Stochastic fusion simulations and experiments suggest passive and active roles of hemagglutinin during membrane fusion

Biophysical Journal

Volumn 106, Issue 4, 2014, Pages 843-854

  Lee, Donald W ^a   Thapar, Vikram ^a   Clancy, Paulette ^a   Daniel, Susan ^a  

^a Cornell University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ;

ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; LIPID BILAYER; METABOLISM; PROTEIN MULTIMERIZATION; STATISTICS; VIRUS ENTRY;

HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; LIPID BILAYERS; MODELS, BIOLOGICAL; PROTEIN MULTIMERIZATION; STOCHASTIC PROCESSES; VIRUS INTERNALIZATION;

EID: 84894471806     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.12.048     Document Type: Article

References (62)

1. R.W. Doms, A. Helenius, and J. White Membrane fusion activity of the influenza virus hemagglutinin. The low pH-induced conformational change J. Biol. Chem. 260 1985 2973 2981
2. J.J. Skehel, and D.C. Wiley Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin Annu. Rev. Biochem. 69 2000 531 569
3. J. Bentz Minimal aggregate size and minimal fusion unit for the first fusion pore of influenza hemagglutinin-mediated membrane fusion Biophys. J. 78 2000 227 245
4. R.W. Doms, and A. Helenius Quaternary structure of influenza virus hemagglutinin after acid treatment J. Virol. 60 1986 833 839
5. K.K. Lee Architecture of a nascent viral fusion pore EMBO J. 29 2010 1299 1311
6. T. Kanaseki, and K. Kawasaki S. Ohnishi Structural features of membrane fusion between influenza virus and liposome as revealed by quick-freezing electron microscopy J. Cell Biol. 137 1997 1041 1056
7. C. Böttcher, and K. Ludwig H. Stark Structure of influenza hemagglutinin at neutral and at fusogenic pH by electron cryo-microscopy FEBS Lett. 463 1999 255 259
8. P.A. Bullough, and F.M. Hughson D.C. Wiley Structure of influenza hemagglutinin at the pH of membrane fusion Nature 371 1994 37 43
9. D.C. Wiley, and J.J. Skehel The structure and function of the hemagglutinin membrane glycoprotein of influenza virus Annu. Rev. Biochem. 56 1987 365 394
10. I.A. Wilson, J.J. Skehel, and D.C. Wiley Structure of the hemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution Nature 289 1981 366 373
11. D.K. Struck, D. Hoekstra, and R.E. Pagano Use of resonance energy transfer to monitor membrane fusion Biochemistry 20 1981 4093 4099
12. J. Otterstrom, and A.M. van Oijen Visualization of membrane fusion, one particle at a time Biochemistry 52 2013 1654 1668
13. M. Imai, T. Mizuno, and K. Kawasaki Membrane fusion by single influenza hemagglutinin trimers. Kinetic evidence from image analysis of hemagglutinin-reconstituted vesicles J. Biol. Chem. 281 2006 12729 12735
14. K. Bundo-Morita, S. Gibson, and J. Lenard Estimation by radiation inactivation of the size of functional units governing Sendai and influenza virus fusion Biochemistry 26 1987 6223 6227
15. S. Gibson, and C.Y. Jung J. Lenard Radiation inactivation analysis of influenza virus reveals different target sizes for fusion, leakage, and neuraminidase activities Biochemistry 25 1986 6264 6268
16. S. Günther-Ausborn, and P. Schoen T. Stegmann Role of hemagglutinin surface density in the initial stages of influenza virus fusion: lack of evidence for cooperativity J. Virol. 74 2000 2714 2720
17. T. Danieli, and S.L. Pelletier J.M. White Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers J. Cell Biol. 133 1996 559 569
18. H. Ellens, and J. Bentz J.M. White Fusion of influenza hemagglutinin-expressing fibroblasts with glycophorin-bearing liposomes: role of hemagglutinin surface density Biochemistry 29 1990 9697 9707
