Skip to main content
SpringerLink
Log in

Inward-rectifier K+ Current in Guinea-pig Ventricular Myocytes Exposed to Hyperosmotic Solutions

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

Abstract

Superfusion of heart cells with hyperosmotic solution causes cell shrinkage and inhibition of membrane ionic currents, including delayed-rectifer K+ currents. To determine whether osmotic shrinkage also inhibits inwardly-rectifying K+ current (IK1), guinea-pig ventricular myocytes in the perforated-patch or ruptured-patch configuration were superfused with a Tyrode’s solution whose osmolarity (T) relative to isosmotic (1T) solution was increased to 1.3–2.2T by addition of sucrose. Hyperosmotic superfusate caused a rapid shrinkage that was accompanied by a negative shift in the reversal potential of Ba2+-sensitive IK1, an increase in the amplitude of outward IK1, and a steepening of the slope of the inward IK1-voltage (V) relation. The magnitude of these effects increased with external osmolarity. To evaluate the underlying changes in chord conductance (GK1) and rectification, GK1-V data were fitted with Boltzmann functions to determine maximal GK1 (GK1max) and voltage at one-half GK1max (V0.5). Superfusion with hyperosmotic sucrose solutions led to significant increases in GK1max (e.g., 28 ± 2% with 1.8T), and significant negative shifts in V0.5 (e.g., −6.7 ± 0.6 mV with 1.8T). Data from myocytes investigated under hyperosmotic conditions that do not induce shrinkage indicate that GK1max and V0.5 were insensitive to hyperosmotic stress per se but sensitive to elevation of intracellular K+. We conclude that the effects of hyperosmotic sucrose solutions on IK1 are related to shrinkage-induced concentrating of intracellular K+.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • D.G. Alien G.L. Smith (1987) ArticleTitleThe effects of hypertonicity on tension and intracellular calcium concentration in ferret ventricular muscle J. Physiol. 383 425–439

    Google Scholar 

  • N. Askenasy G. Navon (1997) ArticleTitleIntermittent ischemia: energy metabolism, cellular volume regulation, adenosine and insights into preconditioning J. Mol. Cell. Cardiol. 29 1715–1730

    Google Scholar 

  • H.F. Clemo C.M. Baumgarten (1997) ArticleTitleSwelling-activated Gd3+-sensitive cation current and cell volume regulation in rabbit ventricular myocytes J. Gen. Physiol. 110 297–312

    Google Scholar 

  • H.F. Clemo B.S. Stambler C.M. Baumgarten (1999) ArticleTitleSwelling-activated chloride current is persistently activated in ventricular myocytes from dogs with tachycardia-induced congestive heart failure Circ. Res. 84 157–165

    Google Scholar 

  • I.S. Cohen D. DiFrancesco N.K. Mulrine P. Pennefather (1989) ArticleTitleInternal and external K+ help gate the inward rectifier Biophys. J. 55 197–202

    Google Scholar 

  • K. Drewnowska C.M. Baumgarten (1991) ArticleTitleRegulation of cellular volume in rabbit ventricular myocytes: bumetanide, chlorothiazide, and ouabain Am. J. Physiol. 260 C122–C131

    Google Scholar 

  • D. Duan L. Ye F. Britton B. Horowitz J.R. Hume (2000) ArticleTitleA novel anionic inward rectifier in native cardiac myocytes Circ. Res. 86 E63–E71

    Google Scholar 

  • H.A. Fozzard C.O. Lee (1976) ArticleTitleInfluence of changes in external potassium and chloride ions on membrane potential and intracellular potassium ion activity in rabbit ventricular muscle J. Physiol. 256 663–689

    Google Scholar 

  • S. Hagiwara M. Yoshii (1979) ArticleTitleEffects of internal potassium and sodium on the anomalous rectification of the starfish egg as examined by internal perfusion J. Physiol. 292 251–265

    Google Scholar 

  • H. Hu F. Sachs (1997) ArticleTitleStretch-activated ion channels in the heart J. Mol. Cell. Cardiol. 29 1511–1523

    Google Scholar 

  • J.R. Hume D. Duan M.L. Collier J. Yamazaki B. Horowitz (2000) ArticleTitleAnion transport in heart Physiol. Rev. 80 31–81

    Google Scholar 

  • J. Ibarra G.E. Morley M. Delmar (1991) ArticleTitleDynamics of the inward rectifier K+ current during the action potential of guinea pig ventricular myocytes Biophys. J. 60 1534–1539

    Google Scholar 

  • G. Isenberg (1976) ArticleTitleCardiac Purkinje fibers: cesium as a tool to block inward rectifying potassium currents Pfluegers Arch. 365 99–106

    Google Scholar 

  • A. Kapus K. Szaszi J. Sun S. Rizoli O.D. Rotstein (1999) ArticleTitleCell shrinkage regulates Src kinases and induces tyrosine phosphorylation of cortactin, independent of the osmotic regulation of Na+/H+ exchangers J. Biol. Chem. 274 8093–8102

