Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

The electric organ ofDiscopyge tschudii: Its innervated face and the biology of acetylcholinesterase

Summary

  1. 1.

    An ultrastructural, histochemical, and biochemical study of the electric organ of the South American Torpedinid ray,Discopyge tschudii, was carried out.

  2. 2.

    Fine structural cytochemical localization of acetylcholinesterase (AChE) indicated that most of the esterase was associated with the basal lamina. Electron microscopy indicated no marked differences in the electrocyte ultrastructure betweenDiscopyge andTorpedo californica.

  3. 3.

    Discopyge electric organ possessed three molecular forms, two asymmetric forms (16 S and 13 S) and one globular hydrophobic form (6.5 S). The asymmetric 16 S AChE form was solubilized by heparin, a sulfated glycosaminoglycan, suggesting that heparin-like macromolecules are involved in the binding of the enzyme to the basal lamina.

  4. 4.

    Our results show that cell-free translated AChE peptides, synthesized usingDiscopyge electric organ poly (A+) RNA, correspond to a main band of 62,000 daltons which probably represents the catalytic subunit of the asymmetric AChE.

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

References

  1. Aviv, H., and Leder, P. (1972). Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose.Proc. Natl. Acad. Sci. USA 691408–1412.

  2. Bennett, M. V. L. (1971). Electric organs.Fish Physiol. 5347–491.

  3. Bloom, F. E., and Barnett, R. J. (1966). Fine structural localization of acetylcholinesterase in electroplaque of the electric eel.J. Cell Biol. 294750–4795.

  4. Boschi, E., and Fenucci, J. L. (1972). Contribución al conocimiento de la fauna marina del Golfo San José.Physis 31155–167.

  5. Chirgwin, J. M., Przybyla, A. E., MacDonald, R. J., and Rutter, W. J. (1979). Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease.Biochemistry 185294–5299.

  6. Craven, G. R., Steers, E., Jr., and Anfinsen, C. B. (1965). Purification, composition and molecular weight of the B-galactosidase ofEscherichia coli K 12.J. Biol. Chem. 2402468–2477.

  7. De Buén, F. (1959). Lampreas, tiburones, rayas y peces en la Estación de Biología Marina de Montemar, Chile.Rev. Biol. Mar. 93–200.

  8. De Buén, F. (1960). Tiburones, rayas y quimeras en la Estación de Biología Marina de Montemar, Chile.Rev. Biol. Mar. 103–50.

  9. Duguid, J. R., and Raftery, M. A. (1973). Fractionation and partial characterization of membrane particles fromTorpedo californica electroplax.Biochemistry 123593–3597.

  10. Ellman, G. L., Courtney, K. D., Andres, V., Jr., and Featherstone, R. M. (1961). A new and rapid colorimetric determination of AChE activity.Biochem. Pharmacol. 788–95.

  11. Fowler, H. W. (1945). Fishes of Chile. Systematic catalog, Part I.Rev. Chil. Hist. Nat. 45–4722–57.

  12. Fowler, H. W. (1951). Analysis of the fishes of Chile.Rev. Chil. Hist. Nat. 51–53263–326.

  13. Gautron, J. (1974). Cytochimie ultrastructurale des acetylcholinesterases.J. Microsc. 21259–264.

  14. Heuser, J. E., and Salpeter, S. R. (1979). Organization of acetylcholine receptors in quick-frozen, deep-etched, and rotatory-replicatedTorpedo postsynaptic membrane.J. Cell Biol. 82150–173.

  15. Hirokawa, N., and Heuser, J. E. (1982). Internal and external differentiations of the postsynaptic membrane at the neuromuscular junction.J. Neurocytol. 11487–510.

  16. Inestrosa, N. C., and Méndez, B. (1983). The A12 acetylcholinesterase and polypeptide composition of electric organ basal lamina ofElectrophorus and someTorpedinidae fishes.Cell Biochem. Funct. 141–48.

  17. Inestrosa, N. C., Méndez, B., and Luco, J. V. (1979a). Acetylcholinesterase like that of skeletal muscle in smooth muscle reinnervated by a motor nerve.Nature (Lond.) 280504–506.

  18. Inestrosa, N. C., Bronfman, M., and Leighton, F. (1979b). Detection of peroxisomal fatty acyl-coenzyme A oxidase activity.Biochem. J. 182779–788.

  19. Inestrosa, N. C., Silberstein, L., and Hall, Z. W. (1982). Association of the synaptic form of acetylcholinesterase with extracellular matrix in cultured mouse muscle cells.Cell 2971–79.

