Membrane Sculpting by F-BAR Domains Studied by Molecular Dynamics Simulations

PLoS Computational Biology

Volumn 9, Issue 1, 2013, Pages

  Yu, Hang ^a,b   Schulten, Klaus ^a,b,c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; ELECTRON MICROSCOPES; ELECTRON MICROSCOPY; MOLECULAR DYNAMICS;

CELLULAR MEMBRANES; CELLULAR MORPHOGENESIS; COARSE-GRAINED; DYNAMICS SIMULATION; EUKARYOTIC CELLS; IN-VITRO; PERIPHERAL PROTEINS; PLANAR MEMBRANES; REGULAR LATTICE; TUBULAR MEMBRANES;

PROTEINS;

AMPHIPHYSIN; MEMBRANE PROTEIN; PROTEIN BIN; PROTEIN RVS; UNCLASSIFIED DRUG;

ARTICLE; CELL MATURATION; CELL MEMBRANE; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; IN VITRO STUDY; MATHEMATICAL ANALYSIS; MEMBRANE SCULPTING; MEMBRANE VESICLE; MOLECULAR DYNAMICS; PLASTICITY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; SIMULATION;

EID: 84873517639     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002892     Document Type: Article

References (86)

1. Marsh M, McMahon HT, (1999) The structural era of endocytosis. Science 285: 215-220.
2. McMahon HT, Gallop JL, (2005) Membrane curvature and mechanisms of dynamic cell membrane remodeling. Nature 438: 590-596.
3. Lecuit T, Pilot F, (2003) Developmental control of cell morphogenesis: a focus on membrane growth. Nature Cell Biology 5: 103-108.
4. Cho W, Stahelin RV, (2005) Membrane-protein interactions in cell signaling and membrane trafficking. Annual Review of Biophysics and Biomolecular Structure 34: 119-151.
5. Kirchhausen T, (2000) Clathrin. Annual Review of Biochemistry 69: 699-727.
6. McMahon HT, Hills IG, (2004) COP and clathrin-coated vesicle budding: different pathways, common approaches. Current Opinion in Cell Biology 16: 379-391.
7. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJG, et al. (2004) BAR domains as sensors of membrane curvature: The amphiphysin BAR structure. Science 303: 495-499.
8. Wiggins P, Phillips R, (2005) Membrane-protein interactions in mechanosensitive channels. Biophysical Journal 88: 880-902.
9. Blood PD, Voth GA, (2006) Direct observation of Bin/amphiphysin/Rvs (BAR) domain-induced membrane curvature by means of molecular dynamics simulations. Proceedings of the National Academy of Sciences USA 103: 15068-15072.
10. Cho W, Stahelin RV, (2006) Membrane binding and subcellular targeting of C2 domains. Biochimica et Biophysica Acta 1761: 838-849.
11. Chandler D, Hsin J, Harrison CB, Gumbart J, Schulten K, (2008) Intrinsic curvature properties of photosynthetic proteins in chromatophores. Biophysical Journal 95: 2822-2836.
12. Blood PD, Swenson RD, Voth GA, (2008) Factors influencing local membrane curvature induction by N-BAR domains as revealed by molecular dynamics simulations. Biophysical Journal 95: 1866-1876.
13. Shimada A, Niwa H, Tsujita K, Suetsugu S, Nitta K, et al. (2007) Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129: 761-772.
14. Wang Q, Navarro MVAS, Peng G, Molinelli E, Lin Goh S, et al. (2009) Molecular mechanism of membrane constriction and tubulation mediated by the f-bar protein pacsin/syndapin. Proceedings of the National Academy of Sciences 106: 12700-12705.
15. Kozlov MM, (2010) Biophysics: Joint effort bends membrane. Nature 463: 439-440.
16. McMahon HT, Kozlov MM, Martens S, (2010) Membrane curvature in synaptic vesicle fusion and beyond. Cell 140: 601-605.
17. Roberts-Galbraith RH, Gould KL, (2010) Setting the F-BAR: functions and regulation of the F-BAR protein family. Cell Cycle 9: 4091-7.
18. Uezu A, Umeda K, Tsujita K, Suetsugu S, Takenawa T, et al. (2011) Characterization of the EFC/F-BAR domain protein, FCHO2. Genes Cells 16: 868-78.
