Counterion-mediated pattern formation in membranes containing anionic lipids

Advances in Colloid and Interface Science

Volumn 208, Issue , 2014, Pages 177-188

  Slochower, David R ^a,b   Wang, Yu Hsiu ^b   Tourdot, Richard W ^c   Radhakrishnan, Ravi ^b,c   Janmey, Paul A ^a,b,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Anionic phospholipids; Divalent counterions; Membrane patterning

Indexed keywords

CELL MEMBRANES; CYTOLOGY; DRUG THERAPY; IONS; LIPID BILAYERS; PH; PHOSPHOLIPIDS; PROTEINS;

ANIONIC PHOSPHOLIPIDS; BIOLOGICAL CONTROLS; DIVALENT COUNTERIONS; ENVIRONMENTAL FACTORS; LATERAL DISTRIBUTIONS; PHOSPHATIDYLINOSITOL; RANDOMLY DISTRIBUTED; TRANS-MEMBRANE PROTEINS;

MEMBRANES;

ANION; ARTIFICIAL MEMBRANE; LIPID BILAYER; MEMBRANE PROTEIN; PHOSPHOLIPID;

ANIMAL; ARTIFICIAL MEMBRANE; BIOLOGICAL MODEL; BIOPHYSICS; CELL MEMBRANE; CHEMISTRY; HUMAN; LIPID BILAYER; METABOLISM; STATIC ELECTRICITY; SURFACE PROPERTY; ULTRASTRUCTURE;

ANIMALS; ANIONS; BIOPHYSICAL PHENOMENA; HUMANS; LIPID BILAYERS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MEMBRANES, ARTIFICIAL; MODELS, BIOLOGICAL; PHOSPHOLIPIDS; STATIC ELECTRICITY; SURFACE PROPERTIES;

EID: 84899951736     PISSN: 00018686     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cis.2014.01.016     Document Type: Review

References (132)

