Skip to main content
SpringerLink
Log in

Bacterial Mechanosensitive Channels

  • Chapter
  • First Online:
Membrane Protein Complexes: Structure and Function

Part of the book series: Subcellular Biochemistry ((SCBI,volume 87))

Abstract

Mechanosensitive (MS) channels protect bacteria against hypo-osmotic shock and fulfil additional functions. Hypo-osmotic shock leads to high turgor pressure that can cause cell rupture and death. MS channels open under these conditions and release unspecifically solutes and consequently the turgor pressure. They can recognise the raised pressure via the increased tension in the cell membrane. Currently, a better understanding how MS channels can sense tension on molecular level is developing because the interaction of the lipid bilayer with the channel is being investigated in detail. The MS channel of large conductance (MscL) and of small conductance (MscS) have been distinguished and studied in molecular detail. In addition, larger channels were found that contain a homologous region corresponding to MscS so that MscS represents a family of channels. Often several members of this family are present in a species. The importance of this family is underlined by the fact that members can be found not only in bacteria but also in higher organisms. While MscL and MscS have been studied for years in particular by electrophysiology, mutagenesis, molecular dynamics, X-ray crystallography and other biophysical techniques, only recently more details are emerging about other members of the MscS-family.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 299.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 379.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 379.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ajouz B, Berrier C, Besnard M et al (2000) Contributions of the different extramembranous domains of the mechanosensitive ion channel MscL to its response to membrane tension. J Biol Chem 275:1015–1022

    Article  CAS  PubMed  Google Scholar 

  • Akitake B, Anishkin A, Sukharev S (2005) The “dashpot” mechanism of stretch-dependent gating in MscS. J Gen Physiol 125:143–154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akitake B, Anishkin A, Liu N, Sukharev S (2007) Straightening and sequential buckling of the pore-lining helices define the gating cycle of MscS. Nat Struct Mol Biol 14:1141–1149

    Article  CAS  PubMed  Google Scholar 

  • Anishkin A, Sukharev S (2004) Water dynamics and dewetting transitions in the small mechanosensitive channel MscS. Biophys J 86:2883–2895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anishkin A, Chiang C-S, Sukharev S (2005) Gain-of-function mutations reveal expanded intermediate states and a sequential action of two gates in MscL. J Gen Physiol 125:155–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anishkin A, Akitake B, Sukharev S (2008a) Characterization of the resting MscS: modeling and analysis of the closed bacterial mechanosensitive channel of small conductance. Biophys J 94:1252–1266

    Article  CAS  PubMed  Google Scholar 

  • Anishkin A, Kamaraju K, Sukharev S (2008b) Mechanosensitive channel MscS in the open state: modeling of the transition, explicit simulations, and experimental measurements of conductance. J Gen Physiol 132:67–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anishkin A, Akitake B, Kamaraju K et al (2010) Hydration properties of mechanosensitive channel pores define the energetics of gating. J Phys Condens Matter 22:454120

    Article  CAS  PubMed  Google Scholar 

  • Anishkin A, Loukin SH, Teng J, Kung C (2014) Feeling the hidden mechanical forces in lipid bilayer is an original sense. Proc Natl Acad Sci U S A 111:7898–7905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balleza D, Gómez-Lagunas F (2009) Conserved motifs in mechanosensitive channels MscL and MscS. Eur Biophys J 38:1013–1027

    Article  PubMed  Google Scholar 

  • Balleza D, Gómez-Lagunas F, Quinto C (2010) Cloning and functional expression of an MscL ortholog from rhizobium etli: characterization of a mechanosensitive channel. J Membr Biol 234:13–27

    Article  CAS  PubMed  Google Scholar 

  • Bartlett JL, Levin G, Blount P (2004) An in vivo assay identifies changes in residue accessibility on mechanosensitive channel gating. Proc Natl Acad Sci U S A 101:10161–10165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bass RB, Strop P, Barclay M, Rees DC (2002) Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science 298:1582–1587

    Article  CAS  PubMed  Google Scholar 

  • Battle AR, Petrov E, Pal P, Martinac B (2009) Rapid and improved reconstitution of bacterial mechanosensitive ion channel proteins MscS and MscL into liposomes using a modified sucrose method. FEBS Lett 583:407–412

    Article  CAS  PubMed  Google Scholar 

  • Battle AR, Ridone P, Bavi N et al (2015) Lipid-protein interactions: lessons learned from stress. Biochim Biophys Acta 1848:1744–1756

    Article  CAS  PubMed  Google Scholar 

  • Bavi N, Cortes DM, Cox CD et al (2016a) The role of MscL amphipathic N terminus indicates a blueprint for bilayer-mediated gating of mechanosensitive channels. Nat Commun 7:11984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bavi O, Cox CD, Vossoughi M et al (2016b) Influence of global and local membrane curvature on mechanosensitive ion channels: a finite element approach. Membr (Basel) 6:14

    Article  CAS  Google Scholar 

  • Becker M, Börngen K, Nomura T et al (2013) Glutamate efflux mediated by Corynebacterium glutamicum MscCG, Escherichia coli MscS, and their derivatives. Biochim Biophys Acta 1828:1230–1240

