Lipid Tail Protrusion in Simulations Predicts Fusogenic Activity of Influenza Fusion Peptide Mutants and Conformational Models

PLoS Computational Biology

Volumn 9, Issue 3, 2013, Pages

  Larsson, Per ^a   Kasson, Peter M ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; FREE ENERGY; MIXING; MOLECULAR DYNAMICS; PEPTIDES;

DYNAMICS SIMULATION; FUSION PEPTIDES; HELICAL HAIRPINS; IMPORTANT FEATURES; LIPID MIXING; MEMBRANE FUSION; MIXING RATES; N-TERMINALS; PEPTIDE STRUCTURES; TRANSITION STATE;

LIPID BILAYERS;

INFLUENZA VIRUS HEMAGGLUTININ; MUTANT PROTEIN; VIRUS FUSION PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; LIPID BILAYER; MEMBRANE FUSION; MOLECULAR DYNAMICS; PROTEIN CONFORMATION; PROTEIN FUNCTION; STRUCTURE ANALYSIS; VIRUS STRAIN;

EID: 84875983059     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002950     Document Type: Article

References (48)

1. Kemble GW, Danieli T, White JM, (1994) Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 76: 383-391 doi:10.1016/0092-8674(94)90344-1.
2. Qiao H, Armstrong RT, Melikyan GB, Cohen FS, White JM, (1999) A specific point mutant at position 1 of the influenza hemagglutinin fusion peptide displays a hemifusion phenotype. Mol Biol Cell 10: 2759-2769.
3. Armstrong RT, Kushnir AS, White JM, (2000) The Transmembrane Domain of Influenza Hemagglutinin Exhibits a Stringent Length Requirement to Support the Hemifusion to Fusion Transition. The Journal of Cell Biology 151: 425-438 doi:10.1083/jcb.151.2.425.
4. Steinhauer DA, Wharton SA, Skehel JJ, Wiley DC, (1995) Studies of the membrane fusion activities of fusion peptide mutants of influenza virus hemagglutinin. J Virol 69: 6643-6651.
5. Langley WA, Thoennes S, Bradley KC, Galloway SE, Talekar GR, et al. (2009) Single residue deletions along the length of the influenza HA fusion peptide lead to inhibition of membrane fusion function. Virology 394: 321-330 doi:10.1016/j.virol.2009.08.031.
6. Lai AL, Park H, White JM, Tamm LK, (2006) Fusion peptide of influenza hemagglutinin requires a fixed angle boomerang structure for activity. J Biol Chem 281: 5760-5770 doi:10.1074/jbc.M512280200.
7. Chernomordik L, Chanturiya A, Green J, Zimmerberg J, (1995) The hemifusion intermediate and its conversion to complete fusion: regulation by membrane composition. Biophysical Journal 69: 922-929 doi:10.1016/S0006-3495(95)79966-0.
8. Malinin VS, Lentz BR, (2004) Energetics of vesicle fusion intermediates: comparison of calculations with observed effects of osmotic and curvature stresses. Biophysical Journal 86: 2951-2964 doi:10.1016/S0006-3495(04)74346-5.
9. Chernomordik LV, Kozlov MM, (2008) Mechanics of membrane fusion. Nat Struct Mol Biol 15: 675-683 doi:10.1038/nsmb.1455.
10. 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 6: e1000829 doi:10.1371/journal.pcbi.1000829.
11. Stevens MJM, Hoh JHJ, Woolf TBT, (2003) Insights into the molecular mechanism of membrane fusion from simulation: evidence for the association of splayed tails. Phys Rev Lett 91: 188102-188102 doi:10.1103/PhysRevLett.91.188102.
12. Mirjanian D, Dickey AN, Hoh JH, Woolf TB, Stevens MJ, (2010) Splaying of aliphatic tails plays a central role in barrier crossing during liposome fusion. J Phys Chem B 114: 11061-11068 doi:10.1021/jp1055182.
13. Smirnova YG, Marrink S-J, 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 doi:10.1021/ja910050x.
14. Huang Q, Chen C-L, Herrmann A, (2004) Bilayer conformation of fusion peptide of influenza virus hemagglutinin: a molecular dynamics simulation study. Biophysical Journal 87: 14-22 doi:10.1529/biophysj.103.024562.
