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Simulating Protein-Mediated Membrane Remodeling at Multiple Scales

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Physics of Biological Membranes

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Abstract

The reshaping of the cell membrane is integral in many important cellular pathways, such as division, immune response, infection, trafficking, and communication. This process is generally modeled by considering lipid membranes to be thin elastic sheets that resist bending and stretching deformations. However, biological membranes are much more complex, as the macroscopically observed behavior of the membrane is deeply connected to the underlying atomic-level interactions between proteins and lipids. Computational methods can be developed to tackle this complex and innately multiscale phenomenon, as they can model the behavior at both the molecular and the macroscopic levels. In this chapter, we discuss the general mechanisms of membrane curvature generation and computational tools developed and applied to study this problem. We focus especially on finite-temperature simulation methods that are designed to model the complex behavior of the system. We review recent efforts in multiscale simulation designed to study the large-scale membrane reshaping by proteins.

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References

  1. Atkins P, de Paula J (2010) Atkins’ physical chemistry. Oxford University Press, Oxford

    Google Scholar 

  2. Ashrafuzzaman M, Tuszynski JA (2012) Membrane biophysics. Springer, New York

    Google Scholar 

  3. Lipowsky R (1991) The conformation of membranes. Nature 349(6309):475–481. https://doi.org/10.1038/349475a0

    Article  CAS  PubMed  Google Scholar 

  4. Alberts B, Johnson A, Lewis J, Morgan D, Raff M, Roberts K, Walter P (2014) Molecular biology of the cell. Taylor & Francis, New York

    Book  Google Scholar 

  5. Evans EA (1983) Bending elastic modulus of red blood cell membrane derived from buckling instability in micropipet aspiration tests. Biophys J 43(1):27–30. https://doi.org/10.1016/S0006-3495(83)84319-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Helfrich W (1973) Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch C 28(11):693–703

    Article  CAS  PubMed  Google Scholar 

  7. Kwok R, Evans E (1981) Thermoelasticity of large lecithin bilayer vesicles. Biophys J 35(3):637–652. https://doi.org/10.1016/S0006-3495(81)84817-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Baumgart T, Hess ST, Webb WW (2003) Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425(6960):821–824. https://doi.org/10.1038/nature02013

    Article  CAS  PubMed  Google Scholar 

  9. Funkhouser CM, Solis FJ, Thornton K (2010) Dynamics of two-phase lipid vesicles: effects of mechanical properties on morphology evolution. Soft Matter 6(15):3462–3466

    Article  CAS  Google Scholar 

  10. Hu JL, Weikl TR, Lipowsky R (2011) Vesicles with multiple membrane domains. Soft Matter 7(13):6092–6102

    Article  CAS  Google Scholar 

  11. Li J, Zhang H, Qiu F (2013) Budding behavior of multi-component vesicles. J Phys Chem B 117(3):843–849. https://doi.org/10.1021/jp308043y

    Article  CAS  PubMed  Google Scholar 

  12. Rim JE, Ursell TS, Phillips R, Klug WS (2011) Morphological phase diagram for lipid membrane domains with entropic tension. Phys Rev Lett 106(5):057801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Semrau S, Idema T, Holtzer L, Schmidt T, Storm C (2008) Accurate determination of elastic parameters for multicomponent membranes. Phys Rev Lett 100(8):088101

    Article  PubMed  Google Scholar 

  14. Sens P, Turner MS (2006) Budded membrane microdomains as tension regulators. Phys Rev E 73(3):Artn 031918. https://doi.org/10.1103/Physreve.73.031918

    Article  Google Scholar 

  15. Taniguchi T (1996) Shape deformation and phase separation dynamics of two-component vesicles. Phys Rev Lett 76(23):4444–4447

    Article  CAS  PubMed  Google Scholar 

  16. Taniguchi T, Yanagisawa M, Imai M (2011) Numerical investigations of the dynamics of two-component vesicles. J Phys Condens Matter 23(28):284103

    Article  PubMed  Google Scholar 

  17. Ursell TS, Klug WS, Phillips R (2009) Morphology and interaction between lipid domains. Proc Natl Acad Sci USA 106(32):13301–13306. https://doi.org/10.1073/Pnas.0903825106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Aimon S, Callan-Jones A, Berthaud A, Pinot M, Toombes GE, Bassereau P (2014) Membrane shape modulates transmembrane protein distribution. Dev Cell 28(2):212–218. https://doi.org/10.1016/j.devcel.2013.12.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Unwin N (2005) Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J Mol Biol 346(4):967–989. https://doi.org/10.1016/j.jmb.2004.12.031

    Article  CAS  PubMed  Google Scholar 

  20. Mackinnon R (2004) Structural biology. Voltage sensor meets lipid membrane. Science 306(5700):1304–1305. https://doi.org/10.1126/science.1105528

    Article  CAS  PubMed  Google Scholar 

  21. Drin G, Antonny B (2010) Amphipathic helices and membrane curvature. FEBS Lett 584:1840–1847

    Article  CAS  PubMed  Google Scholar 

  22. Campelo F, McMahon HT, Kozlov MM (2008) The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophys J 95(5):2325–2339. https://doi.org/10.1529/biophysj.108.133173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zemel A, Ben-Shaul A, May S (2008) Modulation of the spontaneous curvature and bending rigidity of lipid membranes by interfacially adsorbed amphipathic peptides. J Phys Chem B 112(23):6988–6996. https://doi.org/10.1021/jp711107y

    Article  CAS  PubMed  Google Scholar 

  24. Walther TC, Farese RV Jr (2009) The life of lipid droplets. Biochim Biophys Acta 1791(6):459–466. https://doi.org/10.1016/j.bbalip.2008.10.009

    Article  CAS  PubMed  Google Scholar 

  25. Wilson C, Wardell MR, Weisgraber KH, Mahley RW, Agard DA (1991) Three-dimensional structure of the LDL receptor-binding domain of human apolipoprotein E. Science 252(5014):1817–1822

