 |
 Previous Article | Next Article 
The Journal of Neuroscience, September 1, 1998, 18(17):6681-6692
Membrane Tension in Swelling and Shrinking Molluscan Neurons
Jianwu
Dai1,
Michael P.
Sheetz1,
Xiaodong
Wan2, and
Catherine E.
Morris2
1 Department of Cell Biology, Duke University Medical
Center, Durham, North Carolina 27710, and 2 Neurosciences,
Loeb Institute, Ottawa, Ontario, Canada, K1Y 4E9
When neurons undergo dramatic shape and volume changes, how is
surface area adjusted appropriately? The membrane tension
hypothesis namely that high tensions favor recruitment of membrane to
the surface whereas low tensions favor retrievalprovides a simple
conceptual framework for surface area homeostasis.
With membrane tension and area in a feedback loop, tension extremes may
be averted even during excessive mechanical load variations. We tested
this by measuring apparent membrane tension of swelling and shrinking
Lymnaea neurons. With hypotonic medium (50%), tension that was calculated from membrane tether forces increased from 0.04 to
as much as 0.4 mN/m, although at steady state, swollen-cell tension
(0.12 mN/m) exceeded controls only threefold. On reshrinking in
isotonic medium, tension reduced to 0.02 mN/m, and at the substratum, membrane invaginated, creating transient vacuole-like dilations. Swelling increased membrane tension with or without BAPTA chelating cytoplasmic Ca2+, but with BAPTA, unmeasurably large
(although not lytic) tension surges occurred in approximately
two-thirds of neurons. Furthermore, in unarborized neurons
voltage-clamped by perforated-patch in 50% medium, membrane
capacitance increased 8%, which is indicative of increasing membrane
area.
The relatively damped swelling-tension responses of
Lymnaea neurons (no BAPTA) were consistent with feedback
regulation. BAPTA did not alter resting membrane tension, but the large
surges during swelling of BAPTA-loaded neurons demonstrated that 50%
medium was inherently treacherous and that tension regulation was
impaired by subnormal cytoplasmic [Ca2+]. However,
neurons did survive tension surges in the absence of
Ca2+ signaling. The mechanism to avoid high-tension
rupture may be the direct tension-driven recruitment of membrane
stores.
Key words:
surface area; mechanosensitive; cell volume; BAPTA; laser
tweezers; vacuole-like dilations
Copyright © 1998 Society for Neuroscience 0270-6474/98/18176681-12$05.00/0
This article has been cited by other articles:
|
|
|
|
 
W. Liang, J. B. Ray, J. Z. He, P. H. Backx, and M. E. Ward
Regulation of Proliferation and Membrane Potential by Chloride Currents in Rat Pulmonary Artery Smooth Muscle Cells
Hypertension,
August 1, 2009;
54(2):
286 - 293.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Schmidt and R. MacKinnon
Voltage-dependent K+ channel gating and voltage sensor toxin sensitivity depend on the mechanical state of the lipid membrane
PNAS,
December 9, 2008;
105(49):
19276 - 19281.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Sun, N. Northup, F. Marga, T. Huber, F. J. Byfield, I. Levitan, and G. Forgacs
The effect of cellular cholesterol on membrane-cytoskeleton adhesion
J. Cell Sci.,
July 1, 2007;
120(13):
2223 - 2231.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Pieraut, V. Laurent-Matha, C. Sar, T. Hubert, I. Mechaly, C. Hilaire, M. Mersel, E. Delpire, J. Valmier, and F. Scamps
NKCC1 Phosphorylation Stimulates Neurite Growth of Injured Adult Sensory Neurons
J. Neurosci.,
June 20, 2007;
27(25):
6751 - 6759.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. P. Jackson
The growing complexity of platelet aggregation
Blood,
June 15, 2007;
109(12):
5087 - 5095.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. L. Fisher and S. S. Margulies
Modeling the effect of stretch and plasma membrane tension on Na+-K+-ATPase activity in alveolar epithelial cells
Am J Physiol Lung Cell Mol Physiol,
January 1, 2007;
292(1):
L40 - L53.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J.-B. Masson, M.-P. Sauviat, J.-L. Martin, and G. Gallot
Ionic contrast terahertz near-field imaging of axonal water fluxes
PNAS,
March 28, 2006;
103(13):
4808 - 4812.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. L. Fisher, I. Levitan, and S. S. Margulies
Plasma Membrane Surface Increases with Tonic Stretch of Alveolar Epithelial Cells
Am. J. Respir. Cell Mol. Biol.,
August 1, 2004;
31(2):
200 - 208.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Ben-Tabou De-Leon, E. Blotnick, and I. Nussinovitch
Effects of osmotic swelling on voltage-gated calcium channel currents in rat anterior pituitary cells
Am J Physiol Cell Physiol,
October 1, 2003;
285(4):
C840 - C852.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L.-W. Gong, I. Hafez, G. Alvarez de Toledo, and M. Lindau
Secretory Vesicles Membrane Area Is Regulated in Tandem with Quantal Size in Chromaffin Cells
J. Neurosci.,
August 27, 2003;
23(21):
7917 - 7921.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. E. Vlahakis, M. A. Schroeder, R. E. Pagano, and R. D. Hubmayr
Role of Deformation-induced Lipid Trafficking in the Prevention of Plasma Membrane Stress Failure
Am. J. Respir. Crit. Care Med.,
November 1, 2002;
166(9):
1282 - 1289.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Apodaca
Modulation of membrane traffic by mechanical stimuli
Am J Physiol Renal Physiol,
February 1, 2002;
282(2):
F179 - F190.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. E. Morris
Mechanosensitive Membrane Traffic and an Optimal Strategy for Volume and Surface Area Regulation in CNS Neurons
Integr. Comp. Biol.,
August 1, 2001;
41(4):
721 - 727.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
O. P. Hamill and B. Martinac
Molecular Basis of Mechanotransduction in Living Cells
Physiol Rev,
April 1, 2001;
81(2):
685 - 740.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T Tani, R. Allen, and Y Naitoh
Cellular membranes that undergo cyclic changes in tension: Direct measurement of force generation by an in vitro contractile vacuole of Paramecium multimicronucleatum
J. Cell Sci.,
January 2, 2001;
114(4):
785 - 795.
[Abstract]
[PDF]
|
|
|
|
|
|
|
N. E. Vlahakis and R. D. Hubmayr
Cellular Responses to Mechanical Stress: Invited Review: Plasma membrane stress failure in alveolar epithelial cells
J Appl Physiol,
December 1, 2000;
89(6):
2490 - 2496.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Zhang and O. P Hamill
On the discrepancy between whole-cell and membrane patch mechanosensitivity in Xenopus oocytes
J. Physiol.,
February 15, 2000;
523(1):
101 - 115.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Raucher and M. P. Sheetz
Cell Spreading and Lamellipodial Extension Rate Is Regulated by Membrane Tension
J. Cell Biol.,
January 10, 2000;
148(1):
127 - 136.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
X. Wan, P. Juranka, and C. E. Morris
Activation of mechanosensitive currents in traumatized membrane
Am J Physiol Cell Physiol,
February 1, 1999;
276(2):
C318 - C327.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T Tominaga, Y Naitoh, and R. Allen
A key function of non-planar membranes and their associated microtubular ribbons in contractile vacuole membrane dynamics is revealed by electrophysiologically controlled fixation of Paramecium
J. Cell Sci.,
January 11, 1999;
112(21):
3733 - 3745.
[Abstract]
[PDF]
|
|
|
|
|