    Article  CAS  PubMed  Google Scholar 

  • Belyy V, Kamaraju K, Akitake B et al (2010) Adaptive behavior of bacterial mechanosensitive channels is coupled to membrane mechanics. J Gen Physiol 135:641–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berrier C, Besnard M, Ajouz B et al (1996) Multiple mechanosensitive ion channels from Escherichia coli, activated at different thresholds of applied pressure. J Membr Biol 151:175–187

    Article  CAS  PubMed  Google Scholar 

  • Berrier C, Pozza A, de Lacroix de Lavalette A et al (2013) The purified mechanosensitive channel TREK-1 is directly sensitive to membrane tension. J Biol Chem 288:27307–27314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bialecka-Fornal M, Lee HJ, DeBerg HA, Gandhi CS, Phillips R (2012) Single-cell census of mechanosensitive channels in living bacteria. PLoS One 7:e33077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bialecka-Fornal M, Lee HJ, Phillips R (2015) The rate of osmotic downshock determines the survival probability of bacterial mechanosensitive channel mutants. J Bacteriol 197:231–237

    Article  PubMed  CAS  Google Scholar 

  • Bilston LE, Mylvaganam K (2002) Molecular simulations of the large conductance mechanosensitive (MscL) channel under mechanical loading. FEBS Lett 512:185–190

    Article  CAS  PubMed  Google Scholar 

  • Birkner JP, Poolman B, Koçer A (2012) Hydrophobic gating of mechanosensitive channel of large conductance evidenced by single-subunit resolution. Proc Natl Acad Sci U S A 109:12944–12949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blount P, Sukharev SI, Schroeder MJ et al (1996) Single residue substitutions that change the gating properties of a mechanosensitive channel in Escherichia coli. Proc Natl Acad Sci U S A 93:11652–11657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blount P, Sukharev SI, Moe PC et al (1999) Mechanosensitive channels of bacteria. Methods Enzymol 294:458–482

    Article  CAS  PubMed  Google Scholar 

  • Boer M, Anishkin A, Sukharev S (2011) Adaptive MscS gating in the osmotic permeability response in E. coli: the question of time. Biochemistry 50:4087–4096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Booth I (2014) Bacterial mechanosensitive channels: progress towards an understanding of their roles in cell physiology. Curr Opin Microbiol 18:16–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Booth IR, Blount P (2012) The MscS and MscL families of mechanosensitive channels act as microbial emergency release valves. J Bacteriol 194:4802–4809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Booth IR, Edwards MD, Black S et al (2007a) Mechanosensitive channels in bacteria: signs of closure? Nat Rev Microbiol 5:431–440

    Article  CAS  PubMed  Google Scholar 

  • Booth IR, Edwards MD, Black S et al (2007b) Physiological analysis of bacterial mechanosensitive channels. Methods Enzymol 428:47–61

    Article  PubMed  Google Scholar 

  • Booth IR, Rasmussen T, Edwards MD et al (2011) Sensing bilayer tension: bacterial mechanosensitive channels and their gating mechanisms. Biochem Soc Trans 39:733–740

    Article  CAS  PubMed  Google Scholar 

  • Booth IR, Miller S, Müller A, Lehtovirta-Morley L (2015) The evolution of bacterial mechanosensitive channels. Cell Calcium 57:140–150

    Article  CAS  PubMed  Google Scholar 

  • Börngen K, Battle AR, Möker N et al (2010) The properties and contribution of the Corynebacterium glutamicum MscS variant to fine-tuning of osmotic adaptation. Biochim Biophys Acta 1798:2141–2149

    Article  PubMed  CAS  Google Scholar 

  • Böttcher B, Prazak V, Rasmussen A et al (2015) The structure of YnaI implies structural and mechanistic conservation in the MscS family of mechanosensitive channels. Structure 23:1705–1714

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brohawn SG (2015) How ion channels sense mechanical force: insights from mechanosensitive K2P channels TRAAK, TREK1, and TREK2. Ann N Y Acad Sci 1352:20–32

    Article  CAS  PubMed  Google Scholar 

  • Brohawn SG, Campbell EB, MacKinnon R (2014a) Physical mechanism for gating and mechanosensitivity of the human TRAAK K+ channel. Nature 516:126–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brohawn SG, Su Z, MacKinnon R (2014b) Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K + channels. Proc Natl Acad Sci 111:3614–3619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bucarey SA, Penn K, Paul L et al (2012) Genetic complementation of the obligate marine actinobacterium Salinispora tropica with the large mechanosensitive channel gene mscL rescues cells from osmotic downshock. Appl Environ Microbiol 78:4175–4182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buda R, Liu Y, Yang J et al (2016) Dynamics of Escherichia coli ’s passive response to a sudden decrease in external osmolarity. Proc Natl Acad Sci 113:E5838–E5846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caldwell DB, Malcolm HR, Elmore DE, Maurer JA (2010) Identification and experimental verification of a novel family of bacterial cyclic nucleotide-gated (bCNG) ion channels. Biochim Biophys Acta 1798:1750–1756