    Article  CAS  PubMed  Google Scholar 

  26. Mim C, Unger VM (2012) Membrane curvature and its generation by BAR proteins. Trends Biochem Sci 37(12):526–533. https://doi.org/10.1016/j.tibs.2012.09.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Simunovic M, Voth GA, Callan-Jones A, Bassereau P (2015) When physics takes over: BAR proteins and membrane curvature. Trends Cell Biol 25(12):780–792. https://doi.org/10.1016/j.tcb.2015.09.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Callan-Jones A, Bassereau P (2013) Curvature-driven membrane lipid and protein distribution. Curr Opin Solid State Mater Sci 17(4):143–150

    Article  CAS  Google Scholar 

  29. Lipowsky R (2013) Spontaneous tubulation of membranes and vesicles reveals membrane tension generated by spontaneous curvature. Faraday Discuss 161:305–331. https://doi.org/10.1039/C2fd20105d

    Article  CAS  PubMed  Google Scholar 

  30. Lipowsky R, Dobereiner HG (1998) Vesicles in contact with nanoparticles and colloids. Europhys Lett 43(2):219–225

    Article  CAS  Google Scholar 

  31. Johannes L, Wunder C, Bassereau P (2014) Bending “on the rocks”—a cocktail of biophysical modules to build endocytic pathways. Cold Spring Harb Perspect Biol 6(1):a016741. https://doi.org/10.1101/cshperspect.a016741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. McMahon HT, Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438(7068):590–596. https://doi.org/10.1038/nature04396

    Article  CAS  PubMed  Google Scholar 

  33. Bickel T, Jeppesen C, Marques CM (2001) Local entropic effects of polymers grafted to soft interfaces. Eur Phys J E 4(1):33–43

    Article  CAS  Google Scholar 

  34. Breidenich M, Netz RR, Lipowsky R (2000) The shape of polymer-decorated membranes. Europhys Lett 49(4):431–437

    Article  CAS  Google Scholar 

  35. Nikolov V, Lipowsky R, Dimova R (2007) Behavior of giant vesicles with anchored DNA molecules. Biophys J 92(12):4356–4368. https://doi.org/10.1529/biophysj.106.100032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Stachowiak JC, Schmid EM, Ryan CJ, Ann HS, Sasaki DY, Sherman MB, Geissler PL, Fletcher DA, Hayden CC (2012) Membrane bending by protein-protein crowding. Nat Cell Biol 14(9):944–949. https://doi.org/10.1038/ncb2561

    Article  CAS  PubMed  Google Scholar 

  37. Sheetz MP (2001) Cell control by membrane-cytoskeleton adhesion. Nat Rev Mol Cell Biol 2(5):392–396. https://doi.org/10.1038/35073095

    Article  CAS  PubMed  Google Scholar 

  38. Koster G, VanDuijn M, Hofs B, Dogterom M (2003) Membrane tube formation from giant vesicles by dynamic association of motor proteins. Proc Natl Acad Sci USA 100(26):15583–15588. https://doi.org/10.1073/pnas.2531786100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Roux A, Cappello G, Cartaud J, Prost J, Goud B, Bassereau P (2002) A minimal system allowing tubulation with molecular motors pulling on giant liposomes. Proc Natl Acad Sci USA 99(8):5394–5399. https://doi.org/10.1073/pnas.082107299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Qualmann B, Koch D, Kessels MM (2011) Let’s go bananas: revisiting the endocytic BAR code. EMBO J 30(17):3501–3515. https://doi.org/10.1038/emboj.2011.266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Mim C, Cui H, Gawronski-Salerno JA, Frost A, Lyman E, Voth GA, Unger VM (2012) Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149(1):137–145. https://doi.org/10.1016/j.cell.2012.01.048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303(5657):495–499. https://doi.org/10.1126/science.1092586

    Article  CAS  PubMed  Google Scholar 

  43. Simunovic M, Evergren E, Golushko I, Prevost C, Renard HF, Johannes L, McMahon HT, Lorman V, Voth GA, Bassereau P (2016) How curvature-generating proteins build scaffolds on membrane nanotubes. Proc Natl Acad Sci USA 113(40):11226–11231. https://doi.org/10.1073/pnas.1606943113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Sorre B, Callan-Jones A, Manzi J, Goud B, Prost J, Bassereau P, Roux A (2012) Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proc Natl Acad Sci USA 109(1):173–178. https://doi.org/10.1073/pnas.1103594108

    Article  PubMed  Google Scholar 

  45. Suarez A, Ueno T, Huebner R, McCaffery JM, Inoue T (2014) Bin/Amphiphysin/Rvs (BAR) family members bend membranes in cells. Sci Rep 4:4693. https://doi.org/10.1038/srep04693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Ambroso MR, Hegde BG, Langen R (2014) Endophilin A1 induces different membrane shapes using a conformational switch that is regulated by phosphorylation. Proc Natl Acad Sci USA 111(19):6982–6987. https://doi.org/10.1073/pnas.1402233111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Simunovic M, Bassereau P (2014) Reshaping biological membranes in endocytosis: crossing the configurational space of membrane-protein interactions. Biol Chem 395(3):275–283. https://doi.org/10.1515/hsz-2013-0242

    Article  CAS  PubMed  Google Scholar 

  48. Simunovic M, Manneville JB, Renard HF, Evergren E, Raghunathan K, Bhatia D, Kenworthy AK, Voth GA, Prost J, McMahon HT, Johannes L, Bassereau P, Callan-Jones A (2017) Friction mediates scission of tubular membranes scaffolded by BAR proteins. Cell 170(1):172–184.e11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. van Gunsteren WF, Bakowies D, Baron R, Chandrasekhar I, Christen M, Daura X, Gee P, Geerke DP, Glattli A, Hunenberger PH, Kastenholz MA, Oostenbrink C, Schenk M, Trzesniak D, van der Vegt NF, Yu HB (2006) Biomolecular modeling: goals, problems, perspectives. Angew Chem 45(25):4064–4092. https://doi.org/10.1002/anie.200502655

