Membrane bending: The power of protein imbalance

Trends in Biochemical Sciences

Volumn 38, Issue 11, 2013, Pages 576-584

  Derganc, Jure ^a   Antonny, Bruno ^b   Čopič, Alenka ^c  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c INSTITUT JACQUES MONOD   (France)

Author keywords

COPII vesicle budding membrane protein asymmetry; GPI anchored proteins; Membrane bending; Protein coats; Protein crowding

Indexed keywords

COAT PROTEIN COMPLEX II; EPSIN; EPSIN 1; ESCRT PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

BILAYER MEMBRANE; CELL BUDDING; ENDOPLASMIC RETICULUM; LIPID BILAYER; LIPID COMPOSITION; LIPID MEMBRANE; MEMBRANE BENDING; MEMBRANE BIOLOGY; MEMBRANE STRUCTURE; MEMBRANE VESICLE; MOLECULAR CROWDING; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROWDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW;

BASIDIOMYCOTA;

COPII VESICLE BUDDING MEMBRANE PROTEIN ASYMMETRY; GPI-ANCHORED PROTEINS; MEMBRANE BENDING; PROTEIN COATS; PROTEIN CROWDING;

CELL MEMBRANE; LIPID BILAYERS; MEMBRANE PROTEINS;

EID: 84885848514     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2013.08.006     Document Type: Review

References (85)