    Article  CAS  PubMed  Google Scholar 

  • Carney J, East JM, Mall S et al (2006) Fluorescence quenching methods to study lipid-protein interactions. Curr Protoc Protein Sci Chapter 19:Unit 19.12

    Google Scholar 

  • Chang G, Spencer R, Lee A et al (1998) Structure of the MscL homolog from mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 282:2220–2226

    Article  CAS  PubMed  Google Scholar 

  • Chiang C-S, Anishkin A, Sukharev S (2004) Gating of the large mechanosensitive channel in situ: estimation of the spatial scale of the transition from channel population responses. Biophys J 86:2846–2861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colombo G, Marrink SJ, Mark AE (2003) Simulation of MscL gating in a bilayer under stress. Biophys J 84:2331–2337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corry B, Martinac B (2008) Bacterial mechanosensitive channels: experiment and theory. Biochim Biophys Acta 1778:1859–1870

    Article  CAS  PubMed  Google Scholar 

  • Cox C, Nomura T, Ziegler C et al (2013) Selectivity mechanism of the mechanosensitive channel MscS revealed by probing channel subconducting states. Nat Commun 4:2137

    Article  CAS  PubMed  Google Scholar 

  • Cox C, Nakayama Y, Nomura T, Martinac B (2015) The evolutionary “tinkering”of MscS-like channels: generation of structural and functional diversity. Pflugers Arch 467:3–13

    Article  CAS  PubMed  Google Scholar 

  • Cruickshank CC, Minchin RF, Le Dain AC, Martinac B (1997) Estimation of the pore size of the large-conductance mechanosensitive ion channel of Escherichia coli. Biophys J 73:1925–1931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui C, Smith DO, Adler J (1995) Characterization of mechanosensitive channels in Escherichia coli cytoplasmic membrane by whole-cell patch clamp recording. J Membr Biol 144:31–42

    Article  CAS  PubMed  Google Scholar 

  • Doerner JF, Febvay S, Clapham DE (2012) Controlled delivery of bioactive molecules into live cells using the bacterial mechanosensitive channel MscL. Nat Commun 3:990

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dorwart MR, Wray R, Brautigam CA et al (2010) S. aureus MscL is a pentamer in vivo but of variable stoichiometries in vitro: implications for detergent-solubilized membrane proteins. PLoS Biol 8:e1000555

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dowhan W (2013) A retrospective: use of Escherichia coli as a vehicle to study phospholipid synthesis and function. Biochim Biophys Acta 1831:471–494

    Article  CAS  PubMed  Google Scholar 

  • Edwards MD, Li Y, Kim S et al (2005) Pivotal role of the glycine-rich TM3 helix in gating the MscS mechanosensitive channel. Nat Struc. Mol Biol 12:113–119

    CAS  Google Scholar 

  • Edwards MD, Bartlett W, Booth IR (2008) Pore mutations of the Escherichia coli MscS channel affect desensitization but not ionic preference. Biophys J 94:3003–3013

    Article  CAS  PubMed  Google Scholar 

  • Edwards MD, Black S, Rasmussen T et al (2012) Characterization of three novel mechanosensitive channel activities in Escherichia coli. Channels 6:272–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falke LC, Edwards KL, Pickard BG, Misler S (1988) A stretch-activated anion channel in tobacco protoplasts. FEBS Lett 237:141–144

    Article  CAS  PubMed  Google Scholar 

  • Folgering JHA, Moe PC, Schuurman-Wolters GK et al (2005) Lactococcus lactis uses MscL as its principal mechanosensitive channel. J Biol Chem 280:8784–8792

    Article  CAS  PubMed  Google Scholar 

  • Gandhi CS, Walton TA, Rees DC (2011) OCAM: a new tool for studying the oligomeric diversity of MscL channels. Protein Sci 20:313–326

    Article  CAS  PubMed  Google Scholar 

  • Goulian M, Mesquita ON, Fygenson DK et al (1998) Gramicidin channel kinetics under tension. Biophys J 74:328–337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grajkowski W, Kubalski A, Koprowski P (2005) Surface changes of the mechanosensitive channel MscS upon its activation, inactivation, and closing. Biophys J 88:3050–3059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grillet N, Kazmierczak P, Xiong W et al (2009) The mechanotransduction machinery of hair cells. Sci Signal 2:pt5

    Article  PubMed  Google Scholar 

  • Gullingsrud J, Kosztin D, Schulten K (2001) Structural determinants of MscL gating studied by molecular dynamics simulations. Biophys J 80:2074–2081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gustin M, Zhou X, Martinac B, Kung C (1988) A mechanosensitive ion channel in the yeast plasma membrane. Science 242:762–765

    Article  CAS  PubMed  Google Scholar 

  • Hamilton ES, Schlegel AM, Haswell ES (2015) United in diversity: mechanosensitive ion channels in plants. Annu Rev Plant Biol 66:113–137