    Google Scholar 

  • D. Kim C. Fu (1993) ArticleTitleActivation of a nonselective cation channel by swelling in atrial cells J. Membrane Biol. 135 27–37

    Google Scholar 

  • J. Koch C. Korbmacher (1999) ArticleTitleOsmotic shrinkage activates nonselective cation (NSC) channels in various cell types J. Membrane Biol. 168 131–139

    Google Scholar 

  • J.P. Koch C. Korbmacher (2000) ArticleTitleMechanism of shrinkage activation of nonselective cation channels in M-1 mouse cortical collecting duct cells J. Membrane Biol. 177 231–242

    Google Scholar 

  • I. Kocic Y. Hirano M. Hiraoka (2001) ArticleTitleIonic basis for membrane potential changes induced by hypoosmotic stress in guinea-pig ventricular myocytes Cardiovasc. Res. 51 59–70

    Google Scholar 

  • G.C. Kramer T.P. English R.A. Gunther J.W. Holcroft (1989) ArticleTitlePhysiological mechanisms of fluid resuscitation with hyperosmotic/hyperoncotic solutions Prog. Clin. Biol. Res. 299 311–320

    Google Scholar 

  • F. Lang G.L. Busch M. Ritter H. Volkl S. Waldegger E. Gulbins D. Haussinger (1998) ArticleTitleFunctional significance of cell volume regulatory mechanisms Physiol. Rev. 78 247–306

    Google Scholar 

  • C.A. Leech P.R. Stanfield (1981) ArticleTitleInward rectification in frog skeletal muscle fibres and its dependence on membrane potential and external potassium J. Physiol. 319 295–309

    Google Scholar 

  • F. Lesage M. Lazdunski (2000) ArticleTitleMolecular and functional properties of two-pore-domain potassium channels Am. J. Physiol. 279 F793–F801

    Google Scholar 

  • A.N. Lopatin C.G. Nichols (2001) ArticleTitleInward rectifiers in the heart: an update on IK1 J Mol. Cell. Cardiol 33 625–638

    Google Scholar 

  • R.L. Martin S. Koumi R.E. Ten Eick (1995) ArticleTitleComparison of the effects of internal [Mg2+] on IK1 in cat and guinea-pig cardiac ventricular myocytes J. Mol. Cell. Cardiol. 27 673–691

    Google Scholar 

  • N. Matsuda N. Hagiwara M. Shoda H. Kasanuki S. Hosoda (1996) ArticleTitleEnhancement of the L-type Ca2+ current by mechanical stimulation in single rabbit cardiac myocytes Circ. Res. 78 650–659

    Google Scholar 

  • N.A. McCarty R.G. O’Neil (1992) ArticleTitleCalcium signaling in cell volume regulation Physiol. Rev. 72 1037–1061 Occurrence Handle1:CAS:528:DyaK3sXls1OltA%3D%3D Occurrence Handle1332089

    CAS  PubMed  Google Scholar 

  • D.J. Nelson X.Y. Tien W. Xie T.A. Brasitus M.A. Kaetzel J.R. Dedman (1996) ArticleTitleShrinkage activates a nonselective conductance: involvement of a Walker-motif protein and PKC Am. J. Physiol. 270 C179–C191

    Google Scholar 

  • D. Noble (1979) The Initiation of the Heartbeat Oxford University Press Oxford

    Google Scholar 

  • T. Ogura H. Matsuda T. Shibamoto S. Imanishi (2003) ArticleTitleOsmosensitive properties of rapid and slow delayed rectifier K+ currents in guinea-pig heart cells Clin. Exp. Pharmacol. Physiol. 30 616–622

    Google Scholar 

  • T. Ogura L.M. Shuba T.F. McDonald (1995) ArticleTitleAction potentials, ionic currents and cell water in guinea pig ventricular preparations exposed to dimethyl sulfoxide J. Pharmacol. Exp. Ther. 273 1273–1286

    Google Scholar 

  • T. Ogura Y. You T.F. McDonald (1997) ArticleTitleMembrane currents underlying the modified electrical activity of guinea-pig ventricular myocytes exposed to hyperosmotic solution J. Physiol. 504 135–151

    Google Scholar 

  • C. Pascarel P. Brette J.Y. Le Guennec (2001) ArticleTitleEnhancement of the T-type calcium current by hyposmotic shock in isolated guinea-pig ventricular myocytes J. Mol. Cell. Cardiol 33 1363–1369

    Google Scholar 

  • C. Pascarel K. Hongo O. Cazorla E. White J.Y. Le Guennec (1998) ArticleTitleDifferent effects of gadolinium on IKR, IKS, and IK1 in guinea-pig isolated ventricular myocytes Br. J. Pharmacol. 124 356–360

    Google Scholar 

  • S.F. Pedersen J.W. Mills E.K. Hoffmann (1999) ArticleTitleRole of the F-actin cytoskeleton in the RVD and RVI processes in Ehrlich ascites tumor cells Exp. Cell. Res. 252 63–74

