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. 1985 Mar 1;85(3):365–382. doi: 10.1085/jgp.85.3.365

Effects of calcium on electrical propagation in early embryonic precontractile heart as revealed by multiple-site optical recording of action potentials

PMCID: PMC2215791  PMID: 3921654

Abstract

The effects of Ca2+ on electrical propagation in early embryonic precontractile chick hearts were studied optically using a voltage- sensitive merocyanine-rhodanine dye. Spontaneous optical signals, corresponding to action potentials, were recorded simultaneously from 25 separate regions of the eight-to-nine-somite embryonic primitive heart, using a square photodiode array. Electrical propagation was assessed by analyzing the timing of the signals obtained from different regions. Electrical propagation in the heart was suppressed by either lowering or raising extracellular Ca2+. Similar effects were produced by a Ca2+ ionophore (A23187). We have also found that electrical propagation across the primordial fusion line at the midline of the heart was enhanced by increasing, and depressed by lowering, external Ca2+. One possible interpretation is that intercellular communication in the embryonic precontractile heart is regulated by the level of the intracellular Ca2+ concentration, and it is suggested that intercellular communication across the primordial fusion line strongly depends on external Ca2+.

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Selected References

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  1. Cohen L. B., Salzberg B. M. Optical measurement of membrane potential. Rev Physiol Biochem Pharmacol. 1978;83:35–88. doi: 10.1007/3-540-08907-1_2. [DOI] [PubMed] [Google Scholar]
  2. De Mello W. C. Effect of intracellular injection of calcium and strontium on cell communication in heart. J Physiol. 1975 Sep;250(2):231–245. doi: 10.1113/jphysiol.1975.sp011051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. De Mello W. C. Intercellular communication in cardiac muscle. Circ Res. 1982 Jul;51(1):1–9. doi: 10.1161/01.res.51.1.1. [DOI] [PubMed] [Google Scholar]
  4. DeHaan R. L., Hirakow R. Synchronizatin of pulsation rates in isolated cardiac myocytes. Exp Cell Res. 1972 Jan;70(1):214–220. doi: 10.1016/0014-4827(72)90199-1. [DOI] [PubMed] [Google Scholar]
  5. Fujii S., Hirota A., Kamino K. Action potential synchrony in embryonic precontractile chick heart: optical monitoring with potentiometric dyes. J Physiol. 1981;319:529–541. doi: 10.1113/jphysiol.1981.sp013924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fujii S., Hirota A., Kamino K. Optical indications of pace-maker potential and rhythm generation in early embryonic chick heart. J Physiol. 1981 Mar;312:253–263. doi: 10.1113/jphysiol.1981.sp013627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fujii S., Hirota A., Kamino K. Optical recording of development of electrical activity in embryonic chick heart during early phases of cardiogenesis. J Physiol. 1981 Feb;311:147–160. doi: 10.1113/jphysiol.1981.sp013578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fujii S., Hirota A., Kamino K. Optical signals from early embryonic chick heart stained with potential sensitive dyes: evidence for electrical activity. J Physiol. 1980 Jul;304:503–518. doi: 10.1113/jphysiol.1980.sp013339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Goshima K. Formation of nexuses and electrotonic transmission between myocardial and FL cells in monolayer culture. Exp Cell Res. 1970 Nov;63(1):124–130. doi: 10.1016/0014-4827(70)90339-3. [DOI] [PubMed] [Google Scholar]
  10. Goshima K. Synchronized beating of and electrotonic transmission between myocardial cells mediated by heterotypic strain cells in monolayer culture. Exp Cell Res. 1969 Dec;58(2):420–426. doi: 10.1016/0014-4827(69)90523-0. [DOI] [PubMed] [Google Scholar]
  11. Grinvald A., Cohen L. B., Lesher S., Boyle M. B. Simultaneous optical monitoring of activity of many neurons in invertebrate ganglia using a 124-element photodiode array. J Neurophysiol. 1981 May;45(5):829–840. doi: 10.1152/jn.1981.45.5.829. [DOI] [PubMed] [Google Scholar]
  12. Grinvald A., Manker A., Segal M. Visualization of the spread of electrical activity in rat hippocampal slices by voltage-sensitive optical probes. J Physiol. 1982 Dec;333:269–291. doi: 10.1113/jphysiol.1982.sp014453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hirota A., Fujii S., Kamino K. Optical monitoring of spontaneous electrical activity of 8-somite embryonic chick heart. Jpn J Physiol. 1979;29(5):635–639. doi: 10.2170/jjphysiol.29.635. [DOI] [PubMed] [Google Scholar]
  14. Hirota A., Sakai T., Fujii S., Kamino K. Initial development of conduction pattern of spontaneous action potential in early embryonic precontractile chick heart. Dev Biol. 1983 Oct;99(2):517–523. doi: 10.1016/0012-1606(83)90301-9. [DOI] [PubMed] [Google Scholar]
