Line-tension controlled mechanism for influenza fusion

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Risselada, Herre Jelger ^a   Marelli, Giovanni ^b   Fuhrmans, Marc ^b   Smirnova, Yuliya G ^b   Grubmüller, Helmut ^a   Marrink, Siewert Jan ^c   Müller, Marcus ^b  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA FUSION PEPTIDE; INFLUENZA VIRUS HEMAGGLUTININ; MEMBRANE FUSION PROTEIN; MEMBRANE LIPID; SNARE PROTEIN; UNCLASSIFIED DRUG; VIRUS FUSION PROTEIN;

ARTICLE; BILAYER MEMBRANE; CONTROLLED STUDY; HYDROPHILICITY; KINETICS; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; NONHUMAN; PHYSICAL CHEMISTRY; PROTEIN INTERACTION; PROTEIN STABILITY;

CELL MEMBRANE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; LIPID BILAYERS; MEMBRANE FUSION; MOLECULAR DYNAMICS SIMULATION; PEPTIDE FRAGMENTS; POINT MUTATION; PROTEIN CONFORMATION;

EID: 84862991982     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038302     Document Type: Article

References (76)

1. Chernomordik LV, Zimmerberg J, Kozlov MM, (2006) Membranes of the world unite! J cell Biol 175: 201-207.
2. Chernomordik LV, Kozlov MM, (2008) Mechanics of membrane fusion. Nat Struct Mol Biol 15: 675-683.
3. Kozlov MM, Markin VS, (1983) Possible mechanism of membrane fusion. Biofizika 28: 255-261.
4. Katsov K, Müller M, Schick M, (2004) Field theoretic study of bilayer membrane fusion: I. hemifusion mechanism. Biophys J 87: 3277-3290.
5. Schick M, (2011) Membrane fusion; the emergence of a new paradigm. J Stat Phys 142: 1317.
6. Bonnafous P, Stegmann T, (2000) Membrane perturbation and fusion pore formation in inuenza hemagglutinin-mediated membrane fusion. J Biol Chem 275: 6160-6166.
7. Lee KK, (2010) Architecture of a nascent viral fusion pore. EMBO 29: 1299-1311.
8. Engel A, Walter P, (2008) Membrane lysis during biological membrane fusion: collateral damage by misregulated fusion machines. J Cell Biol 183: 181-186.
9. Donald JE, Zhang Y, Fiorin G, Carnevale V, Slochower DR, et al. (2011) Transmembrane orientation and possible role of the fusogenic peptide from parainuenza virus 5 (PIV5) in promoting fusion. Proc Natl Acad Sci 108: 3958-3963.
10. Kasson PM, Pande VS, (2011) A bundeling of viral fusion mechanisms. Proc Natl Acad Sci 108: 3827-3828.
11. Lai AL, Tamm LK, (2010) Shallow boomerang-shaped inuenza hemagglutinin G13A mutant structure promotes leaky membrane fusion. J Biol Chem 285: 37467-37475.
12. Frolov VA, Dunina-Barkovskaya AY, Samsonov AV, Zimmerberg J, (2003) Membrane permeability changes at early stages of inuenza hemagglutininmediated fusion. Biophys J 85: 1725-1733.
13. Kozlovsky Y, Kozlov MM, (2002) Stalk model of membrane fusion: Solution of energy crisis. Biophys J 82: 882-895.
14. Qiao H, Armstrong RT, Melikyan GB, Cohen FS, White JM, (1999) A specific point mutant at position 1 of the inuenza hemagglutinin fusion peptide displays a hemifusion phenotype. Mol Biol Cell 10: 2759-2769.
15. Li Y, Han AL X Lai, Bushweller JH, Cafiso DS, Tamm LK, (2004) Membrane structures of the hemifusion-inducing fusion peptide mutant G1S and the fusion-blocking mutant G1V of inuenza virus hemagglutinin suggest a mechanism for pore opening in membrane fusion. J Virol 79: 12065-12076.
