Dynamics and instabilities of lipid bilayer membrane shapes

Advances in Colloid and Interface Science

Volumn 208, Issue , 2014, Pages 76-88

  Shi, Zheng ^a   Baumgart, Tobias ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Curvature instability; Interleaflet friction; Membrane fluctuation; Membrane shape transition; Membrane tension; Protein density

Indexed keywords

CELL MEMBRANES; CYTOLOGY; DYNAMICS; LIPID BILAYERS; PROTEINS; STABILITY;

CELLULAR MEMBRANES; INSTABILITY CRITERION; LIPID BILAYER MEMBRANES; MEMBRANE FLUCTUATIONS; MEMBRANE MORPHOLOGY; MEMBRANE TENSION; PROTEIN DENSITY; SHAPE TRANSITIONS;

MEMBRANES;

LIPID BILAYER; MEMBRANE PROTEIN;

ALGORITHM; ANIMAL; ANISOTROPY; BIOLOGICAL MODEL; BIOPHYSICS; CELL MEMBRANE; CELL SHAPE; CHEMISTRY; HUMAN; INTRACELLULAR MEMBRANE; LIPID BILAYER; METABOLISM; ORGANELLE SHAPE;

ALGORITHMS; ANIMALS; ANISOTROPY; BIOPHYSICAL PHENOMENA; CELL MEMBRANE; CELL SHAPE; HUMANS; INTRACELLULAR MEMBRANES; LIPID BILAYERS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; ORGANELLE SHAPE;

EID: 84899993800     PISSN: 00018686     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cis.2014.01.004     Document Type: Review

References (159)

1. J.S. Bonifacino, and B.S. Glick The mechanisms of vesicle budding and fusion Cell 116 2004 153 166
2. R. Lipowsky The conformation of membranes Nature 349 1991 475 481
3. H.T. McMahon, and J.L. Gallop Membrane curvature and mechanisms of dynamic cell membrane remodelling Nature 438 2005 590 596
4. Y. Shibata, J.J. Hu, M.M. Kozlov, and T.A. Rapoport Mechanisms shaping the membranes of cellular organelles Annu Rev Cell Dev Biol 25 2009 329 354
5. A.F. Bitbol, J.B. Fournier, M.I. Angelova, and N. Puff Dynamical membrane curvature instability controlled by intermonolayer friction J Phys Condens Matter 23 2011
6. B.J. Reynwar, G. Illya, V.A. Harmandaris, M.M. Muller, K. Kremer, and M. Deserno Aggregation and vesiculation of membrane proteins by curvature-mediated interactions Nature 447 2007 461 464
7. H.T. McMahon, and E. Boucrot Molecular mechanism and physiological functions of clathrin-mediated endocytosis Nat Rev Mol Cell Biol 12 2011 517 533
8. J.B. Fournier, N. Khalifat, N. Puff, and M.I. Angelova Chemically triggered ejection of membrane tubules controlled by intermonolayer friction Phys Rev Lett 102 2009
9. N. Sciaky, J. Presley, C. Smith, K.J.M. Zaal, N. Cole, and J.E. Moreira et al. Golgi tubule traffic and the effects of Brefeldin A visualized in living cells J Cell Biol 139 1997 1137 1155
10. C.A. Mannella, D.R. Pfeiffer, P.C. Bradshaw, I.I. Moraru, B. Slepchenko, and L.M. Loew et al. Topology of the mitochondrial inner membrane: dynamics and bioenergetic implications IUBMB Life 52 2001 93 100
11. C. Lee, and L.B. Chen Dynamic behavior of endoplasmic-reticulum in living cells Cell 54 1988 37 46
12. S.J. Singer, and G.L. Nicolson Fluid mosaic model of structure of cell-membranes Science 175 1972 720
13. P.B. Canham Minimum energy of bending as a possible explanation of biconcave shape of human red blood cell J Theor Biol 26 1970 61
14. W. Helfrich Elastic properties of lipid bilayers - theory and possible experiments Z Naturforsch C 28 1973 693 703
