A balance between membrane elasticity and polymerization energy sets the shape of spherical clathrin coats

Nature Communications

Volumn 6, Issue , 2015, Pages

  Saleem, Mohammed ^a,e   Morlot, Sandrine ^a,f   Hohendahl, Annika ^a   Manzi, John ^b   Lenz, Martin ^c   Roux, Aurélien ^a,d  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b INSTITUT CURIE   (France)

^c UNIVERSITÉ PARIS SUD   (France)

^d Swiss National Centre for Competence in Research Programme Chemical Biology   (Switzerland)

^e NATIONAL INSTITUTE OF TECHNOLOGY   (India)

^f INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; COAT PROTEIN; FLUORESCENT DYE; ACTIN BINDING PROTEIN; LIPOSOME;

INHIBITION; MEMBRANE; OSMOSIS; POLYMERIZATION; TENSION;

ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING SITE; CONCEPTUAL FRAMEWORK; CONFOCAL MICROSCOPY; ELASTICITY; ELECTRON MICROSCOPY; ENERGY; IN VITRO STUDY; MEMBRANE; MICROPIPETTE; OPTICAL TWEEZERS; OSMOTIC STRESS; PROTEIN POLYMERIZATION; RIGIDITY; SURFACE PROPERTY; TENSION; ANIMAL; CHEMISTRY; COATED PIT; METABOLISM; MOLECULAR MODEL; OSMOSIS; PIG; POLYMERIZATION; THERMODYNAMICS; ULTRASTRUCTURE;

ANIMALS; CLATHRIN; COATED PITS, CELL-MEMBRANE; ELASTICITY; MICROFILAMENT PROTEINS; MODELS, MOLECULAR; OSMOSIS; POLYMERIZATION; SUS SCROFA; THERMODYNAMICS; UNILAMELLAR LIPOSOMES;

EID: 84923376044     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7249     Document Type: Article

References (38)