16. Kuzmin PJ, Zimmerberg J, Chizmadzhev YA, Cohen FS, (2001) A quantitative model for membrane fusion based on low-energy intermediates. Proc Natl Acad Sci 98: 7235-7240.
17. May S, (2002) Structure and energy of fusion stalks: the role of membrane edges. Biophys J 83: 2969-2980.
18. Markin SV, Albanesi JP, (2002) Membrane fusion: stalk model revisited. Biophys J 82: 693-712.
19. Siegel DP, (1993) Energetics of intermediates in membrane fusion: Comparison of stalk and inverted micellar intermediate mechanisms. Biophys J 65: 2124-2140.
20. Lee JY, Schick M, (2007) Dependence of the energies of fusion on the intermembrane separation: Optimal and constrained. J Chem Phys 127: 075102.
21. Siegel DP, Epand RM, (2000) Effect of inuenza hemagglutinin fusion peptide on lamellar/inverted phase transitions in dipalmitoleoylphosphatidylethanolamine: implications for membrane fusion mechanisms. Biochim Biophys Acta 1468: 87-98.
22. Li J, Das P, Zhou R, (2010) Single mutation effects on conformational change and membrane deformation of inuenza hemagglutinin fusion peptides. J Phys Chem B 114: 8799-8806.
23. Fuhrmans M, Knecht V, Marrink SJ, (2009) A single bicontinuous cubic phase induced by fusion peptides. J Am Chem Soc 131: 9166-9167.
24. Fuhrmans M, Marrink SJ, (2012) Molecular view of the role of fusion peptides in promoting positive membrane curvature. J Am Chem Soc 134: 1543-1552.
25. Lai AL, Park H, White JM, Tamm LK, (2006) Fusion peptide of inuenza hemagglutinin requires a fixed angle boomerang structure for activity. J Biol Chem 281: 5760-5770.
26. Rowlinson JS, Widom B, (1982) Molecular theory of capillarity. Clarendon Press, Oxford.
27. Schick M, Katsov K, Müller M, (2005) The central role of line tension in the fusion of biological membranes. Mol Phys 103: 3055.
28. Marrink SJ, Risselada HJ, Yefimov S, Tieleman DP, de Vries AH, (2007) The MARTINI force field: Coarse grained model for biomolecular simulations. J Phys Chem B 111: 7812-7824.
29. Monticelli L, Kandasamy SK, Periole X, Larson RG, Tieleman DP, et al. (2008) The martini coarse grained force field: extension to proteins. J Chem Theory Comput 4: 819-834.
30. Risselada HJ, Kutzner C, Grubmüller H, (2011) Caught in the act: Visualization of snare-mediated fusion events in molecular detail. Chem Bio Chem 12: 1049-1055.
31. Baoukina S, Tieleman DP, (2010) Direct simulation of protein-mediated vesicle fusion: lung surfactant protein B. Biophys J 99: 2134-2142.
32. Müller M, Katsov K, Schick M, (2003) A new mechanism of model membrane fusion determined from monte carlo simulation. Biophys J 85: 1611-1623.
33. Katsov K, Müller M, Schick M, (2006) Field theoretic study of bilayer membrane fusion: II. mechanism of a stalk-hole complex. Biophys J 90: 915-926.
34. Marrink SJ, Mark AE, (2004) Molecular view of hexagonal phase formation in phospholipid membranes. Biophys J 87: 3894-3900.
35. Knecht V, Mark AE, Marrink SJ, (2006) Phase behavior of fatty acids/lipid/water mixture studied in atomic detail. J Am Chem Soc 128: 2030-2034.
36. Laradji M, Shi AC, Noolandi J, Desai RC, (1997) Stability of ordered phases in diblock copolymer melts. Macromolecules 30: 3242-3255.