19. S. Schreiber, and K. Ludwig H.G. Holzhütter Stochastic simulation of hemagglutinin-mediated fusion pore formation Biophys. J. 81 2001 1360 1372
20. R. Blumenthal, and D.P. Sarkar S.J. Morris Dilation of the influenza hemagglutinin fusion pore revealed by the kinetics of individual cell-cell fusion events J. Cell Biol. 135 1996 63 71
21. D.L. Floyd, and J.R. Ragains A.M. van Oijen Single-particle kinetics of influenza virus membrane fusion Proc. Natl. Acad. Sci. USA 105 2008 15382 15387
22. T. Stegmann, J.M. White, and A. Helenius Intermediates in influenza induced membrane fusion EMBO J. 9 1990 4231 4241
23. D.A. Costello, and D.W. Lee S. Daniel Influenza virus-membrane fusion triggered by proton uncaging for single particle studies of fusion kinetics Anal. Chem. 84 2012 8480 8489
24. T. Ivanovic, and J.L. Choi S.C. Harrison Influenza-virus membrane fusion by cooperative fold-back of stochastically induced hemagglutinin intermediates eLife 2 2013 e00333
25. M.P. Dobay, and A. Dobay E. Mendoza How many trimers? Modeling influenza virus fusion yields a minimum aggregate size of six trimers, three of which are fusogenic Mol. Biosyst. 7 2011 2741 2749
26. V.I. Razinkov, and G.B. Melikyan F.S. Cohen Effects of spontaneous bilayer curvature on influenza virus-mediated fusion pores J. Gen. Physiol. 112 1998 409 422
27. L. Chernomordik, and A. Chanturiya J. Zimmerberg The hemifusion intermediate and its conversion to complete fusion: regulation by membrane composition Biophys. J. 69 1995 922 929
28. L.V. Chernomordik, and E. Leikina J. Zimmerberg An early stage of membrane fusion mediated by the low pH conformation of influenza hemagglutinin depends upon membrane lipids J. Cell Biol. 136 1997 81 93
29. L. Wessels, and M.W. Elting K. Weninger Rapid membrane fusion of individual virus particles with supported lipid bilayers Biophys. J. 93 2007 526 538
30. N.G. Wrigley Electron microscopy of influenza virus Br. Med. Bull. 35 1979 35 38
31. S.T. Hess, and M. Kumar J. Zimmerberg Quantitative electron microscopy and fluorescence spectroscopy of the membrane distribution of influenza hemagglutinin J. Cell Biol. 169 2005 965 976
32. S. Vijayakrishnan, and C. Loney D. Bhella Cryotomography of budding influenza A virus reveals filaments with diverse morphologies that mostly do not bear a genome at their distal end PLoS Pathog. 9 2013 e1003413
33. A. Harris, and G. Cardone A.C. Steven Influenza virus pleiomorphy characterized by cryoelectron tomography Proc. Natl. Acad. Sci. USA 103 2006 19123 19127
34. R.W.H. Ruigrok, and P.J. Andree J.E. Mellema Characterization of three highly purified influenza virus strains by electron microscopy J. Gen. Virol. 65 1984 799 802
35. J.J. Skehel, and P.M. Bayley D.C. Wiley Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion Proc. Natl. Acad. Sci. USA 79 1982 968 972
36. M.J. Gething, and R.W. Doms J. White Studies on the mechanism of membrane fusion: site-specific mutagenesis of the hemagglutinin of influenza virus J. Cell Biol. 102 1986 11 23
37. P. Schoen, L. Leserman, and J. Wilschut Fusion of reconstituted influenza virus envelopes with liposomes mediated by streptavidin/biotin interactions FEBS Lett. 390 1996 315 318
38. T. Stegmann, I. Bartoldus, and J. Zumbrunn Influenza hemagglutinin- mediated membrane fusion: influence of receptor binding on the lag phase preceding fusion Biochemistry 34 1995 1825 1832
39. J. White, J. Kartenbeck, and A. Helenius Membrane fusion activity of influenza virus EMBO J. 1 1982 217 222
