Bud-Neck Scaffolding as a Possible Driving Force in ESCRT-Induced Membrane Budding

Biophysical Journal

Volumn 108, Issue 4, 2015, Pages 833-843

  Mercker, Moritz ^a   Marciniak Czochra, Anna ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ESCRT PROTEIN;

BIOLOGICAL MODEL; CELL MEMBRANE; CHEMISTRY; METABOLISM; ULTRASTRUCTURE;

CELL MEMBRANE; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; MODELS, BIOLOGICAL;

EID: 84923239956     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.12.040     Document Type: Article

References (78)

1. J.H. Hurley, and E. Boura B. Rózycki Membrane budding Cell 143 2010 875 887
2. T. Kirchhausen Three ways to make a vesicle Nat. Rev. Mol. Cell Biol. 1 2000 187 198
3. T. Wollert, and J.H. Hurley Molecular mechanism of multivesicular body biogenesis by ESCRT complexes Nature 464 2010 864 869
4. J.H. Hurley, and P.I. Hanson Membrane budding and scission by the ESCRT machinery: it's all in the neck Nat. Rev. Mol. Cell Biol. 11 2010 556 566
5. J.H. Hurley The ESCRT complexes Crit. Rev. Biochem. Mol. Biol. 45 2010 463 487
6. R.L. Williams, and S. Urbé The emerging shape of the ESCRT machinery Nat. Rev. Mol. Cell Biol. 8 2007 355 368
7. T.E. Rusten, T. Vaccari, and H. Stenmark Shaping development with ESCRTs Nat. Cell Biol. 14 2012 38 45
8. T. Wollert, and C. Wunder J.H. Hurley Membrane scission by the ESCRT-III complex Nature 458 2009 172 177
9. E. Boura, and B. Rózycki J.H. Hurley Solution structure of the ESCRT-I and -II supercomplex: implications for membrane budding and scission Structure 20 2012 874 886
10. T.R. Graham, and M.M. Kozlov Interplay of proteins and lipids in generating membrane curvature Curr. Opin. Cell Biol. 22 2010 430 436
11. J.R. Mayers, and A. Audhya Vesicle formation within endosomes: an ESCRT marks the spot Commun. Integr. Biol. 5 2012 50 56
12. M.S. Otegui, and R. Buono H. Roschzttardtz ESCRT-Dependent Sorting in Late Endosomes J. Šamaj, Endocytosis in plants 1st ed. 2012 Springer New York 249 270
13. M.S. Kostelansky, and C. Schluter J.H. Hurley Molecular architecture and functional model of the complete yeast ESCRT-I heterotetramer Cell 129 2007 485 498
14. Y.J. Im, and J.H. Hurley Integrated structural model and membrane targeting mechanism of the human ESCRT-II complex Dev. Cell 14 2008 902 913
15. M. Babst, and D.J. Katzmann S.D. Emr Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting Dev. Cell 3 2002 271 282
16. C. Yorikawa, and H. Shibata M. Maki Human CHMP6, a myristoylated ESCRT-III protein, interacts directly with an ESCRT-II component EAP20 and regulates endosomal cargo sorting Biochem. J. 387 2005 17 26
17. J.S. Rossman, and X. Jing R.A. Lamb Influenza virus M2 protein mediates ESCRT-independent membrane scission Cell 142 2010 902 913
18. N.W. Schmidt, and A. Mishra G.C.L. Wong Criterion for amino acid composition of defensins and antimicrobial peptides based on geometry of membrane destabilization J. Am. Chem. Soc. 133 2011 6720 6727
19. A.R. Braun, and E. Sevcsik J.N. Sachs α-Synuclein induces both positive mean curvature and negative Gaussian curvature in membranes J. Am. Chem. Soc. 134 2012 2613 2620
20. B. Rózycki, and E. Boura G. Hummer Membrane-elasticity model of Coatless vesicle budding induced by ESCRT complexes PLOS Comput. Biol. 8 2012 e1002736
21. E. Boura, and V. Ivanov J.H. Hurley Endosomal sorting complex required for transport (ESCRT) complexes induce phase-separated microdomains in supported lipid bilayers J. Biol. Chem. 287 2012 28144 28151
22. I. Fyfe, and A.L. Schuh A. Audhya Association of the endosomal sorting complex ESCRT-II with the Vps20 subunit of ESCRT-III generates a curvature-sensitive complex capable of nucleating ESCRT-III filaments J. Biol. Chem. 286 2011 34262 34270
23. Y.J. Im, and T. Wollert J.H. Hurley Structure and function of the ESCRT-II-III interface in multivesicular body biogenesis Dev. Cell 17 2009 234 243