15. E.A. Evans Bending resistance and chemically-induced moments in membrane bilayers Biophys J 14 1974 923 931
16. H.J. Deuling, and W. Helfrich Red blood-cell shapes as explained on basis of curvature elasticity Biophys J 16 1976 861 868
17. H.J. Deuling, and W. Helfrich Curvature elasticity of fluid membranes - catalog of vesicle shapes J Phys 37 1976 1335 1345
18. L. Miao, U. Seifert, M. Wortis, and H.G. Dobereiner Budding transitions of fluid-bilayer vesicles - the effect of area-difference elasticity Phys Rev E 49 1994 5389 5407
19. U. Seifert Configurations of fluid membranes and vesicles Adv Phys 46 1997 13 137
20. F. Brochard, and J.F. Lennon Frequency spectrum of flicker phenomenon in erythrocytes J Phys 36 1975 1035 1047
21. U. Seifert, and S.A. Langer Viscous modes of fluid bilayer-membranes Europhys Lett 23 1993 71 76
22. O. Rossier, D. Cuvelier, N. Borghi, P.H. Puech, I. Derenyi, and A. Buguin et al. Giant vesicles under flows: extrusion and retraction of tubes Langmuir 19 2003 575 584
23. M. Peltomäki, and G. Gompper Sedimentation of single red blood cells Soft Matter 9 2013 8346 8358
24. P. Cowin, and B. Burke Cytoskeleton-membrane interactions Curr Opin Cell Biol 8 1996 56 65
25. M. Lenz, D.J.G. Crow, and J.F. Joanny Membrane buckling induced by curved filaments Phys Rev Lett 103 2009
26. B. Maugis, J. Brugues, P. Nassoy, N. Guillen, P. Sens, and F. Amblard Dynamic instability of the intracellular pressure drives bleb-based motility J Cell Sci 123 2010 3884 3892
27. P. Friedl, and K. Wolf Tumour-cell invasion and migration: diversity and escape mechanisms Nat Rev Cancer 3 2003 362 374
28. F.Y. Lim, K.H. Chiam, and L. Mahadevan The size, shape, and dynamics of cellular blebs Europhys Lett 100 2012
29. N.L. Gershfeld, and M. Murayama Thermal-instability of Red blood-cell membrane bilayers - temperature-dependence of hemolysis J Membr Biol 101 1988 67 72
30. S. Eskelinen Hemolysis of erythrocytes as a model for membrane instability and rupture J Biol Phys 15 1987 22 25
31. L. Ginsberg, J.R. Atack, S.I. Rapoport, and N.L. Gershfeld Regional specificity of membrane instability in Alzheimers-disease brain Brain Res 615 1993 355 357
32. L. Ginsberg, J.H. Xuereb, and N.L. Gershfeld Membrane instability, plasmalogen content, and Alzheimer's disease J Neurochem 70 1998 2533 2538
33. Emily M. Hatch, Andrew H. Fischer, Thomas J. Deerinck, and Martin W. Hetzer Catastrophic nuclear envelope collapse in cancer cell micronuclei Cell 154 2013 47 60
34. S. Leibler Curvature instability in membranes J Phys 47 1986 507 516
35. D.A. Edwards, K.J. Gooch, I. Zhang, G.H. McKinley, and R. Langer The nucleation of receptor-mediated endocytosis Proc Natl Acad Sci U S A 93 1996 1786 1791
36. H.H. Low, C. Sachse, L.A. Amos, and J. Lowe Structure of a bacterial dynamin-like protein lipid tube provides a mechanism for assembly and membrane curving Cell 139 2009 1342 1352
37. S. Sigismund, S. Confalonieri, A. Ciliberto, S. Polo, G. Scita, and P.P. Di Fiore Endocytosis and signaling: cell logistics shape the eukaryotic cell plan Physiol Rev 92 2012 273 366
38. T. Baumgart, B.R. Capraro, C. Zhu, and S.L. Das Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids S.R. Leone, P.S. Cremer, J.T. Groves, M.A. Johnson, Annual Review of Physical Chemistry vol. 62 2011 483 506
