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. 1987 Jun;387:567–588. doi: 10.1113/jphysiol.1987.sp016589

Electrogenic sodium-calcium exchange in cultured embryonic chick heart cells.

R Jacob 1, M Lieberman 1, S Liu 1
PMCID: PMC1192520  PMID: 2443686

Abstract

1. The membrane potential (Em) of cultured chick embryonic heart cells depolarized to -36 mV after inhibition of the Na+-K+ pump by 0.1 mM-ouabain in a [K+]o of 24 mM: this was accompanied by a rise in Na+ content of approximately 65% in 3 min. Lowering [Na+]o to 27 mM then caused a fall in Na+ content, a rise in Ca2+ content and a small hyperpolarization of approximately 5 mV. The fall in Na+ content indicated a movement of Na+ which was in the opposite direction to the Na+ electrochemical gradient (a countergradient movement). 2. In the presence of 10 mM-Cs+ or 1 mM-Ba2+ the hyperpolarization was approximately 10 or approximately 30 mV, respectively. A 30 mV hyperpolarization took Em negative to the reversal potentials for K+, and Cl- as measured by ion-selective micro-electrodes. 3. The decay of the intracellular Na+ activity alpha iNa, in an [Na+]o of 27 mM followed a simple exponential time course (time constant, 36 s). The initial rate depended on the value to which [Na+]o was lowered in a manner suggesting a simple competitive inhibition of the exchange by external Na+. 4. The low-[Na+]o hyperpolarization was unaffected by amiloride (0.1 or 1 mM) or verapamil (20 microM). Both La3+ (1 mM) and Mn2+ (20 mM) blocked the hyperpolarization sufficiently to prevent Em hyperpolarizing negative to the reversal potentials for K+, Na+ and Cl-. 5. Re-establishing [Na+]o caused a rise in Na+ content and a countergradient drop in Ca2+ content. The effects of verapamil (20 microM), amiloride (0.1 and 1 mM), dichlorobenzamil (0.1 mM), quinidine (1 mM), Mn2+ (20 mM) and La3+ (1 mM) were tested on the movements of Na+ and Ca2+ both during exposure to an [Na+]o of 27 mM and on re-establishing [Na+]o. The only consistent and substantial effects were the attenuation by La3+ and Mn2+ and Ca2+ movements during exposure to an [Na+]o of 27 mM. However, neither La3+ nor Mn2+ affected the movements of Na+ and Ca2+ on re-establishing [Na+]o. 6. We conclude that cultured embryonic chick heart cells contain a Na+-Ca2+ exchange evidenced by the ability to cause movements of Na+ and Ca2+ which are counter to their respective electrochemical gradient and which are accompanied by downhill movements of the counter ion.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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  1. Altschuld R. A., Hohl C. M., Lamka K. G., Brierley G. P. Effects of amiloride on calcium uptake by myocytes isolated from adult rat hearts. Life Sci. 1984 Aug 20;35(8):865–870. doi: 10.1016/0024-3205(84)90412-0. [DOI] [PubMed] [Google Scholar]
  2. Baker P. F., Willis J. S. Potassium ions and the binding of cardiac glycosides to mammalian cells. Nature. 1970 May 9;226(5245):521–523. doi: 10.1038/226521a0. [DOI] [PubMed] [Google Scholar]
  3. Barry W. H., Smith T. W. Mechanisms of transmembrane calcium movement in cultured chick embryo ventricular cells. J Physiol. 1982 Apr;325:243–260. doi: 10.1113/jphysiol.1982.sp014148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bartschat D. K., Cyr D. L., Lindenmayer G. E. Depolarization-induced calcium uptake by vesicles in a highly enriched sarcolemma preparation from canine ventricle. J Biol Chem. 1980 Nov 10;255(21):10044–10047. [PubMed] [Google Scholar]
  5. Bartschat D. K., Lindenmayer G. E. Calcium movements promoted by vesicles in a highly enriched sarcolemma preparation from canine ventricle. Calcium-calcium countertransport. J Biol Chem. 1980 Oct 25;255(20):9626–9634. [PubMed] [Google Scholar]
