Home LiteratureArticle Details
PMID: 3612087 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Calcium- and voltage-activated plateau currents of cardiac Purkinje fibers.

The Journal of general physiology ·Vol. 89 ·No. 6 ·1987-06-00 ·Pages 921-58

Kenyon JL, Sutko JL

Abstract

We have used the two-microelectrode voltage-clamp technique to investigate the components of membrane current that contribute to the formation of the early part of the plateau phase of the action potential of calf cardiac Purkinje fibers. 3,4-Diaminopyridine (50 microM) reduced the net transient outward current elicited by depolarizations to potentials positive to -30 mV but had no consistent effect on contraction. We attribute this effect to the blockade of a voltage-activated transient potassium current component. Ryanodine (1 microM), an inhibitor of sarcoplasmic reticulum calcium release and intracellular calcium oscillations in Purkinje fibers (Sutko, J.L., and J.L. Kenyon. 1983. Journal of General Physiology. 82:385-404), had complex effects on membrane currents as it abolished phasic contractions. At early times during a depolarization (5-30 ms), ryanodine reduced the net outward current. We attribute this effect to the loss of a component of calcium-activated potassium current caused by the inhibition of sarcoplasmic reticulum calcium release and the intracellular calcium transient. At later times during a depolarization (50-200 ms), ryanodine increased the net outward current. This effect was not seen in low-sodium solutions and we could not observe a reversal potential over a voltage range of -100 to +75 mV. These data suggest that the effect of ryanodine on the late membrane current is attributable to the loss of sodium-calcium exchange current caused by the inhibition of sarcoplasmic reticulum calcium release and the intracellular calcium transient. Neither effect of ryanodine was dependent on chloride ions, which suggests that chloride ions do not carry the ryanodine-sensitive current components. Strontium (2.7 mM replacing calcium) and caffeine (10 mM), two other treatments that interfere with sarcoplasmic reticulum function, had effects in common with ryanodine. This supports the hypothesis that the effects of ryanodine may be attributed to the inhibition of sarcoplasmic reticulum calcium release.