19. Karotki L, Huiskonen JT, Stefan CJ, Ziolkowska NE, Roth R, et al. (2011) Eisosome proteins assemble into a membrane scaffold. J Cell Biol 195: 889-902.
20. Chen Y, Sheng R, Kllberg M, Silkov A, Tun M, et al. (2012) Genome-wide functional annotation of dual-specificity protein- and lipid-binding modules that regulate protein interactions. Molecular Cell 46: 226-237.
21. Mim C, Cui H, Gawronski-Salerno JA, Frost A, Lyman E, et al. (2012) Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149: 137-145.
22. Boucrot E, Pick A, Camdere G, Liska N, Evergren E, et al. (2012) Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 149: 124-136.
23. Mim C, Unger VM, (2012) Membrane curvature and its generation by BAR proteins. Trends in Biochemical Sciences 37: 526-33.
24. Yin Y, Arkhipov A, Schulten K, (2009) Simulations of membrane tubulation by lattices of amphiphysin N-BAR domains. Structure 17: 882-892.
25. Yin Y, Arkhipov A, Schulten K (2010) Multi-scale simulations of membrane sculpting by N-BAR domains. In: Biggin P, Sansom M, editors. Molecular Simulations and Biomembranes: From Biophysics to Function. Cambridge: Royal Society of Chemistry. pp. 146-176.
26. Wu M, Huang B, Graham M, Raimondi A, Heuser JE, et al. (2010) Coupling between clathrin-dependent endocytic budding and F-BAR-dependent tubulation in a cell-free system. Nat Cell Biol 12: 902-908.
27. Chen Y, Aardema J, Misra A, Corey SJ, (2012) Bar proteins in cancer and blood disorders. Int J Biochem Mol Biol 3: 198-208.
28. Casal E, Federici L, Zhang W, Fernandez-Recio J, Priego EM, et al. (2006) The crystal structure of the BAR domain from human Bin1/Amphiphysin II and its implications for molecular recognition. Biochemistry 45: 12917-12928.
29. Lee E, Marcucci M, Daniell L, Pypaert M, Weisz OA, et al. (2007) Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297: 1193-1196.
30. Henne WM, Kent HM, Ford MGJ, Hegde BG, Daumke O, et al. (2007) Structure and Analysis of FCHo2 F-BAR Domain: A Dimerizing and Membrane Recruitment Module that Effects Membrane Curvature. Structure 15: 1-14.
31. Ahmed S, Bu W, Lee RTC, Maurer-Stroh S, Goh WI, (2010) F-BAR domain proteins: Families and function. Communicative & Integrative Biology 3: 116-121.
32. Itoh T, Erdmann KS, Roux A, Habermann B, Werner H, et al. (2005) Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Developmental Cell 9: 791-804.
33. He Y, Liwo A, Weinstein H, Scheraga HA, (2011) PDZ binding to the BAR domain of PICK1 is elucidated by coarse-grained molecular dynamics. J Mol Biol 405: 298-314.
34. Ren G, Vajjhala P, Lee JS, Winsor B, Munn AL, (2006) The BAR domain proteins: Molding membranes in fission, fusion, and phagy. Microbiology and molecular biology reviews 70: 37-120.
35. Zimmerberg J, Kozlov MM, (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7: 9-19.
36. Mattila PK, Pykäläinen A, Saarikangas J, Paavilainen VO, Vihinen H, et al. (2007) Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain-like mechanism. Journal of Cell Biology 176: 953-964.
37. Frost A, De Camilli P, Unger VM, (2007) F-BAR proteins join the BAR family fold. Structure 15: 751-3.
38. Frost A, Perera R, Roux A, Spasov K, Destaing O, et al. (2008) Structural basis of membrane invagination by F-BAR domains. Cell 132: 807-817.
39. Weissenhorn W, (2005) Crystal structure of the endophilin-A1 BAR domain. Journal of Molecular Biology 351: 653-661.
40. Millard TH, Bompard G, Heung MY, Dafforn TR, Scott DJ, et al. (2005) Structural basis of filopodia formation induced by the IRSp53/MIM homology domain of human IRSp53. EMBO Journal 24: 240-250.