    Article  CAS  PubMed  Google Scholar 

  • Hase CC, Le Dain AC, Martinac B (1995) Purification and functional reconstitution of the recombinant large mechanosensitive ion channel (MscL) of Escherichia coli. J Biol Chem 270:18329–18334

    Article  CAS  PubMed  Google Scholar 

  • Häse CC, Minchin RF, Kloda A, Martinac B (1997) Cross-linking studies and membrane localization and assembly of radiolabelled large mechanosensitive ion channel (MscL) of Escherichia coli. Biochem Biophys Res Commun 232:777–782

    Article  PubMed  Google Scholar 

  • Haswell ES, Phillips R, Rees DC (2011) Mechanosensitive channels: what can they do and how do they do it? Structure 19:1356–1369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayakawa K, Tatsumi H, Sokabe M (2008) Actin stress fibers transmit and focus force to activate mechanosensitive channels. J Cell Sci 121:496–503

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann T, Boiangiu C, Moses S, Bremer E (2008) Responses of Bacillus subtilis to hypotonic challenges: physiological contributions of mechanosensitive channels to cellular survival. Appl Environ Microbiol 74:2454–2460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubbell WL, Cafiso DS, Altenbach C (2000) Identifying conformational changes with site-directed spin labeling. Nat Struct Biol 7:735–739

    Article  CAS  PubMed  Google Scholar 

  • Iscla I, Blount P (2012) Sensing and responding to membrane tension: the bacterial MscL channel as a model system. Biophys J 103:169–174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iscla I, Levin G, Wray R, Blount P (2007) Disulfide trapping the mechanosensitive channel MscL into a gating-transition state. Biophys J 92:1224–1232

    Article  CAS  PubMed  Google Scholar 

  • Iscla I, Wray R, Blount P (2008) On the structure of the N-terminal domain of the MscL channel: helical bundle or membrane interface. Biophys J 95:2283–2291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iscla I, Wray R, Blount P (2011) The oligomeric state of the truncated mechanosensitive channel of large conductance shows no variance in vivo. Protein Sci 20:1638–1642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iscla I, Eaton C, Parker J et al (2013) Improving the design of a MscL-based triggered nanovalve. Biosensors 3:171–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iscla I, Wray R, Wei S et al (2014) Streptomycin potency is dependent on MscL channel expression. Nat Commun 5:4891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iscla I, Wray R, Blount P et al (2015) A new antibiotic with potent activity targets MscL. J Antibiot (Tokyo) 68:453–462

    Article  CAS  Google Scholar 

  • Kakuda T, Koide Y, Sakamoto A, Takai S (2012) Characterization of two putative mechanosensitive channel proteins of Campylobacter jejuni involved in protection against osmotic downshock. Vet Microbiol 160:53–60

    Article  CAS  PubMed  Google Scholar 

  • Kamaraju K, Gottlieb PA, Sachs F, Sukharev S (2010) Effects of GsMTx4 on bacterial mechanosensitive channels in inside-out patches from giant spheroplasts. Biophys J 99:2870–2878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasha M (1952) Collisional perturbation of spin-orbital coupling and the mechanism of fluorescence quenching. A visual demonstration of the perturbation. J Chem Phys 20:71

    Article  CAS  Google Scholar 

  • Killian JA, von Heijne G (2000) How proteins adapt to a membrane–water interface. Trends Biochem Sci 25:429–434

    Article  CAS  PubMed  Google Scholar 

  • Kloda A, Martinac B (2001a) Structural and functional differences between two homologous mechanosensitive channels of Methanococcus jannaschii. EMBO J 20:1888–1896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kloda A, Martinac B (2001b) Molecular identification of a mechanosensitive channel in archaea. Biophys J 80:229–240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koçer A (2015) Mechanisms of mechanosensing – mechanosensitive channels, function and re-engineering. Curr Opin Chem Biol 29:120–127

    Article  PubMed  CAS  Google Scholar 

  • Koçer A, Walko M, Meijberg W, Feringa BL (2005) A light-actuated nanovalve derived from a channel protein. Science 309:755–758

    Article  PubMed  CAS  Google Scholar 

  • Koçer A, Walko M, Bulten E et al (2006) Rationally designed chemical modulators convert a bacterial channel protein into a pH-sensory valve. Angew Chem Int Ed 45:3126–3130

    Article  CAS  Google Scholar 

  • Koçer A, Walko M, Feringa BL (2007) Synthesis and utilization of reversible and irreversible light-activated nanovalves derived from the channel protein MscL. Nat Protoc 2:1426–1437

    Article  PubMed  CAS  Google Scholar 

  • Kong Y, Shen Y, Warth TE, Ma J (2002) Conformational pathways in the gating of Escherichia coli mechanosensitive channel. Proc Natl Acad Sci U S A 99:5999–6004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koprowski P, Kubalski A (1998) Voltage-independent adaptation of mechanosensitive channels in Escherichia coli protoplasts. J Membr Biol 164:253–262

    Article  CAS  PubMed  Google Scholar 

  • Koprowski P, Grajkowski W, Balcerzak M et al (2015) Cytoplasmic domain of MscS interacts with cell division protein FtsZ: a possible non-channel function of the mechanosensitive channel in Escherichia coli. PLoS One 10:e0127029

