Skip to main content
SpringerLink
Log in

Influence of ryanodine on the mechanical restitution and on the post-extrasystolic potentiation of the guinea-pig ventricular myocardium

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

This paper records the results of an investigation into potentiation and staircase phenomena in rightventricular guinea-pig papillary muscles with particular reference to the sarcoplasmic Ca2+-channel. As a tool to isolate the second (‘late’, ‘1tonic’) component of isoproterenol-induced biphasic contractions ryanodine was used. On the evidence at present available the monophasic ryanodine-resistant component of the twitch represents that portion of the activator calcium which reaches the troponin C directly, that is, not taking the roundabout way through the intracellular storage structures. In order to avoid functional instabilities of the isolated muscle preparation a short-time double rest stimulation programme was used which combines a number of different tests and gives information on (1) the post-rest potentiation, (2) the post-extrasystolic potentiation, (3) the mechanical post-rest recovery, (4) the interval-strength relationship, and (5) the mechanical restitution. The results of the present work show that under the influence of ryanodine (1) the BOWDITCH staircase, a typical feature of normodynamic mammalian ventricular preparations as well as of hypodynamic frog heart preparations, does not exist, (2) the post-extrasystolic potentiation disappears, (3) the curve reflecting the mechanical restitution, under normal in vitro conditions a monotonically increasing function, becomes biphasic within the relative refractory period, (4) the conspicuous depression of the isometric post-rest contraction for long iasting pauses interrupting the regular pacing rhythm, a typical feature of isolated guinea-pig ventricular tissue, is clearly diminished, and (5) the characteristic curve, reflecting the potentiation of the post-extrasystolic post-rest contraction as a function of the delay time preceding the extrastimulus, becomes displaced to the premature interstimulus interval. The concept of an ‘extended 2-calcium-store model’ is supported by this work.

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

Similar content being viewed by others

References

  1. Rosin H, Farah A: Post-stimulation potentiation of contractility in the isolated auricle of the rabbit. Am J Physiol 180: 75–82, 1955

    Google Scholar 

  2. Kruta V, Bravený P: Possible mechanisms involved in potentiation phenomena. In: PF Cranefield, BF Hoffman (eds). Paired Pulse Stimulation of the Heart. Ann Rockefeller University Press, New York, 1968

    Google Scholar 

  3. Wussling M, Szymanski G: Ein Zwei-Ca-Speicher-Modell zur qualitativen Beschreibung von Potentiationserscheinungen am Kaninchenpapillarmuskel. Nova Acta Leopoldina (NF) 211: 141–173, 1973

    Google Scholar 

  4. Wohlfart B: Interval-strength relations of mammalian myocardium interpreted as altered kinetics of activator calcium during the cardiac cycle. Thesis, Univ of Lund, 1982

  5. Szymanski G: Critical remarks concerning potentiation phenomena in Rana esculenta. Zool Jb Physiol 89: 17–42, 1985

    Google Scholar 

  6. Hoffman B, Bindler E, Suckling E: Postextrasystolic potentiation of contraction in cardiac muscle. Am J Physiol 185: 95–102, 1956

    Google Scholar 

  7. Meijler F, van der Bogaard F, van den Tweel H, Durrer D: Post extrasystolic potentiation in the isolated rat heart. Am J Physiol 202: 631–635, 1962

    Google Scholar 

  8. Szymanski G, Wussling M: Physiological experiments and model studies of the postextrasystolic potentiation phenomenon. Zool Jb Physiol 82: 515–529, 1978

    Google Scholar 

  9. Szymanski G, Wussling M: The effect of metabolic inhibitors on staircase, postextrasystolic potentiation phenomenon and restitution of contractility in the mammalian myocardium. Zool Jb Physiol 85: 351–361, 1981

    Google Scholar 

  10. Szymanski G, Wussling M: Measurement of postextrasystolic potentiation and mechanical restitution during and after calcium removal in the mammalian myocardium. Zool Jb Physiol 88: 91–111, 1984

    Google Scholar 

  11. Yue DT, Burkhoff D, Franz MR, Hunter WC, Sagawa K: Postextrasystolic potentiation of the isolated canine left ventricle. Circ Res 56: 340–350, 1985

    Google Scholar 

  12. Cooper M, Lutherer L, Stanton M, Lust R: Postextrasystolic potentiation: analysis of methods of induction. Am Heart J 111: 330–333, 1986

    Google Scholar 

  13. Kuijer P, van der Werft T, Meijler F: Post-extrasystolic potentiation without a compensatory pause in normal and deseased hearts. Br Heart J 63: 284–286, 1990

    Google Scholar 

  14. Sung CS, Mathur V, Garcia E, Castro C, Hall R: Is postextrasystolic potentiation dependent on Starlings law ? Circulation 62: 1032–1035, 1980

    Google Scholar 

  15. Fišer B: Interval-strength relationship in normal perfused and ischaemic rabbit heart. Proc of the XXVIII. IUPS Congress: Abstr 1415, 1980

