Membrane-Mediated Interaction between Strongly Anisotropic Protein Scaffolds

PLoS Computational Biology

Volumn 11, Issue 2, 2015, Pages

  Schweitzer, Yonatan ^a   Kozlov, Michael M ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOTROPY; ENTROPY; GEOMETRY; MOLECULAR BIOLOGY; PROTEINS; SCAFFOLDS (BIOLOGY);

BAR DOMAINS; INTRACELLULAR ORGANELLE; ISOTROPICS; MEDIATED INTERACTION; MEMBRANE BENDING; PARAMETERS CHARACTERIZING; PROTEIN SCAFFOLDS; PROTEIN SHAPE; PROTEIN-PROTEIN INTERACTIONS; SPHERICAL SEGMENT;

MEMBRANES;

SCAFFOLD PROTEIN; LIPID BILAYER; MEMBRANE PROTEIN;

ANISOTROPY; ARTICLE; ELASTICITY; ENDOCYTOSIS; ENTROPY; FORCE; GEOMETRY; LIPID MEMBRANE; MATHEMATICAL COMPUTING; PROTEIN INTERACTION; BIOPHYSICS; CELL MEMBRANE; CHEMICAL MODEL; CHEMISTRY; LIPID BILAYER; PHYSIOLOGY;

ANISOTROPY; BIOPHYSICAL PHENOMENA; CELL MEMBRANE; LIPID BILAYERS; MEMBRANE PROTEINS; MODELS, CHEMICAL;

EID: 84924390055     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004054     Document Type: Article

References (62)