    Article  CAS  Google Scholar 

  50. Frenkel D, Smit B (2001) Understanding molecular simulation: from Algorithms to applications. Elsevier Science, San Diego

    Google Scholar 

  51. Gingold RA, Monaghan JJ (1977) Smoothed particle hydrodynamics: theory and application to non-spherical stars. Mon Not R Astron Soc 181(2):375–389

    Article  Google Scholar 

  52. Lucy LB (1977) A numerical approach to the testing of the fission hypothesis. Astron J 82:1013–1024

    Article  Google Scholar 

  53. Liu MB, Liu GR (2010) Smoothed Particle Hydrodynamics (SPH): an overview and recent developments. Arch Comput Meth Eng 17(1):25–76. https://doi.org/10.1007/S11831-010-9040-7

    Article  CAS  Google Scholar 

  54. Hoogerbrugge PJ, Koelman JMVA (1992) Simulating microscopic hydrodynamic phenomena with dissipative particle dynamics. Europhys Lett 19(3):155–160. https://doi.org/10.1209/0295-5075/19/3/001

    Article  Google Scholar 

  55. Koelman JMVA, Hoogerbrugge PJ (1993) Dynamic simulations of hard-sphere suspensions under steady shear. Europhys Lett 21(3):363–368. https://doi.org/10.1209/0295-5075/21/3/018

    Article  CAS  Google Scholar 

  56. Shillcock JC, Lipowsky R (2002) Equilibrium structure and lateral stress distribution of amphiphilic bilayers from dissipative particle dynamics simulations. J Chem Phys 117(10):5048–5061. https://doi.org/10.1063/1.1498463

    Article  CAS  Google Scholar 

  57. Yamamoto S, Maruyama Y, Hyodo S (2002) Dissipative particle dynamics study of spontaneous vesicle formation of amphiphilic molecules (vol 116, pg 5842). J Chem Phys 117(6):2990. https://doi.org/10.1063/1.1494416

    Article  CAS  Google Scholar 

  58. Warshel A, Levitt M (1976) Theoretical studies of enzymic reactions: dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme. J Mol Biol 103(2):227–249

    Article  CAS  PubMed  Google Scholar 

  59. Izvekov S, Voth GA (2005) A multiscale coarse-graining method for biomolecular systems. J Phys Chem B 109(7):2469–2473

    Article  CAS  PubMed  Google Scholar 

  60. Hodak H (2014) The Nobel Prize in chemistry 2013 for the development of multiscale models of complex chemical systems: a tribute to Martin Karplus, Michael Levitt and Arieh Warshel. J Mol Biol 426(1):1–3. https://doi.org/10.1016/j.jmb.2013.10.037

    Article  CAS  PubMed  Google Scholar 

  61. Karplus M (2014) Development of multiscale models for complex chemical systems: from H+H(2) to biomolecules (Nobel Lecture). Angew Chem 53(38):9992–10005. https://doi.org/10.1002/anie.201403924

    Article  CAS  Google Scholar 

  62. Levitt M (2014) Birth and future of multiscale modeling for macromolecular systems (Nobel Lecture). Angew Chem 53(38):10006–10018. https://doi.org/10.1002/anie.201403691

    Article  CAS  Google Scholar 

  63. Warshel A (2014) Multiscale modeling of biological functions: from enzymes to molecular machines (Nobel Lecture). Angew Chem 53(38):10020–10031. https://doi.org/10.1002/anie.201403689

    Article  CAS  Google Scholar 

  64. Freddolino PL, Arkhipov AS, Larson SB, McPherson A, Schulten K (2006) Molecular dynamics simulations of the complete satellite tobacco mosaic virus. Structure 14(3):437–449. https://doi.org/10.1016/j.str.2005.11.014

    Article  CAS  PubMed  Google Scholar 

  65. Zhao G, Perilla JR, Yufenyuy EL, Meng X, Chen B, Ning J, Ahn J, Gronenborn AM, Schulten K, Aiken C, Zhang P (2013) Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics. Nature 497(7451):643–646. https://doi.org/10.1038/nature12162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Shaw DE, Grossman JP, Bank JA, Batson B, Butts JA, Chao JC, Deneroff MM, Dror RO, Even A, Fenton CH (2014) Anton 2: raising the bar for performance and programmability in a special-purpose molecular dynamics supercomputer. In: Proceedings of the international conference for high performance computing, networking, storage and analysis. IEEE Press, Salt Lake City, pp 41–53

    Chapter  Google Scholar 

  67. Arkhipov A, Shan Y, Das R, Endres NF, Eastwood MP, Wemmer DE, Kuriyan J, Shaw DE (2013) Architecture and membrane interactions of the EGF receptor. Cell 152(3):557–569. https://doi.org/10.1016/j.cell.2012.12.030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Dror RO, Green HF, Valant C, Borhani DW, Valcourt JR, Pan AC, Arlow DH, Canals M, Lane JR, Rahmani R, Baell JB, Sexton PM, Christopoulos A, Shaw DE (2013) Structural basis for modulation of a G-protein-coupled receptor by allosteric drugs. Nature 503(7475):295–299. https://doi.org/10.1038/nature12595

    Article  CAS  PubMed  Google Scholar 

  69. Akitake B, Anishkin A, Liu N, Sukharev S (2007) Straightening and sequential buckling of the pore-lining helices define the gating cycle of MscS. Nat Struct Mol Biol 14(12):1141–1149. https://doi.org/10.1038/nsmb1341

    Article  CAS  PubMed  Google Scholar 

  70. Bjelkmar P, Niemela PS, Vattulainen I, Lindahl E (2009) Conformational changes and slow dynamics through microsecond polarized atomistic molecular simulation of an integral Kv1.2 ion channel. PLoS Comput Biol 5(2):e1000289

