Skip to main content
Log in

Membrane stretch augments the cardiac muscarinic K+ channel activity

  • Articles
  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Abstract

Arachidonic acid has been shown to activate K+-selective, mechanosensitive ion channels in cardiac, neuronal and smooth muscle cells. Since the cardiac G protein (G K )-gated, muscarinic K+ (KACh) channel can also be activated by arachidonic acid, we investigated whether the KACh channel was also sensitive to membrane stretch. In the absence of acetylcholine (ACh), KACh channels were not active, and negative pressure failed to activate these channels. With ACh (10 μm) in the pipette, applying negative pressure (0 to −80 mm Hg) to the membrane caused a reversible, pressure-dependent increase in channel activity in cell-attached and inside-out patches (100 μm GTP in bath). Membrane stretch did not alter the sensitivity of the KACh channel to GTP. When G K was maximally activated with 100 μm GTPγS in inside-out patches, the KACh channel activity could be further increased by negative pressure. Trypsin (0.5 mg/ ml) applied to the membrane caused activation of the KACh channel in the absence of ACh and GTP; KACh channel activity was further increased by stretch. These results indicate that the atrial muscarinic K+ channels are modulated by stretch independently of receptor/G protein, probably via a direct effect on the channel protein/ lipid bilayer.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Breitwieser, G.E., Szabo, G. 1988. Mechanism of musarinic receptor-induced K channel activation as revealed by hydrolysis-resistant GTP analogues. J. Gen. Physiol. 91:469–493

    Google Scholar 

  2. Falke, L.C., Edwards, K.L, Pickard, P.G., Misler, S. 1988. A stretch-activated channel in tobacco protoplasts. FEBS Lett. 237:141–144

    Google Scholar 

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

    Google Scholar 

  4. Hamill, O.P., Marty, A., Neher, E., Sakmann, B., Sigworth, F.J. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pfluegers Arch. 391:85–100

    Google Scholar 

  5. Huang, J.M., Xian, H., Bacaner, M. 1992. Long chain fatty acids activate calcium channels in ventricular myocytes. Proc. Natl. Acad. Sci. USA 89:6452–6456

    Google Scholar 

  6. Kim, D. 1991. Modulation of acetylcholine-activated K+ channel function in rat atrial cells by phosphorylation. J. Physiol. 437:133–155

    Google Scholar 

  7. Kim, D. 1992. A mechanosensitive K+ channel in heart cells: activation by arachidonic acid. J. Gen. Physiol. 100:1–20

    Google Scholar 

  8. Kim, D. 1993. Novel cation-selective mechanosensitive ion channel in the atrial cell membrane. Circ. Res. 72:225–231

    Google Scholar 

  9. Kim, D., Lewis, L.L., Graziadei, L., Neer, E.J., Bar-Sagi, D., Clapham, D.E. 1989. T-protein βγ-subunits activate the cardiac muscarinic K channel via phospholipase A2. Nature 337:557–560

    Google Scholar 

  10. Kim, D., Sladek, C.D., Aguado-Velasco, C., Mathiason, J.R. 1995. Arachidonic acid activation of a new family of K+ channels in cultured rat neuronal cells. J. Physiol. 484.3:643–660

    Google Scholar 

  11. Kirber, M.T., Ordway, R.W., Clapp, L.H., Walsh, J.V. Jr., Singer, J.J. 1992. Both membrane stretch and fatty acids directly activate large conductance Ca2+-activated K+ channels in vascular smooth muscle cells. Fed. Eur. Biochem. Soc. 297:24–28

    Google Scholar 

  12. Kirsch, G.E., Brown, A.M. 1989. Trypsin activation of atrial muscarinic K+ channels. Am. J. Physiol. 257:H334-H338

    Google Scholar 

  13. Kurachi, Y., Ito, H., Sugimoto, T., Shimizu, T., Miki, I., Ui, M. 1989a. Arachidonic acid metabolites as intracellular modulators of the G protein-gated cardiac K+ channel. Nature 337:555–557

    Google Scholar 

  14. Kurachi, Y., Ito, H., Sugimoto, T., Shimizu, T., Miki, I., Ui, M. 1989b. α-adrenergic activation of the muscarinic K channel is mediated by arachidonic acid metabolites. Pfluegers Arch. 414:102–104