24. N.W. Schmidt, and A. Mishra G.C.L. Wong Influenza virus A M2 protein generates negative Gaussian membrane curvature necessary for budding and scission J. Am. Chem. Soc. 135 2013 13710 13719
25. B.J. Reynwar, and G. Illya M. Deserno Aggregation and vesiculation of membrane proteins by curvature-mediated interactions Nature 447 2007 461 464
26. J. Gumbart, and Y. Wang K. Schulten Molecular dynamics simulations of proteins in lipid bilayers Curr. Opin. Struct. Biol. 15 2005 423 431
27. M. Hanulová, and M. Weiss Membrane-mediated interactions - a physico-chemical basis for protein sorting Mol. Membr. Biol. 29 2012 177 185
28. A. Šarić, and A. Cacciuto Mechanism of membrane tube formation induced by adhesive nanocomponents Phys. Rev. Lett. 109 2012 188101
29. J.M.A. Grime, and G.A. Voth Highly scalable and memory efficient ultra-coarse-grained molecular dynamics simulations J. Chem. Theory Comput. 10 2014 423 431
30. H. Ingolfsson, and C. Lopez S. Marrink The power of coarse-graining in biomolecular simulations Wiley Interdiscip. Rev. Comput. Mol. Sci. 4 2014 225 248
31. F.L.H. Brown Elastic modeling of biomembranes and lipid bilayers Annu. Rev. Phys. Chem. 59 2008 685 712
32. T. Baumgart, and S. Das J.T. Jenkins Membrane elasticity in giant vesicles with fluid phase coexistence Biophys. J. 89 2005 1067 1080
33. M. Mercker, and A. Marciniak-Czochra D. Hartmann Modeling and computing of deformation dynamics of inhomogeneous biological surfaces SIAM J. Appl. Math. 73 2013 1768 1792
34. W. Helfrich Elastic properties of lipid bilayers: theory and possible experiments Z. Naturforsch. C 28 1973 693 703
35. J. Cahn, and J. Hilliard Free energy of a nonuniform system. I. Interfacial free energy J. Chem. Phys. 28 1958 258 267
36. M. Mercker, and M. Ptashnyk W. Jäger A multiscale approach to curvature modulated sorting in biological membranes J. Theor. Biol. 301 2012 67 82
37. Reference deleted in proof.
38. Becker, R., M. Braack,⋯, B. Vexler. 2013. Gascoigne 3D - a finite element toolbox (http://www.gascoigne.uni-hd.de).
39. J. Zimmerberg, and M.M. Kozlov How proteins produce cellular membrane curvature Nat. Rev. Mol. Cell Biol. 7 2006 9 19
40. V. Kralj-Iglic, and V. Heinrich B. Zeks Free energy of closed membrane with anisotropic inclusions Eur. Phys. J. B 10 1999 5 8
41. M. Fosnaric, and K. Bohinc S. May The influence of anisotropic membrane inclusions on curvature elastic properties of lipid membranes J. Chem. Inf. Model. 45 2005 1652 1661
42. A. Iglic, and B. Babnik V. Kralj-Iglic On the role of anisotropy of membrane constituents in formation of a membrane neck during budding of a multicomponent membrane J. Biomech. 40 2007 579 585
43. C.M. Chen Theory for the bending rigidity of protein-coated lipid membranes Physica A 281 2000 41 50
44. T. Pott, and C. Gerbeaud P. Méléard Melittin modifies bending elasticity in an unexpected way Chem. Phys. Lipids 185 2015 99 108
45. E.I. Settles, and A.F. Loftus R. Parthasarathy The vesicle trafficking protein Sar1 lowers lipid membrane rigidity Biophys. J. 99 2010 1539 1545
46. A.F. Loftus, and S. Noreng R. Parthasarathy Robust measurement of membrane bending moduli using light sheet fluorescence imaging of vesicle fluctuations Langmuir 29 2013 14588 14594
47. M. Hu, J.J. Briguglio, and M. Deserno Determining the Gaussian curvature modulus of lipid membranes in simulations Biophys. J. 102 2012 1403 1410
48. H.-T. Jung, and S.Y. Lee J.A. Zasadzinski Gaussian curvature and the equilibrium among bilayer cylinders, spheres, and discs Proc. Natl. Acad. Sci. USA 99 2002 15318 15322
49. J.-M. Allain, and C. Storm J.-F. Joanny Fission of a multiphase membrane tube Phys. Rev. Lett. 93 2004 158104
50. T. Baumgart, S.T. Hess, and W.W. Webb Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension Nature 425 2003 821 824