    Google Scholar 

  • R.L. Rasmusson D.G. Davis M. Lieberman (1993) ArticleTitleAmino acid loss during volume regulatory decrease in cultured chick heart cells Am. J. Physiol. 264 C136–C145

    Google Scholar 

  • S.A. Rees J.I. Vandenberg A.R. Wright A. Yoshida T. Powell (1995) ArticleTitleCell swelling has differential effects on the rapid and slow components of delayed rectifier potassium current in guinea pig cardiac myocytes J. Gen. Physiol. 106 1151–1170

    Google Scholar 

  • K.P. Roos (1986) ArticleTitleLength, width, and volume changes in osmotically stressed myocytes Am. J. Physiol. 251 H1373–H1378

    Google Scholar 

  • A. Saigusa H. Matsuda (1988) ArticleTitleOutward currents through the inwardly rectifying potassium channel of guinea-pig ventricular cells Jpn. J. Physiol. 38 77–91

    Google Scholar 

  • B. Sarkadi J.C. Parker (1991) ArticleTitleActivation of ion transport pathways by changes in cell volume Biochim. Biophys. Acta 1071 407–427

    Google Scholar 

  • N. Sasaki T. Mitsuiye A. Noma (1992) ArticleTitleEffects of mechanical stretch on membrane currents of single ventricular myocytes of guinea-pig heart Jpn. J. Physiol. 42 957–970

    Google Scholar 

  • N. Sasaki T. Mitsuiye Z. Wang A. Noma (1994) ArticleTitleIncrease of the delayed rectifier K+ and Na+-K+ pump currents by hypotonic solutions in guinea pig cardiac myocytes Circ. Res. 75 887–895

    Google Scholar 

  • N. Sasaki M. Takano T. Mitsuiye A. Noma (1999) ArticleTitleChanges in cell volume induced by ion channel flux in guinea-pig cardiac myocytes Clin. Exp. Pharmacol Physiol. 26 698–706

    Google Scholar 

  • N.B. Standen P.R. Stanfield (1980) ArticleTitleRubidium block and rubidium permeability of the inward rectifier of frog skeletal muscle fibres J. Physiol. 304 415–435

    Google Scholar 

  • M.A. Suleymanian C.M. Baumgarten (1996) ArticleTitleOsmotic gradient-induced water permeation across the sarcolemma of rabbit ventricular myocytes J. Gen. Physiol. 107 503–514

    Google Scholar 

  • D.R. Wagoner ParticleVan (1993) ArticleTitleMechanosensitive gating of atrial ATP-sensitive potassium channels Circ. Res. 72 973–983

    Google Scholar 

  • C.A. Vandenberg (1987) ArticleTitleInward rectification of a potassium channel in cardiac ventricular cells depends on internal magnesium ions Proc. Natl. Acad. Sci. USA. 84 2560– 2564

    Google Scholar 

  • S. Watanabe K. Kusama-Eguchi H. Kobayashi K. Igarashi (1991) ArticleTitleEstimation of polyamine binding to macromolecules and ATP in bovine lymphocytes and rat liver J. Biol. Chem. 266 20803–20809

    Google Scholar 

  • D.W. Whalley L.C. Hool R.E. Ten Eick H.H. Rasmussen (1993) ArticleTitleEffect of osmotic swelling and shrinkage on Na+-K+ pump activity in mammalian cardiac myocytes Am. J. Physiol. 265 C1201–C1210

    Google Scholar 

  • A.R. Wright S.A. Rees J.I. Vandenberg V.W. Twist T. Powell (1995) ArticleTitleExtracellular osmotic pressure modulates sodium-calcium exchange in isolated guinea-pig ventricular myocytes J. Physiol. 488 293–301

    Google Scholar 

  • Y.Y. Zhou J.A. Yao G.N. Tseng (1997) ArticleTitleRole of tyrosine kinase activity in cardiac slow delayed rectifier channel modulation by cell swelling Pfluegers Arch. 433 750–757

    Google Scholar 

Download references

Acknowledgments

The authors thank Gina Dickie for excellent technical assistance. Funding for the study was provided by the Canadian Institutes of Health Research (CIHR).

Author information

Author notes

  1. T. Ogura

    Present address: Department of Physiology, Kanazawa Medical University, Ishikawa, Japan

Authors and Affiliations

  1. Department of Physiology and Biophysics, Dalhousie University, Halifax, Nova Scotia, B3H 4H7, Canada

    S. Missan, P. Zhabyeyev, O. Dyachok, T. Ogura & T.F. McDonald

Authors
  1. S. Missan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Zhabyeyev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. O. Dyachok
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. Ogura
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T.F. McDonald
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T.F. McDonald.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Missan, S., Zhabyeyev, P., Dyachok, O. et al. Inward-rectifier K+ Current in Guinea-pig Ventricular Myocytes Exposed to Hyperosmotic Solutions. J Membrane Biol 202, 151–160 (2004). https://doi.org/10.1007/s00232-004-0726-3

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00232-004-0726-3

Keywords

Search

Navigation