Dual role of BAR domain-containing proteins in regulating vesicle release catalyzed by the GTPase, dynamin-2

Journal of Biological Chemistry

Volumn 288, Issue 35, 2013, Pages 25119-25128

  Neumann, Sylvia ^a   Schmid, Sandra L ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PARTNERS; COMPLEX PATTERN; DOMAIN-CONTAINING PROTEINS; DUAL ROLE; FUNCTIONAL INTERACTION; MEMBRANE CURVATURE; MEMBRANE FISSION; SPATIO-TEMPORAL;

MOLECULAR BIOLOGY;

CATALYSIS;

AMPHIPHYSIN; DYNAMIN II; ENDOPHILIN; GUANOSINE TRIPHOSPHATASE; SORTING NEXIN; SORTING NEXIN 9; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; LIPID BILAYER; MEMBRANE VESICLE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN PROTEIN INTERACTION;

BAR DOMAIN; DYNAMIN; ENDOCYTOSIS; ENTH DOMAIN; MEMBRANE CURVATURE; MEMBRANE FISSION; MEMBRANE TRAFFICKING; MEMBRANE TRANSPORT; MOLECULAR CELL BIOLOGY; VESICLES;

CATALYSIS; CELL MEMBRANE; DYNAMIN II; ENDOCYTOSIS; HUMANS; NERVE TISSUE PROTEINS; SRC HOMOLOGY DOMAINS;

EID: 84883389095     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.490474     Document Type: Article

References (63)