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lai J, Poon Y, Kaiser J, Rees D (2013) Open and shut: crystal structures of the dodecylmaltoside solubilized mechanosensitive channel of small conductance from Escherichia coli and Helicobacter at 4.4 Å and 4.1 Å resolutions. Protein Sci 22:502–509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levina N, Tötemeyer S, Stokes NR et al (1999) Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J 18:1730–1737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Moe PC, Chandrasekaran S et al (2002) Ionic regulation of MscK, a mechanosensitive channel from Escherichia coli. EMBO J 21:5323–5330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C, Edwards MD, Jeong H et al (2007) Identification of mutations that alter the gating of the Escherichia coli mechanosensitive channel protein, MscK. Mol Microbiol 64:560–574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li G-W, Burkhardt D, Gross C, Weissman JS (2014) Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157:624–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Guo J, Ou X et al (2015) Mechanical coupling of the multiple structural elements of the large-conductance mechanosensitive channel during expansion. Proc Natl Acad Sci U S A 112:10726–10731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Gandhi CS, Rees DC (2009) Structure of a tetrameric MscL in an expanded intermediate state. Nature 461:120–124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Louhivuori M, Risselada HJ, van der Giessen E, Marrink SJ (2010) Release of content through mechano-sensitive gates in pressurized liposomes. Proc Natl Acad Sci U S A 107:19856–19860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Löw C, Yau YH, Pardon E et al (2013) Nanobody mediated crystallization of an archeal mechanosensitive channel. PLoS One 8:e77984

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Machiyama H, Tatsumi H, Sokabe M (2009) Structural changes in the cytoplasmic domain of the mechanosensitive channel MscS during opening. Biophys J 97:1048–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maksaev G, Haswell ES (2012) MscS-Like10 is a stretch-activated ion channel from Arabidopsis thaliana with a preference for anions. Proc Natl Acad Sci U S A 109:19015–19020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malcolm HR, Maurer JA (2012) The mechanosensitive channel of small conductance (MscS) superfamily: not just mechanosensitive channels anymore. Chembiochem 13:2037–2043

    Article  CAS  PubMed  Google Scholar 

  • Malcolm HR, Elmore DE, Maurer JA (2012a) Mechanosensitive behavior of bacterial cyclic nucleotide gated (bCNG) ion channels: insights into the mechanism of channel gating in the mechanosensitive channel of small conductance superfamily. Biochem Biophys Res Commun 417:972–976

    Article  CAS  PubMed  Google Scholar 

  • Malcolm HR, Heo Y-Y, Caldwell DB et al (2012b) Ss-bCNGa: a unique member of the bacterial cyclic nucleotide gated (bCNG) channel family that gates in response to mechanical tension. Eur Biophys J 41:1003–1013

    Article  CAS  PubMed  Google Scholar 

  • Martinac B, Buechner M, Delcour AH et al (1987) Pressure-sensitive ion channel in Escherichia coli. Proc Natl Acad Sci 84:2297–2301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinac B, Adler J, Kung C (1990) Mechanosensitive ion channels of E. coli activated by amphipaths. Nature 348:261–263

    Article  CAS  PubMed  Google Scholar 

  • Mika JT, Birkner JP, Poolman B, Koçer A (2013) On the role of individual subunits in MscL gating: “all for one, one for all?”. FASEB J 27:882–892

    Article  CAS  PubMed  Google Scholar 

  • Moe P, Blount P (2005) Assessment of potential stimuli for mechano-dependent gating of MscL: effects of pressure, tension, and lipid headgroups. Biochemistry 44:12239–12244

    Article  CAS  PubMed  Google Scholar 

  • Moe PC, Blount P, Kung C (1998) Functional and structural conservation in the mechanosensitive channel MscL implicates elements crucial for mechanosensation. Mol Microbiol 28:583–592

    Article  CAS  PubMed  Google Scholar 

  • Moe PC, Levin G, Blount P (2000) Correlating a protein structure with function of a bacterial mechanosensitive channel. J Biol Chem 275:31121–31127

    Article  CAS  PubMed  Google Scholar 

  • Naismith JH, Booth IR (2012) Bacterial mechanosensitive channels – MscS: evolution’s solution to creating sensitivity in function. Annu Rev Biophys 41:157–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Najem JS, Dunlap MD, Rowe ID et al (2015) Activation of bacterial channel MscL in mechanically stimulated droplet interface bilayers. Sci Rep 5:13726

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakamaru Y, Takahashi Y, Unemoto T, Nakamura T (1999) Mechanosensitive channel functions to alleviate the cell lysis of marine bacterium, Vibrio alginolyticus, by osmotic downshock. FEBS Lett 444:170–172

    Article  CAS  PubMed  Google Scholar 

  • Nakamura J, Hirano S, Ito H, Wachi M (2007) Mutations of the Corynebacterium glutamicum NCgl1221 gene, encoding a mechanosensitive channel homolog, induce L-glutamic acid production. Appl Environ Microbiol 73:4491–4498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakayama Y, Iida H (2014) Organellar mechanosensitive channels involved in hypo-osmoregulation in fission yeast. Cell Calcium 56:467–471

