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. 1973 Jul;232(2):313–330. doi: 10.1113/jphysiol.1973.sp010272

Intracellular and intercellular potentials in the early amphibian embryo

Christine Slack, Anne E Warner
PMCID: PMC1350457  PMID: 4737870

Abstract

1. The sensitivity of the membrane potential of cells of early embryos of Xenopus laevis to variations in the extracellular concentrations of sodium and potassium has been determined.

2. Alterations in the extracellular sodium concentration have little effect on the membrane potential at all pregastrular stages tested.

3. Up to the 32 cell stage an increase in the concentration of potassium in the bathing medium causes a fall in cell membrane potential only when membrane newly synthesized in the furrow during cleavage is exposed at the embryo surface, during the second half of the cell division cycle.

4. Beyond the morula stage (48 cells) a fall in membrane potential on raising external potassium can only be demonstrated when the seal which isolates the intercellular fluid from the bathing medium is broken so that cells lining the inner face of the embryo come into contact with the high potassium solution.

5. The results suggest that the egg membrane has little selective permeability whereas membrane synthesized after fertilization is highly potassium permeable.

6. No evidence could be obtained for any potential difference between the intercellular fluid and the external bathing medium.

7. Dinitrophenol, sodium azide and cyanide prevented normal development only if they were injected into the intercellular cavity. Embryos reared in solutions containing these poisons turned into normal tadpoles.

8. The formation of the intercellular cavity could be halted by injecting ouabain into the cavity while it was still small. Embryos reared in ouabain turned into normal tadpoles.