39. M.J. Taylor, D. Perrais, and C.J. Merrifield A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis PLoS Biol 9 2011
40. A. Zilker, H. Engelhardt, and E. Sackmann Dynamic reflection interference contrast (ric-) microscopy - a new method to study surface excitations of cells and to measure membrane bending elastic-moduli J Phys 48 1987 2139 2151
41. T. Betz, and C. Sykes Time resolved membrane fluctuation spectroscopy Soft Matter 8 2012 5317 5326
42. V.L. Kononenko Flicker in erythrocytes. I. Theoretical models and registration techniques Biol Membr 26 2009 352 369
43. V.L. Kononenko Flicker in erythrocytes. 2. Review of experimental studies Biol Membr 26 2009 451 467
44. J.L. van Hemmen, and C. Leibold Elementary excitations of biomembranes: differential geometry of undulations in elastic surfaces Phys Rep-Rev Sec Phys Lett 444 2007 51 99
45. A. Zilker, M. Ziegler, and E. Sackmann Spectral-analysis of erythrocyte flickering in the 0.3-4-Mu-M-1 regime by microinterferometry combined with fast image-processing Phys Rev A 46 1992 7998 8002
46. U. Seifert, and S.A. Langer Hydrodynamics of membranes - the bilayer aspect and adhesion Biophys Chem 49 1994 13 22
47. M. Kraus, and U. Seifert Relaxation modes of an adhering bilayer-membrane J Phys II 4 1994 1117 1134
48. F. Divet, G. Danker, and C. Misbah Fluctuations and instability of a biological membrane induced by interaction with macromolecules Phys Rev E 72 2005
49. M.C. Marchetti, J.F. Joanny, S. Ramaswamy, T.B. Liverpool, J. Prost, and M. Rao et al. Hydrodynamics of soft active matter Rev Mod Phys 85 2013
50. W. Helfrich, and R.M. Servuss Undulations, Steric Interaction And Cohesion Of Fluid Membranes. Nuovo cimento della societa italiana Di fisica D-condensed matter atomic molecular and chemical Phys Fluids Plasmas Biophys 3 1984 137 151
51. U. Seifert Dynamics of a bound membrane Phys Rev E 49 1994 3124 3127
52. A.D. Lieber, S. Yehudai-Resheff, E.L. Barnhart, J.A. Theriot, and K. Keren Membrane tension in rapidly moving cells is determined by cytoskeletal forces Curr Biol 23 2013 1409 1417
53. C.E. Morris, and U. Homann Cell surface area regulation and membrane tension J Membr Biol 179 2001 79 102
54. N. Gov, A.G. Zilman, and S. Safran Cytoskeleton confinement and tension of red blood cell membranes Phys Rev Lett 90 2003
55. S.A. Shkulipa, W.K. den Otter, and W.J. Briels Thermal undulations of lipid bilayers relax by intermonolayer friction at submicrometer length scales Phys Rev Lett 96 2006
56. E. Evans, and A. Yeung Hidden dynamics in rapid changes of bilayer shape Chem Phys Lipids 73 1994 39 56
57. J.E. Rothman, and J. Lenard Membrane asymmetry Science 195 1977 743 753
58. M. Rahimi, and M. Arroyo Shape dynamics, lipid hydrodynamics, and the complex viscoelasticity of bilayer membranes Phys Rev E 86 2012
59. R. Merkel, E. Sackmann, and E. Evans Molecular friction and epitactic coupling between monolayers in supported bilayers J Phys 50 1989 1535 1555
60. A. Horner, S.A. Akimov, and P. Pohl Long and short lipid molecules experience the same interleaflet drag in lipid bilayers Phys Rev Lett 110 2013 268101
