Deformation and flow of membrane into tethers extracted from neuronal growth cones

Robert M. Hochmuth, Jin Yu Shao, Jianwu Dai, Michael Sheetz

Research output: Contribution to journalArticle

272 Citations (Scopus)

Abstract

Membrane tethers are extracted at constant velocity from neuronal growth cones using a force generated by a laser tweezers trap. A thermodynamic analysis shows that as the tether is extended, energy is stored in the tether as bending and adhesion energies and in the cell body as 'nonlocal' bending. It is postulated that energy is dissipated by three viscous mechanisms including membrane flow, slip between the two monolayers that form the bilayer, and slip between membrane and cytoskeleton. The analysis predicts and the experiments show a linear relation between tether force and tether velocity. Calculations based on the analytical results and the experimental measurements of a tether radius of ~0.2 μm and a tether force at zero velocity of ~8 pN give a bending modulus for the tether of 2.7 x 10-19 N · m and an extraordinarily small 'apparent surface tension' in the growth cone of 0.003 mN/m, where the apparent surface tension is the sum of the far- field, in-plane tension and the energy of adhesion. Treatments with cytochalasin B and D, ethanol, and nocodazole affect the apparent surface tension but not bending. ATP depletion affects neither, whereas large concentrations of DMSO affect both. Under conditions of flow, data are presented to show that the dominant viscous mechanism comes from the slip that occurs when the membrane flows over the cytoskeleton. ATP depletion and the treatment with DMSO cause a dramatic drop in the effective viscosity. If it is postulated that the slip between membrane and cytoskeleton occurs in a film of water, then this water film has a mean thickness of only ~10 Å.

Original languageEnglish (US)
Pages (from-to)358-369
Number of pages12
JournalBiophysical Journal
Volume70
Issue number1
DOIs
StatePublished - Jan 1 1996
Externally publishedYes

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Growth Cones
Surface Tension
Cytoskeleton
Membranes
Dimethyl Sulfoxide
Adenosine Triphosphate
Optical Tweezers
Nocodazole
Cytochalasin D
Cytochalasin B
Water
Thermodynamics
Viscosity
Ethanol

ASJC Scopus subject areas

  • Biophysics

Cite this

Deformation and flow of membrane into tethers extracted from neuronal growth cones. / Hochmuth, Robert M.; Shao, Jin Yu; Dai, Jianwu; Sheetz, Michael.

In: Biophysical Journal, Vol. 70, No. 1, 01.01.1996, p. 358-369.

Research output: Contribution to journalArticle

Hochmuth, Robert M. ; Shao, Jin Yu ; Dai, Jianwu ; Sheetz, Michael. / Deformation and flow of membrane into tethers extracted from neuronal growth cones. In: Biophysical Journal. 1996 ; Vol. 70, No. 1. pp. 358-369.
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