37. Stegmann T, (1992) Inuenza hemagglutinin-mediated membrane fusion does not involve inverted phase lipid intermediates. Biochem Mol Biol 268: 1716-1722.
38. Siegel DP, (2008) The gaussian curvature elastic energy of intermediates in membrane fusion. Biophys J 95: 5200-5215.
39. Risselada HJ, Grubmüller H, (2012) How snare molecules mediate membrane fusion: Recent insights from molecular simulations. Curr Opin Struc Biol 22: 187-196.
40. Markvoort AJ, Marrink SJ, (2011) Lipid acrobatics in the membrane fusion arena. Curr Topics in Membranes 68: 259-294.
41. Tolpekina T, den Otter W, Briels W, (2004) Nucleation free energy of pore formation in an amphiphilic bilayer studied by molecular dynamics simulations. J Chem Phys 121: 12060.
42. Aeffner A, Reusch T, Weinhausen B, Salditt T, (2009) Membrane fusion intermediates and the effect of cholesterol: An in-house X-ray scattering study. Eur Phys J E 30: 205-214.
43. Haluska CK, Riske KA, Marchi-Artzner V, Lehn JM, Lipowsky R, et al. (2006) Time scales of membrane fusion revealed by direct imaging of vesicle fusion with high temporal resolution. Proc Natl Acad Sci 103: 15841-15846.
44. Stevens MJ, Hoh JH, Woolf TB, (2003) Insights into the molecular mechanism of membrane fusion from simulation: Evidence for the association of splayed tails. Phys Rev Lett 91: 188102.
45. Smirnova YG, Marrink SJ, Lipowsky R, Knecht V, (2010) Solvent-exposed tails as prestalk transition states for membrane fusion at low hydration. J Am Chem Soc 132: 6710-6718.
46. Kasson PM, Lindahl E, Pande VS, (2010) Atomic-resolution simulations predict a transition state for vesicle fusion defined by contact of a few lipid tails. PLOS Comput Biol.
47. Brewster R, Safran SA, (2010) Line active hybrid lipids determine domain size in phase separation of saturated and unsaturated lipids. Biophys J 98: L21-L23.
48. Schäfer LV, Marrink SJ, (2010) Partitioning of lipids at domain boundaries in model membranes. Biophys J 99: L91-L93.
49. Sengupta D, Leontiadou H, Mark AE, Marrink SJ, (2008) Toroidal pores formed by antimicrobial peptides show significant disorder. Biochim Biophys Acta 1778: 2308-2317.
50. Huang HW, Chen FY, Lee MT, (2004) Molecular mechanism of peptideinduced pores in membranes. Phys Rev Lett 92: 198304.
51. Illya G, Deserno M, (2008) Coarse-grained simulation studies of peptideinduced pore formation. Biophys J 95: 4163-4173.
52. Markosyan RM, Melikyan GB, Cohen FS, (1999) Tension of membranes expressing the hemagglutinin of inuenza virus inhibits fusion. Biophys J 77: 943-952.
53. Kasson PM, Lindahl E, Pande VS, (2011) Water ordering at membrane interfaces controls fusion dynamics. J Am Chem Soc 133: 3812-3815.
54. Morgan CG, Williamson H, Fuller S, Hudson B, (1983) Melittin induces fusion of unilamellar phospholipid vesicles. Biochim Biophys Acta 732: 668-774.
55. Cirac AD, Moiset G, Mika JT, Kocer A, Salvador P, et al. (2011) The molecular basis for antimicrobial activity of pore-forming cyclic peptides. Biophys J 100: 2422-2431.
56. Longo ML, Waring AJ, Hammer DA, (1997) Interaction of the inuenza hemagglutinin fusion peptide with lipid bilayers: area expansion and permeation. Biophys J 73: 1430-1439.
57. Longo ML, Waring LM A J Gordon, Hammer DA, (1998) Area expansion and permeation of phospholipid membrane bilayers by inuenza fusion peptides and melittin. Langmuir 14: 2385-2395.
