Nucleotide-dependent conformational changes in dynamin: Evidence for a mechanochemical molecular spring

Nature Cell Biology

Volumn 1, Issue 1, 1999, Pages 27-32

  Stowell, Michael H B ^a   Marks, Bruno ^a   Wigge, Patrick ^a   McMahon, Harvey T ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; LIPOSOME; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BRAIN LEVEL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; ENDOCYTOSIS; KINETICS; METABOLISM; PROTEIN CONFORMATION; RAT; ULTRASTRUCTURE;

ANIMALS; BRAIN CHEMISTRY; DYNAMINS; ENDOCYTOSIS; GTP PHOSPHOHYDROLASES; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; KINETICS; LIPOSOMES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN CONFORMATION; RATS;

EID: 0033128097     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/8997     Document Type: Article

References (47)

1. Roos, J. & Kelly, R. B. Is dynamin really a 'pinchase'? Trends Cell Biol. 7, 257-259 (1997).
2. McNiven, M. A. Dynamin: a molecular motor with pinchase action. Cell 94, 151-154 (1998).
3. Schmid, S. L. Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem. 66, 511-548 (1997).
4. DeCamilli, P. & Takei, K. Molecular mechanisms in synaptic vesicle endocytosis and recycling. Neuron 16, 481-486 (1996).
5. Poodry, C. A. & Edgar, L. Reversible alterations in the neuromuscular junctions of Drosophila melanogaster bearing a temperature-sensitive mutation, shibire. J. Cell Biol. 81, 520-527 (1979).
6. 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).
7. Ramaswami, M., Krishnan, K. S. & Kelly, R. B. Intermediates in synaptic vesicle recycling revealed by optical imaging of Drosophila neuromuscular junctions. Neuron 13, 363-375 (1994).
8. Takei, K., McPherson, P. S., Schmid, S. L. & DeCamilli, P. Tubular membrane invaginations coated by dynamin rings are induced by GTPγS in nerve terminals. Nature 374, 186-190 (1995).
9. Herskovits, J. S., Burgess, C. C., Obar, R. A. & Vallee, R. B. Effects of mutant rat dynamin on endocytosis. J. Cell Biol. 122, 565-578 (1993).
10. van der Bliek, A. M. et al. Mutations in human dynamin block an intermediate stage in coated vesicle formation. J. Cell Biol. 122, 553-563 (1993).
11. Wigge, P. & McMahon, H. T. The amphiphysin family of proteins and their role in endocytosis at the synapse. Trends Neurosci. 21, 339-344 (1998).
12. Shupliakov, O. et al. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276, 259-263 (1997).
13. Marks, B. & McMahon, H. T. Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr. Biol. 8, 740-749 (1998).
14. Slepnev, V. I., Ochoa, G. C., Butler, M. H., Grabs, D. & DeCamilli, P. Role of phosphorylation in regulation of the assembly of endocytic coat complexes. Science 281, 821-824 (1998).
15. Owen, D. J. et al. Crystal structure of the Amphiphysin-2 SH3 domain and its role in prevention of dynamin ring formation. EMBO J. 17, 5273-5285 (1998).
16. Vallis, Y., Wigge, P., Marks, B., Evans, P. R. & McMahon, H. T. Importance of the pleckstrin homology domain of dynamin in clathrin-mediated endocytosis. Curr. Biol. 9, 257-260 (1999).
17. Achiriloaie, M., Barylko, B. & Albanesi, J. P. Essential role of the dynamin pleckstrin homology domain in receptor mediated endocytosis. Mol. Cell. Biol. 19, 1410-1415 (1999).
18. Zheng, J. et al. Identification of the binding site for acidic phospholipids on the pH domain of dynamin: implications for stimulation of GTPase activity. J. Mol. Biol. 255, 14-21 (1996).
19. Salim, K. et al. Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. EMBO J. 15, 6241-6250 (1996).
20. 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).
21. Barylko, B. et al. Synergistic activation of dynamin GTPase by Grb2 and phosphoinositides. J. Biol. Chem. 273, 3791-3797 (1998).
