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The effect of extracellular Ca2+ concentration on the negative staircase of Ca2+ transient in field-stimulated rat ventricular cells

  • Original Article
  • Heart, Circulation, Respiration, and Blood; Environmental and Exercise Physiology
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Abstract

We performed experiments using the Ca2+ indicator dye, fura-2 to investigate the effect of extracellular Ca2+ concentration ([Ca2+]o) on sarcoplasmic reticulum (SR) Ca2+ release and loading in single rat ventricular cells. In normal Tyrode solution (1.8 mM [Ca2+]o) repetitive stimulation (0.5 Hz) resulted in a gradual decrease in calcium transients (the negative staircase phenomenon) without being accompanied by a gradual decrease in diastolic intracellular Ca2+ concentration. The rate of the slow decline in calcium transient was faster in lower [Ca2+]o. However, the peak of the first calcium transient was relatively invariant over a wide range of [Ca2+]o (0.5–5 mM). The size of the calcium transient elicited by field stimulation was proportional to that induced by 10 mM caffeine, applied following the field stimulation. These results suggest that the size of calcium transients depends mainly on the Ca2+ content of the SR. The quiescent period favoured the replenishment of the SR and this effect was promoted further by increasing the driving force for Ca2+ entry across the sarcolemma during this period. We conclude that in low [Ca2+]o, short stimulation interval may limit Ca2+ influx across the sarcolemma during the quiescent period to cause a gradual reduction in calcium content of the SR and thus the calcium transient.

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References

  1. Aronson RS, Capasso JM (1980) Negative inotropic effect of elevated extracellular calcium in rat myocardium. J Mol Cell Cardiol 12:1305–1309

    Article  PubMed  CAS  Google Scholar 

  2. Berlin JR, Konishi M (1993) Ca2+ transients in cardiac myocytes measured with high and low affinity Ca2+ indicators. Biophys J: 65, 1632–1647

    PubMed  CAS  Google Scholar 

  3. Blinks JR, Koch-Weser J (1962) Analysis of the effect of changes in rate and rhythm upon myocardial contractility. Pharmacol Rev 134:373–389

    Google Scholar 

  4. Bouchard RA, Bose D (1989) Analysis of the interval-force relationship in rat and canine ventricular myocardium. Am J Physiol 257:H2036-H2047

    PubMed  CAS  Google Scholar 

  5. Capogrossi MC, Stern MD, Spurgeon HA, Lakatta EG (1988) Spontaneous Ca2+ release from the sarcoplasmic reticulum limits Ca2+-dependent twitch potentiation in individual cardiac myocytes. J Gen Physiol 91:133–155

    Article  PubMed  CAS  Google Scholar 

  6. Coulombe A, Lefevre IA, Baro I, Coraboeuf E (1989) Barium- and calcium-permeable channels open at negative membrane potentials in rat ventricular myocytes. J Membr Biol 111:57–67

    Article  PubMed  CAS  Google Scholar 

  7. Dubell WH, Houser SR (1989) Voltage and beat dependence of Ca2+ transient in feline ventricular myocytes. Am J Physiol 257:H746-H759

    PubMed  CAS  Google Scholar 

  8. Endo M (1985) Calcium release from sarcoplasmic reticulum. Curr Top Membr Transp 25:181–230

    CAS  Google Scholar 

  9. Forester GV, Mainwood GW (1974) Interval dependent inotropic effects in the rat myocardium and the effect of calcium. Pflügers Arch 352:189–196

    Article  PubMed  CAS  Google Scholar 

  10. Frampton JE, Orchard CH, Boyett MR (1991) Diastolic, systolic and sarcoplasmic reticulum [Ca2+] during inotropic interventions in isolated rat myocytes. J Physiol (Lond) 437:351–375

    CAS  Google Scholar 

  11. Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440–3450

    PubMed  CAS  Google Scholar 

  12. Haworth RA, Griffin P, Saleh B, Goknur AB, Berkoff HA (1987) Contractile function of isolated young and adult rat heart cells. Am J Physiol 253:H1484–1491

    PubMed  CAS  Google Scholar 

  13. Hilgemann DW (1986) Extracellular calcium transients and action potential configulation changes related to post-stimulatory potentiation in rabbit atrium. J Gen Physiol 87:675–706

    Article  PubMed  CAS  Google Scholar 

  14. Hoffman BF, Kelly JJ (1959) Effects of rate and rhythm on contraction of rat papillary muscle. Am J Physiol 197:1199–1204

    PubMed  CAS  Google Scholar 

  15. Horiuti K, Higuchi H, Umazume Y, Konishi M, Okazaki O, Kurihara S (1988) Mechanism of action of 2,3-butanedione 2-monoxime on contraction of frog skeletal muscle fibres. J Muscle Res Cell Motil 9:156–164

    Article  PubMed  CAS  Google Scholar 

  16. Konishi M, Olson A, Hollingworth S, Baylor SM (1988) Myoplasmic binding of fura-2 investigated by steady-state fluorescence and absorbance measurements. Biophys J 54:1089–1104