    Article  PubMed  PubMed Central  Google Scholar 

  71. Cuello LG, Jogini V, Cortes DM, Pan AC, Gagnon DG, Dalmas O, Cordero-Morales JF, Chakrapani S, Roux B, Perozo E (2010) Structural basis for the coupling between activation and inactivation gates in K+ channels. Nature 466(7303):272–U154. https://doi.org/10.1038/Nature09136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Jeon J, Voth GA (2008) Gating of the mechanosensitive channel protein MscL: the interplay of membrane and protein. Biophys J 94(9):3497–3511. https://doi.org/10.1529/biophysj.107.109850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Jogini V, Roux B (2007) Dynamics of the Kv1.2 voltage-gated K+ channel in a membrane environment. Biophys J 93(9):3070–3082. https://doi.org/10.1529/biophysj.107.112540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Arkhipov A, Yin Y, Schulten K (2008) Four-scale description of membrane sculpting by BAR domains. Biophys J 95(6):2806–2821. https://doi.org/10.1529/biophysj.108.132563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Blood PD, Voth GA (2006) Direct observation of Bin/amphiphysin/Rvs (BAR) domain-induced membrane curvature by means of molecular dynamics simulations. Proc Natl Acad Sci USA 103(41):15068–15072. https://doi.org/10.1073/pnas.0603917103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Yu H, Schulten K (2013) Membrane sculpting by F-BAR domains studied by molecular dynamics simulations. PLoS Comput Biol 9(1):e1002892. https://doi.org/10.1371/journal.pcbi.1002892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Lyman E, Cui H, Voth GA (2010) Water under the BAR. Biophys J 99(6):1783–1790. https://doi.org/10.1016/j.bpj.2010.06.074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Blood PD, Swenson RD, Voth GA (2008) Factors influencing local membrane curvature induction by N-BAR domains as revealed by molecular dynamics simulations. Biophys J 95(4):1866–1876. https://doi.org/10.1529/biophysj.107.121160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Cui H, Ayton GS, Voth GA (2009) Membrane binding by the endophilin N-BAR domain. Biophys J 97(10):2746–2753. https://doi.org/10.1016/j.bpj.2009.08.043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Saunders MG, Voth GA (2013) Coarse-graining methods for computational biology. Annu Rev Biophys 42:73–93. https://doi.org/10.1146/annurev-biophys-083012-130348

    Article  CAS  PubMed  Google Scholar 

  81. Izvekov S, Voth GA (2006) Modeling real dynamics in the coarse-grained representation of condensed phase systems. J Chem Phys 125(15):151101. https://doi.org/10.1063/1.2360580

    Article  CAS  PubMed  Google Scholar 

  82. Sundararajan V, Simon SA, Benos DJ, Feller SE (2011) Computational modeling of membrane bilayers. Elsevier Science, San Diego

    Google Scholar 

  83. Noid WG, Chu JW, Ayton GS, Krishna V, Izvekov S, Voth GA, Das A, Andersen HC (2008) The multiscale coarse-graining method. I. A rigorous bridge between atomistic and coarse-grained models. J Chem Phys 128(24):244114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Noid WG, Liu P, Wang Y, Chu JW, Ayton GS, Izvekov S, Andersen HC, Voth GA (2008) The multiscale coarse-graining method. II. Numerical implementation for coarse-grained molecular models. J Chem Phys 128(24):244115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Izvekov S, Voth GA (2006) Multiscale coarse-graining of mixed phospholipid/cholesterol bilayers. J Chem Theory Comput 2(3):637–648

    Article  CAS  PubMed  Google Scholar 

  86. Izvekov S, Voth GA (2009) Solvent-free lipid bilayer model using multiscale coarse-graining. J Phys Chem B 113(13):4443–4455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Lu LY, Voth GA (2009) Systematic coarse-graining of a multicomponent lipid bilayer. J Phys Chem B 113(5):1501–1510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Ayton GS, Voth GA (2009) Hybrid coarse-graining approach for lipid bilayers at large length and time scales. J Phys Chem B 113(13):4413–4424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Gay JG, Berne BJ (1981) Modification of the overlap potential to mimic a linear site-site potential. J Chem Phys 74(6):3316–3319

    Article  CAS  Google Scholar 

  90. Srivastava A, Voth GA (2013) A hybrid approach for highly coarse-grained lipid bilayer models. J Chem Theory Comput 9(1):750–765. https://doi.org/10.1021/ct300751h

    Article  CAS  PubMed  Google Scholar 

  91. Srivastava A, Voth GA (2014) Solvent-free, highly coarse-grained models for charged lipid systems. J Chem Theory Comput 10(10):4730–4744. https://doi.org/10.1021/ct500474a

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Shelley JC, Shelley MY, Reeder RC, Bandyopadhyay S, Klein ML (2001) A coarse grain model for phospholipid simulations. J Phys Chem B 105(19):4464–4470

    Article  CAS  Google Scholar 

  93. Sodt AJ, Head-Gordon T (2010) An implicit solvent coarse-grained lipid model with correct stress profile. J Chem Phys 132(20):205103. https://doi.org/10.1063/1.3408285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Reith D, Putz M, Muller-Plathe F (2003) Deriving effective mesoscale potentials from atomistic simulations. J Comput Chem 24(13):1624–1636. https://doi.org/10.1002/jcc.10307

    Article  CAS  PubMed  Google Scholar 

  95. Lyubartsev AP, Laaksonen A (1995) Calculation of effective interaction potentials from radial-distribution functions—a reverse Monte-Carlo approach. Phys Rev E 52(4):3730–3737

    Article  CAS  Google Scholar 

  96. Lyubartsev AP (2005) Multiscale modeling of lipids and lipid bilayers. Eur Biophys J 35(1):53–61

    Article  CAS  PubMed  Google Scholar 

  97. Murtola T, Falck E, Karttunen M, Vattulainen I (2007) Coarse-grained model for phospholipid/cholesterol bilayer employing inverse Monte Carlo with thermodynamic constraints. J Chem Phys 126(7):075101. https://doi.org/10.1063/1.2646614