1. Schmid, E. M., and McMahon, H. T. (2007) Integrating molecular and network biology to decode endocytosis. Nature 448, 883-888
2. Rao, Y., Rückert, C., Saenger, W., and Haucke, V. (2012) The early steps of endocytosis: from cargo selection to membrane deformation. Eur. J. Cell Biol. 91, 226-233
3. Mettlen, M., Pucadyil, T., Ramachandran, R., and Schmid, S. L. (2009) Dissecting dynamin's role in clathrin-mediated endocytosis. Biochem. Soc. Trans. 37, 1022-1026
4. Aguet, F., Antonescu, C. N., Mettlen, M., Schmid, S. L., and Danuser, G. (2013) Advances in Analysis of Low Signal-to-Noise Images Link Dynamin and AP2 to the Functions of an Endocytic Checkpoint. Dev. Cell, 10.1016/j.devcel.2013. 06.019
5. Schmid, S. L., and Frolov, V. A. (2011) Dynamin: functional design of a membrane fission catalyst. Annu. Rev. Cell Dev. Biol. 27, 79-105
6. Ferguson, S. M., and De Camilli, P. (2012) Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 13, 75-88
7. Pucadyil, T. J., and Schmid, S. L. (2008) Real-Time Visualization of Dynamin-Catalyzed Membrane Fission and Vesicle Release. Cell 135, 1263-1275
8. Pucadyil, T. J., and Schmid, S. L. (2010) Supported bilayers with excess membrane reservoir: a template for reconstituting membrane budding and fission. Biophys. J. 99, 517-525
9. Liu, Y.-W., Neumann, S., Ramachandran, R., Ferguson, S. M., Pucadyil, T. J., and Schmid, S. L. (2011) Differential curvature sensing and generating activities of dynamin isoforms provide opportunities for tissue-specific regulation. Proc. Natl. Acad. Sci. 108, E234-E242
10. Lee, E., Marcucci, M., Daniell, L., Pypaert, M., Weisz, O. A., Ochoa, G.-C., Farsad, K., Wenk, M. R., and De Camilli, P. (2002) Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297, 1193-1196
11. Kamioka, Y., Fukuhara, S., Sawa, H., Nagashima, K., Masuda, M., Matsuda, M., and Mochizuki, N. (2004) A novel dynamin-associating molecule, formin-binding protein 17, induces tubular membrane invaginations and participates in endocytosis. J. Biol. Chem. 279, 40091-40099
12. Peter, B. J., Kent, H. M., Mills, I. G., Vallis, Y., Butler, P. J. G., Evans, P. R., and McMahon, H. T. (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499
13. Itoh, T., Erdmann, K. S., Roux, A., Habermann, B., Werner, H., and De Camilli, P. (2005) Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev. Cell 9, 791-804
14. Masuda, M., Takeda, S., Sone, M., Ohki, T., Mori, H., Kamioka, Y., and Mochizuki, N. (2006) Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO J. 25, 2889-2897
15. Shin, N., Ahn, N., Chang-Ileto, B., Park, J., Takei, K., Ahn, S.-G., Kim, S.-A., Di Paolo, G., and Chang, S. (2008) SNX9 regulates tubular invagination of the plasma membrane through interaction with actin cytoskeleton and dynamin 2. J. Cell Sci. 121, 1252-1263
16. Tarricone, C., Xiao, B., Justin, N., Walker, P. A., Rittinger, K., Gamblin, S. J., and Smerdon, S. J. (2001) The structural basis of Arfaptin-mediated cross-talk between Rac and Arf signalling pathways. Nature 411, 215-219
17. Weissenhorn, W. (2005) Crystal structure of the endophilin-A1 BAR domain. J. Mol. Biol. 351, 653-661
18. Gallop, J. L., Jao, C. C., Kent, H. M., Butler, P. J. G., Evans, P. R., Langen, R., and McMahon, H. T. (2006) Mechanism of endophilin N-BAR domainmediated membrane curvature. EMBO J. 25, 2898-2910
19. Bhatia, V. K., Madsen, K. L., Bolinger, P.-Y., Kunding, A., Hedegård, P., Gether, U., and Stamou, D. (2009) Amphipathic motifs in BAR domains are essential for membrane curvature sensing. EMBO J. 28, 3303-3314
20. Jao, C. C., Hegde, B. G., Gallop, J. L., Hegde, P. B., McMahon, H. T., Haworth, I. S., and Langen, R. (2010) Roles of amphipathic helices and the bin/amphiphysin/rvs (BAR) domain of endophilin in membrane curvature generation. J. Biol. Chem. 285, 20164-20170
21. Ford, M. G. J., Mills, I. G., Peter, B. J., Vallis, Y., Praefcke, G. J. K., Evans, P. R., and McMahon, H. T. (2002) Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366
22. Stahelin, R. V., Long, F., Peter, B. J., Murray, D., De Camilli, P., McMahon, H. T., and Cho, W. (2003) Contrasting membrane interaction mechanisms of AP180 N-terminal homology (ANTH) and epsin N-terminal homology (ENTH) domains. J. Biol. Chem. 278, 28993-28999
