Protein-mediated transformation of lipid vesicles into tubular networks

Biophysical Journal

Volumn 105, Issue 3, 2013, Pages 711-719

  Simunovic, Mijo ^a   Mim, Carsten ^b   Marlovits, Thomas C ^c,d   Resch, Guenter ^c,d   Unger, Vinzenz M ^b   Voth, Gregory A ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^d ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOSOME; MEMBRANE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; DIFFUSION; LIPID BILAYER; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; DIFFUSION; LIPID BILAYERS; LIPOSOMES; MEMBRANE PROTEINS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84881473887     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.06.039     Document Type: Article

References (45)

1. B. Alberts Molecular Biology of the Cell 4th ed. 2002 Garland Science New York
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. G. Ren, and P. Vajjhala A.L. Munn The BAR domain proteins: molding membranes in fission, fusion, and phagy Microbiol. Mol. Biol. Rev. 70 2006 37 120
5. C. Mim, and V.M. Unger Membrane curvature and its generation by BAR proteins Trends Biochem. Sci. 37 2012 526 533
6. B. Qualmann, D. Koch, and M.M. Kessels Let's go bananas: revisiting the endocytic BAR code EMBO J. 30 2011 3501 3515
7. A. Frost, V.M. Unger, and P. De Camilli The BAR domain superfamily: membrane-molding macromolecules Cell 137 2009 191 196
8. B.J. Peter, and H.M. Kent H.T. McMahon BAR domains as sensors of membrane curvature: the amphiphysin BAR structure Science 303 2004 495 499
9. C. Mim, and H. Cui V.M. Unger Structural basis of membrane bending by the N-BAR protein endophilin Cell 149 2012 137 145
10. E. Lee, and M. Marcucci P. De Camilli Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle Science 297 2002 1193 1196
11. A. Frost, and R. Perera V.M. Unger Structural basis of membrane invagination by F-BAR domains Cell 132 2008 807 817
12. J.R. van Weering, and R.B. Sessions P.J. Cullen Molecular basis for SNX-BAR-mediated assembly of distinct endosomal sorting tubules EMBO J. 31 2012 4466 4480
13. P.K. Mattila, and A. Pykäläinen P. Lappalainen Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain-like mechanism J. Cell Biol. 176 2007 953 964
14. F. Campelo, H.T. McMahon, and M.M. Kozlov The hydrophobic insertion mechanism of membrane curvature generation by proteins Biophys. J. 95 2008 2325 2339
15. E. Boucrot, and A. Pick M.M. Kozlov Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains Cell 149 2012 124 136
16. Q. Wang, and M.V. Navarro H. Sondermann Molecular mechanism of membrane constriction and tubulation mediated by the F-BAR protein Pacsin/Syndapin Proc. Natl. Acad. Sci. USA 106 2009 12700 12705
17. B. Sorre, and A. Callan-Jones A. Roux Nature of curvature coupling of amphiphysin with membranes depends on its bound density Proc. Natl. Acad. Sci. USA 109 2012 173 178
18. G.S. Ayton, and G.A. Voth Multiscale simulation of protein mediated membrane remodeling Semin. Cell Dev. Biol. 21 2010 357 362
19. G.S. Ayton, and G.A. Voth Systematic multiscale simulation of membrane protein systems Curr. Opin. Struct. Biol. 19 2009 138 144
20. G.S. Ayton, and E. Lyman G.A. Voth New insights into BAR domain-induced membrane remodeling Biophys. J. 97 2009 1616 1625
21. G.S. Ayton, J.L. McWhirter, and G.A. Voth A second generation mesoscopic lipid bilayer model: connections to field-theory descriptions of membranes and nonlocal hydrodynamics J. Chem. Phys. 124 2006 64906
22. A. Srivastava, and G.A. Voth Hybrid approach for highly coarse-grained lipid bilayer models J. Chem. Theory Comput. 9 2013 750 765
