Estimation of the pore size of the large-conductance mechanosensitive ion channel of Escherichia coli. (original) (raw)
- Journal List
- Biophys J
- v.73(4); 1997 Oct
- PMC1181093
Biophys J. 1997 Oct; 73(4): 1925–1931.
Department of Pharmacology, University of Western Australia, Nedlands.
Abstract
The open channel diameter of Escherichia coli recombinant large-conductance mechanosensitive ion channels (MscL) was estimated using the model of Hille (Hille, B. 1968. Pharmacological modifications of the sodium channels of frog nerve. J. Gen. Physiol. 51:199-219) that relates the pore size to conductance. Based on the MscL conductance of 3.8 nS, and assumed pore lengths, a channel diameter of 34 to 46 A was calculated. To estimate the pore size experimentally, the effect of large organic ions on the conductance of MscL was examined. Poly-L-lysines (PLLs) with a diameter of 37 A or larger significantly reduced channel conductance, whereas spermine (approximately 15 A), PLL19 (approximately 25 A) and 1,1'-bis-(3-(1'-methyl-(4,4'-bipyridinium)-1-yl)-propyl)-4,4'-b ipyridinium (approximately 30 A) had no effect. The smaller organic ions putrescine, cadaverine, spermine, and succinate all permeated the channel. We conclude that the open pore diameter of the MscL is approximately 40 A, indicating that the MscL has one of the largest channel pores yet described. This channel diameter is consistent with the proposed homohexameric model of the MscL.
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- Barry PH, Lynch JW. Liquid junction potentials and small cell effects in patch-clamp analysis. J Membr Biol. 1991 Apr;121(2):101–117. [PubMed] [Google Scholar]
- Berrier C, Besnard M, Ajouz B, Coulombe A, Ghazi A. Multiple mechanosensitive ion channels from Escherichia coli, activated at different thresholds of applied pressure. J Membr Biol. 1996 May;151(2):175–187. [PubMed] [Google Scholar]
- Berrier C, Coulombe A, Szabo I, Zoratti M, Ghazi A. Gadolinium ion inhibits loss of metabolites induced by osmotic shock and large stretch-activated channels in bacteria. Eur J Biochem. 1992 Jun 1;206(2):559–565. [PubMed] [Google Scholar]
- Bezanilla F, Armstrong CM. Negative conductance caused by entry of sodium and cesium ions into the potassium channels of squid axons. J Gen Physiol. 1972 Nov;60(5):588–608. [PMC free article] [PubMed] [Google Scholar]
- Blount P, Sukharev SI, Moe PC, Schroeder MJ, Guy HR, Kung C. Membrane topology and multimeric structure of a mechanosensitive channel protein of Escherichia coli. EMBO J. 1996 Sep 16;15(18):4798–4805. [PMC free article] [PubMed] [Google Scholar]
- Blount P, Sukharev SI, Schroeder MJ, Nagle SK, Kung C. Single residue substitutions that change the gating properties of a mechanosensitive channel in Escherichia coli. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11652–11657. [PMC free article] [PubMed] [Google Scholar]
- Cecchi X, Bull R, Franzoy R, Coronado R, Alvarez O. Probing the pore size of the hemocyanin channel. Biochim Biophys Acta. 1982 Dec 8;693(1):173–176. [PubMed] [Google Scholar]
- Cui C, Smith DO, Adler J. Characterization of mechanosensitive channels in Escherichia coli cytoplasmic membrane by whole-cell patch clamp recording. J Membr Biol. 1995 Mar;144(1):31–42. [PubMed] [Google Scholar]
- Cunningham JT, Wachtel RE, Abboud FM. Mechanosensitive currents in putative aortic baroreceptor neurons in vitro. J Neurophysiol. 1995 May;73(5):2094–2098. [PubMed] [Google Scholar]
- Delcour AH, Martinac B, Adler J, Kung C. Modified reconstitution method used in patch-clamp studies of Escherichia coli ion channels. Biophys J. 1989 Sep;56(3):631–636. [PMC free article] [PubMed] [Google Scholar]
- Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. [PubMed] [Google Scholar]
- Hamill OP, McBride DW., Jr The cloning of a mechano-gated membrane ion channel. Trends Neurosci. 1994 Nov;17(11):439–443. [PubMed] [Google Scholar]
- Hamill OP, McBride DW., Jr The pharmacology of mechanogated membrane ion channels. Pharmacol Rev. 1996 Jun;48(2):231–252. [PubMed] [Google Scholar]
- Hamill OP, McBride DW., Jr Induced membrane hypo/hyper-mechanosensitivity: a limitation of patch-clamp recording. Annu Rev Physiol. 1997;59:621–631. [PubMed] [Google Scholar]
- Harris NL, Presnell SR, Cohen FE. Four helix bundle diversity in globular proteins. J Mol Biol. 1994 Mar 11;236(5):1356–1368. [PubMed] [Google Scholar]