1. Kanaseki, T. & Kadota, K. The "vesicle in a basket". A morphological study of the coated vesicle isolated from the nerve endings of the guinea pig brain, with special reference to the mechanism of membrane movements. J. Cell Biol. 42, 202-220 (1969).
2. Pearse, B. M. Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles. Proc. Natl Acad. Sci. USA 73, 1255-1259 (1976).
3. Crowther, R. A. & Pearse, B. M. Assembly and packing of clathrin into coats. J. Cell Biol. 91, 790-797 (1981).
4. Kirchhausen, T. Bending membranes. Nat. Cell Biol. 14, 906-908 (2012).
5. Ford, M. G. et al. Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291, 1051-1055 (2001).
6. Dannhauser, P. N. & Ungewickell, E. J. Reconstitution of clathrin-coated bud and vesicle formation with minimal components. Nat. Cell Biol. 14, 634-639 (2012).
7. Johannes, L., Wunder, C. & Bassereau, P. Bending "on the rocks"-a cocktail of biophysical modules to build endocytic pathways. Cold Spring Harb. Persp. Biol. 6 (2014).
8. Stachowiak, J. C. et al. Membrane bending by protein-protein crowding. Nat. Cell Biol. 14, 944-949 (2012).
9. Fotin, A. et al. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432, 573-579 (2004).
10. Smith, C. J., Grigorieff, N. & Pearse, B. M. Clathrin coats at 21 A resolution: a cellular assembly designed to recycle multiple membrane receptors. EMBO J. 17, 4943-4953 (1998).
11. Vigers, G. P., Crowther, R. A. & Pearse, B. M. Three-dimensional structure of clathrin cages in ice. EMBO J. 5, 529-534 (1986).
12. Heuser, J. & Kirchhausen, T. Deep-etch views of clathrin assemblies. J. Ultrastruct. Res. 92, 1-27 (1985).
13. McMahon, H. T. & Boucrot, E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517-533 (2011).
14. Owen, D. J., Collins, B. M. & Evans, P. R. Adaptors for clathrin coats: structure and function. Annu. Rev. Cell Dev. Biol. 20, 153-191 (2004).
15. Ahle, S. & Ungewickell, E. Purification and properties of a new clathrin assembly protein. EMBO J. 5, 3143-3149 (1986).
16. Chen, H. et al. Epsin is an EH-domain-binding protein implicated in clathrinmediated endocytosis. Nature 394, 793-797 (1998).
17. Ford, M. G. et al. Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366 (2002).
18. Helfrich, W. Elastic properties of lipid bilayers : theory and possible experiments. Zur Naturforschung 28c, 693-703 (1973).
19. Jin, A. J., Prasad, K., Smith, P. D., Lafer, E. M. & Nossal, R. Measuring the elasticity of clathrin-coated vesicles via atomic force microscopy. Biophys. J. 90, 3333-3344 (2006).
20. Morlot, S. et al. Membrane shape at the edge of the dynamin helix sets location and duration of the fission reaction. Cell 151, 619-629 (2012).
21. Sorre, B. et al. Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proc. Natl Acad. Sci. USA 109, 173-178 (2012).
22. Evans, E., Bowman, H., Leung, A., Needham, D. & Tirrell, D. Biomembrane templates for nanoscale conduits and networks. Science 273, 933-935 (1996).
23. Cuvelier, D., Derenyi, I., Bassereau, P. & Nassoy, P. Coalescence of membrane tethers: experiments, theory, and applications. Biophys. J. 88, 2714-2726 (2005).
24. Baumgart, T., Hess, S. T. & Webb, W. W. Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425, 821-824 (2003).
25. Nossal, R. Energetics of clathrin basket assembly. Traffic 2, 138-147 (2001).
26. den Otter, W. K. & Briels, W. J. The generation of curved clathrin coats from flat plaques. Traffic 12, 1407-1416 (2011).
27. Dai, J., Sheetz, M. P., Wan, X. & Morris, C. E. Membrane tension in swelling and shrinking molluscan neurons. J. Neurosci. 18, 6681-6692 (1998).
28. Sinha, B. et al. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 144, 402-413 (2011).
29. Dai, J. & Sheetz, M. P. Membrane tether formation from blebbing cells. Biophys. J. 77, 3363-3370 (1999).
30. Aghamohammadzadeh, S. & Ayscough, K. R. Differential requirements for actin during yeast and mammalian endocytosis. Nat. Cell Biol. 11, 1039-1042 (2009).
31. Boulant, S., Kural, C., Zeeh, J. C., Ubelmann, F. & Kirchhausen, T. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat. Cell Biol. 13, 1124-1131 (2011).
32. Naim, H. Y., Dodds, D. T., Brewer, C. B. & Roth, M. G. Apical- and basolateralcoated pits of MDCK cells differ in their rates of maturation into coated vesicles, but not in the ability to distinguish between mutant hemagglutinin proteins with different internalization signals. J. Cell Biol. 129, 1241-1250 (1995).
33. Kirchhausen, T. Coated pits and coated vesicles-sorting it all out. Curr. Opin. Struct. Biol. 3, 182-188 (1993).
34. Kohyama, T., Kroll, D. M. & Gompper, G. Budding of crystalline domains in fluid membranes. Phys. Rev. E 68, 061905 (2003).
35. Hinrichsen, L., Meyerholz, A., Groos, S. & Ungewickell, E. J. Bending a membrane: how clathrin affects budding. Proc. Natl Acad. Sci. USA 103, 8715-8720 (2006).
36. Manneville, J. B. et al. COPI coat assembly occurs on liquid-disordered domains and the associated membrane deformations are limited by membrane tension. Proc. Natl Acad. Sci. USA 105, 16946-16951 (2008).
37. Skruzny, M. et al. Molecular basis for coupling the plasma membrane to the actin cytoskeleton during clathrin-mediated endocytosis. Proc. Natl Acad. Sci. USA 109, E2533-E2542 (2012).
38. Neuman, K. & Block, S. M. Optical trapping. Rev. Sci. Instrum. 75, 2787-2809 (2004).