1. Ramakrishnan N, Sunil Kumar PB, Ipsen JH, (2013) Membrane-mediated aggregation of curvature-inducing nematogens and membrane tubulation. Biophys J 104: 1018–1028. doi: 10.1016/j.bpj.2012.12.045 23473484
2. Alberts B, Bray D, Lewis J, Raff M, Roberts K, et al. (2002) Molecualr Biology of the Cell. New York: Garland.
3. Almsherqi ZA, Kohlwein SD, Deng Y, (2006) Cubic membranes: a legend beyond the Flatland* of cell membrane organization. The Journal of Cell Biology 173: 839–844. 16785319
4. Almsherqi ZA, Landh T, Kohlwein SD, Deng Y, Kwang WJ, (2009) Chapter 6 Cubic Membranes: The Missing Dimension of Cell Membrane Organization. International Review of Cell and Molecular Biology: Academic Press. pp. 275–342. doi: 10.1016/S1937-6448(08)02006-6 19349040
5. Devaux PF, (2000) Is lipid translocation involved during endo- and exocytosis? Biochimie 82: 497–509. 10865135
6. Graham TR, Kozlov MM, (2010) Interplay of proteins and lipids in generating membrane curvature. Curr Opin Cell Biol 22: 430–436. doi: 10.1016/j.ceb.2010.05.002 20605711
7. McMahon HT, Gallop JL, (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438: 590–596. 16319878
8. Zimmerberg J, Kozlov MM, (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7: 9–19. 16365634
9. Shibata Y, Hu J, Kozlov MM, Rapoport TA, (2009) Mechanisms shaping the membranes of cellular organelles. Annu Rev Cell Dev Biol 25: 329–354. doi: 10.1146/annurev.cellbio.042308.113324 19575675
10. Bassereau P, Sorre B, Levy A, (2014) Bending lipid membranes: experiments after W. Helfrich’s model. Adv Colloid Interface Sci 208: 47–57. doi: 10.1016/j.cis.2014.02.002 24630341
11. Kozlov MM, Campelo F, Liska N, Chernomordik LV, Marrink SJ, et al. (2014) Mechanisms shaping cell membranes. Curr Opin Cell Biol 29C: 53–60.
12. Iglič A, Hägerstrand H, Veranič P, Plemenitaš A, Kralj-Iglič V, (2006) Curvature-induced accumulation of anisotropic membrane components and raft formation in cylindrical membrane protrusions. Journal of Theoretical Biology 240: 368–373. 16277995
13. Kabaso D, Bobrovska N, Góźdź W, Gov N, Kralj-Iglič V, et al. (2012) On the role of membrane anisotropy and BAR proteins in the stability of tubular membrane structures. Journal of Biomechanics 45: 231–238. doi: 10.1016/j.jbiomech.2011.10.039 22138195
14. 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. 12353027
15. Gallop JL, Jao CC, Kent HM, Butler PJ, Evans PR, et al. (2006) Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J 25: 2898–2910. 16763559
16. Campelo F, McMahon HT, Kozlov MM, (2008) The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophys J 95: 2325–2339. doi: 10.1529/biophysj.108.133173 18515373
17. Drin G, Antonny B, (2010) Amphipathic helices and membrane curvature. FEBS Lett 584: 1840–1847. doi: 10.1016/j.febslet.2009.10.022 19837069
18. 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. doi: 10.1016/j.cell.2012.01.048 22464326
19. Yolcu C, Deserno M, (2012) Membrane-mediated interactions between rigid inclusions: an effective field theory. Phys Rev E Stat Nonlin Soft Matter Phys 86: 031906. 23030943
20. Goulian M, Bruinsma R, Pincus P, (1993) Long-Range Forces in Heterogeneous Fluid Membranes (Vol 22, Pg 145, 1993). Europhysics Letters 23: 155–155.
21. Goulian M, Bruinsma R, Pincus P, (1993) Long-Range Forces in Heterogeneous Fluid Membranes. Europhysics Letters 22: 145–150.
22. Park JM, Lubensky TC, (1996) Interactions between membrane inclusions on fluctuating membranes. Journal De Physique I 6: 1217–1235.
23. Netz RR, (1997) Inclusions in fluctuating membranes: Exact results. Journal De Physique I 7: 833–852.
24. Helfrich W, (1973) Elastic Properties of Lipid Bilayers—Theory and Possible Experiments. Zeitschrift Fur Naturforschung C-a Journal of Biosciences C 28: 693–703.
25. Weikl TR, (2001) Fluctuation-induced aggregation of rigid membrane inclusions. Europhysics Letters 54: 547–553.
26. Weikl TR, Kozlov MM, Helfrich W, (1998) Interaction of conical membrane inclusions: Effect of lateral tension. Physical Review E 57: 6988–6995.
27. Chou T, Kim KS, Oster G, (2001) Statistical thermodynamics of membrane bending-mediated protein-protein attractions. Biophys J 80: 1075–1087. 11222274
28. Kim KS, Neu J, Oster G, (2000) Effect of protein shape on multibody interactions between membrane inclusions. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 61: 4281–4285. 11088224
29. Kim KS, Neu J, Oster G, (1998) Curvature-mediated interactions between membrane proteins. Biophys J 75: 2274–2291. 9788923
30. Dommersnes PG, Fournier JB, (2002) The many-body problem for anisotropic membrane inclusions and the self-assembly of “saddle” defects into an “egg carton”. Biophys J 83: 2898–2905. 12496066
