Skip to main content

Calculated Transsarcolemmal Calcium Movements in Cardiac Muscle

  • Chapter
  • 313 Accesses

Part of the book series: Developments in Cardiovascular Medicine ((DICM,volume 90))

Abstract

The mechanism of excitation-contraction coupling is not established for any type of muscle {1}. In cardiac muscle there is not even universal agreement on whether Ca2+ is released from the sarcoplasmic reticulum (SR) during excitation-contraction coupling. This will be the question addressed in this chapter. In the discussion of the question, emphasis will be placed on the quantification of the Ca2+ fluxes across the sarcolemma and their possible relationships with the Ca2+ movements in and out of the SR. A detailed description of the simple calculations that permit this correlation will provide a tool for a critical analysis of the literature.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Fabiato A, Fabiato F: Calcium release from the sarcoplasmic reticulum. Circ Res 40: 119–129, 1977.

    PubMed  CAS  Google Scholar 

  2. Fabiato A, Baumgarten CM: 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. Boston: Martinus Nijhoff, 1984, pp 215–254.

    Google Scholar 

  3. Eisnet DA, Lederer, WJ: Na-Ca exchange: Stoichiometry and electrogenicity. Am J Physiol 248: C189–C202, 1985.

    Google Scholar 

  4. Hilgemann DW, Noble D: Excitation-conttaction coupling and extracellular calcium transients in rabbit atrium: Reconstruction of basic cellular mechanisms. Proc Roy Soc Lond B 230: 163–205, 1987.

    Article  CAS  Google Scholar 

  5. Sheu SS, Blaustein MP: Sodium/calcium exchange and regulation of cell calcium and contractility in cardiac muscle, with a note about vascular smooth muscle. In: Fozzard HA, Haber E, Jennings RB, Katz AM, Morgan HE (eds) The Heart and Cardiovascular System. New York: Raven Press, 1986, pp 509–535.

    Google Scholar 

  6. Kimura J, Noma A, Irisawa H: Na-Ca exchange current in mammalian heart cells. Nature 319: 596–597, 1986.

    Article  PubMed  CAS  Google Scholar 

  7. Fedida D, Noble D, Shimoni Y, Spindler AJ: Inward current related to contraction in guinea-pig ventricular myocytes. J Physiol 385: 565–589, 1987.

    PubMed  CAS  Google Scholar 

  8. Egan T, Noble D, Noble SG, Powell T, Twist VW: Separation of calcium and {Cai}-activated current in guinea-pig and rabbit ventricular cells. J Physiol 381: 94P, 1987.

    Google Scholar 

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

    Google Scholar 

  10. Hume JR, Uehara A: “Creep currents” in single frog atrial cells may be generated by electrogenic Na/Ca exchange. J Gen Physiol 87: 857–884, 1986.

    Article  PubMed  CAS  Google Scholar 

  11. Hume JR, Uehara A: Properties of “creep currents” in single frog atrial cells. J Gen Physiol 87: 833–855, 1986.

    Article  PubMed  CAS  Google Scholar 

  12. Lee KS, Marban E, Tsien RW: Inactivation of calcium channels in mammalian heart cells: Joint dependence on membrane potential and intracellular calcium. J Physiol 364: 395–411, 1985.

    PubMed  CAS  Google Scholar 

  13. Bean BP: Two kinds of calcium channels in canine atrial cells. Differences in kinetics, selectivity, and pharmacology. J Gen Physiol 86: 1–30, 1985.

    Article  PubMed  CAS  Google Scholar 

  14. Nilius B, Hess P, Lansman JB, Tsien RW: A novel type of cardiac calcium channel in ventricular cells. Nature 316: 443–446, 1985.

    Article  PubMed  Google Scholar 

  15. McDonald TF, Cavalie A, Trautwein W, Pelzer D: Voltage-dependent properties of macroscopic and elementary calcium channel currents in quinea pig ventricular myocytes. Pflügers Arch 406: 437–448, 1986.

    Article  PubMed  CAS  Google Scholar 

  16. Antoni H, Jacob R, Kaufmann R: Mechanische Reaktionen des Frosch und Saugetiermyokards bei Veränderung der Aktionspotential-dauer durch konstante Gleichstromimpulse. Pflügers Arch 306: 33–57, 1969.

