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Effect of ryanodine on atrial natriuretic peptide secretion by contracting and quiescent rat atrium

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Abstract

To elucidate the mechanism involved in the release of atrial natriuretic peptide (ANP), we studied the importance of ryanodine-sensitive Ca2+ release in stretch-secretion coupling. The experiments were made with a left atrial preparation, where the stretch of myocytes was induced by changing the intra-atrial pressure. When external pacing was not applied, the atrial preparation was not spontaneously contracting, and it was therefore possible to investigate the secretory mechanism in the quiescent atrium. The superfusate was collected in 2-min fractions and assayed for ANP immunoreactivity. Filtration analysis revealed that the major fraction in the superfusate in all experimental situations had a similar molecular weight as the ANP 1–28. Ryanodine (1.0 μM and 0.1 μM) inhibited stretch-stimulated ANP secretion dose dependently both in paced and nonpaced atrium, but did not have any effect on basal secretion. The present results support the notion that intracellular Ca2+ transients from the intracellular stores are essential for stretch-stimulated ANP secretion, independently from excitation and contraction. Basal ANP secretion is not inhibited by blocking ryanodine-sensitive Ca2+ channels, either in contracting or in non-contracting atria. In addition our results confirm that the principal stimulus for ANP secretion in response to atrial distension is the stretch of myocytes. Length shortening of myocytes is not essential for ANP release.

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References

  1. Allen DG, Kurihara S (1982) The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol (Lond) 327:79–94

    Google Scholar 

  2. Anderson K, Lai FA, Liu Q, Rousseau E, Ericson HP, Meissner G (1989) Structural and functional characterisation of the purified cardiac ryanodine receptor-Ca2+ release channel complex. J Biol Chem 264:1329–1335

    Google Scholar 

  3. Balden E, Walker AM, Cukierman S (1991) Reconstitution of single calcium channels from secretory granules of rat adenohypophysis in planar lipid membranes. Mol Cell Endocrinol 77:85–90

    Google Scholar 

  4. Bold ML de, Bold AJ de (1989) Effect of manipulations of Ca2+ environment on atrial natriuretic factor release. Am J Physiol 256:H1588-H1594

    Google Scholar 

  5. Bold AJ de, Bold ML de, Sarda IR (1986) Functional-morphological studies on in vitro cardionatrin release. J Hypertens [Suppl] 4:S3-S7

    Google Scholar 

  6. Bristow MR, Port JD (1990) Receptor pharmacology of the human heart. In: Garfein OB (ed) Current concepts in cardiovascular physiology. Academic Press, London, pp 74–117

    Google Scholar 

  7. Cho KW, Seul KH, Kim SH, Koh GY, Seul KM, Hwang YH (1990) Sequential mechanism of atrial natriuretic peptide secretion in isolated perfused rabbit atria. Biochem Biophys Res Commun 172:423–431

    Google Scholar 

  8. Cho KW, Seul KH, Kim SH, Seul KM, Koh GY (1991) Atrial pressure, distension, and pacing frequency in ANP secretion in isolated perfused rabbit atria. Am J Physiol 260:R39-R46

    Google Scholar 

  9. Dietz JR, Nazian SJ, Vesely DL (1991) Release of ANF, proANF 1–98, and proANF 31–67 from isolated rat atria by atrial distension. Am J Physiol 260:H1774-H1778

    Google Scholar 

  10. Edwards BS, Zimmerman RS, Schawab TR, Heublein DM, Burnett JC (1988) Atrial stretch, not pressure, is the principal determinant controlling the acute release of atrial natriuretic factor. Circ Res 62:191–195

    Google Scholar 

  11. Fabiato A (1985) Rapid ionic modifications during the aequorin-detected calcium transient in a skinned canine cardiac purkinje cell. J Gen Physiol 85:189–246

    Google Scholar 

  12. Feher JJ, Lipford GB (1985) Mechanism of action of ryanodine on cardiac sarcoplasmic reticulum. Biochim Biophys Acta 813:77–86

    Google Scholar 

  13. Fleischer S, Ogunbunmi EM, Diwon MC, Fleer EA (1985) Localization of Ca2+ release channels with ryanodine in junctional terminal cisternae of sarcoplasmic reticulum of fast skeletal muscle. Proc Natl Acad Sci USA 82:7256–7259

    Google Scholar 

  14. Haas M, Fischer TA, Diez R (1987) Is atrial distension the physiological stimulus for release of atrial natriuretic peptide? Lancet II:1269–1270

    Google Scholar 

  15. Iida H, Page E (1989) Determinants of atrial natriuretic peptide secretion in cultured atrial myocytes. Am J Physiol 256:C608–C613

