Abstract
Dynamin is a GTPase playing an essential role in ubiquitous intra cellular processes involving separation of vesicles from plasma membranes and membranes of cellular compartments. Recent experimental progress (. Cell. 93:1021-1029;. Cell. 94:131-141) has made it possible to attempt to understand the action of dynamin in physical terms. Dynamin molecules are shown to bind to a lipid membrane, to self-assemble into a helicoidal structure constricting the membrane into a tubule, and, as a result of GTP hydrolysis, to mediate fission of this tubule (). In a similar way, dynamin is supposed to mediate fission of a neck connecting an endocytic bud and the plasma membrane, i.e., to complete endocytosis. We suggest a mechanism of this "pinchase" action of dynamin. We propose that, as a result of GTP hydrolysis, dynamin undergoes a conformational change manifested in growth of the pitch of the dynamin helix. We show that this gives rise to a dramatic change of shape of the tubular membrane constricted inside the helix, resulting in a local tightening of the tubule, which is supposed to promote its fission. We treat this model in terms of competing elasticities of the dynamin helix and the tubular membrane and discuss the predictions of the model in relation to the previous views on the mechanism of dynamin action.
Full Text
The Full Text of this article is available as a PDF (703.4 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bar-Ziv R., Moses E., Nelson P. Dynamic excitations in membranes induced by optical tweezers. Biophys J. 1998 Jul;75(1):294–320. doi: 10.1016/S0006-3495(98)77515-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carr J. F., Hinshaw J. E. Dynamin assembles into spirals under physiological salt conditions upon the addition of GDP and gamma-phosphate analogues. J Biol Chem. 1997 Oct 31;272(44):28030–28035. doi: 10.1074/jbc.272.44.28030. [DOI] [PubMed] [Google Scholar]
- Helfrich W. Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch C. 1973 Nov-Dec;28(11):693–703. doi: 10.1515/znc-1973-11-1209. [DOI] [PubMed] [Google Scholar]
- Henley J. R., Krueger E. W., Oswald B. J., McNiven M. A. Dynamin-mediated internalization of caveolae. J Cell Biol. 1998 Apr 6;141(1):85–99. doi: 10.1083/jcb.141.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hinshaw J. E., Schmid S. L. Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature. 1995 Mar 9;374(6518):190–192. doi: 10.1038/374190a0. [DOI] [PubMed] [Google Scholar]
- Jones S. M., Howell K. E., Henley J. R., Cao H., McNiven M. A. Role of dynamin in the formation of transport vesicles from the trans-Golgi network. Science. 1998 Jan 23;279(5350):573–577. doi: 10.1126/science.279.5350.573. [DOI] [PubMed] [Google Scholar]
- Kirchhausen T. Vesicle formation: dynamic dynamin lives up to its name. Curr Biol. 1998 Nov 5;8(22):R792–R794. doi: 10.1016/s0960-9822(07)00501-5. [DOI] [PubMed] [Google Scholar]
- Kosaka T., Ikeda K. Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. J Neurobiol. 1983 May;14(3):207–225. doi: 10.1002/neu.480140305. [DOI] [PubMed] [Google Scholar]
- Lipowsky R. The morphology of lipid membranes. Curr Opin Struct Biol. 1995 Aug;5(4):531–540. doi: 10.1016/0959-440x(95)80040-9. [DOI] [PubMed] [Google Scholar]
- McNiven M. A. Dynamin: a molecular motor with pinchase action. Cell. 1998 Jul 24;94(2):151–154. doi: 10.1016/s0092-8674(00)81414-2. [DOI] [PubMed] [Google Scholar]
- Oh P., McIntosh D. P., Schnitzer J. E. Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J Cell Biol. 1998 Apr 6;141(1):101–114. doi: 10.1083/jcb.141.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schmid S. L., McNiven M. A., De Camilli P. Dynamin and its partners: a progress report. Curr Opin Cell Biol. 1998 Aug;10(4):504–512. doi: 10.1016/s0955-0674(98)80066-5. [DOI] [PubMed] [Google Scholar]
- Sweitzer S. M., Hinshaw J. E. Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell. 1998 Jun 12;93(6):1021–1029. doi: 10.1016/s0092-8674(00)81207-6. [DOI] [PubMed] [Google Scholar]
- Takei K., Haucke V., Slepnev V., Farsad K., Salazar M., Chen H., De Camilli P. Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell. 1998 Jul 10;94(1):131–141. doi: 10.1016/s0092-8674(00)81228-3. [DOI] [PubMed] [Google Scholar]
- Takei K., McPherson P. S., Schmid S. L., De Camilli P. Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature. 1995 Mar 9;374(6518):186–190. doi: 10.1038/374186a0. [DOI] [PubMed] [Google Scholar]
- Urrutia R., Henley J. R., Cook T., McNiven M. A. The dynamins: redundant or distinct functions for an expanding family of related GTPases? Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):377–384. doi: 10.1073/pnas.94.2.377. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Warnock D. E., Schmid S. L. Dynamin GTPase, a force-generating molecular switch. Bioessays. 1996 Nov;18(11):885–893. doi: 10.1002/bies.950181107. [DOI] [PubMed] [Google Scholar]
- Zhelev D. V. Material property characteristics for lipid bilayers containing lysolipid. Biophys J. 1998 Jul;75(1):321–330. doi: 10.1016/S0006-3495(98)77516-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhelev D. V., Needham D. Tension-stabilized pores in giant vesicles: determination of pore size and pore line tension. Biochim Biophys Acta. 1993 Apr 8;1147(1):89–104. doi: 10.1016/0005-2736(93)90319-u. [DOI] [PubMed] [Google Scholar]