  16. Opitz H: Die Dynamik rhythmusabhängiger Potentiation am Meerschweinchenherzen. Acta Biol Med Germ 39: 561–569, 1980

    Google Scholar 

  17. Koester G: Anwendung des n-Speicher-m-Phasenmodells auf intrazelluläre Ca-Flüsse im Herzmuskel. Chapt 8 in: Habilschr MartinLuther-Universität Halle-Wittenberg, 1979

    Google Scholar 

  18. Wood EH, Hepner RL, Weidmann S: Inotropic effects of electric currents. Circ Res 24: 409–445, 1969

    Google Scholar 

  19. Bass BG: Restitution of the action potential in cat papillary muscle. Am J Physiol 228: 1717–1724, 1975

    Google Scholar 

  20. Anderson TW, Johnson EA: The repolarisation phase of the cardiac action potential: a comparative study of rate-induced changes in its wave form. J Mol Cell Cardiol 8: 103–121, 1976

    Google Scholar 

  21. Hajdu S, Leonard E: Action of ryanodine on mammalian cardiac muscle. Effects on contractility, and reversal of digitalis-induced ventricular arrhythmias. Circ Res 9: 1283–1291, 1961

    Google Scholar 

  22. Jenden DJ, Fairhurst AS: The pharmacology of ryanodine. Pharmacol Rev 21: 1–25, 1969

    Google Scholar 

  23. Sutko JL, Willerson JT: Ryanodine alteration of the contractile state of rat ventricular myocardium. Comparison with dog, cat and rabbit ventricular tissues. Circ Res 46: 332–343, 1980

    Google Scholar 

  24. Fabiato A: Effects of ryanodine in skinned cardiac cells. Federation Proc 44: 2970–2976, 1985

    Google Scholar 

  25. Meissner G: Ryanodine activation and inhibition of the Ca2+ release channel of sarcoplasmic reticulum. J Biol Chem 261: 6300–6306, 1986

    Google Scholar 

  26. Rousseau E, Smith JS, Henderson JS, Meissner G: Single channel and 45Ca2+ flux measurements of the cardiac sarcoplasmic reticulum calcium channel. Biophys J 50: 1009–1014, 1986

    Google Scholar 

  27. Sutko JL, Thompson LJ, Kort AA, Lakatta EG: Comparison of effects of ryanodine and caffeine on rat ventricular myocardium. Am J Physiol 250: H786–H795, 1986

    Google Scholar 

  28. Wier WG, Yue DT: Intracellular calcium transients underlying the short-term force-interval relationship in ferret ventricular myocardium. J Physiol 376: 507–530, 1986

    Google Scholar 

  29. Alderson BH, Feher JJ: The interaction of calcium and ryanodine with cardiac sarcoplasmic reticulum. Biochim Biophys Acta 900: 221–229, 1987

    Google Scholar 

  30. Hansford RG, Lakatta EG: Ryanodine releases calcium from sarcoplasmic reticulum in calcium-tolerant rat cardiac myocytes. J Physiol 390: 453–467, 1987

    Google Scholar 

  31. Malécot CO, Katzung BG: Use-dependence of ryanodine effects on postrest contraction in ferret cardiac muscle. Circ Res 60: 560–567, 1987

    Google Scholar 

  32. Rasmussen CAF, Sutko JL, Barry WH: Effects of ryanodine and caffeine on contractility, membrane voltage, and calcium exchange in cultured heart cells. Circ Res 60: 495–504, 1987

    Google Scholar 

  33. Rousseau E, Smith JS, Meissner G: Ryanodine modifies conductance and gating behaviour of single Ca2+ release channel. Am J Physiol 253: C364–C368, 1987

    Google Scholar 

  34. Callewaert G: Excitation-contraction coupling in mammalian cardiac cells. Cardiovas Res 26: 923–932, 1992

    Google Scholar 

  35. Stern MD, Lakatta EG: Excitation-contraction coupling in the heart: the state of the question. FASEB J 6: 3092–3100, 1992

    Google Scholar 

  36. Kohmoto O, Levi AJ, Bridge JHB: Relation between reverse sodiumcalcium exchange and sarcoplasmic reticulum calcium release in guinea-pig ventricular cells. Circ Res 74: 550–554, 1994

    Google Scholar 

  37. Ogawa Y: Role of ryanodine receptors. Crit Rev Biochem Molec Biol 29(4): 229–274, 1994

    Google Scholar 

  38. de Hemptinne A, Weyne J, Leussen l: Dynamic parameters of myocardial contractility under influence of calcium and strontium. Arch Int Physiol Biochim 75: 96–108, 1967

    Google Scholar 

  39. Bravený P, Šumbera J: Biphasic activation of the myocardial contraction. Physiol Bohemoslov 21: 73–74, 1972

    Google Scholar 

  40. Allen DG, Jewell BR, Wood EH: The rested state contraction and action potential of cat papillary muscle. J Physiol 238: 29P–30P, 1974