41. Farsad K, Camilli PD, (2003) Mechanisms of membrane deformation. Current Opinion in Cell Biology 15: 372-381.
42. Habermann B, (2004) The BAR-domain family of proteins: a case of bending and binding? EMBO reports 5: 250-255.
43. Farsad K, Ringstad N, Takei K, Floyd SR, Rose K, et al. (2001) Generation of high curvature membranes mediated by direct endophilin bilayer interactions. Journal of Cell Biology 155: 193-200.
44. Ford MG, Mills IG, Peter BJ, Vallis Y, Praefcke GJ, et al. (2002) Curvature of clathrin-coated pits driven by epsin. Nature 419: 361-366.
45. Gallop JL, Jao CC, Kent HM, Butler PJ, Evans PR, et al. (2006) Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO Journal 25: 2898-2910.
46. Cui H, Ayton GS, Voth GA, (2009) Membrane binding by the endophilin N-BAR domain. Biophysical Journal 97: 2746-2753.
47. Takei K, Slepnev VI, Haucke V, De Camilli P, (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1: 33-39.
48. Klein ML, Shinoda W, (2008) Large-scale molecular dynamics simulations of self-assembling systems. Science 321: 798-800.
49. Reynwar BJ, Illya G, Harmandaris VA, Müller MM, Kremer K, et al. (2007) Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447: 461-464.
50. Han DS, Golebiewska U, Stolzenberg S, Scarlata SF, Weinstein H, (2011) A dynamic model of membrane-bound phospholipase c2 activation by g subunits. Molecular Pharmacology 80: 434-445.
51. Mondal J, Zhu X, Cui Q, Yethiraj A, (2010) Sequence-dependent interaction of β-peptides with membranes. Journal of Physical Chemistry B 114: 13585-13592.
52. Yoo J, Cui Q, (2009) Curvature generation and pressure profile modulation in membrane by lysolipids: Insights from coarse-grained simulations. Biophys J 97: 2267-2276.
53. Mondal S, Khelashvili G, Shan J, Andersen OS, Weinstein H, (2011) Quantitative modeling of membrane deformations by multihelical membrane proteins: application to G-protein coupled receptors. Biophysical Journal 101: 2092-2101.
54. Miyashita N, Straub JE, Thirumalai D, (2009) Structures of-amyloid peptide 140, 142, and 155the 672726 fragment of appin a membrane environment with implications for interactions with-secretase. J Am Chem Soc 131: 17843-17852.
55. Reynwar BJ, Deserno M, (2011) Membrane-mediated interactions between circular particles in the strongly curved regime. Soft Matter 7: 8567-8575.
56. Illya G, Deserno M, (2008) Coarse-grained simulation studies of peptide-induced pore formation. Biophys J 95: 4163-4173.
57. Loverde SM, Pantano DA, Christian DA, Mahmud A, Klein ML, et al. (2011) Curvature, rigidity, and pattern formation in functional polymer micelles and vesicles from dynamic visualization to molecular simulation. Current Opinion in Solid State and Materials Science 15: 277-284.
58. Ohkubo YZ, Pogorelov TV, Arcario MJ, Christensen GA, Tajkhorshid E, (2012) Accelerating membrane insertion of peripheral proteins with a novel membrane mimetic model. Biophysical Journal 102: 2130-2139.
59. Lyman E, Cui H, Voth GA, (2010) Water under the BAR. Biophysical Journal 99: 1783-1790.
60. Arkhipov A, Yin Y, Schulten K, (2008) Four-scale description of membrane sculpting by BAR domains. Biophysical Journal 95: 2806-2821.
61. Arkhipov A, Yin Y, Schulten K, (2009) Membrane-bending mechanism of amphiphysin N-BAR domains. Biophysical Journal 97: 2727-2735.
62. Lyman E, Cui H, Voth GA, (2011) Reconstructing protein remodeled membranes in molecular detail from mesoscopic models. Phys Chem Chem Phys 13: 10430-6.
63. Campelo F, McMahon HT, Kozlov MM, (2008) The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophysical Journal 95: 2325-2339.
