Skip to main content
Log in

Tension activation and relaxation in frog atrial fibres

Evidence for direct effects of divalent cations (Ca2+, Sr2+, Ba2+) on contractile proteins and Na−Ca exchange

  • Excitable Tissues and Central Nervous Physiology
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

The effect of alkali-earth cations (Ca2+, Sr2+, Ba2+) on the excitation-contraction coupling events of the frog atrial fibres were studied using a double mannitol gap voltage clamp technique coupled with a mechano-electric transducer. Photoremoval of the suppressive effect of nifedipine on the calcium channels allowed to obtain rapid transient Ca2+, Sr2+ or Ba2+ ions current jumps. The effect on the amplitude of the associated contraction was proportional to the current jumps. These results together with portional to the current jumps. These results together with the correlation established between the estimated increase in the internal concentration of divalent cations and the amplitude of the phasic tension suggest that the essential source of divalent cations for activation of contraction is the extracellular space. Also Ba2+ ions reduced the tonic tension and strongly slowed the relaxation of the phasic component whereas Sr2+ exhibited smaller effects. Sr2+ ions could be more efficient than Ba2+ ions in substituting for Ca2+ ions in the Na+−Ca2+ exchange mechanism known to regulate these two mechanical events. The conclusions are that the order of effectiveness of these ions (Ca2+>Sr2+>Ba2+) is the same with regard to transarcolemmal exchange for Na+ ions, presumed uptake by a “second relaxing system”, activation of contraction, and inactivation of the slow inward current.

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

  • Beeler GW, McGuigan JAS (1978) Voltage clamping of multicellular myocardial preparations. Capabilities and limitations of existing methods. Prog Biophys Mol Biol 34:219–254

    Google Scholar 

  • Beeler GW, Reuter H (1970) The relation between membrane potential, membrane currents and activation of contraction in ventricular myocardial fibres. J Physiol (Lond) 207:211–229

    Google Scholar 

  • Bonvallet R, Ildefonse M, Roche M, Rougier O (1981) Inotropic effects of potassium rich solutions on frog cardiac muscle. Pflügers Arch 390:237–245

    Google Scholar 

  • Caillé J, Ildefonse M, Rougier O (1978) Existence of a sodium current in the tubular membrane of frog twitch muscle fibre; its possible role in the activation of contraction. Pflügers Arch 374:167–177

    Google Scholar 

  • Chapman RA (1979) Excitation-contraction coupling in cardiac muscle. Prog Biophys Mol Biol 35:1–52

    Google Scholar 

  • Chapman RA (1983) Control of cardiac contractility at the cellular level. Am J Physiol 245:H535-H553

    Google Scholar 

  • Chapman RA, Rodrigo GC (1985) The dependence of the relaxation of tension of frog atrial trabeculae on the sodium-calcium exchange: a voltage-clamp study. Q J Exp Physiol 70:447–460

    Google Scholar 

  • Chapman RA, Tunstall J (1980) The interaction of sodium ions at the cell membrane and the control of contractile strength in frog atrial muscle. J Physiol (Lond) 305:109–123

    Google Scholar 

  • Chapman RA, Tunstall J (1981) The tension-depolarization relationship of frog atrial trabeculae as determinated by potassium contractures. J Physiol (Lond) 310:97–116

    Google Scholar 

  • Dresdner KP, Kline RP (1985) Extracellular calcium ion depletion in frog cardiac ventricular muscle. Biophys J 48:33–45

    Google Scholar 

  • Duval A, Leoty C (1978) Ionic currents in mammalian fast skeletal muscle. J Physiol (Lond) 278:403–423

    Google Scholar 

  • Duvert M, Verna A (1985) Ultrastructural and architecture of the sarcoplasmic reticulum in frog sino-atrial fibres: a comparative study with various preparatory procedures. J Mol Cell Cardiol 17:43–56

    Google Scholar 

  • Ebashi S, Endo M (1968) Calcium ion and muscle contraction. Prog Biophys Mol Biol 18:128–183

    Google Scholar 

  • Einwächter HM, Haas HG, Kern R (1972) Membrane current and contraction in frog atrial fibres. J Physiol (Lond) 227:141–171

    Google Scholar 

  • Eisner DA, Lederer WJ (1985) Na−Ca exchange stoichiometry and electrogenicity. Am J Physiol 248:C189-C202

    Google Scholar 

  • Fabiato A (1983) Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol 245:C1-C14

    Google Scholar 

  • Fabiato A (1985) Effects of ryanodine in, skinned cardiac cells. Fed Proc 44:2970–2976

    Google Scholar 

  • Fabiato A, Baumgarten CM (1984) Methods for detecting calcium release from the sarcoplasmic reticulum of skinned cardiac cells and the relationships between calculated transsarcolemmal calcium movements and calcium release. In: Sperelakis N (ed) Physiology and pathophysiology of the heart, chap 11

  • Fabiato A, Fabiato F (1978) Calcium-induced release of calcium from the sarcoplasmic reticulum of skinned cells from adult human, dog, cat, rabbit, rat and frog hearts and from foetal and new-born rat ventricles. Annu NY Acad Sc 107:491–522