    Article  PubMed  CAS  Google Scholar 

  17. Boyett MR, Jewell BR: Analysis of the effects of changes in rate and rhythm upon electrical activity in the heart. Prog Biophys Mol Biol 36: 1–52, 1980.

    Article  PubMed  CAS  Google Scholar 

  18. Wohlfart B, Noble MIM: The cardiac excitation-contraction cycle. Pharmacol Ther 16: 1–43, 1982.

    Article  PubMed  CAS  Google Scholar 

  19. Chapman RA: Control of cardiac contractility at the cellular level. Am J Physiol 245: H535–H552, 1983.

    PubMed  CAS  Google Scholar 

  20. Blinks JR, Olson CB, Jewell BR, Braveny P: Influence of caffeine and other methylxanthines on mechanical properties of isolated mammalian heart muscle: Evidence for a dual mechanism of action. Circ Res 30: 367–392, 1972.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  22. Solaro RJ, Briggs FN: Estimating the functional capabilities of the sarcoplasmic reticulum in cardiac muscle: Calcium binding. Circ Res 34: 531–540, 1974.

    PubMed  CAS  Google Scholar 

  23. Fabiato A: Myoplasmic free calcium concentration reached during the twitch of an intact isolated cardiac cell and during calcium-induced release of calcium from the sarcoplasmic reticulum of skinned cardiac cell from the adult rat or rabbit ventricle. J Gen Physiol 78: 457–497, 1981.

    Article  PubMed  CAS  Google Scholar 

  24. Levitsky DO, Benevolensky DS, Levchenki TS, Smir-nov VN, Chazov EI: Calcium-binding rate and capacity of cardiac sarcoplasmic reticulum. J Mol Cell Cardiol 13: 785–796, 1981.

    Article  PubMed  CAS  Google Scholar 

  25. Fabiato A, Fabiato F: Calcium-induced release of calcium from the sarcoplasmic reticulum of skinned cells from adult human, dog, cat, rabbit, rat, and frog hearts and from fetal and new-born rat ventricles. Ann NY Acad Sei 307: 491–522, 1978.

    Article  CAS  Google Scholar 

  26. Fabiato A: Calcium release in skinned cardiac cells: Variations with species, tissues, and development. Fed Proc 41: 2258–2244, 1982.

    Google Scholar 

  27. Affolter H, Chiesi M, Dabrowska R, Carafoli E: Calcium regulation in heart cells: The interaction of mitochondrial and sarcoplasmic reticulum with troponin-bound calcium. Eur J Biochem 67: 389–396, 1976.

    Article  PubMed  CAS  Google Scholar 

  28. Scarpa A, Graziotti P: Mechanisms for intracellular calcium regulation in heart. I. Stopped-flow measurements of Ca++ uptake by cardiac mitochondria. J Gen Physiol 62: 756–772, 1973.

    Article  PubMed  CAS  Google Scholar 

  29. Somlyo AP, Somlyo AV, Shuman H, Scarpa A, Endo M, Inesi G: Mitochondria do not accumulate significant Ca concentrations in normal cells. In: Bronner F, Peterlik M (eds) Calcium and Phosphate Transport Across Biomembranes. New York: Academic Press, 1981, pp 87–93.

    Google Scholar 

  30. Lullman H, Peters T, Preuner J: Role of the plasmalemma in calcium-homeostasis and for excitation-contraction coupling in cardiac muscle. In: Noble MIM, Drake A (eds) Cardiac Metabolism. London: Wiley and sons, 1983, pp 1–18.

    Google Scholar 

  31. Philipson KD, Bers DM, Nishimoto AY: The role of phospholipids in the Ca2+ binding of isolated cardiac sarcolemma. J Mol Cell Cardiol 12: 1159–1173, 1980.

    Article  PubMed  CAS  Google Scholar 

  32. Bers DM, Philipson KD, Langer GA: Cardiac contractility and sarcolemmal calcium binding in several cardiac muscle preparations. Am J Physiol 240: H576–H583, 1981.

    PubMed  CAS  Google Scholar 

  33. Bers DM: A correlation of the effects of cationic uncouples on intact cardiac muscle and on Ca2+ bound to isolated cardiac muscle plasma membranes. Ph D Thesis, UCLA, 1978. Ann Arbor MI: University Microfilms.