- Häse CC, Le Dain AC, Martinac B. Purification and functional reconstitution of the recombinant large mechanosensitive ion channel (MscL) of Escherichia coli. J Biol Chem. 1995 Aug 4;270(31):18329–18334. [PubMed] [Google Scholar]
- Häse CC, Le Dain AC, Martinac B. Molecular dissection of the large mechanosensitive ion channel (MscL) of E. coli: mutants with altered channel gating and pressure sensitivity. J Membr Biol. 1997 May 1;157(1):17–25. [PubMed] [Google Scholar]
- Häse CC, Minchin RF, Kloda A, Martinac B. Cross-linking studies and membrane localization and assembly of radiolabelled large mechanosensitive ion channel (MscL) of Escherichia coli. Biochem Biophys Res Commun. 1997 Mar 27;232(3):777–782. [PubMed] [Google Scholar]
- Hille B. Pharmacological modifications of the sodium channels of frog nerve. J Gen Physiol. 1968 Feb;51(2):199–219. [PMC free article] [PubMed] [Google Scholar]
- Howard J, Roberts WM, Hudspeth AJ. Mechanoelectrical transduction by hair cells. Annu Rev Biophys Biophys Chem. 1988;17:99–124. [PubMed] [Google Scholar]
- Lansman JB, Hallam TJ, Rink TJ. Single stretch-activated ion channels in vascular endothelial cells as mechanotransducers? Nature. 325(6107):811–813. [PubMed] [Google Scholar]
- Lewis CA. Ion-concentration dependence of the reversal potential and the single channel conductance of ion channels at the frog neuromuscular junction. J Physiol. 1979 Jan;286:417–445. [PMC free article] [PubMed] [Google Scholar]
- Martinac B, Adler J, Kung C. Mechanosensitive ion channels of E. coli activated by amphipaths. Nature. 1990 Nov 15;348(6298):261–263. [PubMed] [Google Scholar]
- Neher E, Eibl H. The influence of phospholipid polar groups on gramicidin channels. Biochim Biophys Acta. 1977 Jan 4;464(1):37–44. [PubMed] [Google Scholar]
- Oliet SH, Bourque CW. Mechanosensitive channels transduce osmosensitivity in supraoptic neurons. Nature. 1993 Jul 22;364(6435):341–343. [PubMed] [Google Scholar]
- Opsahl LR, Webb WW. Transduction of membrane tension by the ion channel alamethicin. Biophys J. 1994 Jan;66(1):71–74. [PMC free article] [PubMed] [Google Scholar]
- Sabovcik R, Li J, Kucera P, Prod'hom B. Permeation properties of a Ca(2+)-blockable monovalent cation channel in the ectoderm of the chick embryo: pore size and multioccupancy probed with organic cations and Ca2+. J Gen Physiol. 1995 Aug;106(2):149–174. [PMC free article] [PubMed] [Google Scholar]
- Sackin H. A stretch-activated K+ channel sensitive to cell volume. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1731–1735. [PMC free article] [PubMed] [Google Scholar]
- Sackin H. Mechanosensitive channels. Annu Rev Physiol. 1995;57:333–353. [PubMed] [Google Scholar]
- Schwarzmann G, Wiegandt H, Rose B, Zimmerman A, Ben-Haim D, Loewenstein WR. Diameter of the cell-to-cell junctional membrane channels as probed with neutral molecules. Science. 1981 Jul 31;213(4507):551–553. [PubMed] [Google Scholar]
- Sokabe M, Sachs F. The structure and dynamics of patch-clamped membranes: a study using differential interference contrast light microscopy. J Cell Biol. 1990 Aug;111(2):599–606. [PMC free article] [PubMed] [Google Scholar]
- Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, Gouaux JE. Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science. 1996 Dec 13;274(5294):1859–1866. [PubMed] [Google Scholar]
- Sukharev SI, Blount P, Martinac B, Blattner FR, Kung C. A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature. 1994 Mar 17;368(6468):265–268. [PubMed] [Google Scholar]
- Sukharev SI, Blount P, Martinac B, Kung C. Mechanosensitive channels of Escherichia coli: the MscL gene, protein, and activities. Annu Rev Physiol. 1997;59:633–657. [PubMed] [Google Scholar]
- Sukharev SI, Martinac B, Arshavsky VY, Kung C. Two types of mechanosensitive channels in the Escherichia coli cell envelope: solubilization and functional reconstitution. Biophys J. 1993 Jul;65(1):177–183. [PMC free article] [PubMed] [Google Scholar]
- Villarroel A, Burnashev N, Sakmann B. Dimensions of the narrow portion of a recombinant NMDA receptor channel. Biophys J. 1995 Mar;68(3):866–875. [PMC free article] [PubMed] [Google Scholar]
- Yang J. Ion permeation through 5-hydroxytryptamine-gated channels in neuroblastoma N18 cells. J Gen Physiol. 1990 Dec;96(6):1177–1198. [PMC free article] [PubMed] [Google Scholar]
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