    Google Scholar 

  • Goto M, Kimoto Y, Saito M, Wada Y, (1972) Tension fall after contraction of bull-frog atrial muscle examined with the voltage clamp technique. Jpn J Physiol 22:637–650

    Google Scholar 

  • Gurney AM, Nerbonne JM, Lester HA (1985) Photoinduced removal of nifedipine reveals mechanisms of calcium antagonist action on single heart cells. J Gen Physiol 86:353–380

    Google Scholar 

  • Hilgemann DW, Langer GA (1984) Extracellular calcium transients in frog ventricle measured with antipyrylazo III and tetramethylmurexide. Fed Proc 43:82D

    Google Scholar 

  • Horackova M (1984) Transmembrane calcium transport and the activation of cardiac contraction. Can J Physiol Pharmacol 62:874–883

    Google Scholar 

  • Horackova M, Vassort G (1976) Calcium conductance in relation to contractility in frog myocardium. J Physiol (Lond) 259:597–616

    Google Scholar 

  • Horackova M, Vassort G (1979) Sodium-calcium exchange in regulation of cardiac contractility. Evidence for an electrogenic, voltage-dependent mechanism. J Gen Physiol 73:403–424

    Google Scholar 

  • Hume JR (1985) Do catecholamines directly modulate the delayed plateau potassium current in frog atrium? J Mol Cell Cardiol 17:813–816

    Google Scholar 

  • Hume JR, Giles W (1983) Ionic currents in single frog atrial cells may be generated by electrogenic Na−Ca exchange. J Gen Physiol 87:857–884

    Google Scholar 

  • Katz AM (1970) Contractile proteins of the heart. Physiol Rev 50:63–158

    Google Scholar 

  • Kawata H (1979) Contractility of the frog ventricular myocardium in sodium-free lithium solution. Jpn J Physiol 29:609–625

    Google Scholar 

  • King BW, Bose D (1983) Mechanism of biphasic contractions in strontium-treated ventricular muscle. Circ Res 52:65–75

    Google Scholar 

  • Leoty C, Raymond G (1972) Mechanical activity and ionic currents in frog atrial trabeculae. Pflügers Arch 334:114–128

    Google Scholar 

  • Marban E, Tsien RW (1982) Effects of mystatin-mediated intracellular ion substitution on membrane currents in calf Purkinje fibres. J Physiol (Lond) 329:569–587

    Google Scholar 

  • Marban E, Wier WG (1985) Ryanodine as a tool to determine the contributions of calcium entry and calcium release to the calcium transient and contraction of cardiac Purkinje fibres. Circ Res 56:133–138

    Google Scholar 

  • Mascher D (1973) Electrical and mechanical responses in ventricular muscle fibers during barium perfusion. Pflügers Arch 342:325–346

    Google Scholar 

  • McClellan GB, Winegrad S (1977) Membrane control of cardiac contractility. Nature 268:261–262

    Google Scholar 

  • Mentrard D, Vassort G, Fischmeister R (1984) Changes in external Na induce a membrane current related to the Na−Ca exchange in cesium-loaded frog heart cells. J Gen Physiol 84:201–220

    Google Scholar 

  • Morad D, Goldman YE, Trentham GJ (1983) Rapid photochemical inactivation of Ca2+ entry directly activates contraction in frog heart. Nature 304:635–637

    Google Scholar 

  • Nargeot J, Lester HA, Birdsall NJM, Stockton J, Wassermann NH, Erlanger BF (1982) A photoisomerizable muscarinic antagonist: study of a binding and conductance relaxations in frog heart. J Gen Physiol 79:657–678

    Google Scholar 

  • Nerbonne JM, Richard S, Nargeot J (1985) Calcium channels are “unblocked” within a few milliseconds after photoremoval of nifedipine. J Mol Cell Cardiol 17:511–516

    Google Scholar 

  • Niedergerke R, Page S (1981) 2 physiological agents that appear to facilitate calcium discharge from the sarcoplasmic reticulum in frog heart cells: adrenalin and ATP. Proc Roy Soc (Lond) 213:325–344

    Google Scholar 

  • Niedergerke R, Ogden DC, Page S (1976) Contractile activation and calcïum movements in heart cells. Symp Soc Exp Biol 30:381–395

    Google Scholar 

  • Page SG, Niedergerke R (1972) Structures of physiological interest in the frog heart ventricle. J Cell Sci 11:179–203

    Google Scholar 

  • Penefsky ZJ (1974) Studies on the mechanism of inhibition of cardiac muscle contractile tension by ryanodine. PflÜgers Arch 347:173–184

    Google Scholar 

  • Potreau D (1975) Effects des ions divalents Mg, Ca, Sr, Ba, sur les perméabilités de la membrane cardiaque. Thèse de 3ème cycle Université de Poitiers

  • Potreau D (1982) Slow responses of frog myocardial fibers in sodium-free medium containing divalent cations. J Physiol (Paris) 78:243–250