    Article  CAS  PubMed  Google Scholar 

  98. Murtola T, Falck E, Patra M, Karttunen M, Vattulainen I (2004) Coarse-grained model for phospholipid/cholesterol bilayer. J Chem Phys 121(18):9156–9165. https://doi.org/10.1063/1.1803537

    Article  CAS  PubMed  Google Scholar 

  99. Wang ZJ, Deserno M (2010) A systematically coarse-grained solvent-free model for quantitative phospholipid bilayer simulations. J Phys Chem B 114(34):11207–11220. https://doi.org/10.1021/jp102543j

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Mirzoev A, Lyubartsev AP (2014) Systematic implicit solvent coarse graining of dimyristoylphosphatidylcholine lipids. J Comput Chem 35(16):1208–1218. https://doi.org/10.1002/jcc.23610

    Article  CAS  PubMed  Google Scholar 

  101. Drouffe JM, Maggs AC, Leibler S (1991) Computer simulations of self-assembled membranes. Science 254(5036):1353–1356

    Article  CAS  PubMed  Google Scholar 

  102. Marrink SJ, Risselada HJ, Yefimov S, Tieleman DP, de Vries AH (2007) The MARTINI force field: coarse grained model for biomolecular simulations. J Phys Chem B 111(27):7812–7824

    Article  CAS  PubMed  Google Scholar 

  103. Marrink SJ, de Vries AH, Mark AE (2004) Coarse grained model for semiquantitative lipid simulations. J Phys Chem B 108(2):750–760

    Article  CAS  Google Scholar 

  104. Brannigan G, Brown FL (2004) Solvent-free simulations of fluid membrane bilayers. J Chem Phys 120(2):1059–1071. https://doi.org/10.1063/1.1625913

    Article  CAS  PubMed  Google Scholar 

  105. Farago O (2003) “Water-free” computer model for fluid bilayer membranes. J Chem Phys 119(1):596–605

    Article  CAS  Google Scholar 

  106. Noguchi H, Takasu M (2001) Fusion pathways of vesicles: a Brownian dynamics simulation. J Chem Phys 115(20):9547–9551

    Article  CAS  Google Scholar 

  107. Cooke IR, Kremer K, Deserno M (2005) Tunable generic model for fluid bilayer membranes. Phys Rev E Stat Nonlin Soft Matter Phys 72(1 Pt 1):011506

    Article  PubMed  Google Scholar 

  108. Noguchi H (2011) Solvent-free coarse-grained lipid model for large-scale simulations. J Chem Phys 134(5):055101

    Article  PubMed  Google Scholar 

  109. Wang ZJ, Frenkel D (2005) Modeling flexible amphiphilic bilayers: a solvent-free off-lattice Monte Carlo study. J Chem Phys 122(23):234711

    Article  PubMed  Google Scholar 

  110. Baumgartner A, Ho JS (1990) Crumpling of fluid vesicles. Phys Rev A 41(10):5747–5750

    Article  CAS  PubMed  Google Scholar 

  111. Ho JS, Baumgartner A (1990) Simulations of fluid self-avoiding membranes. Europhys Lett 12(4):295–300

    Article  Google Scholar 

  112. Kantor Y, Kardar M, Nelson DR (1986) Statistical mechanics of tethered surfaces. Phys Rev Lett 57(7):791–794

    Article  CAS  PubMed  Google Scholar 

  113. Ramakrishnan N, Kumar PBS, Ipsen JH (2010) Monte Carlo simulations of fluid vesicles with in-plane orientational ordering. Phys Rev E Stat Nonlin Soft Matter Phys 81(4):041922

    Article  CAS  PubMed  Google Scholar 

  114. Sreeja K, Ipsen JH, Kumar PS (2015) Monte Carlo simulations of fluid vesicles. J Phys Condens Matter 27(27):273104

    Article  CAS  PubMed  Google Scholar 

  115. Canham PB (1970) The minimum energy of bending as a possible explanation of the biconcave shape of the human red blood cell. J Theor Biol 26(1):61–81

    Article  CAS  PubMed  Google Scholar 

  116. Del Popolo MG, Ballone P (2008) Melting behavior of an idealized membrane model. J Chem Phys 128(2):024705. https://doi.org/10.1063/1.2804423

    Article  CAS  PubMed  Google Scholar 

  117. Kohyama T (2009) Simulations of flexible membranes using a coarse-grained particle-based model with spontaneous curvature variables. Physica A 388(17):3334–3344

    Article  CAS  Google Scholar 

  118. Noguchi H, Gompper G (2006) Meshless membrane model based on the moving least-squares method. Phys Rev E Stat Nonlin Soft Matter Phys 73(2):021903

    Article  PubMed  Google Scholar 

  119. Pasqua A, Maibaum L, Oster G, Fletcher DA, Geissler PL (2010) Large-scale simulations of fluctuating biological membranes. J Chem Phys 132(15):154107. https://doi.org/10.1063/1.3382349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Shiba H, Noguchi H (2011) Estimation of the bending rigidity and spontaneous curvature of fluid membranes in simulations. Phys Rev E Stat Nonlin soft Matter Phys 84(3 Pt 1):031926

    Article  PubMed  Google Scholar 

  121. Bond PJ, Sansom MS (2007) Bilayer deformation by the Kv channel voltage sensor domain revealed by self-assembly simulations. Proc Natl Acad Sci USA 104(8):2631–2636. https://doi.org/10.1073/pnas.0606822104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Delemotte L, Klein ML, Tarek M (2012) Molecular dynamics simulations of voltage-gated cation channels: insights on voltage-sensor domain function and modulation. Front Pharmacol 3:97. https://doi.org/10.3389/fphar.2012.00097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Maffeo C, Bhattacharya S, Yoo J, Wells D, Aksimentiev A (2012) Modeling and simulation of ion channels. Chem Rev 112(12):6250–6284. https://doi.org/10.1021/cr3002609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Treptow W, Marrink SJ, Tarek M (2008) Gating motions in voltage-gated potassium channels revealed by coarse-grained molecular dynamics simulations. J Phys Chem B 112(11):3277–3282. https://doi.org/10.1021/jp709675e