61. R. Rodriguez-Garcia, L.R. Arriaga, M. Mell, L.H. Moleiro, I. Lopez-Montero, and F. Monroy Bimodal spectrum for the curvature fluctuations of bilayer vesicles: pure bending plus hybrid curvature-dilation modes Phys Rev Lett 102 2009
62. A.R. Honerkamp-Smith, F.G. Woodhouse, V. Kantsler, and R.E. Goldstein Membrane viscosity determined from shear-driven flow in giant vesicles Phys Rev Lett 111 2013 038103
63. B.A. Camley, C. Esposito, T. Baumgart, and F.L.H. Brown Lipid bilayer domain fluctuations as a probe of membrane viscosity Biophys J 99 2010 L44 L46
64. A.F. Bitbol, N. Puff, Y. Sakuma, M. Imai, J.B. Fournier, and M.I. Angelova Lipid membrane deformation in response to a local pH modification: theory and experiments Soft Matter 8 2012 6073 6082
65. A.F. Bitbol, and J.B. Fournier Membrane properties revealed by spatiotemporal response to a local inhomogeneity Biochim Biophys Acta Biomembr 2013 1828 1241 1249
66. S. Levin, and R. Korenstein Membrane fluctuations in erythrocytes are linked to mgatp-dependent dynamic assembly of the membrane skeleton Biophys J 60 1991 733 737
67. M. Staykova, D.P. Holmes, C. Read, and H.A. Stone Mechanics of surface area regulation in cells examined with confined lipid membranes Proc Natl Acad Sci U S A 108 2011 9084 9088
68. E. Evans, and W. Rawicz Entropy-driven tension and bending elasticity in condensed-fluid membranes Phys Rev Lett 64 1990 2094 2097
69. F. Brochard, P.G. Degennes, and P. Pfeuty Surface-tension and deformations of membrane structures - relation to 2-dimensional phase-transitions J Phys 37 1976 1099 1104
70. N. Borghi, O. Rossier, and F. Brochard-Wyart Hydrodynamic extrusion of tubes from giant vesicles Europhys Lett 64 2003 837 843
71. A. Tian, and T. Baumgart Sorting of lipids and proteins in membrane curvature gradients Biophys J 96 2009 2676 2688
72. M. Staykova, M. Arroyo, M. Rahimi, and H.A. Stone Confined bilayers passively regulate shape and stress Phys Rev Lett 110 2013
73. J. Neder, B. West, P. Nielaba, and F. Schmid Coarse-grained simulations of membranes under tension J Chem Phys 132 2010
74. S.T. Milner, and S.A. Safran Dynamical fluctuations of droplet microemulsions and vesicles Phys Rev A 36 1987 4371 4379
75. U. Seifert The concept of effective tension for fluctuating vesicles Z Phys B Condens Matter 97 1995 299 309
76. P. Girard, F. Julicher, and J. Prost Fluid membranes exchanging material with external reservoirs Eur Phys J E 14 2004 387 394
77. J. Solon, J. Pécréaux, P. Girard, M.-C. Fauré, J. Prost, and P. Bassereau Negative tension induced by lipid uptake Phys Rev Lett 97 2006 098103
78. J.C. Shillcock, and R. Lipowsky Tension-induced fusion of bilayer membranes and vesicles Nat Mater 4 2005 225 228
79. B. Sinha, D. Koster, R. Ruez, P. Gonnord, M. Bastiani, and D. Abankwa et al. Cells respond to mechanical stress by rapid disassembly of caveolae Cell 144 2011 402 413
80. T.A. Masters, B. Pontes, V. Viasnoff, Y. Li, and N.C. Gauthier Plasma membrane tension orchestrates membrane trafficking, cytoskeletal remodeling, and biochemical signaling during phagocytosis Proc Natl Acad Sci U S A 110 2013 11875 11880
81. A. Diz-Munoz, D.A. Fletcher, and O.D. Weiner Use the force: membrane tension as an organizer of cell shape and motility Trends Cell Biol 23 2013 47 53
