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Biophys J, June 2001, p. 2678-2693, Vol. 80, No. 6
Department of Medicine, University of Ottawa, Neurosciences, Ottawa Health Research Institute, The Ottawa Hospital, Ottawa, Ontario K1Y 4K9, Canada
Mechanosensitive (MS) ion channels are ubiquitous in
eukaryotic cell types but baffling because of their contentious
physiologies and diverse molecular identities. In some cellular
contexts mechanically responsive ion channels are undoubtedly
mechanosensory transducers, but it does not follow that all MS channels
are mechanotransducers. Here we demonstrate, for an archetypical
voltage-gated channel (Shaker-IR; inactivation-removed),
robust MS channel behavior. In oocyte patches subjected to stretch,
Shaker-IR exhibits both stretch-activation (SA) and
stretch-inactivation (SI). SA is seen when prestretch
Popen (set by voltage) is low, and SI is
seen when it is high. The stretch effects occur in cell-attached and excised patches at both macroscopic and single-channel levels. Were one
ignorant of this particular MS channel's identity, one might propose
it had been designed as a sophisticated reporter of bilayer tension.
Knowing Shaker-IR's provenance and biology, however,
such a suggestion would be absurd. We argue that the MS responses of
Shaker-IR reflect not overlooked "mechano-gating" specializations of Shaker, but a common property of
multiconformation membrane proteins: inherent susceptibility to bilayer
tension. The molecular diversity of MS channels indicates that
susceptibility to bilayer tension is hard to design out of dynamic
membrane proteins. Presumably the cost of being insusceptible to
bilayer tension often outweighs the benefits, especially where the in
situ milieu of channels can provide mechanoprotection.
Biophys J, June 2001, p. 2678-2693, Vol. 80, No. 6
© 2001 by the Biophysical Society 0006-3495/01/06/2678/16 $2.00
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