1. 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
2. J.L. Sampaio, M.J. Gerl, C. Klose, C.S. Ejsing, H. Beug, and K. Simons et al. Membrane lipidome of an epithelial cell line Proc Natl Acad Sci U S A 108 2011 1903 1907
3. M.J. Gerl, J.L. Sampaio, S. Urban, L. Kalvodova, J.M. Verbavatz, and B. Binnington et al. Quantitative analysis of the lipidomes of the influenza virus envelope and MDCK cell apical membrane J Cell Biol 196 2012 213 221
4. J.E. Cronan Bacterial membrane lipids: where do we stand? Annu Rev Microbiol 57 2003 203 224
5. A.J.M. Verhoeven, O.-B. Tysnes, G.M. Aarbakke, C.A. Cook, and H. Holmsen Turnover of the phosphomonoester groups of polyphospoinositol lipids in unstimulated human platelets Eur J Biochem 166 1987 3 9
6. P.A. Janmey, and P.K. Kinnunen Biophysical properties of lipids and dynamic membranes Trends Cell Biol 16 2006 538 546
7. J. Liu, and J.C. Conboy Direct measurement of the transbilayer movement of phospholipids by sum-frequency vibrational spectroscopy J Am Chem Soc 126 2004 8376 8377
8. E.M. Bruckheimer, and A.J. Schroit Membrane phospholipid asymmetry: host response to the externalization of phosphatidylserine J Leukoc Biol 59 1996 784 788
9. S.E. Horvath, and G. Gaum Lipids of the mitochondria Prog Lipid Res 52 2013 590 614
10. M. Numata, Y. Nagashima, M.L. Moore, K.Z. Berry, M. Chan, and P. Kandasamy et al. Phosphatidylglycerol provides short-term prophylaxis against respiratory syncytial virus infection J Lipid Res 54 2013 2133 2143
11. J.L. Harwood Plant lipid biosynthesis: fundamentals and agricultural applications 1998 Cambridge University Press
12. H. Tsuchiya, T. Ueno, M. Mizogami, and K. Takakura Local anesthetics structure-dependently interact with anionic phospholipid membranes to modify the fluidity Chem Biol Interact 183 2010 19 24
13. K. Matsumoto, J. Kusaka, A. Nishibori, and H. Hara Lipid domains in bacterial membranes Mol Microbiol 61 2006 1110 1117
14. R.M. Epand Lipid polymorphism and protein-lipid interactions Biochim Biophys Acta 1376 1998 353 368
15. S. McLaughlin The electrostatic properties of membranes Annu Rev Biophys Biophys Chem 18 1989 113 136
16. S. McLaughlin, N. Mulrine, T. Gresalfi, G. Vaio, and A. McLaughlin Adsorption of divalent cations to bilayer membranes containing phosphatidylserine J Gen Physiol 77 1981 445 473
17. Y.-H. Wang, A. Collins, L. Guo, K.B. Smith-Dupont, F. Gai, and T. Svitkina et al. Divalent cation-induced cluster formation by polyphosphoinositides in model membranes J Am Chem Soc 134 2012 3387 3395
18. V.L. Shapovalov, M.E. Ryskin, O.V. Konovalov, A. Hermelink, and G. Brezesinski Elemental analysis within the electrical double layer using total reflection X-ray fluorescence technique J Phys Chem B 111 2007 3927 3934
19. V.L. Shapovalov, and G. Brezesinski Breakdown of the Gouy-Chapman model for highly charged Langmuir monolayers: counterion size effect J Phys Chem B 110 2006 10032 10040
20. D.M. Haverstick, and M. Glaser Visualization of Ca2 +-induced phospholipid domains Proc Natl Acad Sci U S A 84 1987 4475 4479
21. A. Honigmann, G. van den Bogaart, E. Iraheta, H.J. Risselada, D. Milovanovic, and V. Mueller et al. Phosphatidylinositol 4,5-bisphosphate clusters act as molecular beacons for vesicle recruitment Nat Struct Mol Biol 20 2013 679
22. G. van den Bogaart, K. Meyenberg, H.J. Risselada, H. Amin, K.I. Willig, and B.E. Hubrich et al. Membrane protein sequestering by ionic protein-lipid interactions Nature 479 2011 552 555
23. J.J. Sieber, K.I. Willig, C. Kutzner, C. Gerding-Reimers, B. Harke, and G. Donnert et al. Anatomy and dynamics of a supramolecular membrane protein cluster Science 317 2007 1072 1076
24. W.J. Wang, N.A. Anderson, A. Travesset, and D. Vaknin Regulation of the electric charge in phosphatidic acid domains J Phys Chem B 116 2012 7213 7220
