Characterization of three novel mechanosensitive channel activities in<i>Escherichia coli</i>

Edwards, Michelle D.; Black, Susan; Rasmussen, Tim; Rasmussen, Akiko; Stokes, Neil R.; Stephen, Terri‐Leigh; Miller, Samantha; Booth, Ian R.

doi:10.4161/chan.20998

Cited by 121 publications

(189 citation statements)

References 50 publications

Supporting

Mentioning

178

Contrasting

Order By: Relevance

“…In E. coli, the native expression of just MscL or MscS is sufficient to provide survival rates of 80% or higher against a 0.5 M NaCl shock (6). On the other hand, the remaining five channels in E. coli, expressed at native levels in various combinations, can lead to survival rates of 5% to 10% (2,6), calling into question the physiological significance of these channels. A summary of these results, including the error and presumed resolution, can be found in Table S1 in the supplemental material.…”

mentioning

confidence: 99%

“…The first bacterial mechanosensitive channels were discovered in 1987 (1), and in the intervening period several more channels have been discovered. For example, seven different types (MscL and 6 MscS homologs) have been demonstrated in Escherichia coli (2). More generally, the trend of having multiple MscS homologs seems to occur in many other bacterial species as well (3,4).…”

mentioning

confidence: 99%

See 1 more Smart Citation

The Rate of Osmotic Downshock Determines the Survival Probability of Bacterial Mechanosensitive Channel Mutants

2015

View full text Add to dashboard Cite

Mechanosensitive (MS) channels allow cells to sense and respond to environmental changes. In bacteria, these channels are believed to protect against an osmotic shock. The physiological function of these channels has been characterized primarily by a standardized assay, where aliquots of batch-cultured cells are rapidly pipetted into a hypotonic medium. Under this method, it has been inferred many types of MS channels (MscS homologs in Escherichia coli) demonstrate limited effectiveness against shock, typically rescuing less than 10% of the cells when expressed at native levels. We introduce a single-cell-based assay which allows us to control how fast the osmolarity changes, over time scales ranging from a fraction of a second to several minutes. We find that the protection provided by MS channels depends strongly on the rate of osmotic change, revealing that, under a slow enough osmotic drop, MscS homologs can lead to survival rates comparable to those found in wild-type strains. Further, after the osmotic downshift, we observe multiple death phenotypes, which are inconsistent with the prevailing paradigm of how cells lyse. Both of these findings require a reevaluation of our basic understanding of the physiology of MS channels. Mechanosensation is a ubiquitous phenomenon found across all domains of life. In bacteria, one of the manifestations of such processes is in the context of osmoprotection, where it has been proposed that the presence of mechanosensitive (MS) channels in the cell membrane allows these cells to survive immersion into hypotonic environments. These channels gate in response to an increase in membrane tension and prevent membrane rupture by mediating net flux of water and small molecules. The first bacterial mechanosensitive channels were discovered in 1987 (1), and in the intervening period several more channels have been discovered. For example, seven different types (MscL and 6 MscS homologs) have been demonstrated in Escherichia coli (2). More generally, the trend of having multiple MscS homologs seems to occur in many other bacterial species as well (3, 4). One of the puzzles left unresolved in the wake of the discovery of this mechanosensitive protein diversity is why there are so many distinct mechanosensitive channels and the nature of their significance for cell physiology. Perhaps cues can be taken from examining the cell's native environment, but at present, it is not known (at least to the authors) which environmental factors are crucial.The physiology of MS channels has been studied extensively over the past 20 years. Specifically, until now, the in vivo function of these channels has been characterized mainly by "hypo-osmotic challenge" assays, where an aliquot from batch culture is suddenly diluted into a lower-osmolarity medium, typically by hand pipetting. The resulting survival fraction is inferred several hours after the shock by counting colonies of plated dilutions or monitoring the optical density from the resulting mixture. The comparison of the batch survival rate fo...

show abstract

mentioning

confidence: 99%

mentioning

confidence: 99%

The Rate of Osmotic Downshock Determines the Survival Probability of Bacterial Mechanosensitive Channel Mutants