    Google Scholar 

  34. Langer GA: Events at the cardiac sarcolemma: Localization and movement of contractile-dependent calcium. Fed Proc 35: 1274–1278, 1976.

    PubMed  CAS  Google Scholar 

  35. Mensing HJ, Hilgemann DW: Inotropic effects of activation and pharmacological mechanisms in cardiac muscle. Trends Pharmacol Sei 2: 303–307, 1981.

    Article  CAS  Google Scholar 

  36. Ringer S: A further contribution regarding the influence of the different constituents of the blood on the contraction of the heart. J Physiol (Lond) 4: 29–42, 1883.

    PubMed  CAS  Google Scholar 

  37. Mines GR: On functional analysis by the action of electrolytes. J Physiol (Lond) 46: 188–235, 1913.

    PubMed  CAS  Google Scholar 

  38. Langer GA: The role of calcium in the control of myocardial contractility: An update. J Mol Cell Cardiol 12: 231–239, 1980.

    Article  PubMed  CAS  Google Scholar 

  39. Fabiato, A: Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol 245: C1–C14, 1983.

    PubMed  CAS  Google Scholar 

  40. Fabiato A: Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. In: Fleischer S, Fleischer B (eds) Methods in Enzymology, Biomembranes, Vol 157: ATP-Driven Pumps and Related Transport. Orlando: Academic Press, 1988, pp 378–417.

    Google Scholar 

  41. Philipson KD, Bers DM, Nishimoto AY, Langer GA: Binding of Ca2+ and Na+ to sarcolemmal membranes: Relation to control of myocardial contractility. Am J Physiol 238: H373–H378, 1980.

    PubMed  CAS  Google Scholar 

  42. Solomon AK: Compartmental methods of kinetic analysis. In: Comar CL, Bronner F (eds) Mineral Metabolism: An Advanced Treatise. Vol 1: Principles, Processes, and Systems, Part A. New York: Academic Press, 1960, pp 119–167.

    Google Scholar 

  43. Bers DM: Early transient depletion of extracellular Ca during individual cardiac muscle contractions. Am J Physiol 244: H462–H468, 1983.

    PubMed  CAS  Google Scholar 

  44. Bers DM, MacLeod KT: Cumulative depletions of extracellular calcium in rabbit ventricular muscle monitored with calcium-selective microelectrodes. Circ Res 58: 769–782, 1986.

    PubMed  CAS  Google Scholar 

  45. Bers DM, Bridge JHB, MacLeod KT: The mechanism of ryanodine action in rabbit ventricular muscle evaluated with Ca-selective microelectrodes and rapid cooling contractures. Can J Physiol Pharmacol 65: 610–618, 1987.

    Article  PubMed  CAS  Google Scholar 

  46. MacLeod KT, Bers DM: The effects of rest duration and ryanodine on changes of extracellular calcium concentration in cardiac muscle from rabbits. Am J Physiol 253: C398–C407, 1987.

    PubMed  CAS  Google Scholar 

  47. Bers DM: Ca influx and sarcoplasmic reticulum Ca release in cardiac muscle activation during postrest recovery. Am J Physiol 248: H366–H381, 1985.

    PubMed  CAS  Google Scholar 

  48. Hilgemann DW, Delay MJ, Langer GA: Activation-dependent cumulative depletions of extracellular free calcium in guinea pig atrium measured with anti-pyrylazo III and tetramethylmurexide. Circ Res 53: 779–793, 1983.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  50. Hilgemann DW: Extracellular calcium transients at single excitations in rabbit atrium measured with tetramethylmurexide. J Gen Physiol 87: 707–735, 1986.

    Article  PubMed  CAS  Google Scholar 

  51. Pizarro G, Cleemann L, Morad M: Optical measurement of voltage-dependent Ca2+ influx in frog heart. Proc Natl Acad Sei USA 82: 1864–1868, 1985.

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  53. Reuter H, Scholz H: A study of the ion selectivity and the kinetic properties of the calcium dependent slow inward current in mammalian cardiac muscle. J Physiol (Lond) 264: 17–47, 1977.

    PubMed  CAS  Google Scholar 

  54. Siegelbaum SA, Tsien RW: Calcium-activated transient outward current in calf cardiac Purkinje fibres. J Physiol (Lond) 299: 485–506, 1980.

