Membrane tension in swelling and shrinking molluscan neurons

Jianwu Dai, Michael Sheetz, Xiaodong Wan, Catherine E. Morris

Research output: Contribution to journalArticle

146 Citations (Scopus)

Abstract

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 retrieval-provides 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.

Original languageEnglish (US)
Pages (from-to)6681-6692
Number of pages12
JournalJournal of Neuroscience
Volume18
Issue number17
StatePublished - Sep 1 1998
Externally publishedYes

Fingerprint

Neurons
Membranes
Lymnaea
Vacuoles
Rupture
Dilatation
Homeostasis
1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid

Keywords

  • BAPTA
  • Cell volume
  • Laser tweezers
  • Mechanosensitive
  • Surface area
  • Vacuole- like dilations

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Dai, J., Sheetz, M., Wan, X., & Morris, C. E. (1998). Membrane tension in swelling and shrinking molluscan neurons. Journal of Neuroscience, 18(17), 6681-6692.

Membrane tension in swelling and shrinking molluscan neurons. / Dai, Jianwu; Sheetz, Michael; Wan, Xiaodong; Morris, Catherine E.

In: Journal of Neuroscience, Vol. 18, No. 17, 01.09.1998, p. 6681-6692.

Research output: Contribution to journalArticle

Dai, J, Sheetz, M, Wan, X & Morris, CE 1998, 'Membrane tension in swelling and shrinking molluscan neurons', Journal of Neuroscience, vol. 18, no. 17, pp. 6681-6692.
Dai, Jianwu ; Sheetz, Michael ; Wan, Xiaodong ; Morris, Catherine E. / Membrane tension in swelling and shrinking molluscan neurons. In: Journal of Neuroscience. 1998 ; Vol. 18, No. 17. pp. 6681-6692.
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