31. Yolcu C, Haussman RC, Deserno M, (2014) The Effective Field Theory approach towards membrane-mediated interactions between particles. Adv Colloid Interface Sci 208C: 89–109.
32. Helfrich W, Weikl TR, (2001) Two direct methods to calculate fluctuation forces between rigid objects embedded in fluid membranes. European Physical Journal E 5: 423–439.
33. Golestanian R, Goulian M, Kardar M, (1996) Fluctuation-induced interactions between rods on a membrane. Physical Review E 54: 6725–6734. 9965898
34. Dommersnes PG, Fournier JB, (1999) Casimir and mean-field interactions between membrane inclusions subject to external torques. Europhysics Letters 46: 256–261.
35. Netz RR, Pincus P, (1995) Inhomogeneous Fluid Membranes—Segregation, Ordering, and Effective Rigidity. Physical Review E 52: 4114–4128. 9963884
36. Kim KS, Neu JC, Oster GF, (1999) Many-body forces between membrane inclusions: A new pattern-formation mechanism. Europhysics Letters 48: 99–105. 10333430
37. Reynwar BJ, Deserno M, (2011) Membrane-mediated interactions between circular particles in the strongly curved regime. Soft Matter 7: 8567–8575.
38. Goulian M, (1996) Inclusions in membranes. Current Opinion in Colloid & Interface Science 1: 358–361.
39. Dommersnes PG, Fournier JB, (1999) N-body study of anisotropic membrane inclusions: Membrane mediated interactions and ordered aggregation. European Physical Journal B 12: 9–12.
40. Reynwar BJ, Illya G, Harmandaris VA, Muller MM, Kremer K, et al. (2007) Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447: 461–464. 17522680
41. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, et al. (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303: 495–499. 14645856
42. 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. doi: 10.1016/j.cell.2007.12.041 18329367
43. Frost A, Unger VM, De Camilli P, (2009) The BAR domain superfamily: membrane-molding macromolecules. Cell 137: 191–196. doi: 10.1016/j.cell.2009.04.010 19379681
44. Henne WM, Kent HM, Ford MG, 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: 839–852. 17540576
45. Schmid SL, Frolov VA, (2011) Dynamin: functional design of a membrane fission catalyst. Annu Rev Cell Dev Biol 27: 79–105. doi: 10.1146/annurev-cellbio-100109-104016 21599493
46. Praefcke GJ, McMahon HT, (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5: 133–147. 15040446
47. Hinshaw JE, (2000) Dynamin and its role in membrane fission. Annu Rev Cell Dev Biol 16: 483–519. 11031245
48. Danino D, Moon KH, Hinshaw JE, (2004) Rapid constriction of lipid bilayers by the mechanochemical enzyme dynamin. J Struct Biol 147: 259–267. 15450295
49. Daumke O, Lundmark R, Vallis Y, Martens S, Butler PJ, et al. (2007) Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 449: 923–927. 17914359
50. Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA, (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124: 573–586. 16469703
51. Hu J, Shibata Y, Voss C, Shemesh T, Li Z, et al. (2008) Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science 319: 1247–1250. doi: 10.1126/science.1153634 18309084
52. McMahon HT, http://www2.mrc-lmb.cam.ac.uk/groups/hmm/index.html.
53. Spivak M, (1970) A comprehensive introduction to differential geometry: Brandeis University.
54. Brakke KA, (1992) The Surface Evolver. Experimental Mathematics 1: 141–165.
55. Fournier J-B, Dommersnes PG, Galatola P, (2003) Dynamin recruitment by clathrin coats: a physical step? Comptes Rendus Biologies 326: 467–476. 12886874
56. 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: 20396–20401. doi: 10.1073/pnas.1309819110 24284177
57. Shibata Y, Shemesh T, Prinz WA, Palazzo AF, Kozlov MM, et al. (2010) Mechanisms determining the morphology of the peripheral ER. Cell 143: 774–788. doi: 10.1016/j.cell.2010.11.007 21111237
58. Terasaki M, Shemesh T, Kasthuri N, Klemm RW, Schalek R, et al. (2013) Stacked endoplasmic reticulum sheets are connected by helicoidal membrane motifs. Cell 154: 285–296. doi: 10.1016/j.cell.2013.06.031 23870120
59. Shemesh T, Klemm RW, Romano FB, Wang S, Vaughan JC, et al. (2014) A model for the generation and interconversion of ER morphologies. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1419997111 25552562
60. Kim KS, Neu J, Oster G, (1998) Curvature-mediated interactions between membrane proteins. Biophysical Journal 75: 2274–2291. 9788923
61. Kozlov MM, Markin VS, (1991) Interface Mechanics—the Shape of Membrane Cylinder. Journal De Physique Ii 1: 805–820.
62. Dommersnes PG, Fournier JB, Galatola P, (1998) Long-range elastic forces between membrane inclusions in spherical vesicles. Europhysics Letters 42: 233–238.