    Google Scholar 

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

    Google Scholar 

  17. Katoh S, Toyama J, Aoyama M, Miyamoto N, Seo H, Matsui N, Kodama I, Yamada K (1990) Mechanisms of atrial natriuretic peptide (ANP) secretion by rat hearts perfused in vitro: Ca2+ dependent signal transduction for ANP release by mechanical stretch. Jpn Circ J 54:1283–1294

    Google Scholar 

  18. Kuroski-de Bold ML, Bold AJ de (1991) Stretch-secretion coupling in atrial cardiocytes. Dissociation between atrial natriuretic factor release and mechanical activity. Hypertension 18:[Suppl III] 169–178

    Google Scholar 

  19. Lang RE, Thölken H, Ganten D, Luft FC, Ruskoaho H, Unger T (1985) Atrial natriuretic factor — a circulating hormone stimulated by volume loading. Nature 314:264–266

    Google Scholar 

  20. Ledsome JR, Wilson N, Courneya CA, Rankin AJ (1985) Release of atrial natriuretic peptide by atrial distension. Can J Physiol Pharmacol 63:739–742

    Google Scholar 

  21. 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 fibers. Circ Res 56:133–138

    Google Scholar 

  22. Page E, Goings GE, Power B, Upshaw-Earley J (1990) Basal and stretch-augmented natriuretic peptide secretion by quiescent rat atria. Am J Physiol 259:C801–C818

    Google Scholar 

  23. Page E, Upshaw-Earley J, Goings GE, Hanck DA (1991) Inhibition of atrial peptide secretion at different stages of the secretory process: Ca2+ dependence. Am J Physiol 261:C1162–C1172

    Google Scholar 

  24. Page E, Upshaw-Earley J, Goings GE, Hanck DA (1991) Effect of external Ca2+ concentration on stretch-augmented natriuretic peptide secretion by rat atria. Am J Physiol 260:C756–C762

    Google Scholar 

  25. Penner T, Neher E (1988) The role of calcium in stimulussecretion coupling in excitable and non-excitable cells. J Exp Biol 139:329–345

    Google Scholar 

  26. Rankin AJ, Courneya CA, Wilson N, Ledsome JR (1987) Tachycardia releases atrial natriuretic peptide in the anesthetized rabbit. Life Sci 38:1951–1957

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  29. Ruskoaho H (1992) Atrial natriuretic peptide: synthesis, release, and metabolism. Pharmacol Rev 44:479–602

    Google Scholar 

  30. Ruskoaho H, Toth M, Lang RE (1985) Atrial natriuretic peptide secretion: synergistic effect of phorbolester and A23187. Biochem Biophys Res Commun 133:581–588

    Google Scholar 

  31. Ruskoaho H, Thölken H, Lang RE (1986) Increase in atrial pressure releases atrial natriuretic peptide from isolated perfused rat hearts. Pflügers Arch 407:170–174

    Google Scholar 

  32. Schiebinger RJ (1989) Calcium — its role in isoprotenol-stimulated atrial natriuretic peptide secretion by superfused rat atria. Circ Res 65:600–606

    Google Scholar 

  33. Schiebinger RJ, Linden J (1986) Effect of atrial contraction frequency on atrial natriuretic peptide secretion. Am J Physiol 251:H1095-H1099

    Google Scholar 

  34. Schiebinger RJ, Parr HG, Cragoe EJ (1992) Calcium: Its role in α 1-adrenergic stimulation of atrial natriuretic peptide secretion. Endocrinology 130:1017–1023

    Google Scholar 

  35. Smith JS, Imagawa T, Ma J, Fill M, Campbell KP, Coronado R (1988) Purified ryanodine receptor from rabbit skeletal muscle is the calcium release channel of sarcoplasmic reticulum. J Gen Physiol 92:1–26

    Google Scholar 

  36. Vuolteenaho O, Arjamaa O, Ling N (1985) Atrial natriuretic polypeptides (ANP): Rat atria store high molecular weight precursor but secrete processed peptides of 25–35 amino acids. Biochem Biophys Res Commun 129:82–88

    Google Scholar 

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Authors and Affiliations

  1. Department of Physiology, University of Oulu, Kajaanintie 52 A, SF-90220, Oulu, Finland

    Mika Laine, Matti Weckström, Olli Vuolteenaho & Olli Arjamaa

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  1. Mika Laine
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  2. Matti Weckström
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  3. Olli Vuolteenaho
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Laine, M., Weckström, M., Vuolteenaho, O. et al. Effect of ryanodine on atrial natriuretic peptide secretion by contracting and quiescent rat atrium. Pflügers Arch. 426, 276–283 (1994). https://doi.org/10.1007/BF00374782

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  • DOI: https://doi.org/10.1007/BF00374782

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