GTPase Cycle of Dynamin Is Coupled to Membrane Squeeze and Release, Leading to Spontaneous Fission

Pavel V. Bashkirov, Sergey A. Akimov, Alexey I. Evseev, Sandra L. Schmid, Joshua Zimmerberg, Vadim A. Frolov

Research output: Contribution to journalArticle

215 Citations (Scopus)

Abstract

The GTPase dynamin is critically involved in membrane fission during endocytosis. How does dynamin use the energy of GTP hydrolysis for membrane remodeling? By monitoring the ionic permeability through lipid nanotubes (NT), we found that dynamin was capable of squeezing NT to extremely small radii, depending on the NT lipid composition. However, long dynamin scaffolds did not produce fission: instead, fission followed GTPase-dependent cycles of assembly and disassembly of short dynamin scaffolds and involved a stochastic process dependent on the curvature stress imposed by dynamin. Fission happened spontaneously upon NT release from the scaffold, without leakage. Our calculations revealed that local narrowing of NT could induce cooperative lipid tilting, leading to self-merger of the inner monolayer of NT (hemifission), consistent with the absence of leakage. We propose that dynamin transmits GTP's energy to periodic assembling of a limited curvature scaffold that brings lipids to an unstable intermediate.

Original languageEnglish (US)
Pages (from-to)1276-1286
Number of pages11
JournalCell
Volume135
Issue number7
DOIs
StatePublished - Dec 26 2008

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Dynamins
GTP Phosphohydrolases
Nanotubes
Membranes
Scaffolds
Lipids
Guanosine Triphosphate
Stochastic Processes
Endocytosis
Random processes
Hydrolysis
Monolayers
Permeability
Monitoring
Chemical analysis

Keywords

  • CELLBIO

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Bashkirov, P. V., Akimov, S. A., Evseev, A. I., Schmid, S. L., Zimmerberg, J., & Frolov, V. A. (2008). GTPase Cycle of Dynamin Is Coupled to Membrane Squeeze and Release, Leading to Spontaneous Fission. Cell, 135(7), 1276-1286. https://doi.org/10.1016/j.cell.2008.11.028

GTPase Cycle of Dynamin Is Coupled to Membrane Squeeze and Release, Leading to Spontaneous Fission. / Bashkirov, Pavel V.; Akimov, Sergey A.; Evseev, Alexey I.; Schmid, Sandra L.; Zimmerberg, Joshua; Frolov, Vadim A.

In: Cell, Vol. 135, No. 7, 26.12.2008, p. 1276-1286.

Research output: Contribution to journalArticle

Bashkirov, PV, Akimov, SA, Evseev, AI, Schmid, SL, Zimmerberg, J & Frolov, VA 2008, 'GTPase Cycle of Dynamin Is Coupled to Membrane Squeeze and Release, Leading to Spontaneous Fission', Cell, vol. 135, no. 7, pp. 1276-1286. https://doi.org/10.1016/j.cell.2008.11.028
Bashkirov, Pavel V. ; Akimov, Sergey A. ; Evseev, Alexey I. ; Schmid, Sandra L. ; Zimmerberg, Joshua ; Frolov, Vadim A. / GTPase Cycle of Dynamin Is Coupled to Membrane Squeeze and Release, Leading to Spontaneous Fission. In: Cell. 2008 ; Vol. 135, No. 7. pp. 1276-1286.
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