23. Yoon, Y., Tong, J., Lee, P. J., Albanese, A., Bhardwaj, N., Källberg, M., Digman, M. A., Lu, H., Gratton, E., Shin, Y.-K., and Cho, W. (2010) Molecular basis of the potent membrane-remodeling activity of the epsin 1 N-terminal homology domain. J. Biol. Chem. 285, 531-540
24. Lai, C.-L., Jao, C. C., Lyman, E., Gallop, J. L., Peter, B. J., McMahon, H. T., Langen, R., and Voth, G. A. (2012) Membrane binding and self-association of the epsin N-terminal homology domain. J. Mol. Biol. 423, 800-817
25. Gout, I., Dhand, R., Hiles, I. D., Fry, M. J., Panayotou, G., Das, P., Truong, O., Totty, N. F., Hsuan, J., and Booker, G. W. (1993) The GTPase dynamin binds to and is activated by a subset of SH3 domains. Cell 75, 25-36
26. Herskovits, J. S., Shpetner, H. S., Burgess, C. C., and Vallee, R. B. (1993) Microtubules and Src homology 3 domains stimulate the dynamin GTPase via its C-terminal domain. Proc. Natl. Acad. Sci. U.S.A. 90, 11468-11472
27. Wigge, P., Köhler, K., Vallis, Y., Doyle, C. A., Owen, D., Hunt, S. P., and McMahon, H. T. (1997) Amphiphysin heterodimers: potential role in clathrin-mediated endocytosis. Mol. Biol. Cell 8, 2003-2015
28. Owen, D. J., Wigge, P., Vallis, Y., Moore, J. D., Evans, P. R., and McMahon, H. T. (1998) Crystal structure of the amphiphysin-2 SH3 domain and its role in the prevention of dynamin ring formation. EMBO J. 17, 5273-5285
29. Yoshida, Y., Kinuta, M., Abe, T., Liang, S., Araki, K., Cremona, O., Di Paolo, G., Moriyama, Y., Yasuda, T., De Camilli, P., and Takei, K. (2004) The stimulatory action of amphiphysin on dynamin function is dependent on lipid bilayer curvature. EMBO J. 23, 3483-3491
30. Soulet, F., Yarar, D., Leonard, M., and Schmid, S. L. (2005) SNX9 regulates dynamin assembly and is required for efficient clathrin-mediated endocytosis. Mol. Biol. Cell 16, 2058-2067
31. Ramachandran, R., and Schmid, S. L. (2008) Real-time detection reveals that effectors couple dynamin's GTP-dependent conformational changes to the membrane. EMBO J. 27, 27-37
32. Boucrot, E., Pick, A., Çamdere, G., Liska, N., Evergren, E., McMahon, H. T., and Kozlov, M. M. (2012) Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 149, 124-136
33. Ramachandran, R., Pucadyil, T. J., Liu, Y.-W., Acharya, S., Leonard, M., Lukiyanchuk, V., and Schmid, S. L. (2009) Membrane insertion of the pleckstrin homology domain variable loop 1 is critical for dynamin-catalyzed vesicle scission. Mol. Biol. Cell 20, 4630-4639
34. Stowell, M. H., Marks, B., Wigge, P., and McMahon, H. T. (1999) Nucleotide- dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nat. Cell Biol. 1, 27-32
35. Neumann, S., Pucadyil, T. J., and Schmid, S. L. (2013) Analyzing membrane remodeling and fission using supported bilayers with excess membrane reservoir. Nat. Protoc. 8, 213-222
36. Leonard, M., Song, B. D., Ramachandran, R., and Schmid, S. L. (2005) Robust colorimetric assays for dynamin's basal and stimulated GTPase activities. Methods Enzymol. 404, 490-503
37. Doyon, J. B., Zeitler, B., Cheng, J., Cheng, A. T., Cherone, J. M., Santiago, Y., Lee, A. H., Vo, T. D., Doyon, Y., Miller, J. C., Paschon, D. E., Zhang, L., Rebar, E. J., Gregory, P. D., Urnov, F. D., and Drubin, D. G. (2011) Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells. Nat. Cell Biol. 13, 331-337
38. Ramachandran, R., Surka, M., Chappie, J. S., Fowler, D. M., Foss, T. R., Song, B. D., and Schmid, S. L. (2007) The dynamin middle domain is critical for tetramerization and higher-order self-assembly. EMBO J. 26, 559-566
39. Liu, Y.-W., Mattila, J.-P., and Schmid, S. L. (2013) Dynamin-catalyzed membrane fission requires coordinated GTP hydrolysis. PLoS ONE 8, e55691
40. Shnyrova, A. V., Bashkirov, P. V., Akimov, S. A., Pucadyil, T. J., Zimmerberg, J., Schmid, S. L., and Frolov, V. A. (2013) Geometric catalysis of membrane fission driven by flexible dynamin rings. Science 339, 1433-1436
41. Bashkirov, P. V., Akimov, S. A., Evseev, A. I., Schmid, S. L., Zimmerberg, J., and Frolov, V. A. (2008) GTPase cycle of dynamin is coupled to membrane squeeze and release, leading to spontaneous fission. Cell 135, 1276-1286
42. Pylypenko, O., Lundmark, R., Rasmuson, E., Carlsson, S. R., and Rak, A. (2007) The PX-BAR membrane-remodeling unit of sorting nexin 9. EMBO J. 26, 4788-4800
