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Pflügers Archiv

, Volume 429, Issue 6, pp 797–804 | Cite as

Intracellular citrate induces regenerative calcium release from sarcoplasmic reticulum in guinea-pig atrial myocytes

  • G. Callewaert
  • K. R. Sipido
  • E. Carmeliet
  • L. Pott
  • P. Lipp
Original Article Heart, Circulation, Respiration and Blood; Environmental and Exercise Physiology

Abstract

Ca2+ release from the sarcoplasmic reticulum was studied in voltage-clamped guinea-pig atrial myocytes. Cells were dialysed with a pipette solution containing the Ca2+ indicator 1- [2-amino-5-(6-carboxyindol-2-yl) phenoxy]-2-(2′-amino-5′-methylphenoxy) ethane-N,N,N′,N′-tetraacetic acid](Indo-1, 100 μM) and as main anion either chloride or the low-affinity Ca2+ buffer citrate. Intracellular Ca2+ transients (Cai transients) were elicited by depolarizations from a holding potential of −50 mV. In chloride-dialysed cells, Cai transients showed a bell-shaped dependence on the amplitude of the depolarizing pulse. In citratedialysed cells, membrane depolarizations were associated with a small rise in [Ca2+]i. These small changes in [Ca2+]i were either followed by a large Cai. transient or failed to induce large changes in [Ca2+]i. The peak amplitude of the large Cai transient did not vary with the amplitude of the depolarizing pulse. These results demonstrate that in the presence of intracellular chloride, Ca2+ release in atrial cells is a graded process triggered by Ca2+ influx. Using citrate as the main intracellular anoin, Ca2+ release triggered by Ca2+ entry was no longer graded but occurred in a regenerative manner. The results are discussed in terms of two models in which citrate, affects the spatial distribution of [Ca2+]i or the loading state of the sarcoplasmic reticulum.