MeSH Terms
Action Potentials Aminopyridines/pharmacology Animals Calcium/metabolism Cattle Cell Membrane/drug effects,physiology Chlorides/metabolism Electric Conductivity Heart Conduction System/physiology Microelectrodes Purkinje Fibers/drug effects,physiology Ryanodine/pharmacology Sarcoplasmic Reticulum/metabolism
Chemicals
Aminopyridines Chlorides Ryanodine Calcium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Kenyon J L
Sutko J L
References (63)
63 references, click to expand
  1. Membrane currents, contractions, and aftercontractions in cardiac Purkinje fibers.
    Am J Physiol. 1982 Jul;243(1):H77-86 PMID: 7091381
  2. VOLTAGE CLAMP TECHNIQUE IN MAMMALIAN CARDIAC FIBRES.
    Pflugers Arch Gesamte Physiol Menschen Tiere. 1964 Jun 9;280:50-62 PMID: 14251605
  3. A calcium-dependent transient outward current in Xenopus laevis oocytes.
    Proc R Soc Lond B Biol Sci. 1982 Jul 22;215(1201):491-7 PMID: 6127718
  4. Effects of nystatin-mediated intracellular ion substitution on membrane currents in calf purkinje fibres.
    J Physiol. 1982 Aug;329:569-87 PMID: 6292409
  5. Early outward current in rat single ventricular cells.
    Circ Res. 1984 Feb;54(2):157-62 PMID: 6319044
  6. Caffeine induces a transient inward current in cultured cardiac cells.
    Nature. 1983 Jan 20;301(5897):248-50 PMID: 6296694
  7. Lyotropic anions. Na channel gating and Ca electrode response.
    J Gen Physiol. 1983 Feb;81(2):255-81 PMID: 6302198
  8. Ryanodine modification of cardiac muscle responses to potassium-free solutions. Evidence for inhibition of sarcoplasmic reticulum calcium release.
    J Gen Physiol. 1983 Sep;82(3):385-404 PMID: 6631403
  9. A transient calcium-dependent chloride current in the immature Xenopus oocyte.
    J Physiol. 1983 Sep;342:309-25 PMID: 6313909
  10. Transient outward current and rate dependence of action potential duration in rabbit cardiac ventricular muscle.
    Pflugers Arch. 1983 Oct;399(2):87-92 PMID: 6647007
  11. Electrical properties of sheep Purkinje strands. Electrical and chemical potentials in the clefts.
    Biophys J. 1983 Nov;44(2):225-48 PMID: 6360228
  12. The dynamic chloride component of membrane current in Purkinje fibers.
    Pflugers Arch Gesamte Physiol Menschen Tiere. 1967;295(3):197-212 PMID: 5241426
  13. The positive dynamic current and its inactivation properties in cardiac Purkinje fibres.
    J Physiol. 1973 Nov;234(3):569-86 PMID: 4764430
  14. Reconstruction of the electrical activity of cardiac Purkinje fibres.
    J Physiol. 1975 Sep;251(1):1-59 PMID: 1185607
  15. Heart: excitation and contraction.
    Annu Rev Physiol. 1971;33:479-532 PMID: 4951054
  16. Activities of potassium and sodium ions in rabbit heart muscle.
    J Gen Physiol. 1975 Jun;65(6):695-708 PMID: 1194884
  17. Control of action potential duration by calcium ions in cardiac Purkinje fibers.
    J Gen Physiol. 1976 May;67(5):599-617 PMID: 1271045
  18. The role of the positive dynamic current on the action potential of cardiac Purkinje fibers.
    Jpn J Physiol. 1975;25(6):705-17 PMID: 1226006
  19. Reduction of potassium permeability by chloride substitution in cardiac cells.
    J Physiol. 1977 Feb;265(1):193-206 PMID: 850161
  20. Effect of changing the composition of the bathing solutions upon the isometric tension-pCa relationship in bundles of crustacean myofibrils.
    J Physiol. 1977 Sep;270(3):627-52 PMID: 20499
  21. The effects of external cations and ouabain on the intracellular sodium activity of sheep heart Purkinje fibres.
    J Physiol. 1977 Dec;273(1):211-40 PMID: 599421
  22. 3,4-diaminopyridine. A potent new potassium channel blocker.
    Biophys J. 1978 Jun;22(3):507-12 PMID: 667299
  23. Role of calcium ions in transient inward currents and aftercontractions induced by strophanthidin in cardiac Purkinje fibres.
    J Physiol. 1978 Aug;281:187-208 PMID: 702368
  24. Sodium-calcium ion exchange in cardiac membrane vesicles.
    Proc Natl Acad Sci U S A. 1979 Feb;76(2):590-4 PMID: 284383
  25. The generation of electric currents in cardiac fibers by Na/Ca exchange.
    Am J Physiol. 1979 Mar;236(3):C103-10 PMID: 371415
  26. Ryanodine: its alterations of cat papillary muscle contractile state and responsiveness to inotropic interventions and a suggested mechanism of action.
    J Pharmacol Exp Ther. 1979 Apr;209(1):37-47 PMID: 430377
  27. Influence of chloride, potassium, and tetraethylammonium on the early outward current of sheep cardiac Purkinje fibers.
    J Gen Physiol. 1979 Feb;73(2):117-38 PMID: 438768
  28. 4-Aminopyridine and the early outward current of sheep cardiac Purkinje fibers.
    J Gen Physiol. 1979 Feb;73(2):139-57 PMID: 220376
  29. Three-micro-electrode voltage clamp experiments in calf cardiac Purkinje fibres: is slow inward current adequately measured?
    J Physiol. 1979 May;290(2):201-25 PMID: 469751
  30. Activation of contraction of arterial smooth muscle in the presence of nitrate and other anions.
    Pflugers Arch. 1979 Jul;381(1):63-9 PMID: 573455
  31. Effects of chloride on the electrical and mechanical properties of guinea pig ventricle.
    Pflugers Arch. 1979 Aug;381(2):171-7 PMID: 574258
  32. Non-passive chloride distribution in mammalian heart muscle: micro-electrode measurement of the intracellular chloride activity.