1. Engelman D.M. Membranes are more mosaic than fluid. Nature 2005, 438:578-580.
2. Zimmerberg J., Kozlov M.M. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 2006, 7:9-19.
3. Bigay J., Antonny B. Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dev. Cell 2013, 23:886-895.
4. Hurley J.H., et al. Membrane budding. Cell 2010, 143:875-887.
5. Faini M., et al. Vesicle coats: structure, function, and general principles of assembly. Trends Cell Biol. 2013, 23:279-288.
6. Shibata Y., et al. Mechanisms shaping the membranes of cellular organelles. Annu. Rev. Cell Dev. Biol. 2009, 25:329-354.
7. Sens P., et al. Biophysical approaches to protein-induced membrane deformations in trafficking. Curr. Opin. Cell Biol. 2008, 20:476-482.
8. Decher G., et al. Interactions of amphiphilic polymers with model membranes. Die Angew. Makromolek. Chem. 1989, 166/167:71-80.
9. Hiergeist C., Lipowsky R. Elastic properties of polymer-decorated membranes. J. Phys. II 1996, 6:1465-1481.
10. Stachowiak J.C., et al. Steric confinement of proteins on lipid membranes can drive curvature and tubulation. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:7781-7786.
11. Copic A., et al. ER cargo properties specify a requirement for COPII coat rigidity mediated by Sec13p. Science 2012, 335:1359-1362.
12. Stachowiak J.C., et al. Membrane bending by protein-protein crowding. Nat. Cell Biol. 2012, 14:944-949.
13. Miller E.A., Schekman R. COPII - a flexible vesicle formation system. Curr. Opin. Cell Biol. 2013, 25:420-427.
14. Miller E.A., et al. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 2003, 114:497-509.
15. Mossessova E., et al. SNARE selectivity of the COPII coat. Cell 2003, 114:483-495.
16. Fath S., et al. Structure and organization of coat proteins in the COPII cage. Cell 2007, 129:1325-1336.
17. Miller E.A., Barlowe C. Regulation of coat assembly - sorting things out at the ER. Curr. Opin. Cell Biol. 2010, 22:447-453.
18. Elrod-Erickson M.J., Kaiser C.A. Genes that control the fidelity of endoplasmic reticulum to Golgi transport identified as suppressors of vesicle budding mutations. Mol. Biol. Cell 1996, 7:1043-1058.
19. Jin L., et al. Ubiquitin-dependent regulation of COPII coat size and function. Nature 2012, 482:495-500.
20. Venditti R., et al. Sedlin controls the ER export of procollagen by regulating the Sar1 cycle. Science 2012, 337:1668-1672.
21. Faini M., et al. The structures of COPI-coated vesicles reveal alternate coatomer conformations and interactions. Science 2012, 336:1451-1454.
22. Leventis R., Silvius J.R. Quantitative experimental assessment of macromolecular crowding effects at membrane surfaces. Biophys. J. 2010, 99:2125-2133.
23. Carnahan N.F., Starling K.E. Equation of state for nonattracting rigid spheres. J. Chem. Phys. 1969, 51:635-637.
24. Ellis R.J. Macromolecular crowding: obvious but underappreciated. Trends Biochem. Sci. 2001, 26:597-604.
25. Mitra K., et al. Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:4083-4088.
26. Takamori S., et al. Molecular anatomy of a trafficking organelle. Cell 2006, 127:831-846.
27. Dupuy A.D., Engelman D.M. Protein area occupancy at the center of the red blood cell membrane. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:2848-2852.
28. English A.R., Voeltz G.K. Endoplasmic reticulum structure and interconnections with other organelles. Cold Spring Harb. Perspect. Biol. 2013, 5:a013227.
29. Muniz M., et al. The Emp24 complex recruits a specific cargo molecule into endoplasmic reticulum-derived vesicles. J. Cell Biol. 2000, 148:925-930.
30. Malkus P., et al. Concentrative sorting of secretory cargo proteins into COPII-coated vesicles. J. Cell Biol. 2002, 159:915-921.
31. Schekman R., Orci L. Coat proteins and vesicle budding. Science 1996, 271:1526-1533.
32. Scheve C.S., et al. Steric pressure between membrane-bound proteins opposes lipid phase separation. J. Am. Chem. Soc. 2013, 135:1185-1188.
33. Wehrle-Haller B. Structure and function of focal adhesions. Curr. Opin. Cell Biol. 2012, 24:116-124.
34. Rawicz W., et al. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys. J. 2000, 79:328-339.
35. Holthuis J.C.M., Levine T.P. Lipid traffic: floppy drives and a superhighway. Nat. Rev. Mol. Cell Biol. 2005, 6:209-220.
36. Van Meer G., et al. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 2008, 9:112-124.
37. Callan-Jones A., et al. Curvature-driven lipid sorting in biomembranes. Cold Spring Harb. Perspect. Biol. 2011, 3:a004648.
38. Sharpe H.J., et al. A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 2010, 142:158-169.
39. Raucher D., et al. Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 2000, 100:221-228.
40. Upadhyaya A., Sheetz M.P. Tension in tubulovesicular networks of Golgi and endoplasmic reticulum membranes. Biophys. J. 2004, 86:2923-2928.
41. McMahon H.T., Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 2011, 12:517-533.
42. Dannhauser P.N., Ungewickell E.J. Reconstitution of clathrin-coated bud and vesicle formation with minimal components. Nat. Cell Biol. 2012, 14:634-639.
43. Ford M.G.J., et al. Curvature of clathrin-coated pits driven by epsin. Nature 2002, 419:361-366.
44. Antonescu C.N., et al. Phosphatidylinositol-(4,5)-bisphosphate regulates clathrin-coated pit initiation, stabilization, and size. Mol. Biol. Cell 2011, 22:2588-2600.