Key words

Ca2+ release Sarcoplasmic reticulum Atrial myocyte Heart Citrate 

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References

  1. 1.
    Allbritton NL, Meyer T, Stryer L (1992) Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258:1812–1815Google Scholar
  2. 2.
    Ashley RH, Williams AJ (1990) Divalent cation activation and inhibition of single calcium release channels from sheep cardiac sarcoplasmic reticulum. J Gen Physiol 95:981–1005Google Scholar
  3. 3.
    Bechem M, Pott L (1985) Removal of Ca2+ current inactivation in dialysed guinea-pig atrial cardioballs by Ca2+ chelators. Pflügers Arch 440:10–20Google Scholar
  4. 4.
    Bechem M, Pott L, Rennebaum H (1983) Atrial muscle cells from hearts of adult guinea-pigs in culture: a new preparation for cardiac cellular electrophysiology. Eur J Cell Biol 31:366–369Google Scholar
  5. 5.
    Benham CD (1989) Voltage-gated and agonist-mediated rises in intracellular Ca2+ in rat clonal pituitary cells (GH3) held under voltage clamp. J Physiol (Lond) 415:143–158Google Scholar
  6. 6.
    Bers DM, Hryshko LV, Harrison SM, Dawson DD (1991) Citrate decreases contraction and Ca2+ current in cardiac muscle independent of its buffering action. Am J Physiol 260:C900-C909Google Scholar
  7. 7.
    Beuckelmann DJ, Wier WG (1988) Mechanism of release of calcium from sarcoplasmic reticulum of guinea-pig cardiac cells. J Physiol (Lond) 405:233–255Google Scholar
  8. 8.
    Bielen FV, Glitsch HG, Verdonck F (1991) Changes of the subsarcolemmal Na+ concentration in internally perfused cardiac cells. Biochem Biophys Acta 1065:269–271Google Scholar
  9. 9.
    Callewaert G (1992) Excitation-contraction coupling in mammalian cardiac cells. Cardiovasc Res 26:923–932Google Scholar
  10. 10.
    Callewaert G, Lipp P, Pott L, Carmeliet E (1991) High-resolution measurement and calibration of Ca2+-transients using Indo-1 in guinea-pig atrial myocytes under voltage clamp. Cell Calcium 12:269–277Google Scholar
  11. 11.
    Callewaert G, Lipp P. Sipido KR, Pott L, Carmeliet E (1991) Regenerative Ca2+ release in guinea-pig atrial myocytes (abstract) J Physiol (Lond) 446:146PGoogle Scholar
  12. 12.
    Earm YE, Noble D (1990) A model of the single atrial cell:relation between calcium current and calcium release. Proc R Soc Lond [Biol] 240:83–96Google Scholar
  13. 13.
    Earm YE, Ho WK, So IS (1990) Inward current generated by Na+-Ca2+ exchange during the action potential in single atrial cells of the rabbit. Proc R Soc Lond B 240:61–81Google Scholar
  14. 14.
    Fabiato A (1983) Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol 245:C1-C14Google Scholar
  15. 15.
    Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440–3450Google Scholar
  16. 16.
    Györke S, Fill M (1993) Ryanodine receptor adaptation:control mechanism of Ca2+-induced Ca2+ release in heart. Science 260:807–809Google Scholar
  17. 17.
    Hasselbach W (1964) Relaxing factor and the relaxation of muscle. Prog Biophys Mol Biol 14:167–222Google Scholar
  18. 18.
    Leblanc N, Hume JR (1990) Sodium current-induced release of calcium from cardiac sarcoplasmic reticulum. Science 248:372–376Google Scholar
  19. 19.
    Lipp P, Niggli E (1994) Sodium current-induced calcium signals in isolated guinea-pig ventricular myocytes. J Physiol (Lond) 474:439–446Google Scholar
  20. 20.
    Lipp P, Pott L (1988) Transient inward current in guinea-pig atrial myocytes reflects a change of sodium-calcium exchange current. J Physiol (Lond) 397:601–630Google Scholar
  21. 21.
    Lipp P, Pott L (1990) Inward currents caused by Ca2+-release from the sarcoplasmic reticulum of cardiac myocytes are influenced by the Ca2+-chelating properties of the internal solution (abstract) J Physiol (Lond) 429:118PGoogle Scholar
  22. 22.
    Lipp P, Pott L, Callewaert G, Carmeliet E (1990) Simultaneous recording of Indo-1 fluorescence and Na+/Ca2+ exchange current reveals two components of Ca2+-release from sarcoplasmic reticulum of cardiac atrial myocytes. FEBS Lett 271:181–184Google Scholar
  23. 23.
    Lipp P, Pott L, Callewaert G, Carmeliet E (1992) Calcium transients caused by calcium entry are influenced by the sarcoplasmic reticulum in guinea-pig atrial myocytes. J Physiol (Lond) 454:321–338Google Scholar
  24. 24.
    Meissner G, Rousseau E, Lai FA, Liu QY, Anderson KA (1988) Biochemical characterization of the Ca2+ release channel of skeletal and cardiac sarcoplasmic reticulum. Mol Cell Biochem 82:59–65Google Scholar
  25. 25.
    Näbauer M, Morad M (1990) Ca2+-induced Ca2+ release as examined by photolysis of caged Ca2+ in single ventricular myocytes. Am J Physiol 258:C189-C193Google Scholar
  26. 26.
    Niggli E, Lipp P (1993) Subcellular restricted spaces:significance for cell signaling and excitation-contraction coupling. J Muscle Res Cell Motil 14:288–291Google Scholar
  27. 27.
    Petersen CCH, Toescu EC, Petersen OH (1991) Different patterns of receptor-activated cytoplasmic Ca2+ oscillations in single pancreatic acinar cells dependence on receptor type, agonist concentration and intracellular Ca2+ buffering. EMBO J 10:527–533Google Scholar
  28. 28.
    Pott L, Mechmann S (1990) Large-conductance ion channel measured by whole-cell voltage clamp in single cardiac cells:modulation by β-adrenergic stimulation and inhibition by ocranol. J Membr Biol 117:189–199Google Scholar
  29. 29.
    Robbins J, Cloues R, Brown DA (1992) Intracellular Mg2+ inhibits the IP3-activated IK(ca) in NG108-15 cells. [Why intracellular citrate can be useful for recording IK(ca)]. Pflügers Arch 420:347–353Google Scholar
  30. 30.
    Stern MD (1992) Theory of excitation-contraction coupling in cardiac muscle. Biophys J 63:497–517Google Scholar
  31. 31.
    Stern MD, Capogrossi MC, Lakatta EG (1988) Spontaneous calcium release from the sarcoplasmic reticulum in myocardial cells:mechanisms and consequences. Cell Calcium 9:247–256Google Scholar
  32. 32.
    Zhou Z, Lipsius SL (1993) Na+-Ca2+ exchange current in latent pacemaker cells isolated from cat right atrium. J Physiol (Lond) 466:263–285Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • G. Callewaert
    • 1
  • K. R. Sipido
    • 1
  • E. Carmeliet
    • 1
  • L. Pott
    • 2
  • P. Lipp
    • 3
  1. 1.Laboratory of PhysiologyUniversity of LeuvenLeuvenBelgium
  2. 2.Institute of PhysiologyRuhr UniversityBochumGermany
  3. 3.Department of PhysiologyUniversity of BerneBerneSwitzerland

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