Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell. 76:383-391.
31. Kozlov, M.M., and V.S. Markin. 1983. Possible mechanism of membrane fusion. Biofizika. 28:255-261.
32. Kramp, W., G. Pieroni, R.N. Pinckard, and D.J. Hanahan. 1984. Observations on the critical micellar concentration of 1-O-alkyl-2-acetyl-sn-glycero-3-phosphocholine and a series of its homologs and analogs. Chem. Phys. Lipids. 35:49-62.
33. Leenhouts, J.M., and B. De Kruijff. 1995. Membrane potential-driven translocation of a lipid-conjugated rhodamine. Biochim. Biophys. Acta. 1237:121-126.
34. Lindau, M., and W. Almers. 1995. Structure and function of fusion pores in exocytosis and ectoplasmic membrane fusion. Curr. Opin. Cell Biol. 7:509-517.
35. MacDonald, R.L. 1990. Characteristics of self-quenching of the fluorescence of lipid-conjugated rhodamine in membranes. J. Biol. Chem. 265:13533-13539.
36. Madden, T.D., and P.R. Cullis. 1982. Stabilization of bilayer structure for unsaturated phosphatidylethanolamines by detergents. Biochim. Biophys. Acta. 684:149-153.
37. 2-terminal SIV fusion peptide into the lipid bilayer. FEBS Lett. 333:325-330.
38. 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.
39. 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.
40. Melikyan, G.B., W.D. Niles, V.A. Ratinov, M. Karhanek, J. Zimmerberg, and F.S. Cohen. 1995b. Comparison of transient and successful fusion pores connecting influenza hemagglutinin expressing cells to planar membranes. J. Gen. Physiol. 106:803-819.
41. Melikyan, G.B., J.M. White, and F.S. Cohen. 1995c. GPI-anchored influenza hemagglutinin induces hemifusion to both red blood cell and planar bilayer membranes. J. Cell Biol. 131:679-691.
42. Melikyan, G.B., B.N. Deny, D.C. Ok, and F.S. Cohen. 1996. Voltage-dependent translocation of R18 and Dil across lipid bilayers leads to fluorescence changes, Biophys. J. 71:2680-2691.
43. Mohandas, N., J. Wyatt, S.F. Mel, M.E. Rossi, and S.B. Shohet. 1982. Lipid translocation across the human erythrocyte membrane. Regulatory factors. J. Biol. Chem. 257:6537-6543.
44. Monck, J.R., and J.M. Fernandez. 1992. The exocytotic fusion pore. J. Cell Biol. 119:1395-1404.
45. Morris, S.J., J. Zimmerberg, D.P. Sarkar, and R. Blumenthal. 1993. Kinetics of cell fusion mediated by viral spike glycoproteins. Methods Enzymol 221:42-58.
46. Nagao, T., T. Kubo, R. Fujimoto, H. Nishio, T. Takeuchi, and F. Hata. 1995. Ca(2+)-independent fusion of secretory granules with phospholipase A2-treated plasma membranes in vitro. Biochem J. 307:563-569.
47. Ohki, S. 1988. Surface tension, hydration energy and membrane fusion. In Molecular Mechanisms of Membrane Fusion. S. Ohki, D. Doyle, T.D. Flanagan, S.W. Hui, and M.E., editors. Plenum Press, New York. 123-139.
48. Paiement, J., C. Lavoie, G.R. Gavino, and V.C. Gavino. 1994. Modulation of GTP-dependent fusion by linoleic and arachidonic acid in derivatives of rough endoplasmic reticulum from rat liver. Biochim. Biophvs. Acta. 1190: 199-212.
49. Rand, R.P., and V.A. Parsegian. 1989. Hydration forces between phospholipid bilayers. Biochim. Biophys. Acta. 988:351-376.
50. Sarkar, O.P., S.J. Morris, O. Eidelman, J. Zimmerberg, and R. Blumenthal. 1989. Initial stages of influenza hemagglutinin-induced cell fusion monitored simultaneously by two fluorescent events: cytoplasmic continuity and lipid mixing. J. Cell Biol. 109:113-122.
51. Schoch, C., and R. Blumenthal. 1993. Role of the fusion peptide sequence in initial stages of influenza hemagglutinin-induced cell fusion. J. Biol. Chem. 268:9267-9274.
52. Schoch, C., R. Blumenthal, and M.J. Clague. 1992. A long-lived state for influenza virus-erythrocyte complexes committed to fusion at neutral pH. FEBS Lett. 311:221-225.
