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. 1991 Nov;60(5):1120–1127. doi: 10.1016/S0006-3495(91)82147-6

Mechanosensitive ion channels as reporters of bilayer expansion. A theoretical model.

V S Markin 1, B Martinac 1
PMCID: PMC1260167  PMID: 1722115

Abstract

Various amphipathic compounds have been found to activate mechanosensitive (MS) ion channels in the bacterium Escherichia coli. These results were interpreted qualitatively in terms of the bilayer couple hypothesis. Here we present a mathematical model that describes the results quantitatively. According to the model, the uneven partitioning of amphipaths between the monolayers of the cell membrane causes one monolayer to be compressed and the other expanded. Because the open probability (Po) of the E. coli channels increased independently of which monolayer the amphipaths partitioned into, the model suggests that Po of the MS channels is determined by the monolayer having higher tension. We derived a relation between Po and amphipath concentration. The kinetics of Po variation after exposure of the cell membrane to the amphipaths was calculated based on this relation. The results fit satisfactorily the experimental data obtained with the cationic amphipath chlorpromazine and with the anionic amphipath trinitrophenol. Experiments which should further test the predictions following from the model are discussed.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Cooper K. E., Tang J. M., Rae J. L., Eisenberg R. S. A cation channel in frog lens epithelia responsive to pressure and calcium. J Membr Biol. 1986;93(3):259–269. doi: 10.1007/BF01871180. [DOI] [PubMed] [Google Scholar]
  2. Delcour A. H., 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. doi: 10.1016/S0006-3495(89)82710-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Evans E. A., Waugh R., Melnik L. Elastic area compressibility modulus of red cell membrane. Biophys J. 1976 Jun;16(6):585–595. doi: 10.1016/S0006-3495(76)85713-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Falke L. C., Edwards K. L., Pickard B. G., Misler S. A stretch-activated anion channel in tobacco protoplasts. FEBS Lett. 1988 Sep 12;237(1-2):141–144. doi: 10.1016/0014-5793(88)80188-1. [DOI] [PubMed] [Google Scholar]
  5. Guharay F., Sachs F. Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J Physiol. 1984 Jul;352:685–701. doi: 10.1113/jphysiol.1984.sp015317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gustin M. C., Zhou X. L., Martinac B., Kung C. A mechanosensitive ion channel in the yeast plasma membrane. Science. 1988 Nov 4;242(4879):762–765. doi: 10.1126/science.2460920. [DOI] [PubMed] [Google Scholar]
  7. Hudspeth A. J. The ionic channels of a vertebrate hair cell. Hear Res. 1986;22:21–27. doi: 10.1016/0378-5955(86)90070-5. [DOI] [PubMed] [Google Scholar]
  8. Israelachvili J. N., Marcelja S., Horn R. G. Physical principles of membrane organization. Q Rev Biophys. 1980 May;13(2):121–200. doi: 10.1017/s0033583500001645. [DOI] [PubMed] [Google Scholar]
  9. Koslov M. M., Markin V. S. A theory of osmotic lysis of lipid vesicles. J Theor Biol. 1984 Jul 7;109(1):17–39. doi: 10.1016/s0022-5193(84)80108-3. [DOI] [PubMed] [Google Scholar]
  10. Markin V. S. Lateral organization of membranes and cell shapes. Biophys J. 1981 Oct;36(1):1–19. doi: 10.1016/S0006-3495(81)84713-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Martinac B., Adler J., Kung C. Mechanosensitive ion channels of E. coli activated by amphipaths. Nature. 1990 Nov 15;348(6298):261–263. doi: 10.1038/348261a0. [DOI] [PubMed] [Google Scholar]
  12. Martinac B., Buechner M., Delcour A. H., Adler J., Kung C. Pressure-sensitive ion channel in Escherichia coli. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2297–2301. doi: 10.1073/pnas.84.8.2297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Morris C. E. Mechanosensitive ion channels. J Membr Biol. 1990 Feb;113(2):93–107. doi: 10.1007/BF01872883. [DOI] [PubMed] [Google Scholar]
  14. Ohmori H. Studies of ionic currents in the isolated vestibular hair cell of the chick. J Physiol. 1984 May;350:561–581. doi: 10.1113/jphysiol.1984.sp015218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Sheetz M. P., Singer S. J. Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc Natl Acad Sci U S A. 1974 Nov;71(11):4457–4461. doi: 10.1073/pnas.71.11.4457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Sokabe M., Sachs F., Jing Z. Q. Quantitative video microscopy of patch clamped membranes stress, strain, capacitance, and stretch channel activation. Biophys J. 1991 Mar;59(3):722–728. doi: 10.1016/S0006-3495(91)82285-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Stockbridge L. L., French A. S. Stretch-activated cation channels in human fibroblasts. Biophys J. 1988 Jul;54(1):187–190. doi: 10.1016/S0006-3495(88)82944-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Yeagle P. L. Lipid regulation of cell membrane structure and function. FASEB J. 1989 May;3(7):1833–1842. [PubMed] [Google Scholar]
  19. Zoratti M., Petronilli V. Ion-conducting channels in a gram-positive bacterium. FEBS Lett. 1988 Nov 21;240(1-2):105–109. doi: 10.1016/0014-5793(88)80348-x. [DOI] [PubMed] [Google Scholar]

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