GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission

Nature

Volumn 441, Issue 7092, 2006, Pages 528-531

  Roux, Aurélien ^a   Uyhazi, Katherine ^a   Frost, Adam ^b   De Camilli, Pietro ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; HYDROLYSIS; LIPIDS; NUCLEIC ACIDS;

GTPASES; LIPID TUBULES; MEMBRANE FISSION; NUCLEOTIDES;

BIOLOGICAL MEMBRANES;

DYNAMIN; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; KINESIN; LIPID; LIPOSOME; NUCLEOTIDE;

ENZYME ACTIVITY; EXPERIMENTAL STUDY; MEMBRANE;

ARTICLE; HYDROLYSIS KINETICS; MEMBRANE; MICROTUBULE; MOTOR ACTIVITY; PRIORITY JOURNAL; ROTATION; TENSION; ANIMAL; BIOMECHANICS; HYDROLYSIS; MEMBRANE FUSION; METABOLISM; PHYSIOLOGY; RAT; TIME;

ANIMALS; BIOMECHANICS; DYNAMINS; GUANOSINE TRIPHOSPHATE; HYDROLYSIS; KINESIN; LIPOSOMES; MEMBRANE FUSION; MICROTUBULES; RATS; ROTATION; TIME FACTORS;

EID: 33745026786     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature04718     Document Type: Article

References (30)

1. Koenig, J. H. & Ikeda, K. Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci. 9, 3844-3860 (1989).
2. Sever, S., Damke, H. & Schmid, S. L. Garrotes, springs, ratchets, and whips: putting dynamin models to the test. Traffic 1, 385-392 (2000).
3. Thompson, H. M. & McNiven, M. A. Dynamin: switch or pinchase? Curr. Biol. 11, R850 (2001).
4. Takei, K., McPherson, P. S., Schmid, S. L. & De Camilli, P. Tubular membrane invaginations coated by dynamin rings are induced by GTP-γS in nerve terminals. Nature 374, 186-190 (1995).
5. Hinshaw, J. E. & Schmid, S. L. Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature 374, 190-192 (1995).
6. Praefcke, G. J. & McMahon, H. T. The dynamin superfamily: universal membrane tubulation and fission molecules? Nature Rev. Mol. Cell Biol. 5, 133-147 (2004).
7. Sever, S., Muhlberg, A. B. & Schmid, S. L. Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature 398, 481-486 (1999).
8. Stowell, M. H., Marks, B., Wigge, P. & McMahon, H. T. Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nature Cell Biol. 1, 27-32 (1999).
9. Slepnev, V. I. & De Camilli, P. Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nature Rev. Neurosci. 1, 161-172 (2000).
10. Merrifield, C. J., Perrais, D. & Zenisek, D. Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121, 593-606 (2005).
11. 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).
12. Qualmann, B., Kessels, M. M. & Kelly, R. B. Molecular links between endocytosis and the actin cytoskeleton. J. Cell Biol. 150, F111-F116 (2000).
13. Cao, H. et al. Cortactin is a component of clathrin-coated pits and participates in receptor-mediated endocytosis. Mol. Cell. Biol. 23, 2162-2170 (2003).
14. Sweitzer, S. M. & Hinshaw, J. E. Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021-1029 (1998).
15. Takei, K., Slepnev, V. I., Haucke, V. & De Camilli, P. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nature Cell Biol. 1, 33-39 (1999).
16. Farsad, K. et al. Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell Biol. 155, 193-200 (2001).
17. Danino, D., Moon, K. H. & Hinshaw, J. E. Rapid constriction of lipid bilayers by the mechanochemical enzyme dynamin. J. Struct. Biol. 147, 259-267 (2004).
18. Tsafrir, I., Caspi, Y., Guedeau-Boudeville, M. A., Arzi, T. & Stavans, J. Budding and tubulation in highly oblate vesicles by anchored amphiphilic molecules. Phys. Rev. Lett. 91, 138102 (2003).
19. Roux, A. et al. A minimal system allowing tubulation with molecular motors pulling on giant liposomes. Proc. Natl Acad. Sci. USA 99, 5394-5399 (2002).
20. Leduc, C. et al. Cooperative extraction of membrane nanotubes by molecular motors. Proc. Natl Acad. Sci. USA 101, 17096-17101 (2004).
21. Chen, Y. J., Zhang, P., Egelman, E. H. & Hinshaw, J. E. The stalk region of dynamin drives the constriction of dynamin tubes. Nature Struct. Mol. Biol. 11, 574-575 (2004).
22. Shpetner, H. S. & Vallee, R. B. Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules. Cell 59, 421-432 (1989).
23. Obar, R. A., Collins, C. A., Hammarback, J. A., Shpetner, H. S. & Vallee, R. B. Molecular cloning of the microtubule-associated mechanochemical enzyme dynamin reveals homology with a new family of GTP-binding proteins. Nature 347, 256-261 (1990).
24. Zhang, P. & Hinshaw, J. E. Three-dimensional reconstruction of dynamin in the constricted state. Nature Cell Biol. 3, 922-926 (2001).
25. Charvin, G., Bensimon, D. & Croquette, V. Single-molecule study of DNA unlinking by eukaryotic and prokaryotic type-II topoisomerases. Proc. Natl Acad. Sci. USA 100, 9820-9825 (2003).
26. Orth, J. D. & McNiven, M. A. Dynamin at the actin-membrane interface. Curr. Opin. Cell Biol. 15, 31-39 (2003).
27. Schafer, D. A. Regulating actin dynamics at membranes: a focus on dynamin. Traffic 5, 463-469 (2004).
28. Kaksonen, M., Toret, C. P. & Drubin, D. G. A modular design for the clathrin-and actin-mediated endocytosis machinery. Cell 123, 305-320 (2005).
29. Roux, A. et al. Role of curvature and phase transition in lipid sorting and fission of membrane tubules. EMBO J. 24, 1537-1545 (2005).
30. Moscho, A., Orwar, O., Chiu, D. T., Modi, B. P. & Zare, R. N. Rapid preparation of giant unilamellar vesicles. Proc. Natl Acad. Sci. USA 93, 11443-11447 (1996).