Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1976 Apr 1;69(1):19–28. doi: 10.1083/jcb.69.1.19

Structural complexes in the squid giant axon membrane sensitive to ionic concentrations and cardiac glycosides

GM Villegas, J Villegas
PMCID: PMC2110964  PMID: 1254642

Abstract

Giant nerve fibers of squid Sepioteuthis sepiodea were incubated for 10 min in artificial sea water (ASW) under control conditions, in the absence of various ions, and in the presence of cardiac glycosides. The nerve fibers were fixed in OsO(4) and embedded in Epon, and structural complexes along the axolemma were studied. These complexes consist of a portion of axolemma exhibiting a three-layered substructure, an undercoating of a dense material (approximately 0.1μm in length and approximately 70-170 A in thickness), and a narrowing to disappearance of the axon-Schwann cell interspace. In the controls, the incidence of complexes per 1,000μm of axon perimeter was about 137. This number decreased to 10-25 percent when magnesium was not present in the incubating media, whatever the calcium concentration (88, 44, or 0 mM). In the presence of magnesium, the number and structural features of the complexes were preserved, though the number decreased to 65 percent when high calcium was simultaneously present. The complexes were also modified and decreased to 26-32 percent by incubating the nerves in solutions having low concentrations of sodium and potassium. The adding of 10(-5) M ouabain or strophanthoside to normal ASW incubating solution decreased them to 20-40 percent. Due to their sensitivity to changes in external ionic concentrations and to the presence of cardiac glycosides, the complexes are proposed to represent the structural correlate of specialized sites for active ion transport, although other factors may be involved.

Full Text

The Full Text of this article is available as a PDF (1.8 MB).

Selected References

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

  1. ANDRES K. H. UBER DIE FEINSTRUKTUR BESONDERER EINRICHTUNGEN IN MARKHALTIGEN NERVENFASERN DES KLEINHIRNS DER RATTE. Z Zellforsch Mikrosk Anat. 1965 Feb 24;65:701–712. [PubMed] [Google Scholar]
  2. BAKER P. F., HODGKIN A. L., SHAW T. I. Replacement of the axoplasm of giant nerve fibres with artificial solutions. J Physiol. 1962 Nov;164:330–354. doi: 10.1113/jphysiol.1962.sp007025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. ELFVIN L. G. The ultrastructure of the nodes of Ranvier in cat sympathetic nerve fibers. J Ultrastruct Res. 1961 Aug;5:374–387. doi: 10.1016/s0022-5320(61)80014-2. [DOI] [PubMed] [Google Scholar]
  4. GRAY E. G. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat. 1959 Oct;93:420–433. [PMC free article] [PubMed] [Google Scholar]
  5. Goodenough D. A., Revel J. P. A fine structural analysis of intercellular junctions in the mouse liver. J Cell Biol. 1970 May;45(2):272–290. doi: 10.1083/jcb.45.2.272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hillman D. E., Llinás R. Calcium-containing electron-dense structures in the axons of the squid giant synapse. J Cell Biol. 1974 Apr;61(1):146–155. doi: 10.1083/jcb.61.1.146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. PALAY S. L. The morphology of synapses in the central nervous system. Exp Cell Res. 1958;14(Suppl 5):275–293. [PubMed] [Google Scholar]
  8. Palay S. L., Sotelo C., Peters A., Orkand P. M. The axon hillock and the initial segment. J Cell Biol. 1968 Jul;38(1):193–201. doi: 10.1083/jcb.38.1.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Pappas G. D., Asada Y., Bennett M. V. Morphological correlates of increased coupling resistance at an electrotonic synapse. J Cell Biol. 1971 Apr;49(1):173–188. doi: 10.1083/jcb.49.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Peracchia C. Low resistance junctions in crayfish. II. Structural details and further evidence for intercellular channels by freeze-fracture and negative staining. J Cell Biol. 1973 Apr;57(1):54–65. doi: 10.1083/jcb.57.1.54. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Peracchia C., Robertson J. D. Increase in osmiophilia of axonal membranes of crayfish as a result of electrical stimulation, asphyxia, or treatment with reducing agents. J Cell Biol. 1971 Oct;51(1):223–239. doi: 10.1083/jcb.51.1.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Peters A. The node of Ranvier in the central nervous system. Q J Exp Physiol Cogn Med Sci. 1966 Jul;51(3):229–236. doi: 10.1113/expphysiol.1966.sp001852. [DOI] [PubMed] [Google Scholar]
  13. Revel J. P., Karnovsky M. J. Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J Cell Biol. 1967 Jun;33(3):C7–C12. doi: 10.1083/jcb.33.3.c7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Sabatini M. T., Dipolo R., Villegas R. Adenosine triphosphatase activity in the membranes of the squid nerve fiber. J Cell Biol. 1968 Jul;38(1):176–183. doi: 10.1083/jcb.38.1.176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Schatzmann H. J., Rossi G. L. (Ca 2+ + Mg 2+ )-activated membrane ATPases in human red cells and their possible relations to cation transport. Biochim Biophys Acta. 1971 Aug 13;241(2):379–392. doi: 10.1016/0005-2736(71)90037-x. [DOI] [PubMed] [Google Scholar]
  16. Sloper J. J., Powell T. P. Observations on the axon initial segment and other structures in the neocortex using conventional staining and ethanolic phosphotungstic acid. Brain Res. 1973 Feb 14;50(1):163–169. doi: 10.1016/0006-8993(73)90602-1. [DOI] [PubMed] [Google Scholar]
  17. Sotelo C., Llinás R. Specialized membrane junctions between neurons in the vertebrate cerebellar cortex. J Cell Biol. 1972 May;53(2):271–289. doi: 10.1083/jcb.53.2.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Villegas G. M. Electron microscopic study of the giant nerve fiber of the giant squid Dosidicus gigas. J Ultrastruct Res. 1969 Mar;26(5):501–504. doi: 10.1016/s0022-5320(69)90054-9. [DOI] [PubMed] [Google Scholar]
  19. Villegas G. M., Villegas J. Acetylcholinesterase localization in the giant nerve fiber of the squid. J Ultrastruct Res. 1974 Jan;46(1):149–163. doi: 10.1016/s0022-5320(74)80028-6. [DOI] [PubMed] [Google Scholar]
  20. Villegas G. M., Villegas R. Ultrastructural studies of the squid nerve fibers. J Gen Physiol. 1968 May;51(5 Suppl):44S+–44S+. [PubMed] [Google Scholar]
  21. Villegas J. Axon-Schwann cell interaction in the squid nerve fibre. J Physiol. 1972 Sep;225(2):275–296. doi: 10.1113/jphysiol.1972.sp009940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Villegas J. Effects of tubocurarine and eserine on the axon-Schwann cell relationship in the squid nerve fibre. J Physiol. 1973 Jul;232(1):193–208. doi: 10.1113/jphysiol.1973.sp010264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Villegas J., Villegas R., Giménez M. Nature of the Schwann cell electrical potential. Effects of the external ionic concentrations and a cardiac glycoside. J Gen Physiol. 1968 Jan;51(1):47–64. doi: 10.1085/jgp.51.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES