Mesoscopic membrane physics: concepts, simulations, and selected applications.

The window of a few tens to a few hundred nanometers in length scale is a booming field in lipid membrane research, owing largely to two reasons. First, many exciting biophysical and cell biological processes take place within it. Second, experimental techniques manage to zoom in on this sub-optical scale, while computer simulations zoom out to system sizes previously unattainable, and both will be meeting soon. This paper reviews a selection of questions and concepts in this field and demonstrates that they can often be favorably addressed with highly simplified simulation models. Among the topics discussed are membrane adhesion to substrates, mixed lipid bilayers, lipid curvature coupling, pore formation by antimicrobial peptides, composition-driven protein aggregation, and curvature driven vesiculation.

[1]  Gregoria Illya,et al.  Coarse-grained simulation studies of peptide-induced pore formation. , 2008, Biophysical journal.

[2]  Pore nucleation in mechanically stretched bilayer membranes. , 2005, The Journal of chemical physics.

[3]  Berend Smit,et al.  Mesoscopic models of biological membranes , 2006 .

[4]  Oded Farago,et al.  Mode excitation Monte Carlo simulations of mesoscopically large membranes. , 2008, The Journal of chemical physics.

[5]  Sergei Izvekov,et al.  Multiscale Coarse-Graining of Mixed Phospholipid/Cholesterol Bilayers. , 2006, Journal of chemical theory and computation.

[6]  R. C. Reeder,et al.  A Coarse Grain Model for Phospholipid Simulations , 2001 .

[7]  F. Maxfield,et al.  Role of Membrane Organization and Membrane Domains in Endocytic Lipid Trafficking , 2000, Traffic.

[8]  Jemal Guven,et al.  Stresses in lipid membranes , 2002 .

[9]  J. Majewski,et al.  Characterization of single biological membranes at the solid–liquid interface by X-ray reflectivity , 2006 .

[10]  CRITICAL CASIMIR FORCES BETWEEN SPHERICAL PARTICLES IN FLUIDS , 1998 .

[11]  W. Webb,et al.  Membrane elasticity in giant vesicles with fluid phase coexistence. , 2005, Biophysical journal.

[12]  T. Salditt,et al.  Grazing incidence X-ray diffraction of highly aligned phospholipid membranes containing the antimicrobial peptide magainin 2 , 2000, European Biophysics Journal.

[13]  Wan-Chen Lin,et al.  Lipid asymmetry in DLPC/DSPC-supported lipid bilayers: a combined AFM and fluorescence microscopy study. , 2006, Biophysical journal.

[14]  J. Gesell,et al.  Two-dimensional 1H NMR experiments show that the 23-residue magainin antibiotic peptide is an α-helix in dodecylphosphocholine micelles, sodium dodecylsulfate micelles, and trifluoroethanol/water solution , 1997, Journal of biomolecular NMR.

[15]  Evans,et al.  Entropy-driven tension and bending elasticity in condensed-fluid membranes. , 1990, Physical review letters.

[16]  Frank L. H. Brown,et al.  Implicit solvent simulation models for biomembranes , 2005, European Biophysics Journal.

[17]  W. Knoll,et al.  The polymer-supported phospholipid bilayer: tethering as a new approach to substrate-membrane stabilization. , 2002, Biomacromolecules.

[18]  Assaf Zemel,et al.  Energetics and self-assembly of amphipathic peptide pores in lipid membranes. , 2003, Biophysical journal.

[19]  A. Tian,et al.  Sorting of lipids and proteins in membrane curvature gradients. , 2009, Biophysical journal.

[20]  D. Andreu,et al.  Animal antimicrobial peptides: an overview. , 1998, Biopolymers.

[21]  P. De Camilli,et al.  Generation of high curvature membranes mediated by direct endophilin bilayer interactions , 2001, The Journal of cell biology.

[22]  B. Ninham,et al.  Theory of self-assembly of hydrocarbon amphiphiles into micelles and bilayers , 1976 .

[23]  H. Noguchi,et al.  Self-assembly of amphiphiles into vesicles: a Brownian dynamics simulation. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[24]  Bianca Habermann,et al.  Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. , 2005, Developmental cell.

[25]  T. Lubensky,et al.  Interactions between membrane Inclusions on Fluctuating Membranes , 1996, cond-mat/9601006.

[26]  K. Brogden.  Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? , 2005, Nature Reviews Microbiology.

[27]  Grace Brannigan,et al.  Solvent-free simulations of fluid membrane bilayers. , 2004, The Journal of chemical physics.

[28]  Alessandro Tossi,et al.  Amphipathic, α‐helical antimicrobial peptides , 2000 .

[29]  A. Louis,et al.  Effective potentials for polymers and colloids: beyond the van der Waals picture of fluids? , 2001, Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[30]  Geometry of lipid vesicle adhesion. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[31]  Grace Brannigan,et al.  Flexible lipid bilayers in implicit solvent. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[32]  P. Stroeve,et al.  Mobile Phospholipid Bilayers Supported on a Polyion/Alkylthiol Layer Pair , 2000 .

[33]  Marcus Mueller,et al.  Biological and synthetic membranes: What can be learned from a coarse-grained description? , 2006 .

[34]  H. Mcconnell,et al.  Supported phospholipid bilayers. , 1985, Biophysical journal.

[35]  A. Kolb,et al.  Optimized Constant Pressure Stochastic Dynamics , 1999 .

[36]  L. Frink,et al.  Computational investigations of pore forming peptide assemblies in lipid bilayers. , 2006, Physical review letters.

[37]  Michael L Klein,et al.  Understanding nature's design for a nanosyringe. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[38]  M. Lösche,et al.  Enzyme activity to augment the characterization of tethered bilayer membranes. , 2006, The journal of physical chemistry. B.

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

[40]  D. K. Schwartz,et al.  Linactants: surfactant analogues in two dimensions. , 2008, Physical review letters.

[41]  M. M. Nicolson,et al.  The interaction between floating particles , 1949, Mathematical Proceedings of the Cambridge Philosophical Society.

[42]  W. Briels,et al.  The bending rigidity of an amphiphilic bilayer from equilibrium and nonequilibrium molecular dynamics , 2003 .

[43]  F. Brown,et al.  Contributions of Gaussian curvature and nonconstant lipid volume to protein deformation of lipid bilayers. , 2007, Biophysical journal.

[44]  C. Morris,et al.  Cell Surface Area Regulation and Membrane Tension , 2001, The Journal of Membrane Biology.

[45]  T. Ihle,et al.  Stochastic rotation dynamics: a Galilean-invariant mesoscopic model for fluid flow. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[46]  Daan Frenkel,et al.  Modeling flexible amphiphilic bilayers: a solvent-free off-lattice Monte Carlo study. , 2005, The Journal of chemical physics.

[47]  Frank L. H. Brown.  Simple models for biomembrane structure and dynamics , 2007, Comput. Phys. Commun..

[48]  Markus Deserno,et al.  A novel method for measuring the bending rigidity of model lipid membranes by simulating tethers. , 2006, Journal of Chemical Physics.

[49]  Y. Shai,et al.  Mode of action of linear amphipathic α-helical antimicrobial peptides , 1998 .

[50]  Joachim O. Rädler,et al.  MEMBRANE MEDIATED ATTRACTION AND ORDERED AGGREGATION OF COLLOIDAL PARTICLES BOUND TO GIANT PHOSPHOLIPID VESICLES , 1999 .

[51]  O. Farago.  “Water-free” computer model for fluid bilayer membranes , 2003, cond-mat/0304203.

[52]  L. Yang,et al.  Barrel-stave model or toroidal model? A case study on melittin pores. , 2001, Biophysical journal.

[53]  J. Nagle,et al.  Structure of Gel Phase DMPC Determined by X-Ray Diffraction , 2002 .

[54]  M. Krech.  Casimir forces in binary liquid mixtures , 1997, cond-mat/9703093.

[55]  Solvent-free model for self-assembling fluid bilayer membranes: stabilization of the fluid phase based on broad attractive tail potentials. , 2005, The Journal of chemical physics.

[56]  S. Egelhaaf,et al.  Adhesion promotes phase separation in mixed-lipid membranes , 2008 .

[57]  E. Evans,et al.  Thermoelasticity of large lecithin bilayer vesicles. , 1981, Biophysical journal.

[58]  Kremer,et al.  Molecular dynamics simulation for polymers in the presence of a heat bath. , 1986, Physical review. A, General physics.

[59]  W. Helfrich.  Lyotropic lamellar phases , 1994 .

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

[61]  Daan Frenkel,et al.  Determination of phase diagrams for the hard-core attractive Yukawa system , 1994 .

[62]  M. Kozlov,et al.  The gaussian curvature elastic modulus of N-monomethylated dioleoylphosphatidylethanolamine: relevance to membrane fusion and lipid phase behavior. , 2004, Biophysical journal.

[63]  Bernd Ensing,et al.  Lipid bilayer perturbations around a transmembrane nanotube: a coarse grain molecular dynamics study. , 2005, Biophysical journal.

[64]  A C Maggs,et al.  Computer simulations of self-assembled membranes. , 1991, Science.

[65]  R. Capovilla,et al.  Stress and geometry of lipid vesicles , 2004 .

[66]  P. Dommersnes,et al.  N-body study of anisotropic membrane inclusions: Membrane mediated interactions and ordered aggregation , 1999, cond-mat/9906232.

[67]  Kurt Kremer,et al.  Long time atomistic polymer trajectories from coarse grained simulations: bisphenol-A polycarbonate. , 2006, Soft matter.

[68]  Michael L. Klein,et al.  Simulations of Phospholipids Using a Coarse Grain Model , 2001 .

[69]  Huey W. Huang,et al.  Sigmoidal concentration dependence of antimicrobial peptide activities: a case study on alamethicin. , 2002, Biophysical journal.

[70]  Y. Shai,et al.  Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. , 1999, Biochimica et biophysica acta.

[71]  K. Matsuzaki.  Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. , 1999, Biochimica et biophysica acta.

[72]  P. Dommersnes,et al.  Comment on "Long-range forces in heterogeneous fluid membranes” , 1997 .

[73]  T. Ihle,et al.  Erratum: Multi-particle collision dynamics: Flow around a circular and a square cylinder , 2001, cond-mat/0110148.

[74]  E. Lindahl,et al.  Mesoscopic undulations and thickness fluctuations in lipid bilayers from molecular dynamics simulations. , 2000, Biophysical journal.

[75]  N. Petersen,et al.  Thermodynamic studies of bovine lung surfactant extract mixing with cholesterol and its palmitate derivative. , 2007, Journal of colloid and interface science.

[76]  A. Ladd,et al.  Lattice-Boltzmann Simulations of Particle-Fluid Suspensions , 2001 .

[77]  J. Koelman,et al.  Simulating microscopic hydrodynamic phenomena with dissipative particle dynamics , 1992 .

[78]  Hiroshi Noguchi,et al.  Adhesion of nanoparticles to vesicles: a Brownian dynamics simulation. , 2002, Biophysical journal.

[79]  Zanetti,et al.  Use of the Boltzmann equation to simulate lattice gas automata. , 1988, Physical review letters.

[80]  Berend Smit,et al.  Simulation studies of protein-induced bilayer deformations, and lipid-induced protein tilting, on a mesoscopic model for lipid bilayers with embedded proteins. , 2005, Biophysical journal.

[81]  E. Sackmann,et al.  Supported Membranes: Scientific and Practical Applications , 1996, Science.

[82]  Critical Casimir Forces in Colloidal Suspensions , 2002, cond-mat/0202532.

[83]  B. Różycki,et al.  Stable patterns of membrane domains at corrugated substrates. , 2008, Physical review letters.

[84]  A. Malevanets,et al.  Mesoscopic model for solvent dynamics , 1999 .

[86]  J. Nagle,et al.  Fluid phase structure of EPC and DMPC bilayers. , 1998, Chemistry and physics of lipids.

[87]  Matthew I. Hoopes,et al.  Coarse-grained modeling of interactions of lipid bilayers with supports. , 2008, The Journal of chemical physics.

[88]  Martin Michael Müller,et al.  Contact lines for fluid surface adhesion. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[89]  Grace Brannigan,et al.  A consistent model for thermal fluctuations and protein-induced deformations in lipid bilayers. , 2006, Biophysical journal.

[90]  Yeomans,et al.  Lattice Boltzmann simulations of liquid-gas and binary fluid systems. , 1996, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[91]  Paul J. Atzberger,et al.  A stochastic immersed boundary method for fluid-structure dynamics at microscopic length scales , 2007, J. Comput. Phys..

[92]  D. Tieleman,et al.  The MARTINI force field: coarse grained model for biomolecular simulations. , 2007, The journal of physical chemistry. B.

[93]  R. Cantor,et al.  Lipid composition and the lateral pressure profile in bilayers. , 1999, Biophysical journal.

[94]  Seifert,et al.  Adhesion of vesicles. , 1990, Physical review. A, Atomic, molecular, and optical physics.

[95]  A. Mark,et al.  Coarse grained model for semiquantitative lipid simulations , 2004 .

[96]  Kurt Kremer,et al.  Ethylbenzene Diffusion in Polystyrene: United Atom Atomistic/ Coarse Grained Simulations and Experiments , 2007 .

[97]  E. Evans,et al.  Bending resistance and chemically induced moments in membrane bilayers. , 1974, Biophysical journal.

[98]  Gerhard Gompper,et al.  Low-Reynolds-number hydrodynamics of complex fluids by multi-particle-collision dynamics , 2004 .

[99]  Yeomans,et al.  Lattice Boltzmann simulation of nonideal fluids. , 1995, Physical review letters.

[100]  Berend Smit,et al.  Molecular simulations of lipid-mediated protein-protein interactions. , 2008, Biophysical journal.

[101]  A. Ladd.  Numerical simulations of particulate suspensions via a discretized Boltzmann equation. Part 1. Theoretical foundation , 1993, Journal of Fluid Mechanics.

[102]  E. Evans,et al.  Effect of chain length and unsaturation on elasticity of lipid bilayers. , 2000, Biophysical journal.

[103]  Gregory A Voth,et al.  A multiscale coarse-graining method for biomolecular systems. , 2005, The journal of physical chemistry. B.

[104]  M. Longo,et al.  Obstructed diffusion in phase-separated supported lipid bilayers: a combined atomic force microscopy and fluorescence recovery after photobleaching approach. , 2002, Biophysical journal.

[105]  R. Faller,et al.  Interactions of lipid bilayers with supports: a coarse-grained molecular simulation study. , 2008, The journal of physical chemistry. B.

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

[107]  H. Noguchi,et al.  Structural changes of pulled vesicles: a Brownian dynamics simulation. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[108]  Markus Deserno,et al.  Membrane composition-mediated protein-protein interactions , 2008, Biointerphases.

[109]  Fachbereich Physik,et al.  Interaction of conical membrane inclusions: Effect of lateral tension , 1998 .

[110]  M S Turner,et al.  Interactions between proteins bound to biomembranes. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[111]  Hiroshi Noguchi,et al.  Fusion pathways of vesicles: A Brownian dynamics simulation , 2001 .

[112]  J. M. Yeomans,et al.  Dynamics of short polymer chains in solution , 2000 .

[113]  P. Canham.  The minimum energy of bending as a possible explanation of the biconcave shape of the human red blood cell. , 1970, Journal of theoretical biology.

[114]  T. V. Tolpekina,et al.  Simulations of stable pores in membranes: system size dependence and line tension. , 2004, The Journal of chemical physics.

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

[116]  M. Deserno,et al.  Coupling between lipid shape and membrane curvature. , 2006, Biophysical journal.

[117]  Mark Goulian,et al.  Long-Range Forces in Heterogeneous Fluid Membranes , 1993 .

[118]  Netz.  Colloidal flocculation in near-critical binary mixtures. , 1996, Physical review letters.

[119]  J. Kasianowicz,et al.  Molecular-scale structural and functional characterization of sparsely tethered bilayer lipid membranes , 2007, Biointerphases.

[120]  Kurt Kremer,et al.  Tunable generic model for fluid bilayer membranes. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[121]  M. Bloom,et al.  Mattress model of lipid-protein interactions in membranes. , 1984, Biophysical journal.

[122]  M. Deserno,et al.  Interface-mediated interactions between particles: a geometrical approach. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[123]  J. Litster,et al.  Stability of lipid bilayers and red blood cell membranes , 1975 .

[124]  C. Hall,et al.  Polymer-induced phase separations in nonaqueous colloidal suspensions , 1983 .

[125]  Hans-Jörg Limbach,et al.  ESPResSo - an extensible simulation package for research on soft matter systems , 2006, Comput. Phys. Commun..