22. McPherson, P.S. et al. A presynaptic inositol-5-phosphatase. Nature 379, 353-357 (1996).
23. Takei, K. et al. Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell 94, 131-141 (1998).
24. Sweitzer, S. M. & Hinshaw, J. E. Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021-1029 (1998).
25. Koenig, J. H. & Ikeda, K. Synaptic vesicles have two distinct recycling pathways. J. Cell Biol. 135, 797-808 (1996).
26. Deutsch, J. W. & Kelly, R. B. Lipids of synaptic vesicles: relevance to the mechanism of membrane fusion. Biochemistry 20, 378-385 (1981).
27. Tuma, P. L., Stachniak, M. C. & Collins, C. A. Activation of dynamin GTPase by acidic phospholipids and endogenous rat brain vesicles. J. Biol. Chem. 268, 17240-17246 (1993).
28. Steinweis, P. C. & Gilman, A. G. Aluminium: a requirement for activation of the regulatory component of adenylate cyclase by fluoride. Proc. Natl Acad. Sci. USA 79, 4888-4891 (1982).
29. Carr, J. F. & Hinshaw, I. E. Dynamin assembles into spirals under physiological salt conditions upon the addition of GDP and gamma-phosphate analogues. J. Biol. Chem. 272, 28030-28035 (1997).
30. Shpetner, H. S. & Vallee, R. B. Dynamin is a GTPase stimulated to high levels of activity by microtubules. Nature 355, 733-735 (1992).
31. Gout, I. et al. The GTPase dynamin binds to and is activated by a subset of SH3 domains. Cell 75, 25-36 (1993).
32. Herskovits, J. S., Shpetner, H. S., Burgess, C. C. & Vallee, R. B. Microtubules and src homology 3 domains stimulate the dynamin GTPase via its C-terminal domain. Proc. Natl Acad. Sci. USA 90, 11468-11472 (1993).
33. Robinson, P. J. et al. Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals. Nature 365, 107-108 (1993).
34. Tuma, P. L. & Collins, C. A. Activation of dynamin GTPase is a result of positive cooperativity. J. Biol. Chem. 269, 30842-30847 (1994).
35. Warnock, D. E., Hinshaw, J. E. & Schmid, S. L. Dynamin self-assembly stimulates its GTPase activity. J. Biol. Chem. 271, 22310-22314 (1996).
36. Shpetner, H. S. & Vallee, R. B. Identification of dynamin, a novel mechanochemical enzyme that mediates interactions among microtubules. Cell 59, 421-432 (1989).
37. Otero, A. D. Transphosphorylation and G protein activation. Biochem. Pharmacol. 39, 1399-1404 (1990).
38. Monod, J., Wyman, J. & Changeux, J.-P. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12, 88-118 (1965).
39. Smith, C. J., Grigorieff, N. & Pearse, B. M. Clathrin coats at 21 Å resolution: a cellular assembly designed to recycle multiple membrane receptors. EMBO J. 17, 4943-4953 (1998).
40. Heuser, J. E. The role of coated vesicles in recycling of synaptic vesicle membrane. Cell Biol. Int. Report 13, 1063-1076 (1989).
41. Needham, D. & Nunn, R. S. Elastic deformation and failure of lipid bilayer membranes containing cholesterol. Biophys. J. 58, 997-1009 (1990).
42. Block, S. M. Nanometers and piconewtons - the macromolecular mechanics of kinesin. Trends Cell Biol. 5, 169 (1995).
43. Takei, K., Slepnev, V. I., Hauck, V. & De Camilli, P. Amphiphysin tubulates protein free liposomes and regulates the formation of clathrin- and dynamin-coated structures in vitro. Mol. Biol. Cell Abstr. 9-S, 130 (1998).
44. Polyakov, A., Severinova, E. & Darst, S. A. Three dimensional structure of E coli core RNA polymerase: promoter binding and elongation conformations of the enzyme. Cell 83, 365-373 (1995).
45. Warnock, D. E. & Schmid, S. L. Dynamin GTPase, a force-generating molecular switch. Bioessays 18, 885-894 (1996).
46. Goldstein, A. S., Lukyanov, A. N., Carlson, P. A., Yager, P. & Gelb, M. H. Formation of high-axial-ratio-microstructures from natural and synthetic sphingolipids. Chem. Phys. Lipids 88, 21-36 (1997).
47. Wigge, P. et al. Amphiphysin heterodimers: potential role in clathrin-mediated endocytosis. Mol. Biol. Cell 8, 2003-2015 (1997).