Reversible merger of membranes at the early stage of influenza hemagglutinin-mediated fusion

Molecular Biology of the Cell

Volumn 11, Issue 7, 2000, Pages 2359-2371

  Leikina, Eugenia ^a   Chernomordik, Leonid V ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ;

ARTICLE; CELL FUSION; ENERGY; HUMAN; HUMAN CELL; INFLUENZA VIRUS; LIPID TRANSPORT; NONHUMAN; PRIORITY JOURNAL; TEMPERATURE; VIRUS CELL INTERACTION;

HUMAN INFLUENZA VIRUS; INFLUENZA VIRUS;

EID: 0033916032     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.11.7.2359     Document Type: Article

References (42)

1. Benz, J. (2000). Minimal aggregate size and minimal fusion unit for the first fusion pore of influenza hemagglutinin-mediated membrane fusion. Biophys J. 78, 227-245.
2. Blumenthal, R., Pak, C.C., Raviv, Y., Krumbiegel, M., Bergelson, L.D., Morris, S.J., and Lowy, R.J. (1995). Transient domains induced by influenza hemagglutinin during membrane fusion. Mol. Membr. Biol. 12, 135-142.
3. Blumenthal, R., Sarkar, D.P., Durell, S., Howard, D.E., and Morris, S.J. (1996). Dilation of the influenza hemagglutinin fusion pore revealed by the kinetics of individual cell-cell fusion events. J. Cell Biol. 135, 63-71.
4. Bullough, P.A., Hughson, P.M., Skehel, J.J., and Wiley, D.C. (1994). Structure of influenza hemagglutinin at the pH of membrane fusion. Nature 371, 37-43.
5. Carr, C.M., Chaudhry, C., and Kim, P.S. (1997). Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc. Natl. Acad. Sci. USA 94, 14306-14313.
6. Carr, C.M., and Kim, P.S. (1993). A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73, 823-832.
7. Chen, J., Skehel, J.J., and Wiley, D.C. (1999). N- and C-terminal. residues combine in the fusion-pH influenza hemagglutinin HA(2) subunit to form an N cap that terminates the triple-stranded coiled coil. Proc. Natl. Acad. Sci. USA 96, 8967-8972.
8. Chernomordik, L. (1996). Non-bilayer lipids and biological fusion intermediates. Chem. Phys. Lipids 81, 203-213.
9. Chernomordik, L., Kozlov, M., and Zimmerberg, J. (1995). Lipids in biological membrane fusion. J. Membr. Biol. 146, 1-14.
10. Chernomordik, L.V., Frolov, V.A., Leikina, E., Bronk, P., and Zimmerberg, J. (1998). The pathway of membrane fusion catalyzed by influenza hemagglutinin: restriction of lipids, hemifusion, and lipidic fusion pore formation. J. Cell Biol. 140, 1369-1382.
11. Chernomordik, L.V., Leikina, E., Frolov, V., Bronk, P., and Zimmerberg, J. (1997). An early stage of membrane fusion mediated by the low pH conformation of influenza hemagglutinin depends upon membrane lipids. J. Cell Biol. 136, 81-94.
12. Clague, M.J., Schoch, C., and Blumenthal, R. (1991). Delay time for influenza virus hemagglutinin-induced membrane fusion depends on hemagglutinin surface density. J. Virol. 65, 2402-2407.
13. Danieli, T., Pelletier, S.L., Henis, Y.I., and White, J.M. (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., Douglas, A.R., Skehel, J.J., and Wiley, D.C. (1983). Analyses of the antigenicity of influenza hemagglutinin at the pH optimum for virus-mediated membrane fusion. J. Gen. Virol. 64, 1657-1662.
15. Doxsey, S.J., Sambrook, J., Helenius, A., and White, J. (1985). An efficient method for introducing macromolecules into living cells. J. Cell Biol. 101, 19-27.
16. Epand, R.F., Macosko, J.C., Russell, C.J., Shin, Y.K., and Epand, R.M. (1999). The ectodomain of HA2 of influenza virus promotes rapid pH dependent membrane fusion. J. Mol. Biol. 286, 489-503.
17. Gaudin, Y., Ruigrok, R.W.H., and Brunner, J. (1995). Low-pH induced conformational changes in viral fusion proteins: implications for the fusion mechanism. J. Gen. Virol. 76, 1541-1556.
18. Gray, C., and Tamm, L.K. (1998). pH-induced conformational changes of membrane-bound influenza hemagglutinin and its effect on target lipid bilayers. Protein Sci. 7, 2359-2373.
19. Gunther-Ausborn, S., Schoen, P., Bartoldus, I., Wilschut, J., and Stegmann, T. (2000). Role of hemagglutinin surface density in the initial stages of influenza virus fusion: lack of evidence for cooperativity. J. Virol. 74, 2714-2720.
20. Junankar, P.R., and Cherry, R.J. (1986). Temperature and pH dependence of the hemolytic activity of influenza virus and of the rotational mobility of the spike glycoproteins. Biochim. Biophys. Acta 854, 198-206.