    PubMed  CAS  Google Scholar 

  55. Kass RS Tsien RW: Multiple effects of calcium antagonists on plateau currents in cardiac Purkinje fibers. J Gen Physiol 66: 169–192, 1975.

    Article  PubMed  CAS  Google Scholar 

  56. McDonald TF: The slow inward calcium current in the heart. Ann Rev Physiol 44: 425–434, 1982.

    Article  CAS  Google Scholar 

  57. Kass RS, Siegelbaum S, Tsien RW: Incomplete inactivation of the slow inward current in cardiac Pur-kinje fibres. J Physiol (Lond) 263: 127P–128P, 1976.

    PubMed  CAS  Google Scholar 

  58. Isenberg G, Klockner U: Glycocalyx is not required for slow inward calcium current in isolated rat heart myocytes. Nature 284: 358–360, 1980.

    Article  PubMed  CAS  Google Scholar 

  59. Lee KS, Tsien RW: Reversal of current through calcium channels in dialyzed single heart cells. Nature 297: 498–501, 1982.

    Article  PubMed  CAS  Google Scholar 

  60. Hino N, Orchi R: Effect of acetylcholine on membrane currents in guinea-pig papillary muscle. J Physiol (Lond) 307: 183–197, 1980.

    PubMed  CAS  Google Scholar 

  61. McDonald TF, Pelzer D, Trautwein W: Does the calcium current modulate the contraction of the accompanying beat? A study of EC coupling in mammalian ventricular muscle using cobalt ions. Circ Res 49: 576–583, 1981.

    CAS  Google Scholar 

  62. Nawrath H, Ten Eick RE, McDonald TF, Trautwein W: On the mechanism underlying the action of D-600 on slow inward current and tension in mammalian myocardium. Circ Res 40: 408–414, 1977.

    PubMed  CAS  Google Scholar 

  63. Noma A, Kotake H, Irisawa H: Slow inward current and its role mediating the chronotropic effect of epinephrine in the rabbit sinoatrial node. Pflügers Arch 388: 1–9, 1980.

    Article  PubMed  CAS  Google Scholar 

  64. Ehra T, Kaufman R: The voltage- and time-dependent effects of (-)-verapamil on the slow inward current in isolated cat ventricular myocardium. J Pharmacol Exp Ther 207: 49–55, 1987.

    Google Scholar 

  65. Mobley BA Page E: The surface area of sheep cardiac Purkinje fibres. J Physiol (Lond) 220: 547–563, 1972.

    PubMed  CAS  Google Scholar 

  66. Fabiato A: Appraisal of the hypothesis of the “depolarization-induced” release of calcium from the sarcoplasmic reticulum in skinned cardiac cells from the rat or pigeon ventricle. In: Fleischer S, Tonomura Y (eds) Structure and Function of the Sarcoplasmic Reticulum. New York: Academic Press, 1985, pp 479–519.

    Google Scholar 

  67. Stewart JM, Page E: Improved stereological techniques for studying myocardial cell growth: Application to external sarcolemma, T system, and intercalated disks of rabbit and rat hearts. J Ultrasttuct Res 65: 119–134, 1978.

    Article  CAS  Google Scholar 

  68. Isenbetg G: Ca entry and contraction as studied in isolated bovine ventricular myocytes. Z Naturforsch 37c: 502–512, 1982.

    Google Scholar 

  69. Baumgarten CM: A program for calculation of activity coefficients at selected concentrations and temperatures. Comput Biol Med 11: 189–196, 1981.

    Article  PubMed  CAS  Google Scholar 

  70. Sheu SS, Fozzard HA: Transmembrane Na+ and Ca2+ electrochemical gradients in cardiac muscle and their relationship to force development. J Gen Physiol 80: 325–351, 1982.

    Article  PubMed  CAS  Google Scholar 

  71. Marban E, Rink TJ, Tsien RW, Tsien RY: Free calcium in heart muscle at test and during contraction measured with Ca2+-sensitive microelectrodes. Nature 286: 845–850, 1980.

    Article  PubMed  CAS  Google Scholar 

  72. Lee CO: Ionic activities in cardiac muscle cells and application of ion-selective microelectrodes. Am J Physiol 241: H459–H478, 1981.

