Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1978 Sep 1;78(3):785–809. doi: 10.1083/jcb.78.3.785

Electron microscope localization of acetylcholinesterase and butyrylcholinesterase in the superior cervical ganglion of the cat. I. Normal ganglion

PMCID: PMC2110197  PMID: 701360

Abstract

The distributions of acetylcholinesterase (AChE) and butyrylcholinesterase (BuChE) in the superior cervical ganglion (SCG) of the cat were determined by electron microscopy (EM) with the bis- (thioacetoxy)aurate (I), or Au(TA)2, method. Before the infusion of fixative, one of the enzymes was selectively, irreversibly inactivated in vivo, as confirmed by light microscope (LM) examination of sections of the stellate ganglion stained by the more specific copper thiocholine method. Physostigmine-treated controls, for inhibition of AChE or BuChE, were stained concomitantly with tissue for enzyme localization by the Au(TA)2 method for EM examination in each experiment. It was concluded that most of the AChE of the cat SCG is present in the plasma membranes of the preganglionic axons and their terminals, and in the dendritic and perikaryonal plasma membranes of the postsynaptic ganglion cells. BuChE is confined largely to the postsynaptic neuronal plasma membranes. Reasons for the discrepancies between the localizations found by the present direct EM observations and those deduced earlier from LM comparisons of normal and denervated SCG are discussed. It is proposed that a trophic factor released by the preganglionic terminals is probably required for the synthesis of postsynaptic neuronal AChE, and that BuChE may serve as a precursor of AChE at that site.

Full Text

The Full Text of this article is available as a PDF (8.0 MB).

