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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
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