    Article  CAS  PubMed  Google Scholar 

  125. Yefimov S, van der Giessen E, Onck PR, Marrink SJ (2008) Mechanosensitive membrane channels in action. Biophys J 94(8):2994–3002. https://doi.org/10.1529/biophysj.107.119966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Braun AR, Lacy MM, Ducas VC, Rhoades E, Sachs JN (2014) Alpha-synuclein-induced membrane remodeling is driven by binding affinity, partition depth, and interleaflet order asymmetry. J Am Chem Soc 136(28):9962–9972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Fuhrmans M, Marrink SJ (2012) Molecular view of the role of fusion peptides in promoting positive membrane curvature. J Am Chem Soc 134(3):1543–1552. https://doi.org/10.1021/ja207290b

    Article  CAS  PubMed  Google Scholar 

  128. Ingolfsson HI, Melo MN, van Eerden FJ, Arnarez C, Lopez CA, Wassenaar TA, Periole X, de Vries AH, Tieleman DP, Marrink SJ (2014) Lipid organization of the plasma membrane. J Am Chem Soc 136(41):14554–14559. https://doi.org/10.1021/ja507832e

    Article  CAS  PubMed  Google Scholar 

  129. Koldso H, Shorthouse D, Helie J, Sansom MSP (2014) Lipid clustering correlates with membrane curvature as revealed by molecular simulations of complex lipid bilayers. PLoS Comput Biol 10(10):e1003911

    Article  PubMed  PubMed Central  Google Scholar 

  130. Lindau M, Hall BA, Chetwynd A, Beckstein O, Sansom MS (2012) Coarse-grain simulations reveal movement of the synaptobrevin C-terminus in response to piconewton forces. Biophys J 103(5):959–969. https://doi.org/10.1016/j.bpj.2012.08.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Risselada HJ, Kutzner C, Grubmuller H (2011) Caught in the act: visualization of SNARE-mediated fusion events in molecular detail. Chembiochem 12(7):1049–1055. https://doi.org/10.1002/cbic.201100020

    Article  CAS  PubMed  Google Scholar 

  132. Reynwar BJ, Illya G, Harmandaris VA, Muller MM, Kremer K, Deserno M (2007) Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447(7143):461–464. https://doi.org/10.1038/nature05840

    Article  CAS  PubMed  Google Scholar 

  133. Reynwar BJ, Deserno M (2011) Membrane-mediated interactions between circular particles in the strongly curved regime. Soft Matter 7(18):8567–8575

    Article  CAS  Google Scholar 

  134. Matthews R, Likos CN (2013) Dynamics of self-assembly of model viral capsids in the presence of a fluctuating membrane. J Phys Chem B 117(27):8283–8292. https://doi.org/10.1021/jp4037099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Ruiz-Herrero T, Hagan MF (2015) Simulations show that virus assembly and budding are facilitated by membrane microdomains. Biophys J 108(3):585–595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Lyman E, Pfaendtner J, Voth GA (2008) Systematic multiscale parameterization of heterogeneous elastic network models of proteins. Biophys J 95(9):4183–4192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Sinitskiy AV, Voth GA (2013) Coarse-graining of proteins based on elastic network models. Chem Phys 422:165–174

    Article  CAS  Google Scholar 

  138. Tirion MM (1996) Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys Rev Lett 77(9):1905–1908

    Article  CAS  PubMed  Google Scholar 

  139. Simunovic M, Srivastava A, Voth GA (2013) Linear aggregation of proteins on the membrane as a prelude to membrane remodeling. Proc Natl Acad Sci USA 110(51):20396–20401. https://doi.org/10.1073/pnas.1309819110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Dommersnes PG, Fournier JB (1999) N-body study of anisotropic membrane inclusions: Membrane mediated interactions and ordered aggregation. Eur Phys J B 12(1):9–12

    Article  CAS  Google Scholar 

  141. Saric A, Cacciuto A (2012) Fluid membranes can drive linear aggregation of adsorbed spherical nanoparticles. Phys Rev Lett 108(11):118101

    Article  PubMed  Google Scholar 

  142. Koltover I, Radler JO, Safinya CR (1999) Membrane mediated attraction and ordered aggregation of colloidal particles bound to giant phospholipid vesicles. Phys Rev Lett 82(9):1991–1994. https://doi.org/10.1103/Physrevlett.82.1991

    Article  CAS  Google Scholar 

  143. McDonald NA, Vander Kooi CW, Ohi MD, Gould KL (2015) Oligomerization but not membrane bending underlies the function of certain F-BAR proteins in cell motility and cytokinesis. Dev Cell 35(6):725–736. https://doi.org/10.1016/j.devcel.2015.11.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Traub LM (2015) F-BAR/EFC domain proteins: some assembly required. Dev Cell 35(6):664–666. https://doi.org/10.1016/j.devcel.2015.12.003

    Article  CAS  PubMed  Google Scholar 

  145. Bahrami AH, Lipowsky R, Weikl TR (2012) Tubulation and aggregation of spherical nanoparticles adsorbed on vesicles. Phys Rev Lett 109(18):188102

    Article  PubMed  Google Scholar 

  146. Saric A, Cacciuto A (2012) Mechanism of membrane tube formation induced by adhesive nanocomponents. Phys Rev Lett 109(18):188101

    Article  PubMed  Google Scholar 

  147. Simunovic M, Voth GA (2015) Membrane tension controls the assembly of curvature-generating proteins. Nat Commun 6:7219. https://doi.org/10.1038/ncomms8219