  6. Baumgarten C. M., Fozzard H. A. Intracellular chloride activity in mammalian ventricular muscle. Am J Physiol. 1981 Sep;241(3):C121–C129. doi: 10.1152/ajpcell.1981.241.3.C121. [DOI] [PubMed] [Google Scholar]
  7. Bridge J. H., Bassingthwaighte J. B. Uphill sodium transport driven by an inward calcium gradient in heart muscle. Science. 1983 Jan 14;219(4581):178–180. doi: 10.1126/science.6849128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chapman R. A., Coray A., McGuigan J. A. Sodium/calcium exchange in mammalian ventricular muscle: a study with sodium-sensitive micro-electrodes. J Physiol. 1983 Oct;343:253–276. doi: 10.1113/jphysiol.1983.sp014891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cohen I. S., Falk R. T., Mulrine N. K. Actions of barium and rubidium on membrane currents in canine Purkinje fibres. J Physiol. 1983 May;338:589–612. doi: 10.1113/jphysiol.1983.sp014691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Croaboeuf E., Gautier P., Giuraudou P. Potential and tension changes induced by sodium removal in dog Purkinje fibres: role of an electrogenic sodium-calcium exchange. J Physiol. 1981 Feb;311:605–622. doi: 10.1113/jphysiol.1981.sp013607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dagostino M., Lee C. O. Neutral carrier Na+- and Ca2+-selective microelectrodes for intracellular application. Biophys J. 1982 Dec;40(3):199–207. doi: 10.1016/S0006-3495(82)84475-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Deitmer J. W., Ellis D. Changes in the intracellular sodium activity of sheep heart Purkinje fibres produced by calcium and other divalent cations. J Physiol. 1978 Apr;277:437–453. doi: 10.1113/jphysiol.1978.sp012283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Deitmer J. W., Ellis D. Interactions between the regulation of the intracellular pH and sodium activity of sheep cardiac Purkinje fibres. J Physiol. 1980 Jul;304:471–488. doi: 10.1113/jphysiol.1980.sp013337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. DiFrancesco D. Block and activation of the pace-maker channel in calf purkinje fibres: effects of potassium, caesium and rubidium. J Physiol. 1982 Aug;329:485–507. doi: 10.1113/jphysiol.1982.sp014315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. DiFrancesco D., Ferroni A., Visentin S. Barium-induced blockade of the inward rectifier in calf Purkinje fibres. Pflugers Arch. 1984 Dec;402(4):446–453. doi: 10.1007/BF00583946. [DOI] [PubMed] [Google Scholar]
  16. Désilets M., Horackova M. Effect of quinidine on Na-dependent 45Ca transport in isolated adult cardiac cells. Can J Physiol Pharmacol. 1984 May;62(5):575–580. doi: 10.1139/y84-092. [DOI] [PubMed] [Google Scholar]
  17. Ebihara L., Mathias R. T. Linear impedance studies of voltage-dependent conductances in tissue cultured chick heart cells. Biophys J. 1985 Sep;48(3):449–460. doi: 10.1016/S0006-3495(85)83800-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ellis D. The effects of external cations and ouabain on the intracellular sodium activity of sheep heart Purkinje fibres. J Physiol. 1977 Dec;273(1):211–240. doi: 10.1113/jphysiol.1977.sp012090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Erdreich A., Rahamimoff H. The inhibition of Ca uptake in cardiac membrane vesicles by verapamil. Biochem Pharmacol. 1984 Jul 15;33(14):2315–2323. doi: 10.1016/0006-2952(84)90672-5. [DOI] [PubMed] [Google Scholar]
  20. Floreani M., Luciani S. Amiloride: relationship between cardiac effects and inhibition of Na+/Ca2+ exchange. Eur J Pharmacol. 1984 Oct 15;105(3-4):317–322. doi: 10.1016/0014-2999(84)90624-1. [DOI] [PubMed] [Google Scholar]
  21. Frelin C., Vigne P., Lazdunski M. The role of the Na+/H+ exchange system in the regulation of the internal pH in cultured cardiac cells. Eur J Biochem. 1985 May 15;149(1):1–4. doi: 10.1111/j.1432-1033.1985.tb08884.x. [DOI] [PubMed] [Google Scholar]