53. Shangguan, T., D. Alford, and J. Bentz. 1996. Influenza-virus lipid mixing is leaky and largely insensitive to the material properties of the target membrane. Biochemistry. 35:4956-4965.
54. Siegel, D.P. 1993a. Energetics of intermediates in membrane fusion: comparison of stalk and inverted micellar intermediate mechanisms. Biophys. J. 65: 2124-2140.
55. Siegel, D.P. 1993a. Modeling protein-induced fusion mechanisms: insights from the relative stability of lipidic structures. In Viral Fusion. J. Bentz, editor. CRS Press, Boca Raton. FL. 477-512.
56. Spruce, A.E., A. Iwata, J.M. White, and W. Almers. 1989. Patch clamp studies of single cell-fusion events mediated by a viral fusion protein. Nature (Lond.), 342:555-558.
57. Stegmann, T. 1993. Influenza hemagglutinin-mediated membrane fusion does not involve inverted phase lipid intermediates. J. Biol. Chem. 268:1716-1722.
58. Stegmann, T., D. Hoekstra, G, Scherphof, and J. Wilschut. 1985. Kinetics of pH-dependent fusion between influenza virus and liposomes. Biochemistry. 24: 3107-3113.
59. Stegmann, T., J.M. Delfino, P.M. Richards, and A. Helenius. 1991. The HA2 subunit of influenza hemagglutinin inserts into the target membrane before fusion. J. Biol. Chem. 266:18404-18410.
60. Tatulian, S.A., P. Hinterdorfer, G. Baber, and L.K. Tamm. 1995. Influenza hemagglutinin assumes a tilted conformation during membrane fusion as determined by attenuated total reflection FTIR spectroscopy. EMBO (Eur. Mol. Biol. Organ.) J. 14:5514-5523.
61. 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.
62. 2-terminal segment during influenza virus-induced membrane fusion. J. Biol. Chem. 267:20225-20232.
63. van Meer, G., J. Davoust, and K. Simons. 1985. Parameters affecting low-pH-mediated fusion of liposomes with the plasma membrane of cells infected with influenza virus. Biochemistry. 24:3593-3602.
64. Weber, T., G. Paesold, C. Galli, R. Mischler, G. Semenza, and J. Brunner. 1994. Evidence for H( + )-induced insertion of influenza hemagglutinin HA2 N-terminal segment into viral membrane. J. Biol. Chem. 269:18353-18358.
65. Weltzien, H.U. 1979. Cytolytic and membrane-perturbing properties of lysophosphatidylcholine. Biochim. Biophys. Acta. 559:259-287.
66. White, J. 1996. Membrane fusion: the influenza paradigm. Cold Spring Harbor Symp. Quant. Biol. 60:581-588.
67. White, J., J. Kartenbeck, and A. Helenius. 1982. Membrane fusion activity of influenza virus. EMBO (Eur. Mol. Biol. Organ.) J. 1:217-222.
68. White, J., M. Kielian, and A. Helenius. 1983. Membrane fusion proteins of enveloped animal viruses. Q. Rev. Biophys. 16:151-195.
69. White, J.M. 1992. Membrane fusion. Science (Wash. DC). 258:917-924.
70. 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.
71. 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 (Lond.). 289:366-373.
72. Yeagle, P.L., F.T. Smith, J.E. Young, and T.D. Flanagan. 1994. Inhibition of membrane fusion by lysophosphatidylcholine. Biochemistry. 33:1820-1827.
73. Yoshimura, A., K. Kuroda, K. Kawasaki, S. Yamashina, T. Maeda, and S. Ohnishi. 1982. Infectious cell entry mechanism of influenza virus. J. Virol 43:284-293.
74. Zimmerberg, J. 1993. Simultaneous electrical and optical measurements of individual membrane fusion events during exocytosis. Methods Enzymol. 221: 99-112.
75. Zimmerberg, J., M. Curran, and F.S. Cohen. 1991. A lipid/protein complex hypothesis for exocytotic fusion pore formation. Annu. NY Acad. Sci. 635:307-317.
76. Zimmerberg, J., S.S. Vogel, and L.V. Chernomordik. 1993. Mechanisms of membrane fusion. Annu. Rev. Biophys. Biomol. Struct. 22:433-466.
77. Zimmerberg, J., R. Blumenthal, M. Curran, D. Sarkar, and S. Morris. 1994. Restricted movement of lipid and aqueous dyes through pores formed by influenza hemagglutinin during cell fusion. 7. Cell Biol. 127:1885-1894.