21. Kemble, G.W., Danieli, T., and White, J.M. (1994). Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 76, 383-391.
22. Kemble, G.W., Henis, Y.I., and White, J.M. (1993). GPI- and transmembrane-anchored influenza hemagglutinin differ in structure and receptor binding activity. J. Cell Biol. 122, 1253-1265.
23. Kim, C.H., Macosko, J.C., and Shin, Y.K. (1998). The mechanism for low-pH-induced clustering of phospholipid vesicles carrying the HA2 ectodomain of influenza hemagglutinin. Biochemistry 37, 137-144.
24. Korte, T., Ludwig, K., Booy, F.P., Blumenthal, R., and Herrmann, A. (1999). Conformational intermediates and fusion activity of influenza virus hemagglutinin. J. Virol. 73, 4567-4574.
25. Kozlov, M.M., and Chernomordik, L.V. (1998). A mechanism of protein-mediated fusion: coupling between refolding of the influenza hemagglutinin and lipid rearrangements. Biophys. J. 75, 1384-1396.
26. Krumbiegel, M., Herrmann, A., and Blumenthal, R. (1994). Kinetics of the low pH-induced Conformational changes and fusogenic activity of influenza hemagglutinin. Biophys. J. 67, 2355-2360.
27. Melikyan, G.B., Brener, S.A., Ok, D.C., and Cohen, F.S. (1997). Inner but not outer membrane leaflets control the transition from glycosylphosphatidylinositol-anchored influenza hemagglutinin-induced hemifusion to full fusion. J. Cell Biol. 136, 995-1005.
28. Melikyan, G.B., Lin, S., Roth, M.G., and Cohen, F.S. (1999). Amino acid sequence requirements of the transmembrane and cytoplasmic domains of influenza virus hemagglutinin for viable membrane fusion. Mol. Biol. Cell 10, 1821-1836.
29. Melikyan, G.B., Niles, W.D, Peeples, M.E., and Cohen, F.S. (1993). Influenza hemagglutinin-mediated fusion pores connecting cells to planar membranes: flickering to final expansion. J. Gen. Physiol. 102, 1131-1149.
30. Melikyan, G.B., Niles, W.D., Ratinov, V.A., Karhanek, M., Zimmerberg, J., and Cohen, F.S. (1995a). Comparison of transient and successful fusion pores connecting influenza hemagglutinin expressing cells to planar membranes. J. Gen. Physiol. 106, 803-819.
31. Melikyan, G.B., White, J.M., and Cohen, F.S. (1995b). GPI-anchored influenza hemagglutinin induces hemifusion to both red blood cell and planar bilayer membranes. J. Cell Biol. 131, 679-691.
32. Murphy, R.F., Powers, S., and Cantor, C.R. (1984). Endosome pH measured in single cells by dual fluorescence flow cytometry: rapid acidification of insulin to pH 6. J. Cell Biol. 98, 1757-1762.
33. Roederer, M., Bowser, R., and Murphy, R.F. (1987). Kinetics and temperature dependence of exposure of endocytosed material to proteolytic enzymes and low pH: evidence for a maturation model for the formation of lysosomes. J. Cell Physiol. 131, 200-209.
34. Schoch, C., Blumenthal, R., and Clague, M.J. (1992). A long-lived state for influenza virus-erythrocyte complexes committed to fusion at neutral pH. FEBS Lett. 311, 221-225.
35. Stegmann, T., White, J.M., and Helenius, A. (1990). Intermediates in influenza induced membrane fusion. EMBO J. 9, 4231-4241.
36. Tse, F.W., Iwata, A., and Almers, W. (1993). Membrane flux through the pore formed by a fusogenic viral envelope protein during cell fusion. J. Cell Biol. 121, 543-552.
37. Weissenhorn, W., Dessen, A., Harrison, S.C., Skehel, J.J., and Wiley, D.C. (1997). Atomic structure of the ectodomain from HIV-1 gp41. Nature 387, 426-430.
38. White, J. (1996). Membrane fusion: the influenza paradigm. Cold Spring Harbor Symp. 60, 581-588.
39. White, J., Matlin, K., and Helenius, A. (1981). Cell fusion by Semliki Forest, influenza, and vesicular stomatitis viruses. J. Cell Biol. 89, 674-679.
40. White, J.M., and Wilson, I.A. (1987). Anti-peptide antibodies detect steps in a protein conformational change: low-pH activation of the influenza virus hemagglutinin. J. Cell Biol. 105, 2887-2896.
41. Wiley, D.C., and Skehel, J.J. (1987). The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 56, 365-394.
42. Zimmerberg, J., Blumenthal, R., Sarkar, D.P., Curran, M., and Morris, S.J. (1994). Restricted movement of lipid and aqueous dyes through pores formed by influenza hemagglutinin during cell fusion. J. Cell Biol. 127, 1885-1894.