  22. Harrow J. A., Dhalla N. S. Effects of quinidine on calcium transport activities of the rabbit heart mitochondria and sarcotubular vesicles. Biochem Pharmacol. 1976 Apr 15;25(8):897–902. doi: 10.1016/0006-2952(76)90311-7. [DOI] [PubMed] [Google Scholar]
  23. Horackova M., Vassort G. Sodium-calcium exchange in regulation of cardiac contractility. Evidence for an electrogenic, voltage-dependent mechanism. J Gen Physiol. 1979 Apr;73(4):403–424. doi: 10.1085/jgp.73.4.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Horres C. R., Lieberman M., Purdy J. E. Growth orientation of heart cells on nylon monofilament. Determination of the volume-to-surface area ratio and intracellular potassium concentration. J Membr Biol. 1977 Jun 15;34(4):313–329. doi: 10.1007/BF01870306. [DOI] [PubMed] [Google Scholar]
  25. Isenberg G. Cardiac Purkinje fibres: [Ca2+]i controls steady state potassium conductance. Pflugers Arch. 1977 Oct 19;371(1-2):71–76. doi: 10.1007/BF00580774. [DOI] [PubMed] [Google Scholar]
  26. Isenberg G. Cardiac Purkinje fibres: [Ca2+]i controls the potassium permeability via the conductance components gK1 and gK2. Pflugers Arch. 1977 Oct 19;371(1-2):77–85. doi: 10.1007/BF00580775. [DOI] [PubMed] [Google Scholar]
  27. Iwatsuki N., Petersen O. H. Inhibition of Ca2+-activated K+ channels in pig pancreatic acinar cells by Ba2+, Ca2+, quinine and quinidine. Biochim Biophys Acta. 1985 Oct 10;819(2):249–257. doi: 10.1016/0005-2736(85)90180-4. [DOI] [PubMed] [Google Scholar]
  28. Jacob R., Lieberman M., Murphy E., Piwnica-Worms D. Effects of sodium-potassium pump inhibition and low sodium on membrane potential in cultured embryonic chick heart cells. J Physiol. 1987 Jun;387:549–566. doi: 10.1113/jphysiol.1987.sp016588. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Karlish S. J., Stein W. D. Cation activation of the pig kidney sodium pump: transmembrane allosteric effects of sodium. J Physiol. 1985 Feb;359:119–149. doi: 10.1113/jphysiol.1985.sp015578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Katzung B. G., Reuter H., Porzig H. Lanthanum inhibits Ca inward current but not Na-Ca exchange in cardiac muscle. Experientia. 1973 Sep 15;29(9):1073–1075. doi: 10.1007/BF01946727. [DOI] [PubMed] [Google Scholar]
  31. Kimura J., Noma A., Irisawa H. Na-Ca exchange current in mammalian heart cells. Nature. 1986 Feb 13;319(6054):596–597. doi: 10.1038/319596a0. [DOI] [PubMed] [Google Scholar]
  32. Lederer W. J., Spindler A. J., Eisner D. A. Thick slurry bevelling: a new technique for bevelling extremely fine microelectrodes and micropipettes. Pflugers Arch. 1979 Sep;381(3):287–288. doi: 10.1007/BF00583261. [DOI] [PubMed] [Google Scholar]
  33. Ledvora R. F., Hegyvary C. Dependence of Na+-Ca2+ exchange and Ca2+-Ca2+ exchange on monovalent cations. Biochim Biophys Acta. 1983 Mar 23;729(1):123–136. doi: 10.1016/0005-2736(83)90463-7. [DOI] [PubMed] [Google Scholar]
  34. Lindenmayer G. E., Schwartz A., Thompson H. K., Jr A kinetic description for sodium and potassium effects on (Na+ plus K+)-adenosine triphosphatase: a model for a two-nonequivalent site potassium activation and an analysis of multiequivalent site models for sodium activation. J Physiol. 1974 Jan;236(1):1–28. doi: 10.1113/jphysiol.1974.sp010419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Mentrard 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 Gen Physiol. 1984 Aug;84(2):201–220. doi: 10.1085/jgp.84.2.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Murphy E., Wheeler D. M., LeFurgey A., Jacob R., Lobaugh L. A., Lieberman M. Coupled sodium-calcium transport in cultured chick heart cells. Am J Physiol. 1986 Mar;250(3 Pt 1):C442–C452. doi: 10.1152/ajpcell.1986.250.3.C442. [DOI] [PubMed] [Google Scholar]