    Article  CAS  PubMed  Google Scholar 

  148. Shi Z, Baumgart T (2015) Membrane tension and peripheral protein density mediate membrane shape transitions. Nat Commun 6:5974. https://doi.org/10.1038/ncomms6974

    Article  CAS  PubMed  Google Scholar 

  149. Renard HF, Simunovic M, Lemiere J, Boucrot E, Garcia-Castillo MD, Arumugam S, Chambon V, Lamaze C, Wunder C, Kenworthy AK, Schmidt AA, McMahon HT, Sykes C, Bassereau P, Johannes L (2015) Endophilin-A2 functions in membrane scission in clathrin-independent endocytosis. Nature 517(7535):493–496. https://doi.org/10.1038/nature14064

    Article  CAS  PubMed  Google Scholar 

  150. Noguchi H (2015) Membrane tubule formation by banana-shaped proteins with or without intermediate network structure. Sci Rep 6:20935

    Article  Google Scholar 

  151. Noguchi H (2014) Two- or three-step assembly of banana-shaped proteins coupled with shape transformation of lipid membranes. EPL 108(4):48001

    Article  Google Scholar 

  152. Ramakrishnan N, Sunil Kumar PB, Ipsen JH (2013) Membrane-mediated aggregation of curvature-inducing nematogens and membrane tubulation. Biophys J 104(5):1018–1028. https://doi.org/10.1016/j.bpj.2012.12.045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Simunovic M, Mim C, Marlovits TC, Resch G, Unger VM, Voth GA (2013) Protein-mediated transformation of lipid vesicles into tubular networks. Biophys J 105(3):711–719. https://doi.org/10.1016/j.bpj.2013.06.039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Yin Y, Arkhipov A, Schulten K (2009) Simulations of membrane tubulation by lattices of amphiphysin N-BAR domains. Structure 17(6):882–892. https://doi.org/10.1016/j.str.2009.03.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Cui H, Mim C, Vazquez FX, Lyman E, Unger VM, Voth GA (2013) Understanding the role of amphipathic helices in N-BAR domain driven membrane remodeling. Biophys J 104(2):404–411. https://doi.org/10.1016/j.bpj.2012.12.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Prevost C, Zhao H, Manzi J, Lemichez E, Lappalainen P, Callan-Jones A, Bassereau P (2015) IRSp53 senses negative membrane curvature and phase separates along membrane tubules. Nat Commun 6:8529. https://doi.org/10.1038/ncomms9529

    Article  CAS  PubMed  Google Scholar 

  157. McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12(8):517–533. https://doi.org/10.1038/nrm3151

    Article  CAS  PubMed  Google Scholar 

  158. Fotin A, Cheng Y, Sliz P, Grigorieff N, Harrison SC, Kirchhausen T, Walz T (2004) Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432(7017):573–579. https://doi.org/10.1038/nature03079

    Article  CAS  PubMed  Google Scholar 

  159. Kirchhausen T (2000) Clathrin. Annu Rev Biochem 69:699–727. https://doi.org/10.1146/annurev.biochem.69.1.699

    Article  CAS  PubMed  Google Scholar 

  160. den Otter WK, Renes MR, Briels WJ (2010) Asymmetry as the key to clathrin cage assembly. Biophys J 99(4):1231–1238. https://doi.org/10.1016/j.bpj.2010.06.011

    Article  CAS  Google Scholar 

  161. den Otter WK, Renes MR, Briels WJ (2010) Self-assembly of three-legged patchy particles into polyhedral cages. J Phys Condens Matter 22(10):104103

    Article  Google Scholar 

  162. Matthews R, Likos CN (2012) Influence of fluctuating membranes on self-assembly of patchy colloids. Phys Rev Lett 109(17):178302

    Article  PubMed  Google Scholar 

  163. Matthews R, Likos CN (2013) Structures and pathways for clathrin self-assembly in the bulk and on membranes. Soft Matter 9(24):5794–5806

    Article  CAS  Google Scholar 

  164. Ramakrishnan N, Sunil Kumar PB, Radhakrishnan R (2014) Mesoscale computational studies of membrane bilayer remodeling by curvature-inducing proteins. Phys Rep 543(1):1–60. https://doi.org/10.1016/j.physrep.2014.05.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Heinrich V, Svetina S, Zeks B (1993) Nonaxisymmetric vesicle shapes in a generalized bilayer-couple model and the transition between oblate and prolate axisymmetrical shapes. Phys Rev E 48(4):3112–3123. https://doi.org/10.1103/Physreve.48.3112

    Article  CAS  Google Scholar 

  166. Iglic A, Kralj-Iglic V, Bozic B, Bobrowska-Hagerstrand M, Isomaa B, Hagerstrand H (2000) Torocyte shapes of red blood cell daughter vesicles. Bioelectrochemistry 52(2):203–211

    Article  CAS  PubMed  Google Scholar 

  167. Miao L, Seifert U, Wortis M, Dobereiner HG (1994) Budding transitions of fluid-bilayer vesicles: the effect of area-difference elasticity. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Top 49(6):5389–5407

    CAS  Google Scholar 

  168. Svetina S, Zeks B (1989) Membrane bending energy and shape determination of phospholipid-vesicles and red blood-cells. Eur Biophys J 17(2):101–111

    Article  CAS  PubMed  Google Scholar 

  169. Auth T, Gompper G (2009) Budding and vesiculation induced by conical membrane inclusions. Phys Rev E 80(3):031901

    Article  Google Scholar 

  170. Bozic B, Kralj-Iglic V, Svetina S (2006) Coupling between vesicle shape and lateral distribution of mobile membrane inclusions. Phys Rev E 73(4):041915

    Article  Google Scholar 

  171. Kabaso D, Bobrovska N, Gozdz W, Gov N, Kralj-Iglic V, Veranic P, Iglic A (2012) On the role of membrane anisotropy and BAR proteins in the stability of tubular membrane structures. J Biomech 45(2):231–238. https://doi.org/10.1016/j.jbiomech.2011.10.039