40. W.D. Niles, and F.S. Cohen Single event recording shows that docking onto receptor alters the kinetics of membrane fusion mediated by influenza hemagglutinin Biophys. J. 65 1993 171 176
41. S.A. Wharton, J.J. Skehel, and D.C. Wiley Studies of influenza hemagglutinin-mediated membrane fusion Virology 149 1986 27 35
42. M.P. Sheetz Membrane skeletal dynamics: role in modulation of red cell deformability, mobility of transmembrane proteins, and shape Semin. Hematol. 20 1983 175 188
43. M. Krumbiegel, A. Herrmann, and R. Blumenthal Kinetics of the low pH-induced conformational changes and fusogenic activity of influenza hemagglutinin Biophys. J. 67 1994 2355 2360
44. B. Efron, and R. Tibshirani An Introduction to the Bootstrap Vol. 57 1993 CRC Press Boca Raton, FL
45. B.R. Lentz, and J.K. Lee Poly(ethylene glycol) (PEG)-mediated fusion between pure lipid bilayers: a mechanism in common with viral fusion and secretory vesicle release? Mol. Membr. Biol. 16 1999 279 296
46. J. Lee, and B.R. Lentz Evolution of lipidic structures during model membrane fusion and the relation of this process to cell membrane fusion Biochemistry 36 1997 6251 6259
47. D.T. Gillespie General method for numerically simulating stochastic time evolution of coupled chemical reactions J. Comput. Phys. 22 1976 403 434
48. F.J. Massey The Kolmogorov-Smirnov test for goodness of fit J. Am. Stat. Assoc. 46 1951 68 78
49. N. Smirnov Table for estimating the goodness of fit of empirical distributions Ann. Math. Stat. 19 1948 279 281
50. A. Bar Massada, and Y. Carmel Incorporating output variance in local sensitivity analysis for stochastic models Ecol Model. 213 2008 463 467
51. R.A. Böckmann, and A. Hac H. Grubmüller Effect of sodium chloride on a lipid bilayer Biophys. J. 85 2003 1647 1655
52. G. Pabst, and A. Hodzic P. Laggner Rigidification of neutral lipid bilayers in the presence of salts Biophys. J. 93 2007 2688 2696
53. D.L. Floyd, S.C. Harrison, and A.M. van Oijen Analysis of kinetic intermediates in single-particle dwell-time distributions Biophys. J. 99 2010 360 366
54. F.S. Cohen, and G.B. Melikyan The energetics of membrane fusion from binding, through hemifusion, pore formation, and pore enlargement J. Membr. Biol. 199 2004 1 14
55. P.I. Kuzmin, and J. Zimmerberg F.S. Cohen A quantitative model for membrane fusion based on low-energy intermediates Proc. Natl. Acad. Sci. USA 98 2001 7235 7240
56. Y.A. Chizmadzhev The mechanisms of lipid-protein rearrangements during viral infection Bioelectrochemistry 63 2004 129 136
57. Y. Kozlovsky, and M.M. Kozlov Stalk model of membrane fusion: solution of energy crisis Biophys. J. 82 2002 882 895
58. Q. Huang, and R.P. Sivaramakrishna A. Herrmann Early steps of the conformational change of influenza virus hemagglutinin to a fusion active state: stability and energetics of the hemagglutinin Biochim. Biophys. Acta 1614 2003 3 13
59. D. Axelrod, and D.E. Koppel W.W. Webb Mobility measurement by analysis of fluorescence photobleaching recovery kinetics Biophys. J. 16 1976 1055 1069
60. D. Bernstein Simulating mesoscopic reaction-diffusion systems using the Gillespie algorithm Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71 2005 041103
61. S.N. Arjunan, and M. Tomita A new multicompartmental reaction-diffusion modeling method links transient membrane attachment of E. coli MinE to E-ring formation Syst. Synth. Biol. 4 2010 35 53
62. A.M. Klein, and V. Nikolaidou-Neokosmidou B.D. Simons Patterning as a signature of human epidermal stem cell regulation J. R. Soc. Interface 8 2011 1815 1824