  15. Kamino K., Hirota A., Fujii S. Localization of pacemaking activity in early embryonic heart monitored using voltage-sensitive dye. Nature. 1981 Apr 16;290(5807):595–597. doi: 10.1038/290595a0. [DOI] [PubMed] [Google Scholar]
  16. Loewenstein W. R. Junctional intercellular communication and the control of growth. Biochim Biophys Acta. 1979 Feb 4;560(1):1–65. doi: 10.1016/0304-419x(79)90002-7. [DOI] [PubMed] [Google Scholar]
  17. Loewenstein W. R. Junctional intercellular communication: the cell-to-cell membrane channel. Physiol Rev. 1981 Oct;61(4):829–913. doi: 10.1152/physrev.1981.61.4.829. [DOI] [PubMed] [Google Scholar]
  18. Loewenstein W. R., Nakas M., Socolar S. J. Junctional membrane uncoupling. Permeability transformations at a cell membrane junction. J Gen Physiol. 1967 Aug;50(7):1865–1891. doi: 10.1085/jgp.50.7.1865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Loewenstein W. R. Permeability of membrane junctions. Ann N Y Acad Sci. 1966 Jul 14;137(2):441–472. doi: 10.1111/j.1749-6632.1966.tb50175.x. [DOI] [PubMed] [Google Scholar]
  20. Manasek F. J. Embryonic development of the heart. I. A light and electron microscopic study of myocardial development in the early chick embryo. J Morphol. 1968 Jul;125(3):329–365. doi: 10.1002/jmor.1051250306. [DOI] [PubMed] [Google Scholar]
  21. Muir A. R. The effects of divalent cations on the ultrastructure of the perfused rat heart. J Anat. 1967 Apr;101(Pt 2):239–261. [PMC free article] [PubMed] [Google Scholar]
  22. Nakas M., Higashino S., Loewenstein W. R. Uncoupling of an epithelial cell membrane junction by calcium-ion removal. Science. 1966 Jan 7;151(3706):89–91. doi: 10.1126/science.151.3706.89. [DOI] [PubMed] [Google Scholar]
  23. Orbach H. S., Cohen L. B. Optical monitoring of activity from many areas of the in vitro and in vivo salamander olfactory bulb: a new method for studying functional organization in the vertebrate central nervous system. J Neurosci. 1983 Nov;3(11):2251–2262. doi: 10.1523/JNEUROSCI.03-11-02251.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rose B., Loewenstein W. R. Permeability of a cell junction and the local cytoplasmic free ionized calcium concentration: a study with aequorin. J Membr Biol. 1976 Aug 27;28(1):87–119. doi: 10.1007/BF01869692. [DOI] [PubMed] [Google Scholar]
  25. Sakai T., Fujii S., Hirota A., Kamino K. Optical evidence for calcium-action potentials in early embryonic precontractile chick heart using a potential-sensitive dye. J Membr Biol. 1983;72(3):205–212. doi: 10.1007/BF01870587. [DOI] [PubMed] [Google Scholar]
  26. Sakai T., Hirota A., Fujii S., Kamino K. Flexibility of regional pacemaking priority in early embryonic heart monitored by simultaneous optical recording of action potentials from multiple sites. Jpn J Physiol. 1983;33(3):337–350. doi: 10.2170/jjphysiol.33.337. [DOI] [PubMed] [Google Scholar]
  27. Salzberg B. M., Grinvald A., Cohen L. B., Davila H. V., Ross W. N. Optical recording of neuronal activity in an invertebrate central nervous system: simultaneous monitoring of several neurons. J Neurophysiol. 1977 Nov;40(6):1281–1291. doi: 10.1152/jn.1977.40.6.1281. [DOI] [PubMed] [Google Scholar]
  28. Salzberg B. M., Obaid A. L., Senseman D. M., Gainer H. Optical recording of action potentials from vertebrate nerve terminals using potentiometric probes provides evidence for sodium and calcium components. Nature. 1983 Nov 3;306(5938):36–40. doi: 10.1038/306036a0. [DOI] [PubMed] [Google Scholar]
  29. Senseman D. M., Shimizu H., Horwitz I. S., Salzberg B. M. Multiple-site optical recording of membrane potential from a salivary gland. Interaction of synaptic and electrotonic excitation. J Gen Physiol. 1983 Jun;81(6):887–908. doi: 10.1085/jgp.81.6.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Spray D. C., Stern J. H., Harris A. L., Bennett M. V. Gap junctional conductance: comparison of sensitivities to H and Ca ions. Proc Natl Acad Sci U S A. 1982 Jan;79(2):441–445. doi: 10.1073/pnas.79.2.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Weidmann S. Electrical constants of trabecular muscle from mammalian heart. J Physiol. 1970 Nov;210(4):1041–1054. doi: 10.1113/jphysiol.1970.sp009256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Winegrad S. Studies of cardiac muscle with a high permeability to calcium produced by treatment with ethylenediaminetetraacetic acid. J Gen Physiol. 1971 Jul;58(1):71–93. doi: 10.1085/jgp.58.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ypey D. L., Clapham D. E., DeHaan R. L. Development of electrical coupling and action potential synchrony between paired aggregates of embryonic heart cells. J Membr Biol. 1979 Dec 12;51(1):75–96. doi: 10.1007/BF01869344. [DOI] [PubMed] [Google Scholar]
  34. de Mello W. C., Motta G. E., Chapeau M. A study on the healing-over of myocardial cells of toads. Circ Res. 1969 Mar;24(3):475–487. doi: 10.1161/01.res.24.3.475. [DOI] [PubMed] [Google Scholar]

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