    Article  CAS  PubMed  Google Scholar 

  • Nakayama Y, Yoshimura K, Iida H (2012) Organellar mechanosensitive channels in fission yeast regulate the hypo-osmotic shock response. Nat Commun 3:1020

    Article  PubMed  CAS  Google Scholar 

  • Nakayama Y, Yoshimura K, Iida H (2013) Electrophysiological characterization of the mechanosensitive channel MscCG in Corynebacterium glutamicum. Biophys J 105:1366–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakayama Y, Mustapić M, Ebrahimian H et al (2015) Magnetic nanoparticles for “smart liposomes”. Eur Biophys J 44:647–654

    Article  CAS  PubMed  Google Scholar 

  • Nanatani K, Shijuku T, Akai M et al (2014) Characterization of the role of a mechanosensitive channel in osmotic down shock adaptation in Synechocystis sp PCC 6803. Channels 7:238–242

    Article  Google Scholar 

  • Neder J, West B, Nielaba P, Schmid F (2010) Coarse-grained simulations of membranes under tension. J Chem Phys 132:115101

    Article  PubMed  CAS  Google Scholar 

  • Nomura T, Sokabe M, Yoshimura K (2006) Lipid-protein interaction of the MscS mechanosensitive channel examined by scanning mutagenesis. Biophys J 91:2874–2881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nomura T, Cranfield CG, Deplazes E et al (2012) Differential effects of lipids and lyso-lipids on the mechanosensitivity of the mechanosensitive channels MscL and MscS. Proc Natl Acad Sci U S A 109:8770–8775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ou X, Blount P, Hoffman RJ, Kung C (1998) One face of a transmembrane helix is crucial in mechanosensitive channel gating. Proc Natl Acad Sci 95:11471–11475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perozo E, Rees DC (2003) Structure and mechanism in prokaryotic mechanosensitive channels. Curr Opin Struct Biol 13:432–442

    Article  CAS  PubMed  Google Scholar 

  • Perozo E, Cortes DM, Sompornpisut P et al (2002a) Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature 418:942–948

    Article  CAS  PubMed  Google Scholar 

  • Perozo E, Kloda A, Cortes DM, Martinac B (2002b) Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat Struct Biol 9:696–703

    Article  CAS  PubMed  Google Scholar 

  • Petrov E, Palanivelu D, Constantine M et al (2013) Patch-clamp characterization of the MscS-like Mechanosensitive Channel from Silicibacter pomeroyi. Biophys J 104:1426–1434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips R, Ursell T, Wiggins P, Sens P (2009) Emerging roles for lipids in shaping membrane-protein function. Nature 459:379–385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pivetti CD, Yen M-R, Miller S et al (2003) Two families of mechanosensitive channel proteins. Microbiol Mol Biol Rev 67:66–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pliotas C, Ward R, Branigan E et al (2012) Conformational state of the MscS mechanosensitive channel in solution revealed by pulsed electron-electron double resonance (PELDOR) spectroscopy. Proc Natl Acad Sci U S A 109:E2675–E2682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pliotas C, Dahl ACE, Rasmussen T et al (2015) The role of lipids in mechanosensation. Nat Struct Mol Biol 22:991–998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Powl AM, East JM, Lee AG (2003) Lipid-protein interactions studied by introduction of a tryptophan residue: the mechanosensitive channel MscL. Biochemistry 42:14306–14317

    Article  CAS  PubMed  Google Scholar 

  • Powl AM, East JM, Lee AG (2005a) Heterogeneity in the binding of lipid molecules to the surface of a membrane protein: hot spots for anionic lipids on the mechanosensitive channel of large conductance MscL and effects on conformation. Biochemistry 44:5873–5883

    Article  CAS  PubMed  Google Scholar 

  • Powl AM, Wright JN, East JM, Lee AG (2005b) Identification of the hydrophobic thickness of a membrane protein using fluorescence spectroscopy: studies with the mechanosensitive channel MscL. Biochemistry 44:5713–5721

    Article  CAS  PubMed  Google Scholar 

  • Powl AM, East JM, Lee AG (2007) Different effects of lipid chain length on the two sides of a membrane and the lipid annulus of MscL. Biophys J 93:113–122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Powl AM, East JM, Lee AG (2008) Anionic phospholipids affect the rate and extent of flux through the mechanosensitive channel of large conductance MscL. Biochemistry 47:4317–4328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prole DL, Taylor CW (2013) Identification and analysis of putative homologues of mechanosensitive channels in pathogenic protozoa. PLoS One 8:e66068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi Z, Kishigami A, Nakagawa Y et al (2004) A mechanosensitive anion channel in Arabidopsis thaliana mesophyll cells. Plant Cell Physiol 45:1704–1708

    Article  CAS  PubMed  Google Scholar 

  • Rasmussen T (2016) How do mechanosensitive channels sense membrane tension? Biochem Soc Trans 44:1019–1025