23. W.G. Noid, and J.W. Chu H.C. Andersen The multiscale coarse-graining method. I. A rigorous bridge between atomistic and coarse-grained models J. Chem. Phys. 128 2008 244114
24. S. Izvekov, and G.A. Voth A multiscale coarse-graining method for biomolecular systems J. Phys. Chem. B 109 2005 2469 2473
25. G.S. Ayton, E. Lyman, and G.A. Voth Hierarchical coarse-graining strategy for protein-membrane systems to access mesoscopic scales Faraday Discuss. 144 2010 347 357 discussion 445-381
26. E. Lyman, H.S. Cui, and G.A. Voth Reconstructing protein remodeled membranes in molecular detail from mesoscopic models Phys. Chem. Chem. Phys. 13 2011 10430 10436
27. S. Plimpton Fast parallel algorithms for short-range molecular-dynamics J. Comput. Phys. 117 1995 1 19
28. F. Fraternali, C.D. Lorenz, and G. Marcelli On the estimation of the curvatures and bending rigidity of membrane networks via a local maximum-entropy approach J. Comput. Phys. 231 2012 528 540
29. W.G. Hoover, and C.G. Hoover Links between microscopic and macroscopic fluid mechanics Mol. Phys. 101 2003 1559 1573
30. J.L. McWhirter, G. Ayton, and G.A. Voth Coupling field theory with mesoscopic dynamical simulations of multicomponent lipid bilayers Biophys. J. 87 2004 3242 3263
31. C. Suloway, and J. Pulokas B. Carragher Automated molecular microscopy: the new Leginon system J. Struct. Biol. 151 2005 41 60
32. J.R. Kremer, D.N. Mastronarde, and J.R. McIntosh Computer visualization of three-dimensional image data using IMOD J. Struct. Biol. 116 1996 71 76
33. C.A. Schneider, W.S. Rasband, and K.W. Eliceiri NIH Image to ImageJ: 25 years of image analysis Nat. Methods 9 2012 671 675
34. G. Khelashvili, D. Harries, and H. Weinstein Modeling membrane deformations and lipid demixing upon protein-membrane interaction: the BAR dimer adsorption Biophys. J. 97 2009 1626 1635
35. H. Aranda-Espinoza, and Y. Chen D.A. Weitz Electrostatic repulsion of positively charged vesicles and negatively charged objects Science 285 1999 394 397
36. Y. Chen, and P. Nelson Charge-reversal instability in mixed bilayer vesicles Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 62 2000 2608 2619
37. A. Sarić, and A. Cacciuto Fluid membranes can drive linear aggregation of adsorbed spherical nanoparticles Phys. Rev. Lett. 108 2012 118101
38. N. Ramakrishnan, P.B. Sunil Kumar, and J.H. Ipsen Membrane-mediated aggregation of curvature-inducing nematogens and membrane tubulation Biophys. J. 104 2013 1018 1028
39. H. Cui, and C. Mim G.A. Voth Understanding the role of amphipathic helices in N-BAR domain driven membrane remodeling Biophys. J. 104 2013 404 411
40. D. Axelrod Lateral motion of membrane proteins and biological function J. Membr. Biol. 75 1983 1 10
41. M.K. Doeven, and J.H. Folgering B. Poolman Distribution, lateral mobility and function of membrane proteins incorporated into giant unilamellar vesicles Biophys. J. 88 2005 1134 1142
42. Y.A. Domanov, and S. Aimon P. Bassereau Mobility in geometrically confined membranes Proc. Natl. Acad. Sci. USA 108 2011 12605 12610
43. M. Frick, K. Schmidt, and B.J. Nichols Modulation of lateral diffusion in the plasma membrane by protein density Curr. Biol. 17 2007 462 467
44. M.R. Horton, and F. Hofling T. Franosch Development of anomalous diffusion among crowding proteins Soft Matter 6 2010 2648 2656
45. P. Ramesh, and Y.F. Baroji P.M. Bendix FBAR syndapin 1 recognizes and stabilizes highly curved tubular membranes in a concentration dependent manner Sci. Rep. 3 2013 1565