9. The results suggest that the active transfer of sodium ions from the cells to the intercellular spaces is an integral part of the formation of the intercellular fluid. A hypothesis for the mechanism of formation of the cavity is put forward along these lines.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ADRIAN R. H. The effect of internal and external potassium concentration on the membrane potential of frog muscle. J Physiol. 1956 Sep 27;133(3):631–658. doi: 10.1113/jphysiol.1956.sp005615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aivar Iup Vliianie ionov K, Na i Cl na membrannyi potentsial ootsitov R. temporaria. Biofizika. 1969 Mar-Apr;14(2):362–364. [PubMed] [Google Scholar]
  3. Alvarado R. H., Moody A. Sodium and chloride transport in tadpoles of the bullfrog Rana catesbeiana. Am J Physiol. 1970 May;218(5):1510–1516. doi: 10.1152/ajplegacy.1970.218.5.1510. [DOI] [PubMed] [Google Scholar]
  4. Baker P. F., Willis J. S. Binding of the cardiac glycoside ouabain to intact cells. J Physiol. 1972 Jul;224(2):441–462. doi: 10.1113/jphysiol.1972.sp009904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bluemink J. G. The first cleavage of the amphibian egg. An electron microscope study of the onset of cytokinesis in the egg of Ambystoma mexicanum. J Ultrastruct Res. 1970 Jul;32(1):142–166. doi: 10.1016/s0022-5320(70)80042-9. [DOI] [PubMed] [Google Scholar]
  6. DIAMOND J. M. The mechanism of solute transport by the gall-bladder. J Physiol. 1962 May;161:474–502. doi: 10.1113/jphysiol.1962.sp006899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Diamond J. M., Tormey J. M. Role of long extracellular channels in fluid transport across epithelia. Nature. 1966 May 21;210(5038):817–820. doi: 10.1038/210817a0. [DOI] [PubMed] [Google Scholar]
  8. GLYNN I. M. THE ACTION OF CARDIAC GLYCOSIDES ON ION MOVEMENTS. Pharmacol Rev. 1964 Dec;16:381–407. [PubMed] [Google Scholar]
  9. Goldman D. E. POTENTIAL, IMPEDANCE, AND RECTIFICATION IN MEMBRANES. J Gen Physiol. 1943 Sep 20;27(1):37–60. doi: 10.1085/jgp.27.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Haydon D. A., Hladky S. B. Ion transport across thin lipid membranes: a critical discussion of mechanisms in selected systems. Q Rev Biophys. 1972 May;5(2):187–282. doi: 10.1017/s0033583500000883. [DOI] [PubMed] [Google Scholar]
  11. Ito S., Hori N. Electrical characteristics of Triturus egg cells during cleavage. J Gen Physiol. 1966 May;49(5):1019–1027. doi: 10.1085/jgp.49.5.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ito S., Loewenstein W. R. Ionic communication between early embryonic cells. Dev Biol. 1969 Mar;19(3):228–243. doi: 10.1016/0012-1606(69)90062-1. [DOI] [PubMed] [Google Scholar]
  13. Kalt M. R. The relationship between cleavage and blastocoel formation in Xenopus laevis. I. Light microscopic observations. J Embryol Exp Morphol. 1971 Aug;26(1):37–49. [PubMed] [Google Scholar]
  14. Kalt M. R. The relationship between cleavage and blastocoel formation in Xenopus laevis. II. Electron microscopic observations. J Embryol Exp Morphol. 1971 Aug;26(1):51–66. [PubMed] [Google Scholar]
  15. Kostellow A. B., Morrill G. A. Intracellular sodium ion concentration changes in the early amphibian embryo and the influence on nuclear metabolism. Exp Cell Res. 1968 Jun;50(3):639–644. doi: 10.1016/0014-4827(68)90425-4. [DOI] [PubMed] [Google Scholar]
  16. MAENO T. Electrical characteristics and activation potential of Bufo eggs. J Gen Physiol. 1959 Sep;43:139–157. doi: 10.1085/jgp.43.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Morrill G. A., Kostellow A. B., Watson D. E. The electropotential difference between the blastocoel and the external medium in the amphibian embryo: its similarity to the adult frog trans-skin potential. Life Sci. 1966 Apr;5(8):705–709. doi: 10.1016/0024-3205(66)90209-8. [DOI] [PubMed] [Google Scholar]
  18. Morrill G. A., Rosenthal J., Watson D. E. Membrane permeability changes in amphibian eggs at ovulation. J Cell Physiol. 1966 Jun;67(3):375–381. doi: 10.1002/jcp.1040670303. [DOI] [PubMed] [Google Scholar]
  19. Palmer J. F., Slack C. Some bio-electric parameters of early Xenopus embryos. J Embryol Exp Morphol. 1970 Nov;24(3):535–553. [PubMed] [Google Scholar]
  20. Ryman B. E., Whelan W. J. New aspects of glycogen metabolism. Adv Enzymol Relat Areas Mol Biol. 1971;34:285–443. doi: 10.1002/9780470122792.ch6. [DOI] [PubMed] [Google Scholar]
  21. Selman G. G., Perry M. M. Ultrastructural changes in the surface layers of the newt's egg in relation to the mechanism of its cleavage. J Cell Sci. 1970 Jan;6(1):207–227. doi: 10.1242/jcs.6.1.207. [DOI] [PubMed] [Google Scholar]
  22. Slack C., Warner A. E., Warren R. L. The distribution of sodium and potassium in amphibian embryos during early development. J Physiol. 1973 Jul;232(2):297–312. doi: 10.1113/jphysiol.1973.sp010271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. TAYLOR R. E., Jr, BARKER S. B. TRANSEPIDERMAL POTENTIAL DIFFERENCE: DEVELOPMENT IN ANURAN LARVAE. Science. 1965 Jun 18;148(3677):1612–1613. doi: 10.1126/science.148.3677.1612. [DOI] [PubMed] [Google Scholar]
  24. TUFT P. H. The uptake and distribution of water in the embryo of Xenopus laevis (Daudin). J Exp Biol. 1962 Mar;39:1–19. doi: 10.1242/jeb.39.1.1. [DOI] [PubMed] [Google Scholar]
  25. Tuft P. The uptake and distribution of water in the developing amphibian embryo. Symp Soc Exp Biol. 1965;19:385–402. [PubMed] [Google Scholar]
  26. Winne D. Formal kinetics of water and solute absorption with regard to intestinal blood flow. J Theor Biol. 1970 Apr;27(1):1–18. doi: 10.1016/0022-5193(70)90126-8. [DOI] [PubMed] [Google Scholar]
  27. Woodward D. J. Electrical signs of new membrane production during cleavage of Rana pipiens eggs. J Gen Physiol. 1968 Sep;52(3):509–531. doi: 10.1085/jgp.52.3.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Zotin A. I. The uptake and movement of water in embryos. Symp Soc Exp Biol. 1965;19:365–384. [PubMed] [Google Scholar]

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