    J Physiol. 1979 Oct;295:83-109 PMID: 521996
  33. Calcium-activated transient outward current in calf cardiac Purkinje fibres.
    J Physiol. 1980 Feb;299:485-506 PMID: 6770079
  34. K efflux through inward rectifying K channels in voltage clamped Purkinje fibers.
    Pflugers Arch. 1980 Apr;384(3):207-17 PMID: 6251423
  35. The electrogenic Na-Ca exchange and the cardiac electrical activity. I--Simulation on Purkinje fibre action potential.
    J Physiol (Paris). 1981 Sep;77(6-7):705-9 PMID: 7288663
  36. A study of the effect of the rate of stimulation on the transient outward current in sheep cardiac Purkinje fibres.
    J Physiol. 1981;319:1-22 PMID: 7320907
  37. Single Ca2+-activated nonselective cation channels in neuroblastoma.
    Nature. 1982 Mar 25;296(5855):357-9 PMID: 6278324
  38. Existence of two transient outward currents in sheep cardiac Purkinje fibers.
    Pflugers Arch. 1982 Feb;392(4):352-9 PMID: 7070967
  39. Strontium, nifedipine and 4-aminopyridine modify the time course of the action potential in cells from rat ventricular muscle.
    Br J Pharmacol. 1984 Mar;81(3):551-6 PMID: 6697062
  40. Ryanodine prolongs Ca-currents while suppressing contraction in rat ventricular muscle cells.
    Br J Pharmacol. 1984 Jan;81(1):13-5 PMID: 6322890
  41. Excitation-contraction coupling in cardiac Purkinje fibers. Effects of caffeine on the intracellular [Ca2+] transient, membrane currents, and contraction.
    J Gen Physiol. 1984 Mar;83(3):417-33 PMID: 6325589
  42. The stoichiometry of the cardiac sodium-calcium exchange system.
    J Biol Chem. 1984 Jun 25;259(12):7733-9 PMID: 6736024
  43. Characterization of oscillations of intracellular calcium concentration in ferret ventricular muscle.
    J Physiol. 1984 Jul;352:113-28 PMID: 6747885
  44. A Ca-dependent Cl- conductance in cultured mouse spinal neurones.
    Nature. 1984 Oct 11-17;311(5986):567-70 PMID: 6482969
  45. Inactivation of calcium channel current in the calf cardiac Purkinje fiber. Evidence for voltage- and calcium-mediated mechanisms.
    J Gen Physiol. 1984 Nov;84(5):705-26 PMID: 6096480
  46. Ryanodine as a tool to determine the contributions of calcium entry and calcium release to the calcium transient and contraction of cardiac Purkinje fibers.
    Circ Res. 1985 Jan;56(1):133-8 PMID: 2578335
  47. A dihydropyridine (Bay k 8644) that enhances calcium currents in guinea pig and calf myocardial cells. A new type of positive inotropic agent.
    Circ Res. 1985 Jan;56(1):87-96 PMID: 2578336
  48. A model of cardiac electrical activity incorporating ionic pumps and concentration changes.
    Philos Trans R Soc Lond B Biol Sci. 1985 Jan 10;307(1133):353-98 PMID: 2578676
  49. Na-Ca exchange: stoichiometry and electrogenicity.
    Am J Physiol. 1985 Mar;248(3 Pt 1):C189-202 PMID: 2579566
  50. The slow repolarization phase of the action potential in rat heart.
    J Physiol. 1985 Mar;360:13-25 PMID: 3989712
  51. Transient outward current carried by potassium and sodium in quiescent atrioventricular node cells of rabbits.
    Circ Res. 1985 Jul;57(1):65-73 PMID: 2408781
  52. Use of aequorin for the appraisal of the hypothesis of the release of calcium from the sarcoplasmic reticulum induced by a change of pH in skinned cardiac cells.
    Cell Calcium. 1985 Apr;6(1-2):95-108 PMID: 4040434
  53. A calcium-activated chloride current generates the after-depolarization of rat sensory neurones in culture.
    J Physiol. 1985 Jul;364:217-39 PMID: 2411915
  54. Inactivation of calcium channels in mammalian heart cells: joint dependence on membrane potential and intracellular calcium.
    J Physiol. 1985 Jul;364:395-411 PMID: 2411919
  55. Delayed rectification in the calf cardiac Purkinje fiber. Evidence for multiple state kinetics.
    Biophys J. 1985 Oct;48(4):553-67 PMID: 2413917
  56. Ryanodine: a modifier of sarcoplasmic reticulum calcium release in striated muscle.
    Fed Proc. 1985 Dec;44(15):2984-8 PMID: 2415406
  57. A transient outward current in isolated cells from the crista terminalis of rabbit heart.
    J Physiol. 1985 Nov;368:243-64 PMID: 2416913
  58. Na-Ca exchange current in mammalian heart cells.
    Nature. 1986 Feb 13-19;319(6054):596-7 PMID: 3945347
  59. Identification of Na-Ca exchange current in single cardiac myocytes.
    Nature. 1986 Feb 13-19;319(6054):597-9 PMID: 2418367
  60. Existence of a calcium-dependent potassium channel in the membrane of cow cardiac Purkinje cells.
    Pflugers Arch. 1986 Apr;406(4):424-6 PMID: 2423954
  61. Adrenergic modulation of the delayed rectifier potassium channel in calf cardiac Purkinje fibers.
    Biophys J. 1986 Apr;49(4):839-48 PMID: 2424513
  62. "Creep currents" in single frog atrial cells may be generated by electrogenic Na/Ca exchange.
    J Gen Physiol. 1986 Jun;87(6):857-84 PMID: 3723108
  63. Block of outward current in cardiac Purkinje fibers by injection of quaternary ammonium ions.
    J Gen Physiol. 1982 Jun;79(6):1041-63 PMID: 6286842
Article Info
Journal
The Journal of general physiology
Abbr.
J Gen Physiol
ISSN
0022-1295
Published
1987-06-00
Pages
921-58
Language
English
Region
United States
NLM ID
2985110R
PMCID
PMC2215964
Subset
IM
Grants
NHLBI NIH HHS · HL-17669 · United States
NHLBI NIH HHS · HL-26528 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com