Atomistic simulations of pore formation and closure in lipid bilayers

Biophysical Journal

Volumn 106, Issue 1, 2014, Pages 210-219

  Bennett, W F Drew ^a,b   Sapay, Nicolas ^a,c   Tieleman, D Peter ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF WATERLOO   (Canada)

^c BIOASTER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLCHOLINE;

ARTICLE; CHEMISTRY; HYDROGEN BOND; LIPID BILAYER; METABOLISM; MOLECULAR DYNAMICS; THERMODYNAMICS;

HYDROGEN BONDING; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; PHOSPHATIDYLCHOLINES; THERMODYNAMICS;

EID: 84891849262     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.11.4486     Document Type: Article

References (68)

1. R.M. Epand, and H.J. Vogel Diversity of antimicrobial peptides and their mechanisms of action Biochim. Biophys. Acta 1462 1999 11 28
2. L.T. Nguyen, E.F. Haney, and H.J. Vogel The expanding scope of antimicrobial peptide structures and their modes of action Trends Biotechnol. 29 2011 464 472
3. K.A. Brogden Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3 2005 238 250
4. P.T. Vernier, and Y. Sun M.A. Gundersen Nanoelectropulse-induced phosphatidylserine translocation Biophys. J. 86 2004 4040 4048
5. M. Zorko, and U. Langel Cell-penetrating peptides: mechanism and kinetics of cargo delivery Adv. Drug Deliv. Rev. 57 2005 529 545
6. N.B. Last, and A.D. Miranker Common mechanism unites membrane poration by amyloid and antimicrobial peptides Proc. Natl. Acad. Sci. USA 110 2013 6382 6387
7. C.L. Bergstrom, and P.A. Beales J.T. Groves Cytochrome c causes pore formation in cardiolipin-containing membranes Proc. Natl. Acad. Sci. USA 110 2013 6269 6274
8. J.L. MacCallum, W.F.D. Bennett, and D.P. Tieleman Transfer of arginine into lipid bilayers is nonadditive Biophys. J. 101 2011 110 117
9. C.P. Moon, and K.G. Fleming Side-chain hydrophobicity scale derived from transmembrane protein folding into lipid bilayers Proc. Natl. Acad. Sci. USA 108 2011 10174 10177
10. S.H. White, and G. von Heijne How translocons select transmembrane helices Annu. Rev. Biophys 37 2008 23 42
11. G. van Meer, D.R. Voelker, and G.W. Feigenson Membrane lipids: where they are and how they behave Nat. Rev. Mol. Cell Biol. 9 2008 112 124
12. P.T. Vernier, and M.J. Ziegler D.P. Tieleman Nanopore formation and phosphatidylserine externalization in a phospholipid bilayer at high transmembrane potential J. Am. Chem. Soc. 128 2006 6288 6289
13. D.W. Hoskin, and A. Ramamoorthy Studies on anticancer activities of antimicrobial peptides Biochim. Biophys. Acta 1778 2008 357 375
14. N. Sapay, W.F.D. Bennett, and D.P. Tieleman Thermodynamics of flip-flop and desorption for a systematic series of phosphatidylcholine lipids Soft Matter 5 2009 3295 3302
15. R.D. Kornberg, and H.M. McConnell Inside-outside transitions of phospholipids in vesicle membranes Biochemistry 10 1971 1111 1120
16. Y. Toyoshima, and T.E. Thompson Chloride flux in bilayer membranes: chloride permeability in aqueous dispersions of single-walled, bilayer vesicles Biochemistry 14 1975 1525 1531
17. A. Missner, and P. Pohl 110 years of the Meyer-Overton rule: predicting membrane permeability of gases and other small compounds ChemPhysChem 10 2009 1405 1414
18. A.A. Gurtovenko, J. Anwar, and I. Vattulainen Defect-mediated trafficking across cell membranes: insights from in silico modeling Chem. Rev. 110 2010 6077 6103
19. S.J. Marrink, A.H. de Vries, and D.P. Tieleman Lipids on the move: simulations of membrane pores, domains, stalks and curves Biochim. Biophys. Acta 1788 2009 149 168
20. R.A. Böckmann, and B.L. de Groot H. Grubmüller Kinetics, statistics, and energetics of lipid membrane electroporation studied by molecular dynamics simulations Biophys. J. 95 2008 1837 1850
21. D.P. Tieleman, and H. Leontiadou S.J. Marrink Simulation of pore formation in lipid bilayers by mechanical stress and electric fields J. Am. Chem. Soc. 125 2003 6382 6383
