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Adaptive behavior of bacterial mechanosensitive channels is coupled to membrane mechanics

Mechanosensitive channel of small conductance (MscS), a tension-driven osmolyte release valve residing in the inner membrane of Escherichia coli, exhibits a complex adaptive behavior, whereas its functional counterpart, mechanosensitive channel of large conductance (MscL), was generally considered n...

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Autores principales: Belyy, Vladislav, Kamaraju, Kishore, Akitake, Bradley, Anishkin, Andriy, Sukharev, Sergei
Formato: Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2888061/
https://www.ncbi.nlm.nih.gov/pubmed/20513760
http://dx.doi.org/10.1085/jgp.200910371
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author Belyy, Vladislav
Kamaraju, Kishore
Akitake, Bradley
Anishkin, Andriy
Sukharev, Sergei
author_facet Belyy, Vladislav
Kamaraju, Kishore
Akitake, Bradley
Anishkin, Andriy
Sukharev, Sergei
author_sort Belyy, Vladislav
collection PubMed
description Mechanosensitive channel of small conductance (MscS), a tension-driven osmolyte release valve residing in the inner membrane of Escherichia coli, exhibits a complex adaptive behavior, whereas its functional counterpart, mechanosensitive channel of large conductance (MscL), was generally considered nonadaptive. In this study, we show that both channels exhibit similar adaptation in excised patches, a process that is completely separable from inactivation prominent only in MscS. When a membrane patch is held under constant pressure, adaptation of both channels is manifested as a reversible current decline. Their dose–response curves recorded with 1–10-s ramps of pressure are shifted toward higher tension relative to the curves measured with series of pulses, indicating decreased tension sensitivity. Prolonged exposure of excised patches to subthreshold tensions further shifts activation curves for both MscS and MscL toward higher tension with similar magnitude and time course. Whole spheroplast MscS recordings performed with simultaneous imaging reveal activation curves with a midpoint tension of 7.8 mN/m and the slope corresponding to ∼15-nm(2) in-plane expansion. Inactivation was retained in whole spheroplast mode, but no adaptation was observed. Similarly, whole spheroplast recordings of MscL (V23T mutant) indicated no adaptation, which was present in excised patches. MscS activities tried in spheroplast-attached mode showed no adaptation when the spheroplasts were intact, but permeabilized spheroplasts showed delayed adaptation, suggesting that the presence of membrane breaks or edges causes adaptation. We interpret this in the framework of the mechanics of the bilayer couple linking adaptation of channels in excised patches to the relaxation of the inner leaflet that is not in contact with the glass pipette. Relaxation of one leaflet results in asymmetric redistribution of tension in the bilayer that is less favorable for channel opening.
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spelling pubmed-28880612010-12-01 Adaptive behavior of bacterial mechanosensitive channels is coupled to membrane mechanics Belyy, Vladislav Kamaraju, Kishore Akitake, Bradley Anishkin, Andriy Sukharev, Sergei J Gen Physiol Article Mechanosensitive channel of small conductance (MscS), a tension-driven osmolyte release valve residing in the inner membrane of Escherichia coli, exhibits a complex adaptive behavior, whereas its functional counterpart, mechanosensitive channel of large conductance (MscL), was generally considered nonadaptive. In this study, we show that both channels exhibit similar adaptation in excised patches, a process that is completely separable from inactivation prominent only in MscS. When a membrane patch is held under constant pressure, adaptation of both channels is manifested as a reversible current decline. Their dose–response curves recorded with 1–10-s ramps of pressure are shifted toward higher tension relative to the curves measured with series of pulses, indicating decreased tension sensitivity. Prolonged exposure of excised patches to subthreshold tensions further shifts activation curves for both MscS and MscL toward higher tension with similar magnitude and time course. Whole spheroplast MscS recordings performed with simultaneous imaging reveal activation curves with a midpoint tension of 7.8 mN/m and the slope corresponding to ∼15-nm(2) in-plane expansion. Inactivation was retained in whole spheroplast mode, but no adaptation was observed. Similarly, whole spheroplast recordings of MscL (V23T mutant) indicated no adaptation, which was present in excised patches. MscS activities tried in spheroplast-attached mode showed no adaptation when the spheroplasts were intact, but permeabilized spheroplasts showed delayed adaptation, suggesting that the presence of membrane breaks or edges causes adaptation. We interpret this in the framework of the mechanics of the bilayer couple linking adaptation of channels in excised patches to the relaxation of the inner leaflet that is not in contact with the glass pipette. Relaxation of one leaflet results in asymmetric redistribution of tension in the bilayer that is less favorable for channel opening. The Rockefeller University Press 2010-06 /pmc/articles/PMC2888061/ /pubmed/20513760 http://dx.doi.org/10.1085/jgp.200910371 Text en © 2010 Belyy et al. This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).
spellingShingle Article
Belyy, Vladislav
Kamaraju, Kishore
Akitake, Bradley
Anishkin, Andriy
Sukharev, Sergei
Adaptive behavior of bacterial mechanosensitive channels is coupled to membrane mechanics
title Adaptive behavior of bacterial mechanosensitive channels is coupled to membrane mechanics
title_full Adaptive behavior of bacterial mechanosensitive channels is coupled to membrane mechanics
title_fullStr Adaptive behavior of bacterial mechanosensitive channels is coupled to membrane mechanics
title_full_unstemmed Adaptive behavior of bacterial mechanosensitive channels is coupled to membrane mechanics
title_short Adaptive behavior of bacterial mechanosensitive channels is coupled to membrane mechanics
title_sort adaptive behavior of bacterial mechanosensitive channels is coupled to membrane mechanics
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2888061/
https://www.ncbi.nlm.nih.gov/pubmed/20513760
http://dx.doi.org/10.1085/jgp.200910371
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