    Google Scholar 

  15. Logothetis, D.E., Kim, D., Northup, J.K., Neer, E.J., Clapham, D.E. 1988. Specificity of action of guanine nucleotide-binding regulatory protein subunits on the cardiac muscarinic K channel. Proc. Natl. Acad. Sci. USA 85:5814–5818

    Google Scholar 

  16. Martinac, B., Buechner, M., Delcour, A.H., Adler, J., Kung, C. 1987. Mechanosensitive ion channel in Escherichia coli. Proc. Natl. Acad. Sci. USA 84:2297–2301

    CAS  PubMed  Google Scholar 

  17. Morris, C.E. 1990. Mechanosensitive ion channels. J. Membrane Biol. 113:93–107

    CAS  Google Scholar 

  18. Nakajima, T., Sugiimoto, T., Kurachi, Y. 1991. Platelet activating factor activates cardiac G K via arachidonic acid metabolites. Fed. Eur. Biochem. Soc. 289:239–243

    Google Scholar 

  19. Ordway, R.W., Singer, J.J., Walsh, J.V. 1991. Direct regulation of ion channels by fatty acids. Trend. Neurosci. 14:96–100

    Google Scholar 

  20. Piomelli, D., Volterra, A., Dale, N., Siegelbaum, S.A., Kandel, E.R., Schwartz, J.H., Belardetti, F. 1987. Lipoxygenase metabolites of arachidonic acids as second messengers for presynaptic inhibition of Aplasia sensory cells. Nature 328:38–43

    Google Scholar 

  21. Sachs, F. 1991. Mechanical transduction by membrane ion channels; a mini review. Mol. Cell Biochem. 104:57–60

    Google Scholar 

  22. Sackin, H. 1989. A stretch-activated K+ channel sensitive to cell volume. Proc. Natl. Acad. Sci. USA 86:1731–1735

    Google Scholar 

  23. Sakai, H., Okada, Y., Morii, M., Takeguchi, N. 1992. Arachidonic acid and prostaglandin E2 activate small-conductance Cl channels in the basolateral membrane of rabbit parietal cells. J. Physiol. 448:283–306

    Google Scholar 

  24. Scherer, R.W., Lo, F., Breitwieser, G.E. 1993. Leukotriene C4 modulation of muscarinic K+ current activation in bullfrog atrial myocytes. J. Gen. Physiol. 102:125–141

    Google Scholar 

  25. Sigworth, F.J., Sine, S.M. 1987. Data transformations for improved display and fitting of single-channel dwell time histograms. Biophys. J. 52:1047–1054

    Google Scholar 

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

    Google Scholar 

  27. Sukharev, S.I., Martinac, B., Arshavsky, V.Y., Kung, C. 1993. Two types of mechanosensitive channels in the Escherichia coli cell envelope: solubilization and functional reconstitution. Biophys. J. 65:177–183

    Google Scholar 

  28. Taglialatela, M., Wible, B.A., Caporaso, T., Brown, A.M. 1994. Specification of pore properties by the carboxyl terminus of inwardly rectifying K channels. Science 264:844–847

    Google Scholar 

  29. Takao, K., Yoshii, M., Kanda, A., Kokubun, S. Nukada, T. 1994. A region of the muscarinic-gated atrial K+ channel critical for activation by G protein βγ subunits. Neuron 13:747–755

    Google Scholar 

  30. Vandorpe, D.H., Morris, C.E. 1992. Stretch activation of the Aplysia S-channel. J. Membrane Biol. 127:205–214

    Google Scholar 

  31. Yatani, H., Mettera, R., Codina, J. Graf, R., Okabe, K., Padrell, E., Iyengar, R., Brown, A.M., Birnbaumer, L. 1988. The G proteingated atrial K+ channel is stimulated by three distinct Giαsubunits. Nature 366:680–682

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pleumsamran, A., Kim, D. Membrane stretch augments the cardiac muscarinic K+ channel activity. J. Membarin Biol. 148, 287–297 (1995). https://doi.org/10.1007/BF00235046

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00235046

Key words

Navigation