    PubMed  CAS  Google Scholar 

  73. Reuter H: Na-Ca countertransport in cardiac muscle. In: Martonosi AN (ed) Membranes and Transport, Vol 1. New York: Plenum, 1982, pp 623–631.

    Google Scholar 

  74. Lado MG, Sheu SS, Fozzard HA: Changes in intracellular Ca2+ activity with stimulation in sheep cardiac Purkinje strands. Am J Physiol 243: H133–H137, 1982.

    PubMed  CAS  Google Scholar 

  75. Caroni P, Reinlib L, Carafoli E: Charge movements during the Na+-Ca2+ exchange in heart sarcolemmal vesicles. Proc Natl Acad Sei USA 77: 6354–6358, 1980.

    Article  CAS  Google Scholar 

  76. Kadoma M, FroehilichJ, Reeves J, Sutko J: Kinetics of sodium ion induced calcium ion release in calcium ion loaded cardiac sarcolemmal vesicles: determination of initial velocities by stopped-flow spectrophotometry. Biochemistry 21: 1914–1918, 1982.

    CAS  Google Scholar 

  77. Mullins LJ: Interactions between Na/K and Na/Ca pumps. In: Ion Transport in Heart. New York: Raven Press, 1981, pp 61–94.

    Google Scholar 

  78. Sulakhe PV, St Louis PJ: Passive and active calcium fluxes across plasma membranes. Prog Biophys Mol Biol 35: 135–195, 1980.

    Article  PubMed  CAS  Google Scholar 

  79. Jones LR, Besch HR Jr, Flemins JW, McConnaughey MM, Watanabe AM: Separation of vesicles of cardiac sarcolemma from vesicles of cardiac sarcoplasmic reticulum: Comparative biochemical analysis of component activities. J Biol Chem 254: 530–539, 1979.

    CAS  Google Scholar 

  80. Caroni P, Carafoli E: An ATP-dependent Ca2+-pumping system in dog heart sarcolemma. Nature 283: 765–767, 1980.

    Article  PubMed  CAS  Google Scholar 

  81. Caroni P, Carafoli E: The Ca2+-pumping ATPase of heart sarcolemma. J Biol Chem 256: 3263–3270, 1981.

    PubMed  CAS  Google Scholar 

  82. Solaro RJ, Briggs FN: Calcium conservation and the regulation of myocardial contraction. In: Dhalla NS, (ed) Recent Advances in Studies on Cardiac Structure and Metabolism. Myocardial Biology, Vol 4. Baltimore: University Park Press, 1974, pp 359–374.

    Google Scholar 

  83. Van Winkle WB, Schwartz A: Ions and inotropy. Ann Rev Physiol 38: 247–272, 1976.

    Article  Google Scholar 

  84. Morad M, Goldman Y: Excitation-contraction coupling in heart muscle: Membrane control of development of tension. Prog Biophys Mol Biol 27: 257–313, 1973.

    Article  Google Scholar 

  85. Kavaler F, Anderson TW: Indirect evidence that calcium extrusion causes relaxation of frog ventricular muscle. Fed Proc 37: 300, 1978.

    Google Scholar 

  86. Kavaler F, Anderson TW, Fisher VJ: Sarcolemmal site of caffeine’s inotropic action on ventricular muscle of the frog. Circ Res 42: 285–290, 1978.

    CAS  Google Scholar 

  87. Niedergerke R, Page S: Analysis of caffeine action in single trabeculae of the frog heart. Proc Roy Soc Lond B 213: 303–324, 1981.

    Article  CAS  Google Scholar 

  88. Fabiato A: Calcium both activates and inactivates calcium release from cardiac sarcoplasmic reticulum. In: Rubin RP, Weiss GB, Putney JW Jr. (eds) Calcium in Biological Systems. New York: Plenum, 1985, pp 369–375.

    Chapter  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1989 Kluwer Academic Publishers

About this chapter

Cite this chapter

Baumgarten, C.M., Fabiato, A. (1989). Calculated Transsarcolemmal Calcium Movements in Cardiac Muscle. In: Sperelakis, N. (eds) Physiology and Pathophysiology of the Heart. Developments in Cardiovascular Medicine, vol 90. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-0873-7_12

Download citation

  • DOI: https://doi.org/10.1007/978-1-4613-0873-7_12

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-8222-8

  • Online ISBN: 978-1-4613-0873-7

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics