Ion-induced defect permeation of lipid membranes

Biophysical Journal

Volumn 106, Issue 3, 2014, Pages 586-597

  Vorobyov, Igor ^d   Olson, Timothy E ^b   Kim, Jung H ^b   Koeppe II, Roger E ^c   Andersen, Olaf S ^b   Allen, Toby W ^a,d  

^a RMIT UNIVERSITY   (Australia)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF ARKANSAS   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE; POTASSIUM; SODIUM;

ARTICLE; CHEMISTRY; ION TRANSPORT; LIPID BILAYER; METABOLISM; MOLECULAR DYNAMICS; PERMEABILITY;

CHLORIDES; ION TRANSPORT; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; PERMEABILITY; POTASSIUM; SODIUM;

EID: 84893484360     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.12.027     Document Type: Article

References (68)

1. D.W. Deamer, and J. Bramhall Permeability of lipid bilayers to water and ionic solutes Chem. Phys. Lipids 40 1986 167 188
2. S. Paula, A.G. Volkov, and D.W. Deamer Permeation of halide anions through phospholipid bilayers occurs by the solubility-diffusion mechanism Biophys. J. 74 1998 319 327
3. 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
4. C.M. Armstrong, and F. Bezanilla Currents related to movement of the gating particles of the sodium channels Nature 242 1973 459 461
5. D. Schmidt, Q.X. Jiang, and R. MacKinnon Phospholipids and the origin of cationic gating charges in voltage sensors Nature 444 2006 775 779
6. K. Melikov, and L.V. Chernomordik Arginine-rich cell penetrating peptides: from endosomal uptake to nuclear delivery Cell. Mol. Life Sci. 62 2005 2739 2749
7. M. Zasloff Antimicrobial peptides of multicellular organisms Nature 415 2002 389 395
8. T. Hessa, and H. Kim G. von Heijne Recognition of transmembrane helices by the endoplasmic reticulum translocon Nature 433 2005 377 381
9. + channel Nature 423 2003 42 48
10. 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
11. H. Hauser, D. Oldani, and M.C. Phillips Mechanism of ion escape from phosphatidylcholine and phosphatidylserine single bilayer vesicles Biochemistry 12 1973 4507 4517
12. R.C. Macdonald Energetics of permeation of thin lipid membranes by ions Biochim. Biophys. Acta 448 1976 193 198
13. D. Papahadjopoulos, S. Nir, and S. Oki Permeability properties of phospholipid membranes: effect of cholesterol and temperature Biochim. Biophys. Acta 266 1972 561 583
14. A.D. Bangham, M.M. Standish, and J.C. Watkins Diffusion of univalent ions across the lamellae of swollen phospholipids J. Mol. Biol. 13 1965 238 252
15. A. Georgallas, and J.D. Macarthur M.Y. Tse The diffusion of small ions through phospholipid bilayers J. Chem. Phys. 86 1987 7218 7226
16. R.W. Glaser, and S.L. Leikin A.I. Sokirko Reversible electrical breakdown of lipid bilayers: formation and evolution of pores Biochim. Biophys. Acta 940 1988 275 287
17. 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
18. A. Parsegian Energy of an ion crossing a low dielectric membrane: solutions to four relevant electrostatic problems Nature 221 1969 844 846
19. M.A. Wilson, and A. Pohorille Mechanism of unassisted ion transport across membrane bilayers J. Am. Chem. Soc. 118 1996 6580 6587
20. H.L. Tepper, and G.A. Voth Mechanisms of passive ion permeation through lipid bilayers: insights from simulations J. Phys. Chem. B 110 2006 21327 21337
21. 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
22. J.L. MacCallum, W.F.D. Bennett, and D.P. Tieleman Partitioning of amino acid side chains into lipid bilayers: results from computer simulations and comparison to experiment J. Gen. Physiol. 129 2007 371 377
23. A.C.V. Johansson, and E. Lindahl The role of lipid composition for insertion and stabilization of amino acids in membranes J. Chem. Phys. 130 2009 185101
24. I.V. Vorobyov, B. Bekker, and T.W. Allen Electrostatics of deformable lipid membranes Biophys. J. 98 2010 2904 2913
25. L.B. Li, I. Vorobyov, and T.W. Allen Potential of mean force and pKa profile calculation for a lipid membrane-exposed arginine side chain J. Phys. Chem. B 112 2008 9574 9587
26. O.S. Andersen, and M. Fuchs Potential energy barriers to ion transport within lipid bilayers. Studies with tetraphenylborate Biophys. J. 15 1975 795 830
27. R.F. Flewelling, and W.L. Hubbell The membrane dipole potential in a total membrane potential model. Applications to hydrophobic ion interactions with membranes Biophys. J. 49 1986 541 552
28. L.G. Wang, P.S. Bose, and F.J. Sigworth Using cryo-EM to measure the dipole potential of a lipid membrane Proc. Natl. Acad. Sci. USA 103 2006 18528 18533
29. L.B.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
30. W. Shinoda, and M. Mikami M. Hato Molecular dynamics study on the effects of chain branching on the physical properties of lipid bilayers: 2. Permeability J. Phys. Chem. B 108 2004 9346 9356
31. S. Tristram-Nagle, and D.J. Kim J.F. Nagle Structure and water permeability of fully hydrated diphytanoylPC Chem. Phys. Lipids 163 2010 630 637
32. B.R. Brooks, and C.L. Brooks 3rd M. Karplus CHARMM: the biomolecular simulation program J. Comput. Chem. 30 2009 1545 1614