    Article  CAS  PubMed  Google Scholar 

  • Rasmussen A, Rasmussen T, Edwards MD et al (2007) The role of tryptophan residues in the function and stability of the mechanosensitive channel MscS from Escherichia coli. Biochemistry 46:10899–10908

    Article  CAS  PubMed  Google Scholar 

  • Rasmussen T, Edwards MD, Black SS et al (2010) Tryptophan in the pore of the mechanosensitive channel MscS: assessment of pore conformations by fluorescence spectroscopy. J Biol Chem 285:5377–5384

    Article  CAS  PubMed  Google Scholar 

  • Rasmussen T, Rasmussen A, Singh S et al (2015) Properties of the Mechanosensitive Channel MscS pore revealed by tryptophan scanning mutagenesis. Biochemistry 54:4519–4530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reading E, Walton TA, Liko I et al (2015) The effect of detergent, temperature, and lipid on the oligomeric state of MscL constructs: insights from mass spectrometry. Chem Biol 22:593–603

    Article  CAS  PubMed  Google Scholar 

  • Reuter M, Hayward NJ, Black SS et al (2014) Mechanosensitive channels and bacterial cell wall integrity: does life end with a bang or a whimper? J R Soc Interface 11:20130850

    Article  PubMed  PubMed Central  Google Scholar 

  • Rowe I, Elahi M, Huq A, Sukharev S (2013) The mechanoelectrical response of the cytoplasmic membrane of Vibrio cholerae. J Gen Physiol 142:75–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schumann U, Edwards MD, Rasmussen T et al (2010) YbdG in Escherichia coli is a threshold-setting mechanosensitive channel with MscM activity. Proc Natl Acad Sci U S A 107:12664–12669

    Article  PubMed  PubMed Central  Google Scholar 

  • Shaikh S, Cox CD, Nomura T, Martinac B (2014) Energetics of gating MscS by membrane tension in azolectin liposomes and giant spheroplasts. Channels 8:321–326

    Article  PubMed  PubMed Central  Google Scholar 

  • Shapovalov G, Lester HA (2004) Gating transitions in bacterial ion channels measured at 3 microns resolution. J Gen Physiol 124:151–161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shapovalov G, Bass R, Rees DC, Lester HA (2003) Open-state disulfide crosslinking between Mycobacterium tuberculosis mechanosensitive channel subunits. Biophys J 84:2357–2365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sokabe M, Sachs F, Jing ZQ (1991) Quantitative video microscopy of patch clamped membranes stress, strain, capacitance, and stretch channel activation. Biophys J 59:722–728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sotomayor M, Schulten K (2004) Molecular dynamics study of gating in the mechanosensitive channel of small conductance MscS. Biophys J 87:3050–3065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steinbacher S, Bass R, Strop P, Rees DC (2007) Structures of the prokaryotic mechanosensitive channels MscL and MscS. In: Benos DG, Simon SA (eds) Current topics in membranes, mechanosensitive ion channels, part A, vol 58. Elsevier, Amsterdam, pp 1–24

    Chapter  Google Scholar 

  • Stokes NR, Murray HD, Subramaniam C et al (2003) A role for mechanosensitive channels in survival of stationary phase: regulation of channel expression by RpoS. Proc Natl Acad Sci U S A 100:15959–15964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sukharev S (2002) Purification of the small mechanosensitive channel of Escherichia coli (MscS): the subunit structure, conduction, and gating characteristics in liposomes. Biophys J 83:290–298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sukharev SI, Martinac B, Arshavsky VY, Kung C (1993) Two types of mechanosensitive channels in the Escherichia coli cell envelope: solubilization and functional reconstitution. Biophys J 65:177–183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sukharev SI, Blount P, Martinac B et al (1994) A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature 368:265–268

    Article  CAS  PubMed  Google Scholar 

  • Sukharev SI, Blount P, Martinac B, Kung C (1997) Mechanosensitive channels of Escherichia coli: the MscL gene, protein, and activities. Annu Rev Physiol 59:633–657

    Article  CAS  PubMed  Google Scholar 

  • Sukharev SI, Sigurdson WJ, Kung C, Sachs F (1999) Energetic and spatial parameters for gating of the bacterial large conductance mechanosensitive channel, MscL. J Gen Physiol 113:525–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sukharev S, Betanzos M, Chiang CS, Guy HR (2001a) The gating mechanism of the large mechanosensitive channel MscL. Nature 409:720–724

    Article  CAS  PubMed  Google Scholar 

  • Sukharev S, Durell SR, Guy HR (2001b) Structural models of the MscL gating mechanism. Biophys J 81:917–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Syeda R, Florendo MN, Cox CD et al (2016) Piezo1 channels are inherently mechanosensitive. Cell Rep 17:1739–1746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teng J, Loukin S, Anishkin A, Kung C (2015) The force-from-lipid (FFL) principle of mechanosensitivity, at large and in elements. Pflügers. Arch Eur J Physiol 467:27–37

