BIN1/M-Amphiphysin2 induces clustering of phosphoinositides to recruit its downstream partner dynamin

Nature Communications

Volumn 5, Issue , 2014, Pages

  Picas, Laura ^a   Viaud, Julien ^b   Schauer, Kristine ^a   Vanni, Stefano ^c   Hnia, Karim ^d   Fraisier, Vincent ^a   Roux, Aurélien ^e   Bassereau, Patricia ^f   Gaits Iacovoni, Frédérique ^b   Payrastre, Bernard ^b   Laporte, Jocelyn ^d   Manneville, Jean Baptiste ^a   Goud, Bruno ^a  

^a INSTITUT CURIE   (France)

^b Université de Toulouse   (France)

^c CNRS   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e UNIVERSITY OF GENEVA   (Switzerland)

^f INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIN1 PROTEIN; DYNAMIN; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN SH3; UNCLASSIFIED DRUG; BIN1 PROTEIN, HUMAN; FLUORESCENT DYE; GREEN FLUORESCENT PROTEIN; LIPID BILAYER; LIPOSOME; NUCLEAR PROTEIN; PHOSPHATIDYLINOSITOL; PROTEIN BINDING; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ENZYME; LIPID; NUMERICAL MODEL; PROTEIN; REACTION KINETICS;

ARTICLE; BIOGENESIS; CENTRONUCLEAR MYOPATHY; CLUSTER ANALYSIS; CONTROLLED STUDY; DOWNSTREAM PROCESSING; MUSCLE CELL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PURIFICATION; TRANSVERSE TUBULAR SYSTEM; CELL MEMBRANE; CHEMISTRY; ENDOCYTOSIS; HELA CELL LINE; HUMAN; LIPID BILAYER; METABOLISM; MOLECULAR DYNAMICS; MUSCLE; PROTEIN TERTIARY STRUCTURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; CELL MEMBRANE; DYNAMINS; ENDOCYTOSIS; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; LIPID BILAYERS; LIPOSOMES; MOLECULAR DYNAMICS SIMULATION; MUSCLES; NUCLEAR PROTEINS; PHOSPHATIDYLINOSITOLS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TUMOR SUPPRESSOR PROTEINS;

EID: 84923344501     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6647     Document Type: Article

References (40)