    Article  PubMed  CAS  Google Scholar 

  17. Kruta V, Braveny P (1960) Potentiation of contractility in the heart muscle of the rat and some other mammals. Nature 187:327–328

    Article  PubMed  CAS  Google Scholar 

  18. Lefevre T, Coulombe A, Coraboeuf E (1994) Tonically active (background) calcium channels unmasked by phenothiazines in rat ventricular myocytes (abstract). Biophys J 66:32/a

    Google Scholar 

  19. Li T, Sperelakis N, Teneick RE, Solaro RJ (1985) Effects of diacetylmonoxime on cardiac excitation-contraction coupling. J Pharmacol Exp Ther 232:688–695

    PubMed  CAS  Google Scholar 

  20. Li Q, Altschuld RA, Stokes BT (1987) Quantitation of intracellular free calcium in single adult cardiomyocytes by fura-2 fluorescence microscopy: calibration of fura-2 ratios. Biochem Biophys Res Commun 147:120–126

    Article  PubMed  CAS  Google Scholar 

  21. McDowall RJS, Munro AF, Zayat AF (1955) Sodium and cardiac muscle. J Physiol (Lond) 130:615–624

    CAS  Google Scholar 

  22. Mitchell MR, Powell T, Terrar DA, Twist VW (1984) Strontium, nifedipine and 4-aminopyridine modify the time course of the action potential in cells from rat ventricular muscle. Br J Pharmacol 81:551–556

    PubMed  CAS  Google Scholar 

  23. Neher E (1989) Combined fura-2 and patch clamp measurement in rat peritoneal mast cells. In: Sellin LC, Libelius R, Thesleff S (eds) Neuromuscular junction. Elsevier, Amsterdam, pp 65–76

    Google Scholar 

  24. O'Neill SC, Donoso P, Eisner DA (1990) The role of [Ca2+]i and [Ca2+] sensitization in the caffeine contracture of rat myocytes: measurement of [Ca2+]i and [Caffeine]i. J. Physiol (Lond) 425:55–70

    Google Scholar 

  25. Reuter H (1974) Localization of beta adrenergic receptors, and effects of noradrenaline and cyclic nucleotides on action potentials, ionic currents and tension in mammalian cardiac muscle. J Physiol (Lond) 242:429–451

    CAS  Google Scholar 

  26. Schouten VJA (1990) Interval dependence of force and twitch duration in rat heart explained be Ca2+ pump inactivation in sarcoplasmic reticulum. J Physiol (Lond) 431:427–444

    CAS  Google Scholar 

  27. Shattock MJ, Bers DM (1989) Rat vs. rabbit ventricle: Ca flux and intracellular Na assessed by ion-selective microelectrodes. Am J Physiol 256:C813-C822

    PubMed  CAS  Google Scholar 

  28. Smith GL, Valdeolmillos M, Eisner DA, Allen DG (1988) Effects of rapid application of caffeine on intracellular calcium concentration in ferret papillary muscles. J Gen Physiol 92:351–368

    Article  PubMed  CAS  Google Scholar 

  29. Spurgeon HA, Isenberg G, Talo A, Stern MD, Capogrossi MC, Lakatta EG (1988) Negative staircase in cytosolic Ca2+ in rat myocytes is modulated by depolarization duration (abstract). Biophys J 53:601a

    Google Scholar 

  30. Spurgeon HA, Stern MD, Baartz G, Raffaeli S, Hansford RG, Talo A, Lakatta EG, Capogrossi MC (1990) Simultaneous measurement of Ca2+, contraction, and potential in cardiac myocytes. Am J Physiol 258:H574-H586

    PubMed  CAS  Google Scholar 

  31. Tada M, Katz AM (1982) Phosphorylation of the sarcoplasmic reticulum and sarcolemma. Annu Rev Physiol 44:401–423

    Article  PubMed  CAS  Google Scholar 

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Author notes

  1. Norio Suda

    Present address: Max-Planck-Institut for Biophysical Chemistry, D-37077, Göttingen, Germany

Authors and Affiliations

  1. Department of Physiology, Jikei University School of Medicine, 3-25-8 Nishi-shinbashi, Minato-ku, 105, Tokyo, Japan

    Norio Suda

  2. Department of Physiology, Nihon University School of Medicine, 30-1 Oyaguchi kamimachi Itabashi-ku, 173, Tokyo, Japan

    Shinichiro Kokubun

Authors
  1. Norio Suda
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  2. Shinichiro Kokubun
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Suda, N., Kokubun, S. The effect of extracellular Ca2+ concentration on the negative staircase of Ca2+ transient in field-stimulated rat ventricular cells. Pflugers Arch. 429, 7–13 (1994). https://doi.org/10.1007/BF02584024

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  • DOI: https://doi.org/10.1007/BF02584024

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