Selected References

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

  1. BARRNETT R. J. The fine structural localization of acetylcholinesterase at the myoneural junction. J Cell Biol. 1962 Feb;12:247–262. doi: 10.1083/jcb.12.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BRIGHTMAN M. W., ALBERS R. W. Species differences in the distribution of extraneuronal cholinesterases within the vertebrate central nervous system. J Neurochem. 1959 Aug;4:244–250. doi: 10.1111/j.1471-4159.1959.tb13200.x. [DOI] [PubMed] [Google Scholar]
  3. Bell M., Barrnett R. J. The use of thiol-substituted carboxylic acids as histochemical substrates. J Histochem Cytochem. 1965 Nov-Dec;13(8):611–628. doi: 10.1177/13.8.611. [DOI] [PubMed] [Google Scholar]
  4. Birks R. I. The relationship of transmitter release and storage to fine structure in a sympathetic ganglion. J Neurocytol. 1974 Jun;3(2):133–160. doi: 10.1007/BF01098386. [DOI] [PubMed] [Google Scholar]
  5. CAVANAGH J. B., THOMPSON R. H., WEBSTER G. R. The localization of pseudo-cholinesterase activity in nervous tissue. Q J Exp Physiol Cogn Med Sci. 1954;39(3):185–197. doi: 10.1113/expphysiol.1954.sp001070. [DOI] [PubMed] [Google Scholar]
  6. Davis R., Koelle G. B. Electron microscopic localization of acetylcholinesterase and nonspecific cholinesterase at the neuromuscular junction by the gold-thiocholine and gold-thiolacetic acid methods. J Cell Biol. 1967 Jul;34(1):157–171. doi: 10.1083/jcb.34.1.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Droz B., Koenig H. L., Biamberardino L. D., Di Giamberardino L. Axonal migration of protein and glycoprotein to nerve endings. I. Radioautographic analysis of the renewal of protein in nerve endings of chicken ciliary ganglion after intracerebral injection of (3H)lysine. Brain Res. 1973 Sep 28;60(1):93–127. doi: 10.1016/0006-8993(73)90852-4. [DOI] [PubMed] [Google Scholar]
  8. Esterhuizen A. C., Graham J. D., Lever J. D., Spriggs T. L. Catecholamine and acetylcholinesterase distribution in relation to noradrenaline release. An enzyme histochemical and autoradiographic study on the innervation of the cat nictitating muscle. Br J Pharmacol Chemother. 1968 Jan;32(1):46–56. doi: 10.1111/j.1476-5381.1968.tb00428.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Grillo M. A. Electron microscopy of sympathetic tissues. Pharmacol Rev. 1966 Mar;18(1):387–399. [PubMed] [Google Scholar]
  10. Heuser J. E., Reese T. S. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol. 1973 May;57(2):315–344. doi: 10.1083/jcb.57.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Joó F., Lever J. D., Ivens C., Mottram D. R., Presley R. A fine structural and electron histochemical study of axon terminals in the rat superior cervical ganglion after acute and chronic preganglionic denervation. J Anat. 1971 Nov;110(Pt 2):181–189. [PMC free article] [PubMed] [Google Scholar]
  12. KOELLE G. B., STEINER E. C. The cerebral distributions of a tertiary and a quaternary anticholinesterase agent following intravenous and intraventricular injection. J Pharmacol Exp Ther. 1956 Dec;118(4):420–434. [PubMed] [Google Scholar]
  13. KOELLE G. B. The elimination of enzymatic diffusion artifacts in the histochemical localization of cholinesterases and a survey of their cellular distributions. J Pharmacol Exp Ther. 1951 Oct;103(2):153–171. [PubMed] [Google Scholar]
  14. KOELLE G. B. The histochemical identification of acetylcholinesterase in cholinergic, adrenergic and sensory neurons. J Pharmacol Exp Ther. 1955 Jun;114(2):167–184. [PubMed] [Google Scholar]
  15. KOELLE G. B. The histochemical localization of cholinesterases in the central nervous system of the rat. J Comp Neurol. 1954 Feb;100(1):211–235. doi: 10.1002/cne.901000108. [DOI] [PubMed] [Google Scholar]
  16. KOELLE W. A., KOELLE G. B. The localization of external or functional acetylcholinesterase at the synapses of autonomic ganglia. J Pharmacol Exp Ther. 1959 May;126(1):1–8. [PubMed] [Google Scholar]
  17. KOENIG E., KOELLE G. B. Mode of regeneration of acetylcholinesterase in cholinergic neurons following irreversible inactivation. J Neurochem. 1961 Dec;8:169–188. doi: 10.1111/j.1471-4159.1961.tb13542.x. [DOI] [PubMed] [Google Scholar]
  18. Kasa P. Acetylcholinesterase transport in the central and peripheral nervous tissue: the role of tubules in the enzyme transport. Nature. 1968 Jun 29;218(5148):1265–1267. doi: 10.1038/2181265a0. [DOI] [PubMed] [Google Scholar]
  19. Koelle G. B., Davis R., Devlin M. Acetyl disulfide, (CH3COS)2, and bis-(thioacetoy) aurate (I) complex, Au(CH3CHOS)2,-histochemical substrates of unusual properties with acetylcholinesterase. J Histochem Cytochem. 1968 Dec;16(12):754–764. doi: 10.1177/16.12.754. [DOI] [PubMed] [Google Scholar]
  20. Koelle G. B., Davis R., Diliberto E. J., Jr, Koelle W. A. Selective, near-total, irreversible inactivation of peripheral pseudocholinesterase and acetylcholinesterase in cats in vivo. Biochem Pharmacol. 1974 Jan 15;23(2):175–188. doi: 10.1016/0006-2952(74)90408-0. [DOI] [PubMed] [Google Scholar]
  21. Koelle G. B., Davis R., Koelle W. A. Effects of aldehyde fixation and of preganglionic denervation on acetylcholinesterase and butyrocholinesterase of cat autonomic ganglia. J Histochem Cytochem. 1974 Apr;22(4):244–251. doi: 10.1177/22.4.244. [DOI] [PubMed] [Google Scholar]
  22. Koelle G. B., Davis R., Smyrl E. G., Fine A. V. Refinement of the bis-(thioacetoxy) aurate (I) method for the electron microscopic localization of acetylcholinesterase and nonspecific cholinesterase. J Histochem Cytochem. 1974 Apr;22(4):252–259. doi: 10.1177/22.4.252. [DOI] [PubMed] [Google Scholar]
  23. Koelle G. B., Gromadzki C. G. Comparison of the gold-thiocholine and gold-thiolacetic acid methods for the histochemical localization of acetylcholinesterase and cholinesterases. J Histochem Cytochem. 1966 Jun;14(6):443–454. doi: 10.1177/14.6.443. [DOI] [PubMed] [Google Scholar]
  24. Koelle W. A., Hossaini K. S., Akbarzadeh P., Koelle G. B. Histochemical evidence and consequences of the occurrence of isoenzymes of acetylcholinesterase. J Histochem Cytochem. 1970 Nov;18(11):812–819. doi: 10.1177/18.11.812. [DOI] [PubMed] [Google Scholar]
  25. Koelle W. A., Smyrl E. G., Ruch G. A., Siddons V. E., Koelle G. B. Effect of protection of butyrylcholinesterase on regeneration of ganglionic acetylcholinesterase. J Neurochem. 1977 Feb;28(2):307–311. doi: 10.1111/j.1471-4159.1977.tb07749.x. [DOI] [PubMed] [Google Scholar]
  26. Kása P., Csernovszky E. Electron microscopic localization of acetylcholinesterase in the superior cervical ganglion of the rat. Acta Histochem. 1967;28(2):274–285. [PubMed] [Google Scholar]
  27. LUFT J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. doi: 10.1083/jcb.9.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lakos I. Ultrastructure of chronically denervated superior cervical ganglion in the cat and rat. Acta Biol Acad Sci Hung. 1970;21(4):425–427. [PubMed] [Google Scholar]
  29. Lewis P. R., Shute C. C. An electron-microscopic study of cholinesterase distribution in the rat adrenal medulla. J Microsc. 1969;89(2):181–193. doi: 10.1111/j.1365-2818.1969.tb00664.x. [DOI] [PubMed] [Google Scholar]
  30. Matsuura H., Mori M., Kawakatsu K. A histochemical and electron-microscopic study of the trigeminal ganglion of the rat. Arch Oral Biol. 1969 Oct;14(10):1135–1146. doi: 10.1016/0003-9969(69)90153-8. [DOI] [PubMed] [Google Scholar]
  31. PALADE G. E. A study of fixation for electron microscopy. J Exp Med. 1952 Mar;95(3):285–298. doi: 10.1084/jem.95.3.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pysh J. J., Wiley R. G. Synaptic vesicle depletion and recovery in cat sympathetic ganglia electrically stimulated in vivo. Evidence for transmitter secretion by exocytosis. J Cell Biol. 1974 Feb;60(2):365–374. doi: 10.1083/jcb.60.2.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tucek S. Transport of choline acetyltransferase and acetylcholinesterase in the central stump and isolated segments of a peripheral nerve. Brain Res. 1975 Mar 21;86(2):259–270. doi: 10.1016/0006-8993(75)90701-5. [DOI] [PubMed] [Google Scholar]
  34. WOLLEMANN M., ZOLTAN L. Cholinesterase activity of cerebral tumors and tumorous cysts. Arch Neurol. 1962 Feb;6:161–167. doi: 10.1001/archneur.1962.00450200075007. [DOI] [PubMed] [Google Scholar]
  35. Westrum L. E., Broderson S. H. Acetylcholinesterase activity of synaptic structures in the spinal trigeminal nucleus. J Neurocytol. 1976 Oct;5(8):551–563. doi: 10.1007/BF01175569. [DOI] [PubMed] [Google Scholar]

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

RESOURCES