82. N.C. Gauthier, M.A. Fardin, P. Roca-Cusachs, and M.P. Sheetz Temporary increase in plasma membrane tension coordinates the activation of exocytosis and contraction during cell spreading Proc Natl Acad Sci U S A 108 2011 14467 14472
83. N.C. Gauthier, T.A. Masters, and M.P. Sheetz Mechanical feedback between membrane tension and dynamics Trends Cell Biol 22 2012 527 535
84. R. Houk Andrew, A. Jilkine, O. Mejean Cecile, R. Boltyanskiy, R. Dufresne Eric, and B. Angenent Sigurd et al. Membrane tension maintains cell polarity by confining signals to the leading edge during neutrophil migration Cell 148 2012 175 188
85. J. Swift, I.L. Ivanovska, A. Buxboim, T. Harada, P.C.D.P. Dingal, and J. Pinter et al. Nuclear lamin-a scales with tissue stiffness and enhances matrix-directed differentiation Science 341 2013
86. S. Watanabe, B.R. Rost, M. Camacho-Perez, M.W. Davis, B. Sohl-Kielczynski, and C. Rosenmund et al. Ultrafast endocytosis at mouse hippocampal synapses Nature 504 2013 242 247
87. D. Kabaso, R. Shlomovitz, K. Schloen, T. Stradal, and N.S. Gov Theoretical model for cellular shapes driven by protrusive and adhesive forces PLoS Comput Biol 7 2011
88. C.Y. Tay, P. Cai, M.I. Setyawati, W. Fang, L.P. Tan, and C.H.L. Hong et al. Nanoparticles strengthen intracellular tension and retard cellular migration Nano Lett 14 2013 83 88
89. D. Raucher, and M.P. Sheetz Cell spreading and lamellipodial extension rate is regulated by membrane tension J Cell Biol 148 2000 127 136
90. D. Raucher, and M.P. Sheetz Membrane expansion increases endocytosis rate during mitosis J Cell Biol 144 1999 497 506
91. S. Boulant, C. Kural, J.C. Zeeh, F. Ubelmann, and T. Kirchhausen Actin dynamics counteract membrane tension during clathrin-mediated endocytosis Nat Cell Biol 13 2011 1124-U158
92. Y.H. Li, R. Lipowsky, and R. Dimova Membrane nanotubes induced by aqueous phase separation and stabilized by spontaneous curvature Proc Natl Acad Sci U S A 108 2011 4731 4736
93. R. Lipowsky Spontaneous tubulation of membranes and vesicles reveals membrane tension generated by spontaneous curvature Faraday Discuss 161 2013 305 331
94. Y.A. Domanov, and P.K.J. Kinnunen Antimicrobial peptides temporins B and L induce formation of tubular lipid protrusions from supported phospholipid bilayers Biophys J 91 2006 4427 4439
95. Y. Tanaka-Takiguchi, T. Itoh, K. Tsujita, S. Yamada, M. Yanagisawa, and K. Fujiwara et al. Physicochemical analysis from real-time imaging of liposome tubulation reveals the characteristics of individual F-BAR domain proteins Langmuir 29 2012 328 336
96. R. Barziv, and E. Moses Instability and pearling states produced in tubular membranes by competition of curvature and tension Phys Rev Lett 73 1994 1392 1395
97. P. Nelson, T. Powers, and U. Seifert Dynamical theory of the pearling instability in cylindrical vesicles Phys Rev Lett 74 1995 3384 3387
98. Y. Yu, and S. Granick Pearling of lipid vesicles induced by nanoparticles J Am Chem Soc 131 2009 14158
99. I. Tsafrir, Y. Caspi, M.A. Guedeau-Boudeville, T. Arzi, and J. Stavans Budding and tubulation in highly oblate vesicles by anchored amphiphilic molecules Phys Rev Lett 91 2003
100. J. Kas, and E. Sackmann Shape transitions and shape stability of giant phospholipid-vesicles in pure water induced by area-to-volume changes Biophys J 60 1991 825 844
101. M. Jaric, U. Seifert, W. Wintz, and M. Wortis Vesicular instabilities - the prolate-to-oblate transition and other shape instabilities of fluid bilayer-membranes Phys Rev E 52 1995 6623 6634
102. P.B.S. Kumar, and M. Rao Shape instabilities in the dynamics of a two-component fluid membrane Phys Rev Lett 80 1998 2489 2492
103. U. Seifert Curvature-induced lateral phase segregation in 2-component vesicles Phys Rev Lett 70 1993 1335 1338
104. M.P. Sheetz, and S.J. Singer Biological-membranes as bilayer couples - molecular mechanism of drug-erythrocyte interactions Proc Natl Acad Sci U S A 71 1974 4457 4461
105. F. Campelo Modeling morphological instabilities in lipid membranes with anchored amphiphilic polymers J Chem Biol 2 2009 65 80
106. K. Berndl, J. Kas, R. Lipowsky, E. Sackmann, and U. Seifert Shape transformations of giant vesicles - extreme sensitivity to bilayer asymmetry Europhys Lett 13 1990 659 664
107. U. Seifert, K. Berndl, and R. Lipowsky Shape transformations of vesicles - phase-diagram for spontaneous-curvature and bilayer-coupling models Phys Rev A 44 1991 1182 1202
108. M. Seul, and D. Andelman Domain shapes and patterns - the phenomenology of modulated phases Science 267 1995 476 483
109. C. Zhu, S.L. Das, and T. Baumgart Nonlinear sorting, curvature generation, and crowding of endophilin N-BAR on tubular membranes Biophys J 102 2012 1837 1845
110. J.W. Cahn, and J.E. Hilliard Free energy of a nonuniform system.1. Interfacial free energy J Chem Phys 28 1958 258 267
111. J.B. Fournier Nontopological saddle-splay and curvature instabilities from anisotropic membrane inclusions Phys Rev Lett 76 1996 4436 4439
112. D. Kabaso, N. Bobrovska, W. Gozdz, N. Gov, V. Kralj-Iglic, and P. Veranic et al. On the role of membrane anisotropy and BAR proteins in the stability of tubular membrane structures J Biomech 45 2012 231 238
113. S. Loew, A. Hinderliter, and S. May Stability of protein-decorated mixed lipid membranes: the interplay of lipid-lipid, lipid-protein, and protein-protein interactions J Chem Phys 130 2009
114. A. Veksler, and N.S. Gov Phase transitions of the coupled membrane-cytoskeleton modify cellular shape Biophys J 93 2007 3798 3810
115. S. Chiruvolu, H.E. Warriner, E. Naranjo, S.H.J. Idziak, J.O. Radler, and R.J. Plano et al. A phase of liposomes with entangled tubular vesicles Science 266 1994 1222 1225
116. D. Allan, M.M. Billah, J.B. Finean, and R.H. Michell Release of diacylglycerol-enriched vesicles from erythrocytes with increased intracellular Ca2 + Nature 261 1976 58 60
117. C. Leirer, B. Wunderlich, V.M. Myles, and M.F. Schneider Phase transition induced fission in lipid vesicles Biophys Chem 143 2009 106 109
118. D. Kabaso, R. Shlomovitz, T. Auth, V.L. Lew, and N.S. Gov Curling and local shape changes of Red blood cell membranes driven by cytoskeletal reorganization Biophys J 99 2010 808 816
119. S. Leibler, and D. Andelman Ordered and curved meso-structures in membranes and amphiphilic films J Phys 48 1987 2013 2018
