New insights into BAR domain-induced membrane remodeling.

Mesoscopic simulations and electron microscopy of N-BAR domain-induced liposome remodeling are used to characterize the process of liposome tubulation and vesiculation. The overall process of membrane remodeling is found to involve complex couplings among the N-BAR protein density, the degree of N-BAR oligomerization, and the membrane density. A comparison of complex remodeled liposome structures from mesoscopic simulations with those measured by electron microscopy experiments suggests that the process of membrane remodeling can be described via an appropriate mesoscopic free energy framework. Liposome remodeling more representative of F-BAR domains is also presented within the mesoscopic simulation framework.

[1]  L. Peliti,et al.  Strong adsorption in critical binary mixtures , 1983 .

[2]  J. Fournier,et al.  Nontopological saddle-splay and curvature instabilities from anisotropic membrane inclusions. , 1996, Physical review letters.

[3]  M. Kozlov,et al.  The hydrophobic insertion mechanism of membrane curvature generation by proteins. , 2008, Biophysical journal.

[4]  J. Mears,et al.  A corkscrew model for dynamin constriction. , 2007, Structure.

[5]  Saxena,et al.  Phase separation and shape deformation of two-phase membranes , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[6]  G. Rowlands,et al.  Stability analysis for the quartic Landau-Ginzburg model. II , 1990 .

[7]  Soichi Takeda,et al.  Endophilin BAR domain drives membrane curvature by two newly identified structure‐based mechanisms , 2006, The EMBO journal.

[8]  Tuszyński,et al.  Nonlinear magnetization processes in the Landau-Ginzburg model of magnetic inhomogeneities for uniaxial ferromagnets. , 1991, Physical review. B, Condensed matter.

[9]  Diana Murray,et al.  PIP(2) and proteins: interactions, organization, and information flow. , 2002, Annual review of biophysics and biomolecular structure.

[10]  T. Fischer.  Bending stiffness of lipid bilayers. III. Gaussian curvature , 1992 .

[11]  L. Lucy.  A numerical approach to the testing of the fission hypothesis. , 1977 .

[12]  N. Gamper,et al.  Target‐specific PIP2 signalling: how might it work? , 2007, The Journal of physiology.

[13]  Manuel Prieto,et al.  Role of helix 0 of the N-BAR domain in membrane curvature generation. , 2008, Biophysical journal.

[14]  Gregory A Voth,et al.  Factors influencing local membrane curvature induction by N-BAR domains as revealed by molecular dynamics simulations. , 2008, Biophysical journal.

[15]  Gregory A Voth,et al.  Coupling field theory with continuum mechanics: a simulation of domain formation in giant unilamellar vesicles. , 2005, Biophysical journal.

[16]  D. Murray,et al.  Plasma membrane phosphoinositide organization by protein electrostatics , 2005, Nature.

[17]  V Kralj-Iglic,et al.  Stable tubular microexovesicles of the erythrocyte membrane induced by dimeric amphiphiles. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[18]  Pietro De Camilli,et al.  Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis , 1999, Nature Cell Biology.

[19]  M. Laradji.  POLYMER ADSORPTION ON FLUCTUATING SURFACES , 1999 .

[20]  Gregory A. Voth,et al.  Direct observation of Bin/amphiphysin/Rvs (BAR) domain-induced membrane curvature by means of molecular dynamics simulations , 2006, Proceedings of the National Academy of Sciences.

[21]  B. Peter,et al.  BAR Domains as Sensors of Membrane Curvature: The Amphiphysin BAR Structure , 2004, Science.

[22]  Taniguchi,et al.  Shape deformation and phase separation dynamics of two-component vesicles. , 1996, Physical review letters.

[23]  G. Voth,et al.  Mesoscopic modeling of bacterial flagellar microhydrodynamics. , 2006, Biophysical journal.

[24]  E. Sackmann,et al.  Membrane bending energy concept of vesicle‐ and cell‐shapes and shape‐transitions , 1994, FEBS letters.

[25]  Sumio Sugano,et al.  Curved EFC/F-BAR-Domain Dimers Are Joined End to End into a Filament for Membrane Invagination in Endocytosis , 2007, Cell.

[26]  Gregory A Voth,et al.  Coupling field theory with mesoscopic dynamical simulations of multicomponent lipid bilayers. , 2004, Biophysical journal.

[27]  J. Ross,et al.  A derivation and comparison of two equations (Landau–Ginzburg and Cahn) for the kinetics of phase transitions , 1976 .

[28]  A. Bray.  Theory of phase-ordering kinetics , 1994, cond-mat/9501089.

[29]  H. McMahon,et al.  Bar Domains and Membrane Curvature: Bringing Your Curves to the Bar , 2022 .

[30]  Adam Frost,et al.  Structural Basis of Membrane Invagination by F-BAR Domains , 2008, Cell.

[31]  J. Zimmerberg,et al.  Membrane Curvature: How BAR Domains Bend Bilayers , 2004, Current Biology.

[32]  Oyeon Kum,et al.  Smooth particle applied mechanics , 2006 .

[33]  Gregory A Voth,et al.  Membrane remodeling from N-BAR domain interactions: insights from multi-scale simulation. , 2007, Biophysical journal.

[34]  T. Lubensky,et al.  Principles of condensed matter physics , 1995 .

[35]  C. G. Hoover,et al.  Links between microscopic and macroscopic fluid mechanics , 2003 .

[36]  J. Monaghan.  Smoothed particle hydrodynamics , 2005 .

[37]  H. Hägerstrand,et al.  On the role of anisotropy of membrane constituents in formation of a membrane neck during budding of a multicomponent membrane. , 2007, Journal of biomechanics.

[38]  Klaus Schulten,et al.  Four-scale description of membrane sculpting by BAR domains. , 2008, Biophysical journal.

[39]  G. Voth,et al.  Hierarchical coarse-graining strategy for protein-membrane systems to access mesoscopic scales. , 2010, Faraday discussions.

[40]  J. E. Hilliard,et al.  Free Energy of a Nonuniform System. I. Interfacial Free Energy , 1958 .

[41]  W. Helfrich.  Elastic Properties of Lipid Bilayers: Theory and Possible Experiments , 1973, Zeitschrift fur Naturforschung. Teil C: Biochemie, Biophysik, Biologie, Virologie.

[42]  K. Fütterer,et al.  “Wunder” F-BAR Domains: Going from Pits to Vesicles , 2007, Cell.

[43]  Gregory A Voth,et al.  Bridging microscopic and mesoscopic simulations of lipid bilayers. , 2002, Biophysical journal.

[44]  M. Kozlov,et al.  How Synaptotagmin Promotes Membrane Fusion , 2007, Science.

[45]  P. De Camilli,et al.  The stimulatory action of amphiphysin on dynamin function is dependent on lipid bilayer curvature , 2004, The EMBO journal.

[46]  Gregory A Voth,et al.  A second generation mesoscopic lipid bilayer model: connections to field-theory descriptions of membranes and nonlocal hydrodynamics. , 2006, The Journal of chemical physics.

[47]  K. Kremer,et al.  Aggregation and vesiculation of membrane proteins by curvature-mediated interactions , 2007, Nature.