33. S.E. Feller, and A.D. MacKerell An improved empirical potential energy function for molecular simulations of phospholipids J. Phys. Chem. B 104 2000 7510 7515
34. W.L. Jorgensen, and J. Chandrasekhar M.L. Klein Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1983 926 935
35. M.M. Sperotto, and O.G. Mouritsen Monte Carlo simulation studies of lipid order parameter profiles near integral membrane proteins Biophys. J. 59 1991 261 270
36. G.M. Torrie, and J.P. Valleau Nonphysical sampling distributions in Monte Carlo free-energy estimation: umbrella sampling J. Comput. Phys. 23 1977 187 199
37. S. Kumar, and J.M. Rosenberg P.A. Kollman The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method J. Comput. Chem. 13 1992 1011 1021
38. G. Hummer Position-dependent diffusion coefficients and free energies from Bayesian analysis of equilibrium and replica molecular dynamics simulations New J. Phys. 7 2005 34
39. S.-J. Marrink, and H.J.C. Berendsen Simulation of water transport through a lipid membrane J. Phys. Chem. 98 1994 4155 4168
40. D. Bemporad, J.W. Essex, and C. Luttmann Permeation of small molecules through a lipid bilayer: a computer simulation study J. Phys. Chem. B 108 2004 4875 4884
41. B. Roux, and M. Karplus Ion transport in a gramicidin-like channel: dynamics and mobility J. Phys. Chem. 95 1991 4856 4868
42. W.R. Redwood, and F.R. Pfeiffer T.E. Thompson Physical properties of bilayer membranes formed from a synthetic saturated phospholipid in n-decane Biochim. Biophys. Acta 233 1971 1 6
43. D.A. MacInnes The Principles of Electrochemistry 1961 Reinhold New York
44. A.L. Hodgkin, and B. Katz The effect of sodium ions on the electrical activity of giant axon of the squid J. Physiol. 108 1949 37 77
45. A. Finkelstein Water Movement through Lipid Bilayers, Pores, and Plasma Membranes: Theory and Reality 1987 Wiley New York
46. A. Walter, and J. Gutknecht Permeability of small nonelectrolytes through lipid bilayer membranes J. Membr. Biol. 90 1986 207 217
47. P. Schatzberg Diffusion of water through hydrocarbon liquids J. Polym. Sci. C Polym. Symp. 10 1965 87 92
48. A.A. Gurtovenko, and I. Vattulainen Effect of NaCl and KCl on phosphatidylcholine and phosphatidylethanolamine lipid membranes: insight from atomic-scale simulations for understanding salt-induced effects in the plasma membrane J. Phys. Chem. B 112 2008 1953 1962
49. L. Li, I. Vorobyov, and T.W. Allen The different interactions of lysine and arginine side chains with lipid membranes J. Phys. Chem. B 117 2013 11906 11920
50. C. Neale, and C. Madill R. Pomès Accelerating convergence in molecular dynamics simulations of solutes in lipid membranes by conducting a random walk along the bilayer normal J. Chem. Theory Comput. 9 2013 3686 3703
51. A. Finkelstein, and A. Cass Permeability and electrical properties of thin lipid membranes J. Gen. Physiol. 52 1968 145 172
52. O.S. Andersen, and A. Finkelstein A. Cass Effect of phloretin on the permeability of thin lipid membranes J. Gen. Physiol. 67 1976 749 771
53. T. Hanai, D.A. Haydon, and J. Taylor The variation of capacitance and conductance of bimolecular lipid membranes with area J. Theor. Biol. 9 1965 433 443
54. 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
55. I. Vorobyov, L.B. Li, and T.W. Allen Assessing atomistic and coarse-grained force fields for protein-lipid interactions: the formidable challenge of an ionizable side chain in a membrane J. Phys. Chem. B 112 2008 9588 9602
56. - ions and their ion-pair through a zwitterionic dimyristoyl phosphatidylcholine lipid bilayer by umbrella integration with harmonic Fourier beads J. Am. Chem. Soc. 131 2009 1706 1716
57. 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
58. 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
59. 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
60. 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
61. N. Kucerka, S. Tristram-Nagle, and J.F. Nagle Closer look at structure of fully hydrated fluid phase DPPC bilayers Biophys. J. 90 2006 L83 L85
62. G. Szabo, G. Eisenman, and S. Ciani The effects of the macrotetralide actin antibiotics on the electrical properties of phospholipid bilayer membranes J. Membr. Biol. 1 1969 346 382
63. R.O. Dror, and R.M. Dirks D.E. Shaw Biomolecular simulation: a computational microscope for molecular biology Annu. Rev. Biophys. 41 2012 429 452
64. J.B. Klauda, and R.M. Venable R.W. Pastor Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types J. Phys. Chem. B 114 2010 7830 7843
65. T.W. Allen, O.S. Andersen, and B. Roux Energetics of ion conduction through the gramicidin channel Proc. Natl. Acad. Sci. USA 101 2004 117 122
66. L.G. Longsworth Temperature dependence of diffusion in aqueous solutions J. Phys. Chem. 58 1954 770 773
67. C.J. Krauss, and J.W.T. Spinks Temperature coefficients for self-diffusion in solution Can. J. Chem. 32 1954 71 78
68. M. Nina, W. Im, and B. Roux Optimized atomic radii for protein continuum electrostatics solvation forces Biophys. Chem. 78 1999 89 96