    Google Scholar 

  • Potreau D, Raymond G (1980) Slow inward barium current and contraction on frog single muscle fibres. J Physiol (Lond) 303:91–109

    Google Scholar 

  • Potreau D, Raymond G (1982) Existence of a sodium-induced calcium release mechanism on frog skeletal muscle fibres. J Physiol (Lond) 333:463–480

    Google Scholar 

  • Potreau D, Raymond G (1985) Barium inhibition of the tonic component of frog contraction. Pflügers Arch 404:287–289

    Google Scholar 

  • Potreau D, Gourdon I, Cognard C, Raymond G (1986) The effects of changes in the trans-sarcolemmal calcium fluxes on the delayed outward current of frog heart. Proc XXX Int Cong Physiol Sci Vancouver 26:443

    Google Scholar 

  • Raymond G, Potreau D (1977) Barium ions and excitation-contraction coupling of frog single muscle fibres under controlled current and voltage. J Physiol (Paris) 73:617–631

    Google Scholar 

  • Reuter H (1973) Divalent cations as charge carriers in excitable membranes. Progr Biophys Mol Biol 26:1–43

    Google Scholar 

  • Richard S, Nerbonne JM, Nargeot J, Lester HA, Garnier D (1985) Photochemically produced intracellular concentration jumps of cAMP mimic the effects of catecholamines on excitation-contraction coupling in frog atrial fibres. Pflügers Arch 403:312–317

    Google Scholar 

  • Ringer S, Sainsbury H (1883) An investigation regarding the action of strontium and barium salts compared with the action of lime on the ventricle of the frog's heart. Practitioner 31:81–93

    Google Scholar 

  • Rougier O, Ildefonse M, Gargouil YM (1966) Application de la technique du double “sucrose-gap” à l'étude électrophysiologique du muscle cardiaque. CR Acad Sci Paris 263:1482–1485

    Google Scholar 

  • Roulet MJ, Mongo KG, Vassort G, Ventura-Clapier R (1979) The dependence of twitch relaxation on sodium ions and on internal Ca2+ stores in voltage clamped frog atrial fibres. Pflügers Arch 379:259–268

    Google Scholar 

  • Saeki Y, Shibata T, Shiozowa K (1981) Excitation-contraction coupling in mammalian cardiac muscle during Ba2+ induced contracture. Am J Physiol 240:H216-H221

    Google Scholar 

  • Saeki Y, Kato C, Horikoshi T, Yanagisawa K (1984) Effects of Ba++ on the mechanical properties of glycerinated heart muscle. Pflügers Arch 400:235–240

    Google Scholar 

  • Sonborn WG, Langer GA (1974) Effects of contractile activation on the movements of strontium and barium in the rabbit ventricule. Fed Proc 33:302

    Google Scholar 

  • Sanguinetti MC, Kass RS (1984) Voltage dependent block of calcium channel current in the calf cardiac Purkinje fiber by dihydropyridine calcium channel antagonists. Circ Res 55:309–325

    Google Scholar 

  • Shepherd N, Kavaler F (1986) Direct control of contraction force of single frog atrial cells by extracellular ions. Am J Physiol 251:C653-C661

    Google Scholar 

  • Solaro RJ, Wise RM, Shiner JS, Briggs FN (1974) Calcium requirements for cardiac myofibrillar activation. Circ Res 34:523–530

    Google Scholar 

  • Trosper TL, Philipson KD (1983) Effects of divalent and trivalent cations on Na+−Ca2+ exchange in cardiac sarcolemmal vesicles. Biochim Biophys Acta 731:63–68

    Google Scholar 

  • Tung L, Morad M (1985) A comparative electrophysiological study of enzymatically isolated single cells and strips of frog ventricle. Pflügers Arch 405:274–284

    Google Scholar 

  • Vanderkooi JM, Martonosi A (1971) Sarcoplasmic reticulum. XIII — Changes in the fluorescence of 8-anilino-1-napthalene sulfonate during Ca2+ transport. Arch Biochem Biophys 144: 99–106

    Google Scholar 

  • Vassort G (1973) Influence of sodium ions on the regulation of frog myocardial contractility. Pflügers Arch 339:225–240

    Google Scholar 

  • Vassort G, Rougier O (1972) Membrane potential and slow inward current dependence of frog cardiac mechanical activity. Pflügers Arch 331:191–203

    Google Scholar 

  • Weiss RE, Morad M (1983) Birefringence signals in mammalian and frog myocardium; E. C. coupling implications J Gen Physiol 82:79–118

    Google Scholar 

  • Winegrad S (1971) Studies of cardiac muscle with a high permeability to calcium produced by treatment with ethylene diaminetertraacetic acid. J Gen Physiol 58:71–93

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Potreau, D., Richard, S., Nargeot, J. et al. Tension activation and relaxation in frog atrial fibres. Pflugers Arch. 410, 326–334 (1987). https://doi.org/10.1007/BF00580284

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00580284

Key words

Navigation