2015

View full text Add to dashboard Cite

show abstract

“…Tel: +81-45-924-5770; Fax: +81-45-924-5820; E-mail: mwachi@bio.titech.ac.jp and MscS, and five minor MscS-type channels, MscK (KefA) and YbdG, YbiO, YjeP, and YnaI. 23,[26][27][28] Bacillus subitilis has one MscL homolog and three MscS homologs, YkuT, YhdY, and YfkC. 29) On the other hand, C. glutamicum has only one MscL homolog, NCgl0834, and one MscS homolog, NCgl1221.…”

mentioning

confidence: 99%

L-Glutamate Secretion by the N-Terminal Domain of theCorynebacterium glutamicumNCgl1221 Mechanosensitive Channel

Yamashita

Hashimoto

Kumagai

et al. 2013

Bioscience, Biotechnology, and Biochemistry

View full text Add to dashboard Cite

“…Since the first report on the discovery of MS channels in bacteria (95), multiple types of MS channels have been identified in Escherichia coli (44). Based on their primary structures, they can be separated into two different subfamilies-the MscL subfamily and the MscS subfamily.…”

Section: Ms Channels Found In Bacteriamentioning

confidence: 99%

“…An additional difference between MscL and MscS is the typical presence of multiple MscS homologues within an organism, with as many as 10 identified in a single organism, as is the case for Arabidopsis thaliana (60). In E. coli, at least six MscS homologues exist: the canonical MscS, the subsequently identified MscK (potassium-dependent MS channel; originally KefA), MscM (MS channel of miniconductance; originally YbdG), and a further three MscS homologues, which have recently been characterized by electrophysiology and functional analyses (YjeP, YbiO, and YnaI) (44). Current evidence suggests that MscK-like homologues are restricted to Gram-negative bacteria.…”

Section: Fig 2 Mscl and Mscs Families Of Prokaryotic Ms Channelsmentioning

confidence: 99%

Bacterial Mechanosensitive Channels: Models for Studying Mechanosensory Transduction

Martinac

Nomura

Chi

et al. 2014

Antioxidants & Redox Signaling

View full text Add to dashboard Cite

Significance: Sensations of touch and hearing are manifestations of mechanical contact and air pressure acting on touch receptors and hair cells of the inner ear, respectively. In bacteria, osmotic pressure exerts a significant mechanical force on their cellular membrane. Bacteria have evolved mechanosensitive (MS) channels to cope with excessive turgor pressure resulting from a hypo-osmotic shock. MS channel opening allows the expulsion of osmolytes and water, thereby restoring normal cellular turgor and preventing cell lysis. Recent Advances: As biological force-sensing systems, MS channels have been identified as the best examples of membrane proteins coupling molecular dynamics to cellular mechanics. The bacterial MS channel of large conductance (MscL) and MS channel of small conductance (MscS) have been subjected to extensive biophysical, biochemical, genetic, and structural analyses. These studies have established MscL and MscS as model systems for mechanosensory transduction. Critical Issues: In recent years, MS ion channels in mammalian cells have moved into focus of mechanotransduction research, accompanied by an increased awareness of the role they may play in the pathophysiology of diseases, including cardiac hypertrophy, muscular dystrophy, or Xerocytosis. Future Directions: A recent exciting development includes the molecular identification of Piezo proteins, which function as nonselective cation channels in mechanosensory transduction associated with senses of touch and pain. Since research on Piezo channels is very young, applying lessons learned from studies of bacterial MS channels to establishing the mechanism by which the Piezo channels are mechanically activated remains one of the future challenges toward a better understanding of the role that MS channels play in mechanobiology. Antioxid. Redox Signal. 00, 000-000.

show abstract

Characterization of three novel mechanosensitive channel activities inEscherichia coli

Cited by 121 publications

References 50 publications

The Rate of Osmotic Downshock Determines the Survival Probability of Bacterial Mechanosensitive Channel Mutants

The Rate of Osmotic Downshock Determines the Survival Probability of Bacterial Mechanosensitive Channel Mutants

L-Glutamate Secretion by the N-Terminal Domain of theCorynebacterium glutamicumNCgl1221 Mechanosensitive Channel

Bacterial Mechanosensitive Channels: Models for Studying Mechanosensory Transduction

Contact Info

Product

Resources

About