64. Khelashvili G, Harries D, Weinstein H, (2009) Modeling membrane deformations and lipid demixing upon protein-membrane interaction: The bar dimer adsorption. Biophys J 97: 1626-1635.
65. Perutkova S, Kralj-Iglic V, Frank M, Iglic A, (2010) Mechanical stability of membrane nanotubular protrusions influenced by attachment of flexible rod-like proteins. Journal of Biomechanics 43: 1612-1617.
66. Kaback H, Smirnova I, Kasho V, Nie Y, Zhou Y, (2011) The alternating access transport mechanism in LacY. Journal of Molecular Biology 239: 85-93.
67. Sorre B, Callan-Jones A, Manzi J, Goud B, Prost J, et al. (2012) Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proc Natl Acad Sci U S A 109: 173-8.
68. Martens S, McMahon HT, (2008) Mechanisms of membrane fusion: disparate players and common principles. Nature Reviews Molecular Cell Biology 9: 543-556.
69. Kralj-Iglic V, Babnik B, Gauger D, May S, Iglic A, (2006) Quadrupolar ordering of phospholipid molecules in narrow necks of phospholipid vesicles. Journal of Statistical Physics 125: 727-752.
70. Iglic A, Slivnik T, Kralj-Iglic V, (2007) Elastic properties of biological membranes influenced by attached proteins. Journal of Biomechanics 40: 2492-2500.
71. Helfrich W, (1973) Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch 28: 693-703.
72. Duwe H, Kaes J, Sackmann E, (1990) Bending elastic moduli of lipid bilayers: modulation by solutes. J Phys France 51: 945-961.
73. Goetz R, Gompper G, Lipowsky R, (1999) Mobility and elasticity of self-assembled membranes. Phys Rev Lett 82: 221-224.
74. Lindahl E, Edholm O, (2000) Mesoscopic undulations and thickness fluctuations in lipid bilayers from molecular dynamics simulations. Biophysical Journal 79: 426-433.
75. Harmandaris VA, Deserno M, (2006) A novel method for measuring the bending rigidity of model lipid membranes by simulating tethers. Journal of Chemical Physics 125: 204905.
76. Tsujita K, Suetsugu S, Sasaki N, Furutani M, Oikawa T, et al. (2006) Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J Cell Biol 172: 269-79.
77. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. Journal of Computational Chemistry 26: 1781-1802.
78. Humphrey W, Dalke A, Schulten K, (1996) VMD - Visual Molecular Dynamics. Journal of Molecular Graphics 14: 33-38.
79. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML, (1983) Comparison of simple potential functions for simulating liquid water. Journal of Chemical Physics 79: 926-935.
80. MacKerell AD Jr, Bashford D, Bellott M, Dunbrack JRL, Evanseck J, et al. (1992) Self-consistent parameterization of biomolecules for molecular modeling and condensed phase simulations. FASEB Journal 6: A143-A143.
81. MacKerell AD Jr, Bashford D, Bellott M, Dunbrack RL Jr, Evanseck JD, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. Journal of Physical Chemistry B 102: 3586-3616.
82. Martyna GJ, Tobias DJ, Klein ML, (1994) Constant pressure molecular dynamics algorithms. Journal of Chemical Physics 101: 4177-4189.
83. Darden TA, Toukmaji A, Pedersen LG, (1997) Long-range electrostatic effects in biomolecular simulations. Journal de Chimie Physique et de Physico-Chimie Biologique 94: 1346-1364.
84. Arkhipov A, Freddolino PL, Schulten K, (2006) Stability and dynamics of virus capsids described by coarse-grained modeling. Structure 14: 1767-1777.
85. Wells D, Abramkina V, Aksimentiev A, (2007) Exploring transmembrane transport through alpha-hemolysin with grid-steered molecular dynamics. Journal of Chemical Physics 127: 125101-125101-10.
86. Roberts E, Eargle J, Wright D, Luthey-Schulten Z, (2006) MultiSeq: Unifying sequence and structure data for evolutionary analysis. BMC Bioinformatics 7: 382.