120. C.D. Santangelo, and O. Farago Membrane fluctuations around inclusions J Comput Aided Mater Des 14 2007 103 109
121. J.G. Hu, and R. Granek Buckling of amphiphilic monolayers induced by head-tail asymmetry J Phys II 6 1996 999 1022
122. M.M. Lipp, K.Y.C. Lee, D.Y. Takamoto, J.A. Zasadzinski, and A.J. Waring Coexistence of buckled and flat monolayers Phys Rev Lett 81 1998 1650 1653
123. L. Bourdieu, J. Daillant, D. Chatenay, A. Braslau, and D. Colson Buckling of polymerized monomolecular films Phys Rev Lett 72 1994 1502 1505
124. M. Kardar, and R. Golestanian The "friction" of vacuum, and other fluctuation-induced forces Rev Mod Phys 71 1999 1233 1245
125. M. Benhamou Primitive interactions between inclusions on a fluid membrane: the role of thermal fluctuations Eur Phys J E 34 2011
126. H.K. Lin, R. Zandi, U. Mohideen, and L.P. Pryadko Fluctuation-induced forces between inclusions in a fluid membrane under tension Phys Rev Lett 2011 107
127. M. Goulian, R. Bruinsma, and P. Pincus Long-range forces in heterogeneous fluid membranes Europhys Lett 22 1993 145 150
128. C. Yolcu, and M. Deserno Membrane-mediated interactions between rigid inclusions: an effective field theory Phys Rev E 86 2012
129. V. Demery Diffusion of a particle quadratically coupled to a thermally fluctuating field Phys Rev E 87 2013
130. J.B. Manneville, P. Bassereau, S. Ramaswamy, and J. Prost Active membrane fluctuations studied by micropipet aspiration Phys Rev E 64 2001
131. B. Loubet, U. Seifert, and M.A. Lomholt Effective tension and fluctuations in active membranes Phys Rev E 85 2012
132. I. Koltover, J.O. Radler, and C.R. Safinya Membrane mediated attraction and ordered aggregation of colloidal particles bound to giant phospholipid vesicles Phys Rev Lett 82 1999 1991 1994
133. D. Morozova, G. Guigas, and M. Weiss Dynamic structure formation of peripheral membrane proteins PLoS Comput Biol 7 2011
134. N. Ramakrishnan, P.B. Sunil Kumar, and John H. Ipsen Membrane-mediated aggregation of curvature-inducing nematogens and membrane tubulation Biophys J 104 2013 1018 1028
135. S. Weitz, and N. Destainville Attractive asymmetric inclusions in elastic membranes under tension: cluster phases and membrane invaginations Soft Matter 9 2013 7804 7816
136. T. Gil, J.H. Ipsen, O.G. Mouritsen, M.C. Sabra, M.M. Sperotto, and M.J. Zuckermann Theoretical analysis of protein organization in lipid membranes Biochim Biophys Acta 1376 1998 245 266
137. D. Morozova, M. Weiss, and G. Guigas Shape as a determinant of membrane protein cluster formation Soft Matter 8 2012 11905 11910
138. V. Ramanan, N.J. Agrawal, J. Liu, S. Engles, R. Toy, and R. Radhakrishnan Systems biology and physical biology of clathrin-mediated endocytosis Integr Biol 3 2011 803 815
139. E. Cocucci, F. Aguet, S. Boulant, and T. Kirchhausen The first five seconds in the life of a clathrin-coated pit Cell 150 2012 495 507
140. W. Kukulski, M. Schorb, M. Kaksonen, and J.A.G. Briggs Plasma membrane reshaping during endocytosis is revealed by time-resolved electron tomography Cell 150 2012 508 520
141. F.-Z. Idrissi, A. Blasco, A. Espinal, and M.I. Geli Ultrastructural dynamics of proteins involved in endocytic budding Proc Natl Acad Sci 109 2012 E2587 E2594