25. T.M. Khuong, R.L.P. Habets, S. Kuenen, A. Witkowska, J. Kasprowicz, and J. Swerts et al. Synaptic PI(3,4,5)P-3 is required for syntaxin1A clustering and neurotransmitter release Neuron 77 2013 1097 1108
26. M. Menke, V. Gerke, and C. Steinem Phosphatidylserine membrane domain clustering induced by annexin A2/S100A10 heterotetramer Biochemistry 44 2005 15296 15303
27. I. Levental, A. Cebers, and P.A. Janmey Combined electrostatics and hydrogen bonding determine intermolecular interactions between polyphosphoinositides J Am Chem Soc 130 2008 9025 9030
28. D.A. Redfern, and A. Gericke Domain formation in phosphatidylinositol monophosphate/phosphatidylcholine mixed vesicles Biophys J 86 2004 2980 2992
29. D.A. Redfern, and A. Gericke pH-dependent domain formation in phosphatidylinositol polyphosphate/phosphatidylcholine mixed vesicles J Lipid Res 46 2005 504 515
30. F. Fernandes, L.M.S. Loura, A. Fedorov, and M. Prieto Absence of clustering of phosphatidylinositol-(4,5)-bisphosphate in fluid phosphatidylcholine J Lipid Res 47 2006 1521 1525
31. S.K. Ghosh, S. Aeffner, and T. Salditt Effect of PIP2 on bilayer structure and phase behavior of DOPC: an X-ray scattering study ChemPhyschem 12 2011 2633 2640
32. D. Chapman, J. Urbina, and K. Keough Biomembrane phase transitions: studies of lipid-water systems using differential scanning J Biol Chem 249 1974 2512 2521
33. T. Ito, S. Ohnishi, M. Ishinaga, and M. Kito Synthesis of a new phosphatidylserine spin-label and calcium-induced lateral phase separation in phosphatidylserine-phosphatidylcholine membranes Biochemistry 14 1975 3064 3069
34. L.A. Flanagan, C.C. Cunningham, J. Chen, G.D. Prestwich, K.S. Kosik, and Pa Janmey The structure of divalent cation-induced aggregates of PIP2 and their alteration by gelsolin and tau Biophys J 73 1997 1440 1447
35. J. Kielland Individual activity coefficients of ions in aqueous solutions J Am Chem Soc 59 1937 1675 1678
36. A.G. Volkov, S. Paula, and D.W. Deamer Two mechanisms of permeation of small neutral molecules and hydrated ions across phospholipid bilayers Bioelectrochem Bioenerg 42 1997 153 160
37. M. Hirai, T. Takizawa, S. Yabuki, Y. Nakata, T. Hirai, and K. Hayashi Salt-dependent phase behaviour of phosphatidylinositol 4,5-diphosphate-wter system J Chem Soc Faraday Trans 92 1996 1493 1498
38. J.A. Braunger, C. Kramer, D. Morick, and C. Steinem Solid supported membranes doped with PIP2: influence of ionic strength and pH on bilayer formation and membrane organization Langmuir 29 2013 14204 14213
39. S. Ohnishi, and T. Ito Clustering of lecithin molecules in phosphatidylserine membranes induced by calcium-ion binding to phosphatidylserine Biochem Biophys Res Commun 51 1973 132 138
40. S. Ohnishi, and T. Ito Calcium-induced phase separations in phosphatidylserine-phosphatidylcholine membranes Biochemistry 13 1974 881 887
41. K. Carvalho, L. Ramos, C. Roy, and C. Picart Giant unilamellar vesicles containing phosphatidylinositol (4,5)bisphosphate: characterization and functionality Biophys J 95 2008 4348 4360
42. I.L. Salvemini, D.M. Gau, J. Reid, L.A. Bagatolli, A. Macmillan, and P.D. Moens Low PIP2 molar fractions induce nanometer size clustering in giant unilamellar vesicles Chem Phys Lipids 177 2014 51 63
43. I. Levental, D.A. Christian, Y.-H. Wang, J.J. Madara, D.E. Discher, and P.A. Janmey Calcium-dependent lateral organization in phosphatidylinositol 4,5-bisphosphate (PIP2)- and cholesterol-containing monolayers Biochemistry 48 2009 8241 8248
44. W.G. Ellenbroek, Y.H. Wang, D.A. Christian, D.E. Discher, P.A. Janmey, and A.J. Liu Divalent cation-dependent formation of electrostatic PIP2 clusters in lipid monolayers Biophys J 101 2011 2178 2184