43. Yarar, D., Surka, M. C., Leonard, M. C., and Schmid, S. L. (2008) SNX9 activities are regulated by multiple phosphoinositides through both PX and BAR domains. Traffic 9, 133-146
44. Qualmann, B., Koch, D., and Kessels, M. M. (2011) Let's go bananas: revisiting the endocytic BAR code. EMBO J. 30, 3501-3515
45. Farsad, K., Ringstad, N., Takei, K., Floyd, S. R., Rose, K., and De Camilli, P. (2001) Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell Biol. 155, 193-200
46. Gad, H., Ringstad, N., Löw, P., Kjaerulff, O., Gustafsson, J., Wenk, M., Di Paolo, G., Nemoto, Y., Crun, J., Ellisman, M. H., De Camilli, P., Shupliakov, O., and Brodin, L. (2000) Fission and uncoating of synaptic clathrincoated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron 27, 301-312
47. Meinecke, M., Boucrot, E., Camdere, G., Hon, W.-C., Mittal, R., and Mc-Mahon, H. T. (2013) Cooperative recruitment of Dynamin and BAR domain- containing proteins leads to GTP-dependent membrane scission. J. Biol. Chem. 288, 6651-6661
48. Kojima, C., Hashimoto, A., Yabuta, I., Hirose, M., Hashimoto, S., Kanaho, Y., Sumimoto, H., Ikegami, T., and Sabe, H. (2004) Regulation of Bin1 SH3 domain binding by phosphoinositides. EMBO J. 23, 4413-4422
49. Wang, Q., Kaan, H. Y., Hooda, R. N., Goh, S. L., and Sondermann, H. (2008) Structure and plasticity of Endophilin and Sorting Nexin 9. Structure 16, 1574-1587
50. Wang, Q., Navarro, M. V., Peng, G., Molinelli, E., Goh, S. L., Judson, B. L., Rajashankar, K. R., and Sondermann, H. (2009) Molecular mechanism of membrane constriction and tubulation mediated by the F-BAR protein Pacsin/Syndapin. Proc. Natl. Acad. Sci. 106, 12700-12705
51. Rao, Y., Ma, Q., Vahedi-Faridi, A., Sundborger, A., Pechstein, A., Puchkov, D., Luo, L., Shupliakov, O., Saenger, W., and Haucke, V. (2010) Molecular basis for SH3 domain regulation of F-BAR-mediated membrane deformation. Proc. Natl. Acad. Sci. 107, 8213-8218
52. Vázquez, F. X., Unger, V. M., and Voth, G. A. (2013) Autoinhibition of Endophilin in Solution via Interdomain Interactions. Biophys. J. 104, 396-403
53. Goh, S. L., Wang, Q., Byrnes, L. J., and Sondermann, H. (2012) Versatile membrane deformation potential of activated pacsin. PLoSONE 7, e51628
54. Liu, J., Sun, Y., Oster, G. F., and Drubin, D. G. (2010) Mechanochemical crosstalk during endocytic vesicle formation. Curr. Opin. Cell Biol. 22, 36-43
55. Roux, A., Koster, G., Lenz, M., Sorre, B., Manneville, J.-B., Nassoy, P., and Bassereau, P. (2010) Membrane curvature controls dynamin polymerization. Proc. Natl. Acad. Sci. 107, 4141-4146
56. Chappie, J. S., Mears, J. A., Fang, S., Leonard, M., Schmid, S. L., Milligan, R. A., Hinshaw, J. E., and Dyda, F. (2011) A pseudoatomic model of the dynamin polymer identifies a hydrolysis-dependent powerstroke. Cell 147, 209-222
57. Overstreet, E., Chen, X., Wendland, B., and Fischer, J. A. (2003) Either part of a Drosophila epsin protein, divided after the ENTH domain, functions in endocytosis of delta in the developing eye. Curr. Biol. 13, 854-860
58. Shih, S. C., Katzmann, D. J., Schnell, J. D., Sutanto, M., Emr, S. D., and Hicke, L. (2002) Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat. Cell Biol. 4, 389-393
59. Dores, M. R., Schnell, J. D., Maldonado-Baez, L., Wendland, B., and Hicke, L. (2010) The function of yeast epsin and Ede1 ubiquitin-binding domains during receptor internalization. Traffic 11, 151-160
60. Skruzny, M., Brach, T., Ciuffa, R., Rybina, S., Wachsmuth, M., and Kaksonen, M. (2012) Molecular basis for coupling the plasma membrane to the actin cytoskeleton during clathrin-mediated endocytosis. Proc. Natl. Acad. Sci. 109, E2533-E2542
61. Kazazic, M., Bertelsen, V., Pedersen, K. W., Vuong, T. T., Grandal, M. V., Rødland, M. S., Traub, L. M., Stang, E., and Madshus, I. H. (2009) Epsin 1 is involved in recruitment of ubiquitinated EGF receptors into clathrincoated pits. Traffic 10, 235-245
62. Henry, A. G., Hislop, J. N., Grove, J., Thorn, K., Marsh, M., and von Zastrow, M. (2012) Regulation of endocytic clathrin dynamics by cargo ubiquitination. Dev. Cell 23, 519-532
63. Taylor, M. J., Perrais, D., and Merrifield, C. J. (2011) A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol. 9, e1000604