45. Boucrot E., et al. Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 2012, 149:124-136.
46. Kusumi A., et al. Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu. Rev. Biophys. Biomol. Struct. 2005, 34:351-378.
47. Sabharanjak S., et al. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev. Cell 2002, 2:411-423.
48. Nichols B. Endocytosis of lipid-anchored proteins: excluding GEECs from the crowd. J. Cell Biol. 2009, 186:457-459.
49. Refaei M., et al. Assessment of the roles of ordered lipid microdomains in post-endocytic trafficking of glycosyl-phosphatidylinositol-anchored proteins in mammalian fibroblasts. Traffic 2011, 12:1012-1024.
50. Bhagatji P., et al. Steric and not structure-specific factors dictate the endocytic mechanism of glycosylphosphatidylinositol-anchored proteins. J. Cell Biol. 2009, 186:615-628.
51. Boura E., et al. Solution structure of the ESCRT-I and -II supercomplex: implications for membrane budding and scission. Structure 2012, 20:874-886.
52. Henne, William M., et al. The endosomal sorting complex ESCRT-II mediates the assembly and architecture of ESCRT-III helices. Cell 2012, 151:356-371.
53. Macdonald C., et al. Cargo ubiquitination is essential for multivesicular body intralumenal vesicle formation. EMBO Rep. 2012, 13:331-338.
54. Sitaram A., Marks M.S. Mechanisms of protein delivery to melanosomes in pigment cells. Physiology 2012, 27:85-99.
55. Berson J.F., et al. Pmel17 initiates premelanosome morphogenesis within multivesicular bodies. Mol. Biol. Cell 2001, 12:3451-3464.
56. Theos A.C., et al. A lumenal domain-dependent pathway for sorting to intralumenal vesicles of multivesicular endosomes involved in organelle morphogenesis. Dev. Cell 2006, 10:343-354.
57. Van Niel G., et al. The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev. Cell 2011, 21:708-721.
58. Spira F., et al. Patchwork organization of the yeast plasma membrane into numerous coexisting domains. Nat. Cell Biol. 2012, 14:640-648.
59. Davies K.M., et al. Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:13602-13607.
60. Paumard P., et al. The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 2002, 21:221-230.
61. Allen R.D., et al. An investigation of mitochondrial inner membranes by rapid-freeze deep-etch techniques. J. Cell Biol. 1989, 108:2233-2240.
62. Baker L.A., et al. Arrangement of subunits in intact mammalian mitochondrial ATP synthase determined by cryo-EM. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:11675-11680.
63. Linden M., et al. Entropic tension in crowded membranes. PLoS Comput. Biol. 2012, 8:e1002431.
64. Kaksonen M., et al. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 2005, 123:305-320.
65. Kukulski W., et al. Plasma membrane reshaping during endocytosis is revealed by time-resolved electron tomography. Cell 2012, 150:508-520.
66. Cocucci E., et al. The first five seconds in the life of a clathrin-coated pit. Cell 2012, 150:495-507.
67. Wu M., et al. Coupling between clathrin-dependent endocytic budding and F-BAR-dependent tubulation in a cell-free system. Nat. Cell Biol. 2010, 12:902-908.
68. Boulant S., et al. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat. Cell Biol. 2011, 13:1124-1131.
69. Liu J., et al. The mechanochemistry of endocytosis. PLoS Biol. 2009, 7:e1000204.
70. Reynwar B.J., et al. Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 2007, 447:461-464.
71. Mim C., et al. Structural basis of membrane bending by the N-BAR protein endophilin. Cell 2012, 149:137-145.
72. Stagg S.M., et al. Structure of the Sec13/31 COPII coat cage. Nature 2006, 439:234-238.
73. De Groot P.W., et al. Genome-wide identification of fungal GPI proteins. Yeast 2003, 20:781-796.
74. Ghaemmaghami S., et al. Global analysis of protein expression in yeast. Nature 2003, 425:737-741.
75. Dancourt J., Barlowe C. Protein sorting receptors in the early secretory pathway. Annu. Rev. Biochem. 2010, 79:777-802.
76. Stamnes M.A., et al. An integral membrane component of coatomer-coated transport vesicles defines a family of proteins involved in budding. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:8011-8015.
77. Jenne N., et al. Oligomeric state and stoichiometry of p24 proteins in the early secretory pathway. J. Biol. Chem. 2002, 277:46504-46511.
78. Contreras F.X., et al. Molecular recognition of a single sphingolipid species by a protein's transmembrane domain. Nature 2012, 481:525-529.
79. Fujita M., et al. Sorting of GPI-anchored proteins into ER exit sites by p24 proteins is dependent on remodeled GPI. J. Cell Biol. 2011, 194:61-75.
80. Castillon G.A., et al. The yeast p24 complex regulates GPI-anchored protein transport and quality control by monitoring anchor remodeling. Mol. Biol. Cell 2011, 22:2924-2936.
81. Helfrich W. Equation of state for nonattracting rigid spheres. Z. Naturforsch. 1973, 28:693-703.
82. Bozic B., et al. Theoretical analysis of the formation of membrane microtubes on axially strained vesicles. Phys. Rev. E 1997, 55:5834-5842.
83. Derenyi I., et al. Membrane nanotubes. Lect. Notes Phys. 2007, 711:141-159.
84. Diz-Muñoz A., et al. Use the force: membrane tension as an organizer of cell shape and motility. Trends Cell Biol. 2013, 23:47-53.
85. Sorre B., et al. Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:5622-5626.