45. M.Y. Kiriukhin, and K.D. Collins Dynamic hydration numbers for biologically important ions Biophysical chemistry. 99 2002 155 168
46. T. Takizawa, K. Hayashi, S. Yabuki, and Y. Nakata Microcalorimetric studies of Ca2 +-binding to triphosphoinositide and phosphatidylserine Thermochem Acta 123 1988 247 253
47. T. Takizawa, K. Hayashi, and H. Mitomo Differential scanning calorimetry of the triphosphoinositide water-system Thermochem Acta 183 1991 313 321
48. D.R. Slochower, P.J. Huwe, R. Radhakrishnan, and P.A. Janmey Quantum and all-atom molecular dynamics simulations of protonation and divalent ion binding to phosphatidylinositol 4,5-bisphosphate (PIP2) J Phys Chem B 117 2013 8322 8329
49. M. Lösche, and H. Möhwald Electrostatic interactions in phospholipid membranes: II. Influence of divalent ions on monolayer structure J Colloid Interface Sci 131 1989 56 67
50. G.S. Patil, N.J. Dorman, and D.G. Cornwell Effects of ionization and counterion binding on the surface areas of phosphatidic acids in monolayers J Lipid Res 20 1979 663 668
51. J. Faraudo, and A. Travesset Phosphatidic acid domains in membranes: effect of divalent counterions Biophys J 92 2007 2806 2818
52. I. Levental, P.A. Janmey, and A. Cěbers Electrostatic contribution to the surface pressure of charged monolayers containing polyphosphoinositides Biophys J 95 2008 1199 1205
53. E.E. Kooijman, D.P. Tieleman, C. Testerink, T. Munnik, D.T.S. Rijkers, and K.N.J. Burger et al. An electrostatic/hydrogen bond switch as the basis for the specific interaction of phosphatidic acid with proteins J Biol Chem 282 2007 11356 11364
54. E.E. Kooijman, K.E. King, M. Gangoda, and A. Gericke Ionization properties of phosphatidylinositol polyphosphates in mixed model membranes Biochemistry 48 2009 9360 9371
55. T. Ito, and S. Onishi Ca2 +-induced lateral phase separations in phosphatidic acid-phosphatidylcholine membranes Biochim Biophys Acta 352 1974 29 37
56. B.P. Young, J.J. Shin, R. Orij, J.T. Chao, S.C. Li, and X.L. Guan et al. Phosphatidic acid is a pH biosensor that links membrane biogenesis to metabolism Science 329 2010 1085 1088
57. J.J. Shin, and C.J. Loewen Putting the pH into phosphatidic acid signaling BMC Biol 9 2011 85
58. L. Chung, G. Kaloyanides, R. McDaniel, A. McLaughlin, and S. McLaughlin Interaction of gentamicin and spermine with bilayer membranes containing negatively charged phospholipids Biochemistry 24 1985 442 452
59. R.F. Coburn, D.H. Jones, C.P. Morgan, C.B. Baron, and S. Cockcroft Spermine increases phosphatidylinositol 4,5-bisphosphate content in permeabilized and nonpermeabilized HL60 cells Biochim Biophys Acta 1584 2002 20 30
60. R.F. Coburn, E.F. Labelle, and C.B. Baron Polyamines, PI(4,5)P2, and actin polymerization J Cell Physiol 209 2006 405 412
61. P. Meers, K. Hong, J. Bentz, and D. Papahadjopoulos Spermine as a modulator of membrane fusion: interactions with acidic phospholipids Biochemistry 25 1986 3109 3118
62. J.C. Sulpice, C. Moreau, P.F. Devaux, A. Zachowski, and F. Giraud Antagonist effects of Ca2 + and spermine on phosphatidylinositol 4,5-bisphosphate-mediated transmembrane redistribution of phospholipids in large unilamellar vesicles and in erythrocytes Biochemistry 35 1996 13345 13352
63. B. Tadolini, and E. Varani Interaction of spermine with polyphosphoinositides containing liposomes and myo-inositol 1,4,5 triphosphate Biochem Biophys Res Commun 135 1986 58 64
64. M. Toner, G. Vaio, A. McLaughlin, and S. McLaughlin Adsorption of cations to phosphatidylinositol 4,5-bisphosphate Biochemistry 27 1988 7435 7443
65. F. Schuber Influence of polyamines Biochem J 260 1989 1 10
66. H. Hauser, M.C. Phillips, and M.D. Barratt Differences in the interaction of inorganic and organic (hydrophobic) cations with phosphatidylserine membranes Biochim Biophys Acta 413 1975 341 353
67. N.A. Halim, Z.A. Ibrahim, and A.B. Ahmad Intercalation of water and guest molecules within Ca2 +-montmorillonite J Therm Anal Calorim 102 2010 983 988
68. J.C. Sulpice, A. Zachowski, P.F. Devaux, and F. Giraud Requirement for phosphatidylinositol 4,5-bisphosphate in the Ca2 +-induced phospholipid redistribution in the human erythrocyte-membrane J Biol Chem 269 1994 6347 6354
69. S.K. Ballas, N. Mohandas, L.J. Marton, and S.B. Shohet Stabilization of erythrocyte membranes by polyamines Proc Natl Acad Sci U S A 80 1983 1942 1946
70. J. Mager The stabilizing effect of spermine and related polyamines and bacterial protoplasts Biochim Biophys Acta 36 1959 529 531
71. K. Hong, F. Schuber, and D. Papahadjopoulos Polyamines. Biological modulators of membrane fusion Biochim Biophys Acta 732 1983 469 472
72. F. Schuber, K.L. Hong, N. Duzgunes, and D. Papahadjopoulos Polyamines as modulators of membrane-fusion - aggregation and fusion of liposomes Biochemistry 22 1983 6134 6140
73. B.M. Discher, Y.Y. Won, D.S. Ege, J.C.M. Lee, F.S. Bates, and D.E. Discher et al. Polymersomes: tough vesicles made from diblock copolymers Science 284 1999 1143 1146
74. M. Regenbrecht, S. Akari, S. Forster, and H. Mohwald Shape investigations of charged block copolymer micelles on chemically different surfaces by atomic force microscopy J Phys Chem B 103 1999 6669 6675
75. H. Shen, and A. Eisenberg Control of architecture in block-copolymer vesicles. We thank the Petroleum Research Fund, administered by the American Chemical Society, for the support of this work Angew Chem 39 2000 3310 3312
76. D.A. Christian, A. Tian, W.G. Ellenbroek, I. Levental, K. Rajagopal, and P.A. Janmey et al. Spotted vesicles, striped micelles and Janus assemblies induced by ligand binding Nat Mater 8 2009 843 849
77. K. Spinler, A. Tian, D.A. Christian, D.A. Pantano, T. Baumgart, and D.E. Discher Dynamic domains in polymersomes: mixtures of polyanionic and neutral diblocks respond more rapidly to changes in calcium than to pH Langmuir 29 2013 7499 7508
78. R. Bucki, P.A. Janmey, R. Vegners, F. Giraud, and J.-C. Sulpice Involvement of phosphatidylinositol 4,5-bisphosphate in phosphatidylserine exposure in platelets: use of a permeant phosphoinositide-binding peptide Biochemistry 40 2001 15752 15761
79. C. Czaplewski, M. Pasenkiewicz-Gierula, and J. Ciarkowski Molecular dynamics of a vasopressin V2 receptor in a phospholipid bilayer membrane J Recept Signal Transduct Res 19 1999 355 367
80. I. Liepina, C. Czaplewski, P. Janmey, and A. Liwo Molecular dynamics study of a gelsolin-derived peptide binding to a lipid bilayer containing phosphatidylinositol 4,5-bisphosphate Biopolymers 71 2003 49 70
81. C.D. Lorenz, J. Faraudo, and A. Travesset Hydrogen bonding and binding of polybasic residues with negatively charged mixed lipid monolayers Langmuir 24 2008 1654 1658
82. L.G. Cuello, V. Jogini, D.M. Cortes, and E. Perozo Structural mechanism of C-type inactivation in K(+) channels Nature 466 2010 203 208
83. P.J. Stansfeld, R. Hopkinson, F.M. Ashcroft, and M.S. Sansom PIP(2)-binding site in Kir channels: definition by multiscale biomolecular simulations Biochemistry 48 2009 10926 10933
84. D.K. Singh, A. Rosenhouse-Dantsker, C.G. Nichols, D. Enkvetchakul, and I. Levitan Direct regulation of prokaryotic Kir channel by cholesterol J Biol Chem 284 2009 30727 30736
85. O.G. Travkova, J. Andra, H. Mohwald, and G. Brezesinski Influence of arenicin on phase transitions and ordering of lipids in 2D model membranes Langmuir 29 2013 12203 12211
86. C.W. Bock, A. Kaufman, and J.P. Glusker Coordination of water to magnesium cations Inorg Chem 33 1994 419 427
87. T. Lazaridis Implicit solvent simulations of peptide interactions with anionic lipid membranes Proteins 58 2005 518 527