142. I.J. McGough, and P.J. Cullen Clathrin is not required for SNX-BAR-retromer mediated carrier formation J Cell Sci 126 2012 45 52
143. C. Mim, H.S. Cui, J.A. Gawronski-Salerno, A. Frost, E. Lyman, and G.A. Voth et al. Structural basis of membrane bending by the N-BAR protein endophilin Cell 149 2012 137 145
144. A. Frost, R. Perera, A. Roux, K. Spasov, O. Destaing, and E.H. Egelman et al. Structural basis of membrane invagination by F-BAR domains Cell 132 2008 807 817
145. R.A. Hom, M. Vora, M. Regner, O.M. Subach, W. Cho, and V.V. Verkhusha et al. PH-dependent binding of the epsin ENTH domain and the AP180 ANTH domain to PI(4,5)P-2-containing bilayers J Mol Biol 373 2007 412 423
146. Y. Yoon, X. Zhang, and W. Cho Phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) specifically induces membrane penetration and deformation by bin/amphiphysin/rvs (BAR) domains J Biol Chem 287 2012 34078 34090
147. B.R. Capraro, Z. Shi, T. Wu, Z. Chen, J.M. Dunn, and E. Rhoades et al. Kinetics of endophilin N-BAR domain dimerization and membrane interactions J Biol Chem 288 2013 12533 12543
148. H. Cui, C. Mim, X. Vázquez Francisco, E. Lyman, M. Unger Vinzenz, and Gregory A. Voth Understanding the role of amphipathic helices in N-BAR domain driven membrane remodeling Biophys J 104 2013 404 411
149. M. Simunovic, A. Srivastava, and G.A. Voth Linear aggregation of proteins on the membrane as a prelude to membrane remodeling Proc Natl Acad Sci 110 2013 20396 20401
150. B. Sorre, A. Callan-Jones, J. Manzi, B. Goud, J. Prost, and P. Bassereau et al. Nature of curvature coupling of amphiphysin with membranes depends on its bound density Proc Natl Acad Sci U S A 109 2012 173 178
151. E. Atilgan, and S.X. Sun Shape transitions in lipid membranes and protein mediated vesicle fusion and fission J Chem Phys 126 2007
152. W.T. Gozdz Shape transformation of lipid vesicles induced by diffusing macromolecules J Chem Phys 134 2011
153. M. Simunovic, C. Mim, T.C. Marlovits, G. Resch, V.M. Unger, and G.A. Voth Protein-mediated transformation of lipid vesicles into tubular networks Biophys J 105 2013 711 719
154. M. Meinecke, E. Boucrot, G. Camdere, W.C. Hon, R. Mittal, and H.T. McMahon Cooperative recruitment of dynamin and BIN/amphiphysin/Rvs (BAR) domain-containing proteins leads to GTP-dependent membrane scission J Biol Chem 288 2013 6651 6661
155. A.P. Minton Effects of excluded surface area and adsorbate clustering on surface adsorption of proteins. II. Kinetic models Biophys J 80 2001 1641 1648
156. A. Frost, V.M. Unger, and P. De Camilli The BAR domain superfamily: membrane-molding macromolecules Cell 137 2009 191 196
157. P. Xu, R.D. Baldridge, R.J. Chi, C.G. Burd, and T.R. Graham Phosphatidylserine flipping enhances membrane curvature and negative charge required for vesicular transport J Cell Biol 202 2013 875 886
158. M.M. Ouberai, J. Wang, M.J. Swann, C. Galvagnion, T. Guilliams, and C.M. Dobson et al. Alpha-synuclein senses lipid packing defects and induces lateral expansion of lipids leading to membrane remodeling J Biol Chem 288 2013 20883 20895
159. H.S. Cui, E. Lyman, and G.A. Voth Mechanism of membrane curvature sensing by amphipathic helix containing proteins Biophys J 100 2011 1271 1279