Skip to main content
SpringerLink
Log in

Possible role of “prenervous” neurotransmitters in cellular interactions of early embryogenesis: A hypothesis

  • Original Articles
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Evidence is presented in support of the working hypothesis that “prenervous” neurotransmitters directly participate in cell-cell interactions occurring during the first several cleavage divisions of sea urchin embryos, a function which may occur during the early development of higher animals as well. This intercellular signaling could be a link in the evolutionary progression from the use of these substances as intracellular regulators to their participation in cell-cell interactions occurring during synaptic transmission.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Baker, P. C. andQuay, W. B. 1969. 5-Hydroxytryptamine metabolism in early embryogenesis. Brain Res. 12:273–295.

    PubMed  Google Scholar 

  2. Bennett, M. V. L. 1978. Junctional permeability. Pages 25–36,in Feldman, J., Gilula, N. B., andPitts, J. D. (eds.), Intercellular Junctions and Development, Chapman and Hall, London.

    Google Scholar 

  3. Bennett, M. V. L., Spira, M. E., andSpray, D. C. 1978. Permeability of gap junctions between embryonic cells ofFundulus—reevaluation. Dev. Biol. 65:114–125.

    PubMed  Google Scholar 

  4. Blum, J. J. 1970. Biogenic amines and metabolic control in Tetrahymena. Pages 95–118,in Blum, J. J. (ed.), Biogenic Amines as Physiological Regulators, Prentice-Hall, New Jersey.

    Google Scholar 

  5. Bozhkova, V. P., Kvavilashvili, I. S., Rott, N. N., andChailakhyan, L. M. 1974. The correlation between the periods of cyclic changes in the membrane electrical characteristics and the phases of cyto-and karyokinesis in dividing eggs of the loach and the axolotl. Tsitologiya 16:709–716.

    Google Scholar 

  6. Burden, H. W., andLawrence, I. E. 1973. Presence of biogenic amines in early rat development. Am. J. Anat. 136:251–257.

    PubMed  Google Scholar 

  7. Buznikov, G. A. 1967. The Low-Molecular Weight Regulators of Embryonic Development. Nauka, Moscow.

    Google Scholar 

  8. Buznikov, G. A. 1971. The role of neurotransmitters in individual development. Ontogenez 2:5–13.

    Google Scholar 

  9. Buznikov, G. A. 1973. 5-hydroxytryptamine, catecholamines, acetylcholine, and some related substances in early embryogenesis. Pages 593–623,in Michelson, M. J. (ed.), Comparative Pharmacology, Vol. 2, Pergamon Press, London.

    Google Scholar 

  10. Buznikov, G. A., Kost, A. N., Kucherova, N. F., Mndzhoyan, A. L., Suvorov, N. R., andBerdycheva, L. V. 1979. The role of neurohumours in early embryogenesis: III. Pharmacological analysis of the role of neurohumours in cleavage divisions. J. Embryol. Exp. Morphol. 23:343–569.

    Google Scholar 

  11. Buznikov, G. A., Manukhin, B. N., Rakic, L., Aroyan, A. A., Kucherova, N. F., andSuvorov, N. N. 1975. On the mechanism of protective action of acetylcholine and serotonin against their cytotoxic antagonists. Zh. Evol. Biokhim. Fisiol. 11: 128–133.

    Google Scholar 

  12. Buznikov, G. A., Rakic, L., Turpaev, T. M., andMarkova, L. N. 1974. Sensitivity of sea urchin embryos to antagonists of acetylcholine and monamines. Exp. Cell Res. 86:317–324.

    PubMed  Google Scholar 

  13. Buznikov, G. A., Sakharova, A. V., Manukhin, B. N., andMarkova, L. V. 1972. The role of neurohumours in early embryogenesis: IV. Fluorometric and histochemical study of serotonin in cleaving eggs and larvae of sea urchins. J. Embryol. Exp. Morphol. 27:339–351.

    PubMed  Google Scholar 

  14. Buznikov, G. A., andShmukler, Yu. B. 1978. The influence of drugs-antimediators on the intercellular connections in early sea urchin embryos. Ontogenez 9:173–178.

    PubMed  Google Scholar 

  15. Dan-Sohkawa, M., andSatoh, N. 1978. Studies on dwarf larvae developed from isolated blastomeres of the starfish,Asterina pectinifera. J. Embryol. Exp. Morphol. 46:171–185.

    PubMed  Google Scholar 

  16. Deuchar, E. M. 1974. Cellular Interactions in Animal Development, Halsted Press, New York.

    Google Scholar 

  17. Ducibella, T., andAnderson, E. 1975. Cell shape and membrane changes in the eight-cell mouse embryo: Prerequisites for the morphogenesis of the blastocyst. Dev. Biol. 47:45–58.

    PubMed  Google Scholar 

  18. Emanuelsson, H. 1974. Localization of serotonin in cleavage embryos ofOphryotrocha Labronica La Greca and Bacci. Wilhelm Roux Arch. 175:253–271.

    Google Scholar 

  19. Fluck, R. A. 1978. Acetylcholine and acetylcholinesterase activity in the early embryos of the madakaCryzias latipes, a teleost. Dev. Growth Differ. 20: 17–26.

    Google Scholar 

  20. Gilula, N. B. 1978. Structure of intercellular junctions. Pages 3–22,in Feldman, J., Gilula, N. B., andPitts, J. D. (eds.), Intercellular Junctions and Development, Chapman and Hall, London.

    Google Scholar 

  21. Giudice, G. 1973. Developmental Biology of the Sea Urchin Embryo, Academic Press, New York.

    Google Scholar 

  22. Goodenough, D. A., Ito, S., andRevel, J. P. 1968. Electron microscopy of early cleavage stages inArbacia punctulata. Biol. Bull. 135:420–421.