88. R.M. Peitzsch, M. Eisenberg, K.A. Sharp, and S. McLaughlin Calculations of the electrostatic potential adjacent to model phospholipid bilayers Biophys J 68 1995 729 738
89. J.E. Baenziger, M.-L. Morris, T.E. Darsaut, and S.E. Ryan Effect of membrane lipid composition on the conformational equilibria of the nicotinic acetylcholine receptor J Biol Chem 275 2000 777 784
90. R.M. Epand, and S.-W. Hui Effect of electrostatic repulsion on the morphology and thermotropic transitions of anionic phospholipids FEBS Lett 209 1986 257 260
91. S. McLaughlin, J. Wang, A. Gambhir, and D. Murray PIP(2) and proteins: interactions, organization, and information flow Annu Rev Biophys Biomol Struct 31 2002 151 175
92. M.G. Ford, I.G. Mills, B.J. Peter, Y. Vallis, G.J. Praefcke, and P.R. Evans et al. Curvature of clathrin-coated pits driven by epsin Nature 419 2002 361 366
93. C.-L. Lai, C.C. Jao, E. Lyman, J.L. Gallop, B.J. Peter, and H.T. McMahon et al. Membrane binding and self-association of the epsin N-terminal homology domain J Mol Biol 423 2012 800 817
94. J. Zimmerberg, and S. McLaughlin Membrane curvature: how BAR domains bend bilayers Curr Biol 14 2004 R250 R252
95. H. Cui, G.S. Ayton, and G.A. Voth Membrane binding by the endophilin N-BAR domain Biophys J 97 2009 2746 2753
96. A. Arkhipov, Y. Yin, and K. Schulten Membrane-bending mechanism of amphiphysin N-BAR domains Biophys J 97 2009 2727 2735
97. A. Gambhir, G. Hangyas-Mihalyne, I. Zaitseva, D.S. Cafiso, J. Wang, and D. Murray et al. Electrostatic sequestration of PIP2 on phospholipid membranes by basic/aromatic regions of proteins Biophys J 86 2004 2188 2207
98. L.A. Morton, H. Yang, J.P. Saludes, Z. Fiorini, L. Beninson, and E.R. Chapman et al. MARCKS-ED peptide as a curvature and lipid sensor ACS Chem Biol 8 2012 218 225
99. R. Bucki, and P.A. Janmey Interaction of the gelsolin-derived antibacterial PBP 10 peptide with lipid bilayers and cell membranes Antimicrob Agents Chemother 50 2006 2932 2940
100. W. Bu, K. Flores, J. Pleasants, and D. Vaknin Preferential affinity of calcium ions to charged phosphatidic acid surface from a mixed calcium/barium solution: X-ray reflectivity and fluorescence studies Langmuir 25 2009 1068 1073
101. K. Jacobson, and D. Papahadjopoulos Phase transitions and phase separations in phospholipid membranes induced by changes in temperature, pH, and concentration of bivalent cations Biochemistry 14 1975 152 161
102. H. Trauble, and H. Eibl Electrostatic effects on lipid phase transitions: membrane structure and ionic environment Proc Natl Acad Sci U S A 71 1974 214 219
103. D. Papahadjopoulos, W.J. Vail, W.A. Pangborn, and G. Poste Studies on membrane fusion. II. Induction of fusion in pure phospholipid membranes by calcium ions and other divalent metals Biochim Biophys Acta 448 1976 265 283
104. A.J. Verkleij, R. Demaagd, J. Leunissenbijvelt, and B. Dekruijff Divalent-cations and chlorpromazine can induce non-bilayer structures in phosphatidic acid-containing model membranes Biochim Biophys Acta 684 1982 255 262
105. E.E. Kooijman, K.M. Carter, E.G. van Laar, V. Chupin, K.N. Burger, and B. de Kruijff What makes the bioactive lipids phosphatidic acid and lysophosphatidic acid so special? Biochemistry 44 2005 17007 17015
106. C. Testerink, and T. Munnik Phosphatidic acid: a multifunctional stress signaling lipid in plants Trends Plant Sci 10 2005 368 375
107. G. Tigyi, and A.L. Parrill Molecular mechanisms of lysophosphatidic acid action Prog Lipid Res 42 2003 498 526
108. H.T. McMahon, and J.L. Gallop Membrane curvature and mechanisms of dynamic cell membrane remodelling Nature 438 2005 590 596
109. M.C. Watson, E.S. Penev, P.M. Welch, and F.L.H. Brown Thermal fluctuations in shape, thickness, and molecular orientation in lipid bilayers J Chem Phys 135 2011 244701