1. Peter, B. J. et al. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499 (2004).
2. Takei, K., Slepnev, V. I., Haucke, V. & De Camilli, P. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell. Biol. 1, 33-39 (1999).
3. Taylor, M. J., Perrais, D. & Merrifield, C. J. A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol. 9, e1000604 (2011).
4. Nicot, A. S. et al. Mutations in amphiphysin 2 (BIN1) disrupt interaction with dynamin 2 and cause autosomal recessive centronuclear myopathy. Nat. Genet. 39, 1134-1139 (2007).
5. Fugier, C. et al. Misregulated alternative splicing of BIN1 is associated with T tubule alterations and muscle weakness in myotonic dystrophy. Nat. Med. 17, 720-725 (2011).
6. Lee, E. et al. Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297, 1193-1196 (2002).
7. Itoh, T. et al. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev. Cell. 9, 791-804 (2005).
8. 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).
9. Lemmon, M. A., Ferguson, K. M., O'Brien, R., Sigler, P. B. & Schlessinger, J. Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain. Proc. Natl Acad. Sci. USA 92, 10472-10476 (1995).
10. Spiegelhalter, C. et al. From dynamic live cell imaging to 3D ultrastructure: novel integrated methods for high pressure freezing and correlative lightelectron microscopy. PLoS ONE 5, e9014 (2010).
11. Roy, A. & Levine, T. P. Multiple pools of phosphatidylinositol 4-phosphate detected using the pleckstrin homology domain of Osh2p. J. Biol. Chem. 279, 44683-44689 (2004).
12. Gozani, O. et al. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 114, 99-111 (2003).
13. Roux, A. et al. Membrane curvature controls dynamin polymerization. Proc. Natl Acad. Sci. USA 107, 4141-4146 (2010).
14. Klein, D. E., Lee, A., Frank, D. W., Marks, M. S. & Lemmon, M. A. The pleckstrin homology domains of dynamin isoforms require oligomerization for high affinity phosphoinositide binding. J. Biol. Chem. 273, 27725-27733 (1998).
15. Meinecke, M. et al. Cooperative recruitment of dynamin and BIN/ amphiphysin/Rvs (BAR) domain-containing proteins leads to GTP-dependent membrane scission. J. Biol. Chem. 288, 6651-6661 (2013).
16. Grabs, D. et al. The SH3 domain of amphiphysin binds the proline-rich domain of dynamin at a single site that defines a new SH3 binding consensus sequence. J. Biol. Chem. 272, 13419-13425 (1997).
17. Royer, B. et al. The myotubularin-amphiphysin 2 complex in membrane tubulation and centronuclear myopathies. EMBO. Rep. 14, 907-915 (2013).
18. Wu, T., Shi, Z. & Baumgart, T. Mutations in BIN1 Associated with Centronuclear Myopathy Disrupt Membrane Remodeling by Affecting Protein Density and Oligomerization. PLoS ONE 9, e93060 (2014).
19. Itoh, T. & BAR, De Camilli P. F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim. Biophys. Acta. 1761, 897-912 (2006).
20. Ford, M. G. et al. Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366 (2002).
21. Ford, M. G. J. et al. Simultaneous binding of PtdIns(4,5)P-2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291, 1051-1055 (2001).
22. Drin, G. et al. A general amphipathic alpha-helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol. 14, 138-146 (2007).
23. Khelashvili, G., Weinstein, H. & Harries, D. Protein diffusion on charged membranes: a dynamic mean-field model describes time evolution and lipid reorganization. Biophys. J. 94, 2580-2597 (2008).
24. Kalli, A. C. & Sansom, M. S. Interactions of peripheral proteins with model membranes as viewed by molecular dynamics simulations. Biochem. Soc. Trans. 42, 1418-1424 (2014).
25. Bai, J., Hu, Z., Dittman, J. S., Pym, E. C. & Kaplan, J. M. Endophilin functions as a membrane-bending molecule and is delivered to endocytic zones by exocytosis. Cell 143, 430-441 (2010).
26. Zhao, H. et al. Membrane-sculpting BAR domains generate stable lipid microdomains. Cell Rep. 4, 1213-1223 (2013).
27. Golebiewska, U. et al. Membrane-bound basic peptides sequester multivalent (PIP2), but not monovalent (PS), acidic lipids. Biophys. J. 91, 588-599 (2006).
28. Domanov, Y. A. et al. Mobility in geometrically confined membranes. Proc. Natl Acad. Sci. USA 108, 12605-12610 (2011).
29. Posor, Y. et al. Spatiotemporal control of endocytosis by phosphatidylinositol- 3,4-bisphosphate. Nature 499, 233-237 (2013).
30. Schmid, E. M. & McMahon, H. T. Integrating molecular and network biology to decode endocytosis. Nature 448, 883-888 (2007).
31. Carvalho, K., Ramos, L., Roy, C. & Picart, C. Giant unilamellar vesicles containing phosphatidylinositol(4,5)bisphosphate: characterization and functionality. Biophys. J. 95, 4348-4360 (2008).
32. van Meer, G., Voelker, D. R. & Feigenson, G. W. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell. Biol. 9, 112-124 (2008).
33. Hess, B., Kutzner, C., van der Spoel, D. & Lindahl, E. GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory. Comput. 4, 435-447 (2008).
34. Marrink, S. J., Risselada, H. J., Yefimov, S., Tieleman, D. P. & de Vries, A. H. The MARTINI force field: Coarse grained model for biomolecular simulations. J. Phys. Chem. B 111, 7812-7824 (2007).
35. Bussi, G., Donadio, D. & Parrinello, M. Canonical sampling through velocity rescaling. J. Chem. Phys. 126, 014101 (2007).
36. Berendsen, H. J. C., Postma, J. P. M., Vangunsteren, W. F., Dinola, A. & Haak, J. R. Molecular-Dynamics with Coupling to an External Bath. J. Chem. Phys. 81, 3684-3690 (1984).
37. Ford, M. G. J. et al. Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366 (2002).
38. de Jong, D. H. et al. Improved Parameters for the Martini Coarse-Grained Protein Force Field. J. Chem. Theory. Comput. 9, 687-697 (2013).
39. Bonomi, M. et al. PLUMED: A portable plugin for free-energy calculations with molecular dynamics. Comput. Phys. Commun. 180, 1961-1972 (2009).
40. Humphrey, W., Dalke, A. & Schulten, K. VMD: Visual molecular dynamics. J. Mol. Graph. Model. 14, 33-38 (1996).