22. P.T. Vernier, and M.J. Ziegler D.P. Tieleman Nanopore-facilitated, voltage-driven phosphatidylserine translocation in lipid bilayers - in cells and in silico Phys. Biol. 3 2006 233 247
23. Z.A. Levine, and P.T. Vernier Life cycle of an electropore: field-dependent and field-independent steps in pore creation and annihilation J. Membr. Biol. 236 2010 27 36
24. L. Delemotte, and M. Tarek Molecular dynamics simulations of lipid membrane electroporation J. Membr. Biol. 245 2012 531 543
25. A.A. Gurtovenko, and J. Anwar Ion transport through chemically induced pores in protein-free phospholipid membranes J. Phys. Chem. B 111 2007 13379 13382
26. D.P. Tieleman The molecular basis of electroporation BMC Biochem. 5 2004 10
27. H.D. Herce, and A.E. Garcia Molecular dynamics simulations suggest a mechanism for translocation of the HIV-1 TAT peptide across lipid membranes Proc. Natl. Acad. Sci. USA 104 2007 20805 20810
28. S. Yesylevskyy, S.J. Marrink, and A.E. Mark Alternative mechanisms for the interaction of the cell-penetrating peptides penetratin and the TAT peptide with lipid bilayers Biophys. J. 97 2009 40 49
29. K. Huang, and A.E. García Free energy of translocating an arginine-rich cell-penetrating peptide across a lipid bilayer suggests pore formation Biophys. J. 104 2013 412 420
30. H. Leontiadou, A.E. Mark, and S.J. Marrink Antimicrobial peptides in action J. Am. Chem. Soc. 128 2006 12156 12161
31. H. Leontiadou, A.E. Mark, and S.J. Marrink Molecular dynamics simulations of hydrophilic pores in lipid bilayers Biophys. J. 86 2004 2156 2164
32. J.L. MacCallum, W.F.D. Bennett, and D.P. Tieleman Distribution of amino acids in a lipid bilayer from computer simulations Biophys. J. 94 2008 3393 3404
33. N.J. Gleason, and V.V. Vostrikov R.E. Koeppe 2nd Buried lysine, but not arginine, titrates and alters transmembrane helix tilt Proc. Natl. Acad. Sci. USA 110 2013 1692 1695
34. D. van der Spoel, and E. Lindahl H.J. Berendsen GROMACS: fast, flexible, and free J. Comput. Chem. 26 2005 1701 1718
35. B. Hess, and C. Kutzner E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
36. O. Berger, O. Edholm, and F. Jähnig Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature Biophys. J. 72 1997 2002 2013
37. Berendsen, H. J. C., J. P. M. Postma,., J. Hermans. 1981 Interaction models for water in relation to protein hydration. In Book Interaction Models for Water in Relation to Protein Hydration. B. Pullman, editor. D. Reidel, Dordrecht, The Netherlands.
38. U. Essmann, and L. Perera L.G. Pedersen A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 8593
39. T. Darden, D. York, and L. Pedersen Particle mesh Ewald - an N.Log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
40. H.J.C. Berendsen, and J.P.M. Postma J.R. Haak Molecular dynamics with coupling to an external bath J. Chem. Phys. 81 1984 3684 3690
41. S. Miyamoto, and P.A. Kollman SETTLE - an analytical version of the SHAKE and RATTLE algorithm for rigid water models J. Comput. Chem. 13 1992 952 962
42. B. Hess, and H. Bekker J.G.E.M. Fraaije LINCS: a linear constraint solver for molecular simulations J. Comput. Chem. 18 1997 1463 1472
43. S. Kumar, and D. Bouzida J.M. Rosenberg The weighted histogram analysis method for free-energy calculations on biomolecules. 1. The method J. Comput. Chem. 13 1992 1011 1021
44. W.F.D. Bennett, and D.P. Tieleman Water defect and pore formation in atomistic and coarse-grained lipid membranes: pushing the limits of coarse graining J. Chem. Theory Comput. 7 2011 2981 2988
45. J. Wohlert, and W.K. den Otter W.J. Briels Free energy of a trans-membrane pore calculated from atomistic molecular dynamics simulations J. Chem. Phys. 124 2006 154905
