Pflügers Archiv

, Volume 446, Issue 5, pp 523–528

Actin filaments regulate the stretch sensitivity of large-conductance, Ca2+-activated K+ channels in coronary artery smooth muscle cells

Cardiovascular System

Abstract

Using the inside-out patch-clamp technique, large-conductance Ca2+-activated K+ channel (BKCa) currents were recorded from coronary artery smooth muscle cells. Cytochalasin D, an actin filament disrupter, increased channel activity (NPo, where N is the number of channels and Po the open probability), and this increase was reversed by phalloidin, an actin filament stabilizer. NPo was also increased by colchicine, a microtubule disrupter, and decreased by taxol, a microtubule stabilizer. With the stepwise increase of negative pressure in the patch pipettes, the activity of BKCa gradually increased: the maximum effect (527% increase in NPo) was achieved at −40 cmH2O and the half-maximum effect at −25 cmH2O. The increase in NPo in response to negative pressure was abolished by phalloidin but not by taxol. These results imply that both actin filaments and microtubules inhibit the opening of BKCa in coronary artery smooth muscle cells, but that only actin filaments are involved in the stretch sensitivity of BKCa.

Keywords

Vascular smooth muscle Ca2+-activated K+ channel Membrane stretch Cytoskeleton Actin filaments Microtubules 

References

  1. 1.
    Asano M, Masuzawa-Ito K, Imaizumi Y, Watanabe M, Ito K (1993) Functional role of Ca2+-activated K+ channels in resting state of carotid arteries from SHR. Am J Physiol 265:H843–H851PubMedGoogle Scholar
  2. 2.
    Braydn JE, Nelson MT (1992) Regulation of arterial tone by activation of calcium-dependent potassium channels. Science 256:532–535PubMedGoogle Scholar
  3. 3.
    Brenner R, Perez GJ, Bonev AD, Eckman DM, Kosek JC, Wiler SW, Patterson AJ, Nelson MT, Aldrich RW (2000) Vasoregulation by the beta1 subunit of the calcium-activated potassium channel. Nature 407:870–876Google Scholar
  4. 4.
    Dopico AM, Kirber MT, Singer JJ, Walsh JV Jr (1994) Membrane stretch directly activates large conductance Ca2+-activated K+ channels in mesenteric artery smooth muscle cells. Am J Hypertens 7:82–89PubMedGoogle Scholar
  5. 5.
    Dube L, Parent L, Sauve R (1990) Hypotonic shock activates a maxi K+ channel in primary cultured proximal tubule cells. Am J Physiol 259:F348–F356PubMedGoogle Scholar
  6. 6.
    Glogauer M, Ferrier J, McCulloch CA (1995) Magnetic fields applied to collagen-coated ferric oxide beads induce stretch-activated Ca2+ flux in fibroblasts. Am J Physiol 269:C1093–C1104PubMedGoogle Scholar
  7. 7.
    Glogauer M, Arora P, Yao G, Sokholov I, Ferrier J, McCulloch CA (1997) Calcium ions and tyrosine phosphorylation interact coordinately with actin to regulate cytoprotective responses to stretching. J Cell Sci 110:11–21PubMedGoogle Scholar
  8. 8.
    Huang H, Rao Y, Sun P, Gong LW (2002) Involvement of actin cytoskeleton in modulation of Ca2+-activated K+ channels from rat hippocampal CA1 pyramidal neurons. Neurosci Lett 332:141–145CrossRefPubMedGoogle Scholar
  9. 9.
    Jackson WF (2000) Ion channels and vascular tone. Hypertension 35:173–178PubMedGoogle Scholar
  10. 10.
    Kraft R, Benndorf K, Patt S (2000) Large conductance Ca2+-activated K+ channels in human meningioma cells. J Membr Biol 175:25–33PubMedGoogle Scholar
  11. 11.
    Kolias TJ, Chai S, Webb RC (1993) Potassium channel antagonists and vascular reactivity in stroke-prone spontaneously hypertensive rats. Am J Hypertens 6:528–533PubMedGoogle Scholar
  12. 12.
    Lader AS, Kwiatkowski DJ, Cantiello HF (1999) Role of gelsolin in the actin filament regulation of cardiac L-type calcium channels. Am J Physiol 277:C1277–C1283PubMedGoogle Scholar
  13. 13.
    Liu Y, Hudetz AG, Knaus H-G, Rusch NJ (1998) Increased expression of Ca2+-sensitive K+ channels in the cerebral microcirculation of genetically hypertensive rats: evidence for their protection against cerebral vasospasm. Circ Res 82:729–737PubMedGoogle Scholar
  14. 14.
    Mienville J-M, Barker JL, Lange GD (1996) Mechanosensitive properties of BK channels from embryonic rat neuroepithelium. J Membr Biol 153:211–216CrossRefPubMedGoogle Scholar
  15. 15.
    Nakamura M, Sunagawa M, Kosugi T, Sperelakis N (2000) Actin filament disruption inhibits L-type Ca2+ channel current in cultured vascular smooth muscle cells. Am J Physiol 279:C480–C487Google Scholar
  16. 16.
    Nelson MT, Quayle JM (1995) Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol 268:C799–C822PubMedGoogle Scholar
  17. 17.
    Osol G (1995) Mechanotransduction by vascular smooth muscle. J Vasc Res 32:275–292PubMedGoogle Scholar
  18. 18.
    Paterno R, Heistad DD, Faraci FM (2000) Potassium channels modulate cerebral autoregulation during acute hypertension. Am J Physiol 278:H2003–H2007Google Scholar
  19. 19.
    Piao L, Li Y, Li L, Jin NG, Li ZL, Xu WX (2001) The involvement of calcium mobilization in the calcium-activated potassium currents activated by hyposmotic swelling in gastric antral circular myocytes of the guinea-pig. Jpn J Physiol 51:223–30PubMedGoogle Scholar
  20. 20.
    Shin KS, Park JY, Ha DB, Chung CH, Kang MS (1996) Involvement of KCa channels and stretch-activated channels in calcium influx, triggering membrane fusion of chick embryonic myoblasts. Dev Biol 175:14–23CrossRefPubMedGoogle Scholar
  21. 21.
    Taniguchi J, Guggino WB (1989) Membrane stretch: a physiological stimulator of Ca2+-activated K+ channels in thick ascending limb. Am J Physiol 257:F347–F352PubMedGoogle Scholar
  22. 22.
    Undrovinas AI, Maltsev VA (1998) Cytochalasin D alters kinetics of Ca2+ transient in rat ventricular cardiomyocytes: an effect of altered actin cytoskeleton? J Mol Cell Cardiol 30:1665–1670Google Scholar
  23. 23.
    Wallner M, Meera P, Toro L (1999) Large conductance, voltage-gated, and Ca2+-sensitive K+ channels. In: Kurachi Y, Jan LY, Lazdunski M (eds) Potassium ion channels: molecular structure, function, and diseases. Academic Press, San Diego, pp 118–128Google Scholar
  24. 24.
    Wu Z, Wong K, Glogauer M, Ellen RP, McCulloch CA (1999) Regulation of stretch-activated intracellular calcium transients by actin filaments. Biochem Biophys Res Commun 261:419–425CrossRefPubMedGoogle Scholar
  25. 25.
    Xu WX, Kim SJ, So I, Kim KW (1997) Role of actin microfilament in osmotic stretch-induced increase of voltage-operated calcium channel current in guinea-pig gastric myocytes. Pflugers Arch 434:502–504CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag  2003

Authors and Affiliations

  1. 1.National Research Laboratory for Cellular Signalling and Department of PhysiologySeoul National University College of MedicineSeoulKorea

Personalised recommendations