  37. Owen D. G., Segal M., Barker J. L. A Ca-dependent Cl- conductance in cultured mouse spinal neurones. Nature. 1984 Oct 11;311(5986):567–570. doi: 10.1038/311567a0. [DOI] [PubMed] [Google Scholar]
  38. Piwnica-Worms D., Jacob R., Horres C. R., Lieberman M. Na/H exchange in cultured chick heart cells. pHi regulation. J Gen Physiol. 1985 Jan;85(1):43–64. doi: 10.1085/jgp.85.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Piwnica-Worms D., Jacob R., Horres C. R., Lieberman M. Transmembrane chloride flux in tissue-cultured chick heart cells. J Gen Physiol. 1983 May;81(5):731–748. doi: 10.1085/jgp.81.5.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Rahamimoff H., Spanier R. The asymmetric effect of lanthanides on Na+-gradient-dependent Ca2+ transport in synaptic plasma membrane vesicles. Biochim Biophys Acta. 1984 Jun 27;773(2):279–289. doi: 10.1016/0005-2736(84)90092-0. [DOI] [PubMed] [Google Scholar]
  41. Reeves J. P., Hale C. C. The stoichiometry of the cardiac sodium-calcium exchange system. J Biol Chem. 1984 Jun 25;259(12):7733–7739. [PubMed] [Google Scholar]
  42. Reeves J. P., Sutko J. L. Competitive interactions of sodium and calcium with the sodium-calcium exchange system of cardiac sarcolemmal vesicles. J Biol Chem. 1983 Mar 10;258(5):3178–3182. [PubMed] [Google Scholar]
  43. Reeves J. P., Sutko J. L. Sodium-calcium ion exchange in cardiac membrane vesicles. Proc Natl Acad Sci U S A. 1979 Feb;76(2):590–594. doi: 10.1073/pnas.76.2.590. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Reuter H., Seitz N. The dependence of calcium efflux from cardiac muscle on temperature and external ion composition. J Physiol. 1968 Mar;195(2):451–470. doi: 10.1113/jphysiol.1968.sp008467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Siegl P. K., Cragoe E. J., Jr, Trumble M. J., Kaczorowski G. J. Inhibition of Na+/Ca2+ exchange in membrane vesicle and papillary muscle preparations from guinea pig heart by analogs of amiloride. Proc Natl Acad Sci U S A. 1984 May;81(10):3238–3242. doi: 10.1073/pnas.81.10.3238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Spitzer K. W., Walker J. L. Intracellular chloride activity in quiescent cat papillary muscle. Am J Physiol. 1980 Apr;238(4):H487–H493. doi: 10.1152/ajpheart.1980.238.4.H487. [DOI] [PubMed] [Google Scholar]
  47. Su J. Y., Libao R. G. Intracellular mechanism of quinidine action on muscle contraction. A comparison between rabbit cardiac and skeletal muscle. Naunyn Schmiedebergs Arch Pharmacol. 1984 Jul;326(4):375–381. doi: 10.1007/BF00501446. [DOI] [PubMed] [Google Scholar]
  48. Trosper T. L., Philipson K. D. Effects of divalent and trivalent cations on Na+-Ca2+ exchange in cardiac sarcolemmal vesicles. Biochim Biophys Acta. 1983 May 26;731(1):63–68. doi: 10.1016/0005-2736(83)90398-x. [DOI] [PubMed] [Google Scholar]
  49. Vaughan-Jones R. D. Non-passive chloride distribution in mammalian heart muscle: micro-electrode measurement of the intracellular chloride activity. J Physiol. 1979 Oct;295:83–109. doi: 10.1113/jphysiol.1979.sp012956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Vergara C., Latorre R. Kinetics of Ca2+-activated K+ channels from rabbit muscle incorporated into planar bilayers. Evidence for a Ca2+ and Ba2+ blockade. J Gen Physiol. 1983 Oct;82(4):543–568. doi: 10.1085/jgp.82.4.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Wakabayashi S., Goshima K. Comparison of kinetic characteristics of Na+-Ca2+ exchange in sarcolemma vesicles and cultured cells from chick heart. Biochim Biophys Acta. 1981 Jul 20;645(2):311–317. doi: 10.1016/0005-2736(81)90202-9. [DOI] [PubMed] [Google Scholar]
  52. Wallenstein S., Zucker C. L., Fleiss J. L. Some statistical methods useful in circulation research. Circ Res. 1980 Jul;47(1):1–9. doi: 10.1161/01.res.47.1.1. [DOI] [PubMed] [Google Scholar]

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