51. S. Ramadurai, and R. Duurkens B. Poolman Lateral diffusion of membrane proteins: consequences of hydrophobic mismatch and lipid composition Biophys. J. 99 2010 1482 1489
52. J.L.A.N. Murk, and B.M. Humbel M.J. Kleijmeer Endosomal compartmentalization in three dimensions: implications for membrane fusion Proc. Natl. Acad. Sci. USA 100 2003 13332 13337
53. C. Wilhelm, and A. Cebers F. Gazeau Deformation of intracellular endosomes under a magnetic field Eur. Biophys. J. 32 2003 655 660
54. R. Gracià, and N. Bezlyepkina R. Dimova Effect of cholesterol on the rigidity of saturated and unsaturated membranes: fluctuation and electrodeformation analysis of giant vesicles Soft Matter 6 2010 1472 1482
55. Reference deleted in proof.
56. Reference deleted in proof.
57. Reference deleted in proof.
58. R. Lipowsky Spontaneous tubulation of membranes and vesicles reveals membrane tension generated by spontaneous curvature Faraday Discuss. 161 2013 305 331 discussion 419-459
59. L. Lipowsky Budding of membranes induced by intramembrane domains J. Phys. II France 2 1992 1825 1840
60. B.M. Pearse Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles Proc. Natl. Acad. Sci. USA 73 1976 1255 1259
61. R.J. Mashl, and R.F. Bruinsma Spontaneous-curvature theory of clathrin-coated membranes Biophys. J. 74 1998 2862 2875
62. U. Schmidt, G. Guigas, and M. Weiss Cluster formation of transmembrane proteins due to hydrophobic mismatching Phys. Rev. Lett. 101 2008 128104
63. C.D. Blanchette, and W.-C. Lin M.L. Longo Domain nucleation rates and interfacial line tensions in supported bilayers of ternary mixtures containing galactosylceramide Biophys. J. 94 2008 2691 2697
64. R. Parthasarathy, C.H. Yu, and J.T. Groves Curvature-modulated phase separation in lipid bilayer membranes Langmuir 22 2006 5095 5099
65. H. Wang, D. Hu, and P. Zhang Measuring the spontaneous curvature of bilayer membranes by molecular dynamics simulations Commun. Comput. Phys. 13 2013 1093 1106
66. Y. Yin, J. Yin, and J. Wu The second gradient operator and integral theorems for tensor fields on curved surfaces Appl. Math. Sci. 1 2007 1465 1484
67. D. Ni, Y. Yin, and H. Shi Equilibrium shape equation and geometrically permissible condition for two-component lipid bilayer vesicles J. Biol. Phys. 31 2005 135 143
68. O. Zhong-Can, and W. Helfrich Bending energy of vesicle membranes: general expressions for the first, second, and third variation of the shape energy and applications to spheres and cylinders Phys. Rev. A 39 1989 5280 5288
69. S. Das, J. Jenkins, and T. Baumgart Neck geometry and shape transitions in vesicles with co-existing fluid phases: role of Gaussian curvature stiffness vs. spontaneous curvature Europhys. Lett. 86 2009 1 6
70. F. Jülicher, and R. Lipowsky Shape transformations of vesicles with intramembrane domains Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 53 1996 2670 2683
71. Kwak, D. 2008. The sharp-interface limit of the Cahn-Hilliard system with elasticity. PhD thesis, Regensburg University, Regensburg, Germany.
72. C.M. Elliott, and B. Stinner A surface phase field model for two-phase biological membranes SIAM J. Appl. Math. 70 2010 2904 2928
73. S. Kondo, and T. Miura Reaction-diffusion model as a framework for understanding biological pattern formation Science 329 2010 1616 1620
74. J. Murray Mathematical Biology II: Spatial Models and Biomedical Applications 2003 Springer-Verlag Berlin, Heidelberg
75. A.B. Goryachev, and A.V. Pokhilko Dynamics of Cdc42 network embodies a Turing-type mechanism of yeast cell polarity FEBS Lett. 582 2008 1437 1443
76. E. Orlandini, D. Marenduzzo, and A. Goryachev Domain formation on curved membranes: phase separation or Turing patterns? Soft Matter 9 2013 9311 9318
77. 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
78. Y.-S. Ryu, and I.-H. Lee S.-D. Lee Reconstituting ring-rafts in bud-mimicking topography of model membranes Nat. Commun. 5 2014 4507