    Article  PubMed  Google Scholar 

  172. Kralj-Iglic V, Hagerstrand H, Veranic P, Jezernik K, Babnik B, Gauger DR, Iglic A (2005) Amphiphile-induced tubular budding of the bilayer membrane. Eur Biophys J 34(8):1066–1070. https://doi.org/10.1007/s00249-005-0481-0

    Article  CAS  PubMed  Google Scholar 

  173. Mukhopadhyay R, Lim HWG, Wortis M (2002) Echinocyte shapes: bending, stretching, and shear determine spicule shape and spacing. Biophys J 82(4):1756–1772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Su YC, Chen JZ (2015) A model of vesicle tubulation and pearling induced by adsorbing particles. Soft Matter 11(20):4054–4060. https://doi.org/10.1039/c5sm00565e

    Article  CAS  PubMed  Google Scholar 

  175. Ayton GS, McWhirter JL, Voth GA (2006) A second generation mesoscopic lipid bilayer model: connections to field-theory descriptions of membranes and nonlocal hydrodynamics. J Chem Phys 124(6):64906. https://doi.org/10.1063/1.2165194

    Article  CAS  PubMed  Google Scholar 

  176. Ayton GS, McWhirter JL, McMurtry P, Voth GA (2005) Coupling field theory with continuum mechanics: a simulation of domain formation in giant unilamellar vesicles. Biophys J 88(6):3855–3869. https://doi.org/10.1529/biophysj.105.059436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Hoover WG, Hoover CG (2003) Links between microscopic and macroscopic fluid mechanics. Mol Phys 101(11):1559–1573. https://doi.org/10.1080/0026897021000026647

    Article  CAS  Google Scholar 

  178. Ayton GS, Blood PD, Voth GA (2007) Membrane remodeling from N-BAR domain interactions: insights from multi-scale simulation. Biophys J 92(10):3595–3602. https://doi.org/10.1529/biophysj.106.101709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Boucrot E, Pick A, Camdere G, Liska N, Evergren E, McMahon HT, Kozlov MM (2012) Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 149(1):124–136. https://doi.org/10.1016/j.cell.2012.01.047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Ayton GS, Lyman E, Krishna V, Swenson RD, Mim C, Unger VM, Voth GA (2009) New insights into BAR domain-induced membrane remodeling. Biophys J 97(6):1616–1625. https://doi.org/10.1016/j.bpj.2009.06.036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Lin LC, Brown FL (2004) Brownian dynamics in Fourier space: membrane simulations over long length and time scales. Phys Rev Lett 93(25):256001

    Article  PubMed  Google Scholar 

  182. Lin LCL, Brown FLH (2005) Dynamic simulations of membranes with cytoskeletal interactions. Phys Rev E 72(1):Artn 011910. https://doi.org/10.1103/Physreve.72.011910

    Article  Google Scholar 

  183. Ayton GS, Voth GA (2010) Multiscale simulation of protein mediated membrane remodeling. Semin Cell Dev Biol 21(4):357–362. https://doi.org/10.1016/j.semcdb.2009.11.011

    Article  CAS  PubMed  Google Scholar 

  184. Chang R, Ayton GS, Voth GA (2005) Multiscale coupling of mesoscopic- and atomistic-level lipid bilayer simulations. J Chem Phys 122(24):244716. https://doi.org/10.1063/1.1931651

    Article  CAS  PubMed  Google Scholar 

  185. Lyman E, Cui H, Voth GA (2011) Reconstructing protein remodeled membranes in molecular detail from mesoscopic models. Phys Chem Chem Phys 13(22):10430–10436. https://doi.org/10.1039/c0cp02978e

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Liu P, Voth GA (2007) Smart resolution replica exchange: an efficient algorithm for exploring complex energy landscapes. J Chem Phys 126(4):045106. https://doi.org/10.1063/1.2408415

    Article  CAS  PubMed  Google Scholar 

  187. Sigurdsson JK, Brown FLH, Atzberger PJ (2013) Hybrid continuum-particle method for fluctuating lipid bilayer membranes with diffusing protein inclusions. J Comput Phys 252:65–85

    Article  CAS  Google Scholar 

  188. De Nicola A, Zhao Y, Kawakatsu T, Roccatano D, Milano G (2011) Hybrid particle-field coarse-grained models for biological phospholipids. J Chem Theory Comput 7(9):2947–2962. https://doi.org/10.1021/Ct200132n

    Article  PubMed  Google Scholar 

  189. De Nicola A, Zhao Y, Kawakatsu T, Roccatano D, Milano G (2012) Validation of a hybrid MD-SCF coarse-grained model for DPPC in non-lamellar phases. Theor Chem Accounts 131(3):Artn 1167. https://doi.org/10.1007/S00214-012-1167-1

    Article  Google Scholar 

  190. Sarukhanyan E, De Nicola A, Roccatano D, Kawakatsu T, Milano G (2014) Spontaneous insertion of carbon nanotube bundles inside biomembranes: a hybrid particle-field coarse-grained molecular dynamics study. Chem Phys Lett 595:156–166. https://doi.org/10.1016/J.Cplett.2014.01.057

    Article  Google Scholar 

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  1. Department of Chemistry, Institute for Biophysical Dynamics, and James Franck Institute, The University of Chicago, Chicago, IL, USA

    Mijo Simunovic & Gregory A. Voth

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  1. PhysicoChimie Curie (UMR CNRS 168), Institut Curie, Paris, France

    Patricia Bassereau

  2. PhysicoChimie Curie (UMR CNRS 168), Institut Curie, Paris, France

    Pierre Sens

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Simunovic, M., Voth, G.A. (2018). Simulating Protein-Mediated Membrane Remodeling at Multiple Scales. In: Bassereau, P., Sens, P. (eds) Physics of Biological Membranes. Springer, Cham. https://doi.org/10.1007/978-3-030-00630-3_14

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