46. D.P. Tieleman, and S.J. Marrink Lipids out of equilibrium: energetics of desorption and pore mediated flip-flop J. Am. Chem. Soc. 128 2006 12462 12467
47. L.B. Li, I. Vorobyov, and T.W. Allen The role of membrane thickness in charged protein-lipid interactions Biochim. Biophys. Acta 1818 2012 135 145
48. A. Debnath, and B. Mukherjee S.-T. Lin Entropy and dynamics of water in hydration layers of a bilayer J. Chem. Phys. 133 2010 174704
49. T.A. Pascal, W.A. Goddard, and Y. Jung Entropy and the driving force for the filling of carbon nanotubes with water Proc. Natl. Acad. Sci. USA 108 2011 11794 11798
50. M.C. Blok, and E.C.M. van der Neut-Kok J. de Gier The effect of chain length and lipid phase transitions on the selective permeability properties of liposomes Biochim. Biophys. Acta 406 1975 187 196
51. S. Paula, and A.G. Volkov D.W. Deamer Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness Biophys. J. 70 1996 339 348
52. J.C. Mathai, and S. Tristram-Nagle M.L. Zeidel Structural determinants of water permeability through the lipid membrane J. Gen. Physiol. 131 2008 69 76
53. C. Neale, and W.F.D. Bennett R. Pomes Statistical convergence of equilibrium properties in simulations of molecular solutes embedded in lipid bilayers J. Chem. Theory Comput. 7 2011 4175 4188
54. J. Liu, and J.C. Conboy 1,2-diacyl-phosphatidylcholine flip-flop measured directly by sum-frequency vibrational spectroscopy Biophys. J. 89 2005 2522 2532
55. W.C. Wimley, and T.E. Thompson Transbilayer and interbilayer phospholipid exchange in dimyristoylphosphatidylcholine/dimyristoylphosphatidylethanolamine large unilamellar vesicles Biochemistry 30 1991 1702 1709
56. M. Nakano, and M. Fukuda T. Handa Flip-flop of phospholipids in vesicles: kinetic analysis with time-resolved small-angle neutron scattering J. Phys. Chem. B 113 2009 6745 6748
57. M.J. Moreno, L.M.B.B. Estronca, and W.L.C. Vaz Translocation of phospholipids and dithionite permeability in liquid-ordered and liquid-disordered membranes Biophys. J. 91 2006 873 881
58. W.F.D. Bennett, J.L. MacCallum, and D.P. Tieleman Thermodynamic analysis of the effect of cholesterol on dipalmitoylphosphatidylcholine lipid membranes J. Am. Chem. Soc. 131 2009 1972 1978
59. W.F.D. Bennett, and J.L. MacCallum D.P. Tieleman Molecular view of cholesterol flip-flop and chemical potential in different membrane environments J. Am. Chem. Soc. 131 2009 12714 12720
60. N. Sapay, W.F.D. Bennett, and D.P. Tieleman Molecular simulations of lipid flip-flop in the presence of model transmembrane helices Biochemistry 49 2010 7665 7673
61. W.C. Wimley, and S.H. White Experimentally determined hydrophobicity scale for proteins at membrane interfaces Nat. Struct. Biol. 3 1996 842 848
62. T. Hessa, and H. Kim G. von Heijne Recognition of transmembrane helices by the endoplasmic reticulum translocon Nature 433 2005 377 381
63. J.L. MacCallum, and D.P. Tieleman Hydrophobicity scales: a thermodynamic looking glass into lipid-protein interactions Trends Biochem. Sci. 36 2011 653 662
64. J. Gumbart, and B. Roux Determination of membrane-insertion free energies by molecular dynamics simulations Biophys. J. 102 2012 795 801
65. S. Dorairaj, and T.W. Allen On the thermodynamic stability of a charged arginine side chain in a transmembrane helix Proc. Natl. Acad. Sci. USA 104 2007 4943 4948
66. A.H. Dewald, J.C. Hodges, and L. Columbus Physical determinants of β-barrel membrane protein folding in lipid vesicles Biophys. J. 100 2011 2131 2140
67. P.D. Rakowska, and H. Jiang M.G. Ryadnov Nanoscale imaging reveals laterally expanding antimicrobial pores in lipid bilayers Proc. Natl. Acad. Sci. USA 110 2013 8918 8923
68. O.A. Andreev, and A.G. Karabadzhak Y.K. Reshetnyak pH (low) insertion peptide (pHLIP) inserts across a lipid bilayer as a helix and exits by a different path Proc. Natl. Acad. Sci. USA 107 2010 4081 4086