    Article  CAS  Google Scholar 

  • Tsai I-J, Liu Z-W, Rayment J et al (2005) The role of the periplasmic loop residue glutamine 65 for MscL mechanosensitivity. Eur Biophys J 34:403–412

    Article  CAS  PubMed  Google Scholar 

  • van den Berg J, Galbiati H, Rasmussen A et al (2016) On the mobility, membrane location and functionality of mechanosensitive channels in Escherichia coli. Sci Rep 6:32709

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van den Bogaart G, Krasnikov V, Poolman B (2007) Dual-color fluorescence-burst analysis to probe protein efflux through the mechanosensitive channel MscL. Biophys J 92:1233–1240

    Article  PubMed  CAS  Google Scholar 

  • Vásquez V, Sotomayor M, Cordero-Morales J et al (2008a) A structural mechanism for MscS gating in lipid bilayers. Science 321:1210–1214

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vásquez V, Sotomayor M, Cortes DM et al (2008b) Three-dimensional architecture of membrane-embedded MscS in the closed conformation. J Mol Biol 378:55–70

    Article  PubMed  CAS  Google Scholar 

  • Velásquez J, Schuurman-Wolters G, Birkner JP et al (2014) Bacillus Subtilis spore protein SpoVAC functions as a mechanosensitive channel. Mol Microbiol 92:813–823

    Article  PubMed  CAS  Google Scholar 

  • Wahome PG, Setlow P (2008) Growth, osmotic downshock resistance and differentiation of Bacillus Subtilis strains lacking mechanosensitive channels. Arch Microbiol 189:49–58

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Black SS, Edwards MD et al (2008) The structure of an open form of an E. coli mechanosensitive channel at 3.45 a resolution. Science 321:1179–1183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Liu Y, Deberg HA et al (2014) Single molecule FRET reveals pore size and opening mechanism of a mechano-sensitive ion channel. Elife 3:e01834

    PubMed  PubMed Central  Google Scholar 

  • Ward R, Pliotas C, Branigan E et al (2014) Probing the structure of the mechanosensitive channel of small conductance in lipid bilayers with pulsed electron-electron double resonance. Biophys J 106:834–842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wiener M, White S (1991) Transbilayer distribution of bromine in fluid bilayers containing a specifically brominated analog of dioleoylphosphatidylcholine. Biochemistry 30:6997–7008

    Article  CAS  PubMed  Google Scholar 

  • Wilson MME, Maksaev G, Haswell EES (2013) MscS-like mechanosensitive channels in plants and microbes. Biochemistry 52:5708–5722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamashita C, Hashimoto K-I, Kumagai K et al (2013) L-Glutamate Secretion by the N-Terminal Domain of the Corynebacterium glutamicum NCgl1221 mechanosensitive channel. Biosci Biotechnol Biochem 77:1008–1013

    Article  CAS  PubMed  Google Scholar 

  • Yang L-M, Zhong D, Blount P (2013) Chimeras reveal a single lipid-interface residue that controls MscL channel kinetics as well as mechanosensitivity. Cell Rep 3:520–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yilmaz D, Dimitrova AI, Walko M, Kocer A (2015) Study of light-induced MscL gating by EPR spectroscopy. Eur Biophys J 44:557–565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshimura K, Sokabe M (2010) Mechanosensitivity of ion channels based on protein-lipid interactions. J R Soc Interface 7(Suppl 3):S307–S320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshimura K, Batiza A, Schroeder M et al (1999) Hydrophilicity of a single residue within MscL correlates with increased channel mechanosensitivity. Biophys J 77:1960–1972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshimura K, Nomura T, Sokabe M (2004) Loss-of-function mutations at the rim of the funnel of mechanosensitive channel MscL. Biophys J 86:2113–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Wang J, Feng Y et al (2012) Structure and molecular mechanism of an anion-selective mechanosensitive channel of small conductance. Proc Natl Acad Sci U S A 109:18180–18185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XC, Liu Z, Li J (2016) From membrane tension to channel gating: a principal energy transfer mechanism for mechanosensitive channels. Protein Sci 25:1954–1964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong D, Blount P (2013) Phosphatidylinositol is crucial for the mechanosensitivity of Mycobacterium tuberculosis MscL. Biochemistry 52:5415–5420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Biochemie, Rudolf-Virchow-Zentrum, Universität Würzburg, Würzburg, Germany

    Tim Rasmussen & Akiko Rasmussen

Authors
  1. Tim Rasmussen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akiko Rasmussen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tim Rasmussen .

Editor information

Editors and Affiliations

  1. Institute of Zoology, University of Mainz, Mainz, Germany

    J. Robin Harris

  2. Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Groningen, The Netherlands

    Egbert J. Boekema

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Rasmussen, T., Rasmussen, A. (2018). Bacterial Mechanosensitive Channels. In: Harris, J., Boekema, E. (eds) Membrane Protein Complexes: Structure and Function. Subcellular Biochemistry, vol 87. Springer, Singapore. https://doi.org/10.1007/978-981-10-7757-9_4

Download citation

Publish with us

Policies and ethics

Search

Navigation