    Google Scholar 

  41. Coraboeuf E: Membrane electrical activity and double component contraction in cardiac tissue. J Mol Cell Cardiol 6: 215–225, 1974

    Google Scholar 

  42. Seibel K, Karema E, Takeja K, Reiter M: Effect of noradrenaline on an early and a late component of the myocardial contraction. Naunyn Schmiedebergs Arch Pharmacol 305: 65–74, 1978

    Google Scholar 

  43. Bogdanow KY, Zakharow SI, Rosenstraukh LV: The origin of two components in contraction of guinea-pig papillary muscle in the presence of noradrenaline. Can J Physiol Pharmacol 57: 866–871, 1979

    Google Scholar 

  44. Reiter M, Vierling W, Seibel K: Excitation-contraction coupling in rested-state contractions of guinea-pig ventricular myocardium. Naunyn Schmiedebergs Arch pharmacol 325: 159–169, 1984

    Google Scholar 

  45. Honore E, Challice CE, Guilbault P, Dupuis B: Two components of contraction in guinea-pig papillary muscle. Can J Physiol Pharmacol 64: 1153–1159, 1986

    Google Scholar 

  46. Malécot CO, Bers DM, Katzung BG: Biphasic contractions induced by milrinone at low temperature in ferret ventricular muscle: Role of the sarcoplasmic reticulum and transmembrane Ca influx. Circ Res 59: 151–162, 1986

    Google Scholar 

  47. Schüttler K, Szymanski G: Three phasic contractions in mammalian myocardium. Isolation and identification of a late component. Implications for rested state contractions. Biomed Biochim Acta 48: 558–564, 1989

    Google Scholar 

  48. Szymanski G, Zett L: Factors influencing the shape and the potentiation behaviour of monophasic, biphasic and multiphasic contractions of the guinea-pig ventricular myocardium. Zool Jb Physiol 95: 109–133, 1991

    Google Scholar 

  49. Wussling M, Szymanski G, Schrör K: The influence of hypertrophy and hypoxia on potentiation phenomena of the rabbit papillary muscle tested by a double rest programme. Arch Int Pharmacodyn Ther 212: 238–246, 1974

    Google Scholar 

  50. Wussling M, Szymanski G: Simulation by two calcium store models of myocardial properties: Potentiation, staircase and biphasic tension development. Gen Physiol Biophys 5: 135–152, 1986

    Google Scholar 

  51. Antoni H, Jacob R, Kaufmann R: Mechanische Reaktionen des Froschund Säugetiermyokards bei Veränderung der Aktionspotential-Dauer durch konstante Gleichstromimpulse. Pflügers Arch 306: 33–57, 1969

    Google Scholar 

  52. Anderson TW, Hirsch C, Kavaler F: Mechanism of activation of contraction in frog ventricular muscle. Circ Res 41: 472–480, 1977

    Google Scholar 

  53. Bowditch HP: Ñber die Eigenthümlichkeiten der Reizbarkeit, welche die Muskelfasern des Herzens zeigen. Berichte über die Verhandlungen der königlich sächsischen Gesellschaft der Wissenschaften zu Leipzig. Mathematisch-Physikalische Classe 23: 652–689, 1871

    Google Scholar 

  54. Szymanski G, Zett L: Evidence for two kinds of hypodynamia in isolated myocardial tissue of Rana esculenta. Zool Jb Physiol 90: 219–229, 1986

    Google Scholar 

  55. Cooper MW: Postextrasystolic potentiation. Do we really know what it means and how to use it? Circulation 88: 2962–2971, 1993

    Google Scholar 

  56. Adler D, Wong AYK, Mahler Y, Klassen GA: Model of calcium movement in the mammalian myocardium:interval-strength relationship. J Theor Biol 113: 379–394, 1985

    Google Scholar 

  57. Shouten VJA, van Deen JK, de Tombe P, Verdeen AA: Force-intervalrelationship in heart muscle of mammals. A calcium compartment model. Biophys J 51: 13–26, 1987

    Google Scholar 

  58. Stern MD: Theory of excitation contraction coupling in cardiac muscle. Biophys J 63: 495–517, 1990

    Google Scholar 

  59. Oblonczek G: Untersuchung von Potentiations-und Treppenphänomenen am rechtsventrikulären Meerschweinchen-Papillarmuskel unter Einwirkung von Ryanodin. Thesis Martin Luther-Universität Halle-Wittenberg Mathem Naturwiss Techn Fak, 1996

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Julius-Bernstein-Institut für Physiologie, Martin-Luther-Universität Halle-Wittenberg, 06097, Halle/Saale, Germany

    Grit Oblonczek & Gerhard Szymanski

Authors
  1. Grit Oblonczek
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gerhard Szymanski
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oblonczek, G., Szymanski, G. Influence of ryanodine on the mechanical restitution and on the post-extrasystolic potentiation of the guinea-pig ventricular myocardium. Mol Cell Biochem 175, 213–223 (1997). https://doi.org/10.1023/A:1006875617870

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006875617870

Search

Navigation