110. H.J. Deuling, and W. Helfrich Red blood cell shapes as explained on the basis of curvature elasticity Biophys J 16 1976 861 868
111. W. Helfrich Elastic properties of lipid bilayers: theory and possible experiments Z Naturforsch C 28 1973 693 703
112. J. Song, and R.E. Waugh Bending rigidity of SOPC membranes containing cholesterol Biophys J 64 1993 1967 1970
113. S.A. Safran Saddle-splay modulus and the stability of spherical microemulsions Phys Rev A 43 1991 2903 2904
114. Y. Kozlovsky, A. Efrat, D.P. Siegel, and M.M. Kozlov Stalk phase formation: effects of dehydration and saddle splay modulus Biophys J 87 2004 2508 2521
115. M. Hu, J.J. Briguglio, and M. Deserno Determining the Gaussian curvature modulus of lipid membranes in simulations Biophys J 102 2012 1403 1410
116. T. Baumgart, S. Das, W.W. Webb, and J.T. Jenkins Membrane elasticity in giant vesicles with fluid phase coexistence Biophys J 89 2005 1067 1080
117. S. Semrau, T. Idema, L. Holtzer, T. Schmidt, and C. Storm Accurate determination of elastic parameters for multicomponent membranes Phys Rev Lett 100 2008 088101
118. M. Winterhalter, and W. Helfrich Effect of surface charge on the curvature elasticity of membranes J Phys Chem 92 1988 6865 6867
119. V. Vitkova, J. Genova, O. Finogenova, M.D. Mitov, Y.A. Ermakov, and I. Bivas Surface charge effect on the bending elasticity of lipid bilayers C R Acad Bulg Sci 57 2004 11 25
120. H.T. McMahon, and E. Boucrot Molecular mechanism and physiological functions of clathrin-mediated endocytosis Nature reviews Molecular cell biology. 12 2011 517 533
121. J. Liu, Y. Sun, D.G. Drubin, and G.F. Oster The mechanochemistry of endocytosis PLoS Biol 7 2009 e1000204
122. N.J. Agrawal, J. Nukpezah, and R. Radhakrishnan Minimal mesoscale model for protein-mediated vesiculation in clathrin-dependent endocytosis PLoS Comput Biol 6 2010 e1000926
123. Y. Zhao, J. Liu, C. Yang, B.R. Capraro, T. Baumgart, and R.P. Bradley et al. Exo70 generates membrane curvature for morphogenesis and cell migration Dev Cell 26 2013 266 278
124. S. McLaughlin Electrostatic potentials and membrane-solution interfaces F. Bronner, A. Kleinzeller, Curent topics in membranes & transport 1977 Academic Press
125. B.H. Honig, W.L. Hubbell, and R.F. Flewelling Electrostatic interactions in membranes and proteins Annu Rev Biophys Biophys Chem 15 1986 163 193
126. C.A. Helm, L. Laxhuber, M. Lösche, and H. Möhwald Electrostatic interactions in phospholipid-membranes: I Influence of mono-valent ions Collied Polym Sci 264 1986 46 55
127. A. Martin-Molina, C. Rodriguez-Beas, and J. Faraudo Effect of calcium and magnesium on phosphatidylserine membranes: experiments and all-atomic simulations Biophys J 102 2012 2095 2103
128. N. Ben-Tal, B. Honig, R.M. Peitzsch, G. Denisov, and S. McLaughlin Binding of small basic peptides to membranes containing acidic lipids: theoretical models and experimental results Biophys J 71 1996 561 575
129. G. Denisov, S. Wanaski, P. Luan, M. Glaser, and S. McLaughlin Binding of basic peptides to membranes produces lateral domains enriched in the acidic lipids phosphatidylserine and phosphatidylinositol 4,5-bisphosphate: an electrostatic model and experimental results Biophys J 74 1998 731 744
130. P.T. Vernier, M.J. Ziegler, and R. Dimova Calcium binding and head group dipole angle in phosphatidylserine-phosphatidylcholine bilayers Langmuir 25 2009 1020 1027
131. M.A. Lemmon Pleckstrin homology (PH) domains and phosphoinositides Biochem Soc Symp 74 2007 81 93
132. E. Psachoulia, and M.S. Sansom Interactions of the pleckstrin homology domain with phosphatidylinositol phosphate and membranes: characterization via molecular dynamics simulations Biochemistry 47 2008 4211 4220