15. Haque MEM, Koppaka VV, Axelsen PHP, Lentz BRB, (2005) Properties and structures of the influenza and HIV fusion peptides on lipid membranes: implications for a role in fusion. Biophysical Journal 89: 3183-3194 doi:10.1529/biophysj.105.063032.
16. Wasniewski CM, Parkanzky PD, Bodner ML, Weliky DP, (2004) Solid-state nuclear magnetic resonance studies of HIV and influenza fusion peptide orientations in membrane bilayers using stacked glass plate samples. Chemistry and physics of lipids 132: 89-100 doi:10.1016/j.chemphyslip.2004.09.008.
17. Lorieau JL, Louis JM, Bax A, (2010) The complete influenza hemagglutinin fusion domain adopts a tight helical hairpin arrangement at the lipid:water interface. Proc Natl Acad Sci USA 107: 11341-11346 doi:10.1073/pnas.1006142107.
18. Lorieau JL, Louis JM, Bax A, (2011) Helical hairpin structure of influenza hemagglutinin fusion peptide stabilized by charge-dipole interactions between the N-terminal amino group and the second helix. J Am Chem Soc 133: 2824-2827 doi:10.1021/ja1099775.
19. Jang H, Michaud-Agrawal N, Johnston JM, Woolf TB, (2008) How to lose a kink and gain a helix: pH independent conformational changes of the fusion domains from influenza hemagglutinin in heterogeneous lipid bilayers. Proteins 72: 299-312 doi:10.1002/prot.21925.
20. Sammalkorpi M, Lazaridis T, (2007) Configuration of influenza hemagglutinin fusion peptide monomers and oligomers in membranes. Biochimica et Biophysica Acta (BBA)-Biomembranes 1768: 30-38 doi:10.1016/j.bbamem.2006.08.008.
21. Lagüe P, Roux B, Pastor RW, (2005) Molecular dynamics simulations of the influenza hemagglutinin fusion peptide in micelles and bilayers: conformational analysis of peptide and lipids. J Mol Biol 354: 1129-1141 doi:10.1016/j.jmb.2005.10.038.
22. Vaccaro L, Cross KJ, Kleinjung J, Straus SK, Thomas DJ, et al. (2005) Plasticity of influenza haemagglutinin fusion peptides and their interaction with lipid bilayers. Biophysical Journal 88: 25-36 doi:10.1529/biophysj.104.044537.
23. Légaré S, Lagüe P, (2012) The Influenza Fusion Peptide Adopts a Flexible Flat V Conformation in Membranes. Biophysical J 102: 2270-8 doi:10.1016/j.bpj.2012.04.003.
24. Li Y, Han X, Lai AL, Bushweller JH, Cafiso DS, et al. (2005) Membrane structures of the hemifusion-inducing fusion peptide mutant G1S and the fusion-blocking mutant G1V of influenza virus hemagglutinin suggest a mechanism for pore opening in membrane fusion. J Virol 79: 12065-12076 doi:10.1128/JVI.79.18.12065-12076.2005.
25. Columbus L, Lipfert J, Jambunathan K, Fox DA, Sim AYL, et al. (2009) Mixing and matching detergents for membrane protein NMR structure determination. Journal of the American Chemical Society 131: 7320-7326 doi:10.1021/ja808776j.
26. Lai AL, Moorthy AE, Li Y, Tamm LK, (2012) Fusion activity of HIV gp41 fusion domain is related to its secondary structure and depth of membrane insertion in a cholesterol-dependent fashion. J Mol Biol 418: 3-15 doi:10.1016/j.jmb.2012.02.010.
27. Gonen T, Cheng Y, Sliz P, Hiroaki Y, Fujiyoshi Y, et al. (2005) Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438: 633-638 doi:10.1038/nature04321.
28. Xu ZC, Cafiso DS, (1986) Phospholipid packing and conformation in small vesicles revealed by two-dimensional 1H nuclear magnetic resonance cross-relaxation spectroscopy. Biophysical Journal 49: 779-783 doi:10.1016/S0006-3495(86)83705-5.
29. Huster D, Gawrisch K, (1999) NOESY NMR crosspeaks between lipid headgroups and hydrocarbon chains: Spin diffusion or molecular disorder? J Am Chem Soc 121: 1992-1993 doi:10.1021/ja9838413.
30. Mihailescu M, Vaswani RG, Jardón-Valadez E, Castro-Román F, Freites JA, et al. (2011) Acyl-Chain Methyl Distributions of Liquid-Ordered and-Disordered Membranes. Biophysical Journal 100: 1455-1462 doi:10.1016/j.bpj.2011.01.035.
31. Donald JE, Zhang Y, Fiorin G, Carnevale V, Slochower DR, et al. (2011) Transmembrane orientation and possible role of the fusogenic peptide from parainfluenza virus 5 (PIV5) in promoting fusion. Proc Natl Acad Sci USA 108: 3958-3963 doi:10.1073/pnas.1019668108.
32. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, et al. (2008) The influenza virus resource at the National Center for Biotechnology Information. J Virol 82: 596-601.
33. Kasson PM, Pande VS (2006) Predicting structure and dynamics of loosely-ordered protein complexes: influenza hemagglutinin fusion peptide. In: Proceedings of the Pacific Symposium on Biocomputing. 3-7 January 2007; Maui, Hawaii. pp. 40.
34. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, et al. (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J Comput Chem 24: 1999-2012 doi:10.1002/jcc.10349.
35. Berger O, Edholm O, Jähnig F, (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophysical Journal 72: 2002-2013 doi:10.1016/S0006-3495(97)78845-3.
36. Kasson PM, Lindahl E, Pande VS, (2011) Water ordering at membrane interfaces controls fusion dynamics. J Am Chem Soc 133: 3812-3815 doi:10.1021/ja200310d.
37. Kucerka N, Tristram-Nagle S, Nagle JF, (2005) Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains. J Membr Biol 208: 193-202 doi:10.1007/s00232-005-7006-8.
38. Hess B, Kutzner C, van der Spoel D, Lindahl E, (2008) GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation. Journal of Chemical Theory and Computation 4: 435-447 doi:10.1021/ct700301q.
39. Bussi G, Donadio D, Parrinello M, (2007) Canonical sampling through velocity rescaling. J Chem Phys 126: 014101 doi:10.1063/1.2408420.
40. Hess B, (2008) P-LINCS: A parallel linear constraint solver for molecular simulation. Journal of Chemical Theory and Computation 4: 116-122 doi:10.1021/ct700200b.
41. Darden T, York D, Pedersen L, (1993) Particle mesh Ewald: An N{dot operator}log(N) method for Ewald sums in large systems. J Chem Phys 98: 10089-10092 doi:10.1063/1.464397.
42. Pitera JW, Haque I, Swope WC, (2006) Absence of reptation in the high-temperature folding of the trpzip2 β-hairpin peptide. J Chem Phys 124: 141102-141102-4 doi:10.1063/1.2190226.
43. Swope W, Pitera J, Suits F, (2004) Describing Protein Folding Kinetics by Molecular Dynamics Simulations. 1. Theory†. J Phys Chem B 108: 6571-6581.
44. Shirts M, (2000) COMPUTING: Screen Savers of the World Unite!. Science 290: 1903-1904 doi:10.1126/science.290.5498.1903.
45. Han XX, Bushweller JHJ, Cafiso DSD, Tamm LKL, (2001) Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nat Struct Mol Biol 8: 715-720 doi:10.1038/90434.
46. Mura C, McCrimmon CM, Vertrees J, Sawaya MR, (2010) An Introduction to Biomolecular Graphics. PLoS Comput Biol 6: e1000918.
47. Seelig J, Seelig A, (1980) Lipid conformation in model membranes and biological membranes. Quart Rev Biophys 13: 19-61 doi:10.1017/S0033583500000305.
48. Kasson PM, Hess B, Lindahl E, (2013) Probing microscopic material properties inside simulated membranes through spatially resolved three-dimensional local pressure fields and surface tensions. Chemistry and physics of lipids: Epub ahead of print doi:10.1016/j.chemphyslip.2013.01.001.