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      Bacterial mechanosensitive channels: progress towards an understanding of their roles in cell physiology

      review-article
      1 , 2
      Current Opinion in Microbiology
      Current Biology

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          Highlights

          • Multiple mechanosensitive channels are found in most bacteria and archaea.

          • Channels are required to prevent loss of structural integrity during transitions from high to low osmolarity.

          • Channel diversity feeds into the detailed response of cells to hypo-osmotic stress.

          • There is growing evidence that organisms have evolved MS channels that reflect their niche.

          • Structural diversity may reflect roles additional to the observed function of protection of structural integrity.

          Abstract

          Bacterial mechanosensitive channels sense the changes in lateral tension in the bilayer of the cytoplasmic membrane generated by rapid water flow into the cell. Two major structural families are found widely distributed across bacteria and archaea: MscL and MscS. Our understanding of the mechanisms of gating has advanced rapidly through genetic analysis, structural biology and electrophysiology. It is only recently that the analysis of the physiological roles of the channels has kept pace with mechanistic studies. Recent advances have increased our understanding of the role of the channels in preventing structural perturbation during osmotic transitions and its relationship to water flow across the membrane. It is to these recent developments that this review is dedicated.

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          Most cited references37

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          Molecular basis of mechanotransduction in living cells.

          The simplest cell-like structure, the lipid bilayer vesicle, can respond to mechanical deformation by elastic membrane dilation/thinning and curvature changes. When a protein is inserted in the lipid bilayer, an energetic cost may arise because of hydrophobic mismatch between the protein and bilayer. Localized changes in bilayer thickness and curvature may compensate for this mismatch. The peptides alamethicin and gramicidin and the bacterial membrane protein MscL form mechanically gated (MG) channels when inserted in lipid bilayers. Their mechanosensitivity may arise because channel opening is associated with a change in the protein's membrane-occupied area, its hydrophobic mismatch with the bilayer, excluded water volume, or a combination of these effects. As a consequence, bilayer dilation/thinning or changes in local membrane curvature may shift the equilibrium between channel conformations. Recent evidence indicates that MG channels in specific animal cell types (e.g., Xenopus oocytes) are also gated directly by bilayer tension. However, animal cells lack the rigid cell wall that protects bacteria and plants cells from excessive expansion of their bilayer. Instead, a cortical cytoskeleton (CSK) provides a structural framework that allows the animal cell to maintain a stable excess membrane area (i.e., for its volume occupied by a sphere) in the form of membrane folds, ruffles, and microvilli. This excess membrane provides an immediate membrane reserve that may protect the bilayer from sudden changes in bilayer tension. Contractile elements within the CSK may locally slacken or tighten bilayer tension to regulate mechanosensitivity, whereas membrane blebbing and tight seal patch formation, by using up membrane reserves, may increase membrane mechanosensitivity. In specific cases, extracellular and/or CSK proteins (i.e., tethers) may transmit mechanical forces to the process (e.g., hair cell MG channels, MS intracellular Ca(2+) release, and transmitter release) without increasing tension in the lipid bilayer.
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            A possible unifying principle for mechanosensation.

            Ching Kung (2005)
            Of Aristotle's five senses, we know that sight, smell and much of taste are initiated by ligands binding to G-protein-coupled receptors; however, the mechanical sensations of touch and hearing remain without a clear understanding of their molecular basis. Recently, the relevant force-transducing molecules--the mechanosensitive ion channels--have been identified. Such channel proteins purified from bacteria sense forces from the lipid bilayer in the absence of other proteins. Recent evidence has shown that lipids are also intimately involved in opening and closing the mechanosensitive channels of fungal, plant and animal species.
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              Mechanosensitive channels: what can they do and how do they do it?

              While mechanobiological processes employ diverse mechanisms, at their heart are force-induced perturbations in the structure and dynamics of molecules capable of triggering subsequent events. Among the best characterized force-sensing systems are bacterial mechanosensitive channels. These channels reflect an intimate coupling of protein conformation with the mechanics of the surrounding membrane; the membrane serves as an adaptable sensor that responds to an input of applied force and converts it into an output signal, interpreted for the cell by mechanosensitive channels. The cell can exploit this information in a number of ways: ensuring cellular viability in the presence of osmotic stress and perhaps also serving as a signal transducer for membrane tension or other functions. This review focuses on the bacterial mechanosensitive channels of large (MscL) and small (MscS) conductance and their eukaryotic homologs, with an emphasis on the outstanding issues surrounding the function and mechanism of this fascinating class of molecules. Copyright © 2011 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Curr Opin Microbiol
                Curr. Opin. Microbiol
                Current Opinion in Microbiology
                Current Biology
                1369-5274
                1879-0364
                1 April 2014
                April 2014
                : 18
                : 100
                : 16-22
                Affiliations
                [1 ]School of Medical Sciences, University of Aberdeen, Aberdeen, AB25 2ZD, United Kingdom
                [2 ]Visiting Associate in Chemistry, California Institute of Technology, Pasadena, CA 91125, United States
                Article
                S1369-5274(14)00007-1
                10.1016/j.mib.2014.01.005
                4005912
                24607989
                78361cf3-e17d-4692-9a07-b20fd28a383a
                © 2014 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/).

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                Microbiology & Virology
                Microbiology & Virology

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