58. Soltesz SA, Hammer DA, (1997) Lysis of large unilamellar vesicles induced by analogs of the fusion peptide of inuenza virus hemagglutinin. J Coll Int Sci 186: 339-409.
59. Shangguan T, Alford D, Bentz J, (1996) Inuenza virus-liposome lipid mixing is leaky and largely insensitive to the material properties of the target membrane. Biochemistry 35: 4956-4965.
60. Torres O, Bong D, (2011) Determinants of membrane activity from mutational analysis of the HIV fusion peptide. Biochemistry 50: 5195-5207.
61. Lipowsky R, (1992) Budding of membranes induced by intermembrane domains. JPhys II (France) 2: 1825.
62. Armstrong RT, Kushnir AS, White JM, (2000) The transmembrane domain of inuenza hemagglutinin exhibits a stringent length requirement to support the hemifusion to fusion transition. J Cell Biol 151: 425-438.
63. Schroth-Diez B, Ponimaskin E, Reverey H, Schmidt MFG, Herrmann A, (1998) Fusion activity of transmembrane and cytoplasmic domain chimeras of the inuenza virus glycoprotein hemagglutinin. J Virol 72: 133-141.
64. Melikyan GB, Lin S, Roth MG, Cohen FS, (1999) Amino acid sequence requirements of the transmembrane and cytoplasmic domains of inuenza virus hemagglutinin for viable membrane fusion. Mol Biol Cell 10: 1821-1836.
65. Melikyan GB, Markosyan RM, Roth MG, Cohen FS, (2000) A point mutation in the transmembrane domain of the hemagglutinin of inuenza virus stabilizes a hemifusion intermediate that can transit to fusion. Mol Biol Cell 11: 3765-3775.
66. Ujike M, Nakajima K, Nobusawa E, (2006) A point mutation at the C terminus of the cytoplasmic domain of inuenza B virus haemagglutinin inhibits syncytium formation. J Gen Virol 87: 1669-1676.
67. Vaidya NK, Huang H, Takagi S, (2010) Simulation of interaction between hemagglutinin fusion peptides and lipid bilayer membranes. Adv Appl Math Mech 2: 430-450.
68. Chernomordik LV, Kozlov MM, (2002) The protein coat in membrane fusion: Lessons from fussion. Traffic 3: 256-267.
69. Lee J, Schick M, (2008) Calculation of free energy barriers to the fusion of small vesicles. Biophys J 94: 1699-1706.
70. Risselada HJ, Mark AE, Marrink SJ, (2008) Application of mean field boundary potentials in simulations of lipid vesicles. J Chem Phys B 112: 7438-7447.
71. Han X, Bushweller JH, Cafiso DS, Tamm LK, (2001) Membrane structure and fusion triggering conformational change of the fusion domain from inuenza hemagglutinin. Nat Struct Biol 8: 715-720.
72. Sammalkorpi M, Lazaridis T, (2007) Configuration of inuenza hemagglutinin fusion peptide monomers and oligomers in membranes. Biochem Biophys Acta 1768: 430-438.
73. Yesylevskyy S, Schäfer L, Sengupta D, Marrink S, (2010) Polarizable water model for the coarse-grained martini force field. PLoS Comput Biol 6: e1000810.
74. Hess B, Kutzner C, Van Der Spoel D, Lindahl E, (2008) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4: 435.
75. Berendsen HJC, Postma JPM, van Gunsteren WF, Di Nola A, Haak JR, (1984) Molecular-dynamics with coupling to an external bath. J Chem Phys 81: 3684-3690.
76. Marrink SJ, Periole X, Tieleman DP, de Vries AH, (2010) Reply to the comment on on using a too large integration time step in molecular dynamics simulations of coarse-grained molecular models. Phys Chem Chem Phys 12: 2257-2258.