The Bacterial Mechanosensitive Channel MscS and Its Extended Family

Paul Blount; Irene Iscla; Yuezhou Li; Paul C. Moe

doi:10.1128/9781555816452.ch12

Chapter 12 : The Bacterial Mechanosensitive Channel MscS and Its Extended Family

Authors: Paul Blount¹, Irene Iscla¹, Yuezhou Li¹, Paul C. Moe¹

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Affiliations: 1: Department of Physiology, University of Texas Southwestern Medical Center, Dallas, TX 75390-9040

Content Type: Monograph

Publication Year: 2005

Category: Bacterial Pathogenesis; Microbial Genetics and Molecular Biology

Book DOI: 10.1128/9781555816452

Chapter DOI: 10.1128/9781555816452.ch12

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Abstract:

Early studies of channels within Escherichia coli native membranes defined many of the fundamental properties of bacterial mechanosensitive channel (MS) channel activities. The observed activity was reported to be modulated, but not gated, by voltage, and a subsequent study demonstrated that amphipaths that intercalate into the membrane asymmetrically can modulate the sensitivity of the channel. The mscS gene family was discovered by classical genetics. The structure of E. coli MscS was solved to 3.9-Å resolution by X-ray crystallography, residues 27 to 280 were resolved. On the other hand, this study used only molecular simulation to model the permeation of the pore, an approach that inherently entertains many assumptions. As implied by some studies, the MscS extended family is not confined to E. coli. A survey of some of the MscS family members from archaea has shown researchers just how diverse the activities encoded by family members can be in conductance, sensitivity, and ionic preference; some homologs even demonstrate cationic rather than anionic preferences. The MscS-like family of channels is extremely large and diverse. In its most streamlined form, e.g., MscS in E. coli, it has many similarities with its counterpart, MscL. It appears to directly sense membrane tension, and it appears to utilize modification of transmembrane (TM) domains tilt and rotation in its gating sequence. Because the MscS and MscL families are so far removed from each other, these preserved features may reflect conserved mechanisms found in many MS channel families.

Citation: Blount P, Iscla I, Li Y, Moe P. 2005. The Bacterial Mechanosensitive Channel MscS and Its Extended Family, p 247-258. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch12

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The Bacterial Mechanosensitive Channel MscS and Its Extended Family

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/content/10.1128/9781555816452.chap12.fig12-1

Figure 1.

A typical trace obtained from an excised patch from native E. coli membranes. Giant spheroplasts were generated as previously described ( Blount et al., 1999 ). The top trace is the channel activity, while the bottom shows the pressure (negative relative to atmospheric). The strain used is derived from MJF431 ( Levina et al., 1999 ), which is null for mscS and mscK activities. MscS activity was replaced in trans using a pB10 expression vector ( Blount et al., 1999 ). Note the long open-dwell times and the inactivation of the activity with time. Recording conditions were as described ( Blount et al., 1999 ), pH 7.0 and −20 mV in the pipette channel openings are shown as upward for convenience; the closed (C) and open (O1 to O6) states are labeled to the left.

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Figure 1.

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Figure 2.

Hydrophilicity plots of MscK (top) and MscS (bottom). The scale bar is in amino acids. Note that MscK is much larger than MscS and that it is the C terminus of MscK that shows homology. The three TM domains of MscS (and last three of MscK) are indicated by gray boxes between the plots. Proximal to the homologous region, MscK contains an N-terminal periplasmic domain (which is labeled) and eight additional TM domains.

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Figure 2.

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Figure 3.

The structure and pore design of the MscS channel. The model shown is derived from X-ray crystallographic data ( Bass et al., 2002 ). The side (top panels) and top (bottom panels) views are shown. One subunit of the homoheptamer is shown in darker gray for distinction; the pore-forming third TM domain of this subunit is in black (the bracketed arrows point to this TM region). The heptameric (center) and simple trimeric (right; the obstructing subunit structures have been removed) structures are shown. Note the tight packing of the glycines (black CPK residues) and alanines (gray CPK residues) of the three subunits in the right panel.

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Figure 3.

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Figure 4.

A cartoon depicting the current model for the structural rearrangements thought to occur upon closure of the MscS channel. Note that it is thought that it is the open (or inactivated) state of the channel whose structure was solved in the crystallographic study ( Bass et al., 2002 ). The three TM domains are within the bilayer depicted by gray horizontal lines. Note that there are nine pores: one in the bilayer formed by TM3, seven at the interface of the subunits within the cytoplasmic cage, and one at the extreme cytoplasmic tip. Evidence suggests that each of these may constrict upon closure of the channel ( Koprowski and Kubalski, 2003 ; Miller et al., 2003b ; Edwards et al., 2005 ).

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Figure 4.

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