  20. Karlin, A. (1983). Anatomy of a receptor.Neurosci. Comment. 1111–123.

  21. Karnovsky, M. J., and Roots, L. (1964). A “direct coloring” thiocholine method for cholinesterases.J. Histochem. Cytochem. 12219–221.

  22. Kessler, S. W. (1975). Rapid isolation of antigens from cells with aStaphylococcus protein A-antibody adsorbent.J. Immunol. 1151617–1624.

  23. Kruh, J. (1967). Preparation of RNA from rabbit reticulocytes and liver.Methods Enzymol. 12A609–613.

  24. Laemmli, U. (1970). Cleavage of structural proteins during the assembly of the head bacteriophage T4.Nature (Lond.) 227680–685.

  25. Lee, S. L., Camp, S. J., and Taylor, P. (1982). Characterization of a hydrophobic, dimeric form of acetylcholinesterase fromTorpedo.J. Biol. Chem. 25712302–12309.

  26. Mann, G. (1954).La Vida de los Peces en Aguas Chilenas, Inst. Invest. Veter., Santiago, Chile.

  27. Massoulié, J., and Bon, S. (1982). The molecular forms of cholinesterase and acetylcholinesterase in vertebrates.Annu. Rev. Neurosci. 557–106.

  28. Méndez, B. (1982).Molecular Characterization of the Messenger RNA of Synaptic Proteins from the Electric Organ, Ph.D. thesis, Dept. Cell Biol., Catholic University of Chile, Santiago.

  29. Méndez, B., Valenzuela, P., Martial, J., and Baxter, J. (1980). Cell-free synthesis of acetylcholine receptor polypeptides.Science 209695–697.

  30. Morel, N., and Dreyfus, P. (1982). Association of acetylcholinesterase with the external surface of the presynaptic plasma membrane inTorpedo electric organ.Neurochem. Int. 4283–288.

  31. Norman, J. R. (1937). Coast fishes. II. The Patagonian Region.Discovery Rep. 163–152.

  32. Ochoa, E. L. M. (1979).Discopyge tschudii electric organ acetylcholinesterase: Extraction and demonstration of multiple molecular forms.Comp. Biochem. Physiol. 66C99–103.

  33. Oliver, C. (1943).Levantamiento Biológico de la Provincia de Concepción: Catálogo de los Peces Marinos del Litoral de Concepción y Arauco, Instituto Central de Biología, Universidad de Concepción, Concepción, Chile.

  34. Pelham, H. R. B., and Jackson, R. J. (1976). An efficient mRNA-dependent translation system from reticulocytes lysates.Eur. J. Biochem. 67247–256.

  35. Rosenbluth, J. (1975). Synaptic membrane structure inTorpedo electric organ.J. Neurocytol. 4697–712.

  36. Sealock, R., and Kavookjian, A. (1980). Postsynaptic distribution of acetylcholine receptors in electroplax of the Torpedinidae ray,Narcine brasiliensis.Brain Res. 19081–93.

  37. Sheridan, M. N. (1965). The fine structure of the electric organ ofTorpedo marmorata.J. Cell Biol. 24129–141.

  38. Soreq, H., Parvari, R., and Silman, I. (1982). Biosynthesis and secretion of catalytically active acetylcholinesterase inXenopus oocytes microinjected with mRNA from rat brain and fromTorpedo electric organ.Proc. Natl. Acad. Sci. USA 79830–834.

  39. Torres, J. C., and Inestrosa, N. C. (1983). Heparin solubilizes asymmetric acetylcholinesterase from rat neuromuscular junction.FEBS Lett. 154265–268.

  40. Tschudi, J. J. von (1845). Ichthyologie. InUntersuchungen über die Fauna Peruana (Tschudi, J. J. von, Ed.), Druck and Verlag von Scheitlin und Zollikofer, St. Gallen.

  41. Vigny, M., Martin, G. R., and Grotendorst, G. R. (1983). Interactions of asymmetric forms of acetylcholinesterase with basement membrane components.J. Biol. Chem. 2588794–8798.

  42. Whittaker, V. P. (1977). The electromotor system ofTorpedo as a model cholinergic system.Naturwiss. 64606–611.

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Méndez, B., Garrido, J., Maldonado, M. et al. The electric organ ofDiscopyge tschudii: Its innervated face and the biology of acetylcholinesterase. Cell Mol Neurobiol 4, 125–142 (1984). https://doi.org/10.1007/BF00711000

Download citation

Key words

  • 16 S AChE
  • synaptic basal lamina
  • heparan sulfate proteoglycans
  • cell-free synthesis of AChE
  • electric organ
  • acetylcholinesterase
  • Discopyge tschudii