    Google Scholar 

  23. Gustafson, T., andToneby, M. 1970. On the role of serotonin and acetylcholine in sea urchin morphogenesis. Exp. Cell Res. 62:102–117.

    PubMed  Google Scholar 

  24. Hagiwara, S., andMiyazaki, S. 1977. Changes in excitability of the cell membrane during “differentiation without cleavage” in the egg of the annelid,Chaetopterus pergamentaceus. J. Physiol. (London) 272:197–216.

    Google Scholar 

  25. Iwata, H., Kariya, K., andWada, Y. 1973. Adrenergic mechanism inTetrahymena: II. Effect of adrenaline on cell proliferation. Jpn. J. Pharmacol. 23:681–688.

    PubMed  Google Scholar 

  26. Jaffe, L. A., andRobinson, K. R. 1978. Membrane potential of the unfertilized sea urchin egg. Dev. Biol. 62:215–228.

    PubMed  Google Scholar 

  27. Janakidevi, K., Dewey, V. C., andKidder, G. W. 1966. Serotonin in Protozoa. Arch. Biochem. Biophy. 113:758–759.

    Google Scholar 

  28. Janakidevi, K., Dewey, V. C., andKidder, G. W. 1966. The biosynthesis of catecholamines in two genera of Protozoa. J. Biol. Chem. 241:2577–2578.

    Google Scholar 

  29. Kusano, K., Miledi, R., andStinnakre, J. 1977. Acetylcholine receptors in the oocyte membrane. Nature 270:739–741.

    PubMed  Google Scholar 

  30. Kusano, K., Miledi, R., andStinnakre, J. 1978. Neurotransmitter receptors in theXenopus oocyte membrane. Biol. Cell 32:7–8.

    Google Scholar 

  31. Loewenstein, W. R. 1974. Cellular communication by permeable membrane junctions. Hosp. Pract. 11:113.

    Google Scholar 

  32. Manukhin, B. N., Volina, E. V., Markova, L. N., Rakic, L., andBuznikov, G. A. 1980. New data on the biogenic monamines of developing sea urchin embryos. Zh. Evol. Biokhim. Fisiol. (in press).

  33. McMahon, D. 1974. Chemical messengers in development: A hypothesis. Science 185:1012–1021.

    PubMed  Google Scholar 

  34. Okamoto, H., Takahashi, K., andYamashita, N. 1977. Ionic currents through the membrane of the mammalian oocyte and their comparison with those in the tunicate and sea urchin. J. Physiol. (London) 267:465–495.

    Google Scholar 

  35. Powers, R. D., andTupper, J. T. 1977. Intercellular communication in the early embryo. Pages 231–251,in De Mello, W. C. (ed.),Intercellular Communication, Plenum Press, New York.

    Google Scholar 

  36. Richards, J. G. 1978. Permeability of intercellular junctions in brain epithelia and endothelia to exogenous amine. J. Neurocytol. 7:61–70.

    PubMed  Google Scholar 

  37. Sanders, E. J., andDicaprio, R. A. 1976. Intercellular junctions in theXenopus embryo prior to gastrulation. J. Exp. Zool. 197:415–422.

    PubMed  Google Scholar 

  38. Shen, S., andSteinhardt, R. A. 1976. An electrophysiological study of the membrane properties of the immature and mature oocyte of the batstar,Patiria miniata. Dev. Biol. 48:148–162.

    PubMed  Google Scholar 

  39. Sheridan, J. D. 1976. Cell coupling and cell communication during embryogenesis. Pages 409–447,in Poste, G., andNicolson, G. L. (eds.), The Cell Surface in Animal Embryogenesis and Development, North Holland, Amsterdam.

    Google Scholar 

  40. Sullivan, W. D., andSullivan, C. F. 1964. The acetylcholine content and the effects of hexamethonium bromide on this compound at the various phases of division inTetrahymena pyriformis G1. Broteria, Cienc. Natur. 33:17–33.

    Google Scholar 

  41. Toneby, M. 1977. Functional aspects of 5-hydroxytryptamine and dopamine in early embryogenesis of Echinoidea and Asteroidea. University of Stockholm, Stockholm, Sweden.

    Google Scholar 

  42. Tupper, J. T., andSaunders, J. W. 1972. Intercellular permeability in the early Asterias embryo. Dev. Biol. 27:546–557.

    Google Scholar 

  43. Vacquier, V. D. 1968. The connection of blastomeres of sea urchin embryos by filopodia. Exp. Cell Res. 52:571–581.

    PubMed  Google Scholar 

  44. Vacquier, V. D., andMazia, D. 1968. Twinning of sand dollar embryos by means of dithiothreitol: The structural basis of blastomere interactions. Exp. Cell. Res. 52:209–221.

    PubMed  Google Scholar 

  45. Vacquier, V. D., andMazia, D. 1968. Twinning of sea urchin embryos by treatment with dithiothreitol: Roles of cell surface interactions and of the hyaline layer. Exp. Cell Res. 52:459–468.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. N. K. Koltzov Institute of Developmental Biology, USSR Academy of Sciences, Moscow, U.S.S.R.

    G. A. Buznikov & Yu. B. Shmukler

Authors
  1. G. A. Buznikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu. B. Shmukler
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buznikov, G.A., Shmukler, Y.B. Possible role of “prenervous” neurotransmitters in cellular interactions of early embryogenesis: A hypothesis. Neurochem Res 6, 55–68 (1981). https://doi.org/10.1007/BF00963906

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00963906

Keywords

Search

Navigation