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. 1989 Jun 1;108(6):2301–2311. doi: 10.1083/jcb.108.6.2301

Differences in structure and distribution of the molecular forms of acetylcholinesterase

PMCID: PMC2115618  PMID: 2472404

Abstract

Two structurally distinct molecular forms of acetylcholinesterase are found in the electric organs of Torpedo californica. One form is dimensionally asymmetric and composed of heterologous subunits. The other form is hydrophobic and composed of homologous subunits. Sequence- specific antibodies were raised against a synthetic peptide corresponding to the COOH-terminal region (Lys560-Leu575) of the catalytic subunits of the asymmetric form of acetylcholinesterase. These antibodies reacted with the asymmetric form of acetylcholinesterase, but not with the hydrophobic form. These results confirm recent studies suggesting that the COOH-terminal domain of the asymmetric form differs from that of the hydrophobic form, and represent the first demonstration of antibodies selective for the catalytic subunits of the asymmetric form. In addition, the reactive epitope of a monoclonal antibody (4E7), previously shown to be selective for the hydrophobic form of acetylcholinesterase, has been identified as an N-linked complex carbohydrate, thus defining posttranslational differences between the two forms. These two form- selective antibodies, as well as panselective polyclonal and monoclonal antibodies, were used in light and electron microscopic immunolocalization studies to investigate the distribution of the two forms of acetylcholinesterase in the electric organ of Torpedo. Both forms were localized almost exclusively to the innervated surface of the electrocytes. However, they were differentially distributed along the innervated surface. Specific asymmetric-form immunoreactivity was restricted to areas of synaptic apposition and to the invaginations of the postsynaptic membrane that form the synaptic gutters. In contrast, immunoreactivity attributable to the hydrophobic form was selectively found along the non-synaptic surface of the nerve terminals and was not observed in the synaptic cleft or in the invaginations of the postsynaptic membrane. This differential distribution suggests that the two forms of acetylcholinesterase may play different roles in regulating the local concentration of acetylcholine in the synapse.

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Selected References

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  1. Bon S., Méflah K., Musset F., Grassi J., Massoulié J. An immunoglobulin M monoclonal antibody, recognizing a subset of acetylcholinesterase molecules from electric organs of Electrophorus and Torpedo, belongs to the HNK-1 anti-carbohydrate family. J Neurochem. 1987 Dec;49(6):1720–1731. doi: 10.1111/j.1471-4159.1987.tb02429.x. [DOI] [PubMed] [Google Scholar]
  2. Brimijoin S., Rakonczay Z. Immunology and molecular biology of the cholinesterases: current results and prospects. Int Rev Neurobiol. 1986;28:363–410. doi: 10.1016/s0074-7742(08)60112-9. [DOI] [PubMed] [Google Scholar]
  3. Doctor B. P., Camp S., Gentry M. K., Taylor S. S., Taylor P. Antigenic and structural differences in the catalytic subunits of the molecular forms of acetylcholinesterase. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5767–5771. doi: 10.1073/pnas.80.18.5767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Gibney G., MacPhee-Quigley K., Thompson B., Vedvick T., Low M. G., Taylor S. S., Taylor P. Divergence in primary structure between the molecular forms of acetylcholinesterase. J Biol Chem. 1988 Jan 25;263(3):1140–1145. [PubMed] [Google Scholar]
  5. Kushner P. D., Stephenson D. T., Sternberg H., Weber R. Monoclonal antibody Tor 23 recognizes a determinant of a presynaptic acetylcholinesterase. J Neurochem. 1987 Jun;48(6):1942–1953. doi: 10.1111/j.1471-4159.1987.tb05759.x. [DOI] [PubMed] [Google Scholar]
  6. Lee S. L., Camp S. J., Taylor P. Characterization of a hydrophobic, dimeric form of acetylcholinesterase from Torpedo. J Biol Chem. 1982 Oct 25;257(20):12302–12309. [PubMed] [Google Scholar]
  7. Lee S. L., Heinemann S., Taylor P. Structural characterization of the asymmetric (17 + 13) S forms of acetylcholinesterase from Torpedo. I. Analysis of subunit composition. J Biol Chem. 1982 Oct 25;257(20):12282–12291. [PubMed] [Google Scholar]
  8. Lee S. L., Taylor P. Structural characterization of the asymmetric (17 + 13) S species of acetylcholinesterase from Torpedo. II. Component peptides obtained by selective proteolysis and disulfide bond reduction. J Biol Chem. 1982 Oct 25;257(20):12292–12301. [PubMed] [Google Scholar]
  9. Li Z. Y., Bon C. Presence of a membrane-bound acetylcholinesterase form in a preparation of nerve endings from Torpedo marmorata electric organ. J Neurochem. 1983 Feb;40(2):338–349. doi: 10.1111/j.1471-4159.1983.tb11288.x. [DOI] [PubMed] [Google Scholar]
  10. Lindstrom J. Immunological studies of acetylcholine receptors. J Supramol Struct. 1976;4(3):389–403. doi: 10.1002/jss.400040310. [DOI] [PubMed] [Google Scholar]
  11. MacPhee-Quigley K., Taylor P., Taylor S. Primary structures of the catalytic subunits from two molecular forms of acetylcholinesterase. A comparison of NH2-terminal and active center sequences. J Biol Chem. 1985 Oct 5;260(22):12185–12189. [PubMed] [Google Scholar]
  12. Massoulié J., Bon S. The molecular forms of cholinesterase and acetylcholinesterase in vertebrates. Annu Rev Neurosci. 1982;5:57–106. doi: 10.1146/annurev.ne.05.030182.000421. [DOI] [PubMed] [Google Scholar]
  13. Morel N., Manaranche R., Israël M., Gulik-Krzywicki T. Isolation of a presynaptic plasma membrane fraction from Torpedo cholinergic synaptosomes: evidence for a specific protein. J Cell Biol. 1982 May;93(2):349–356. doi: 10.1083/jcb.93.2.349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Rosenbluth J. Synaptic membrane structure in Torpedo electric organ. J Neurocytol. 1975 Dec;4(6):697–712. doi: 10.1007/BF01181631. [DOI] [PubMed] [Google Scholar]
  15. SHERIDAN M. N. THE FINE STRUCTURE OF THE ELECTRIC ORGAN OF TORPEDO MARMORATA. J Cell Biol. 1965 Jan;24:129–141. doi: 10.1083/jcb.24.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Schumacher M., Camp S., Maulet Y., Newton M., MacPhee-Quigley K., Taylor S. S., Friedmann T., Taylor P. Primary structure of Torpedo californica acetylcholinesterase deduced from its cDNA sequence. 1986 Jan 30-Feb 5Nature. 319(6052):407–409. doi: 10.1038/319407a0. [DOI] [PubMed] [Google Scholar]
  17. Schumacher M., Maulet Y., Camp S., Taylor P. Multiple messenger RNA species give rise to the structural diversity in acetylcholinesterase. J Biol Chem. 1988 Dec 15;263(35):18979–18987. [PubMed] [Google Scholar]
  18. Sikorav J. L., Duval N., Anselmet A., Bon S., Krejci E., Legay C., Osterlund M., Reimund B., Massoulié J. Complex alternative splicing of acetylcholinesterase transcripts in Torpedo electric organ; primary structure of the precursor of the glycolipid-anchored dimeric form. EMBO J. 1988 Oct;7(10):2983–2993. doi: 10.1002/j.1460-2075.1988.tb03161.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sikorav J. L., Grassi J., Bon S. Synthesis in vitro of precursors of the catalytic subunits of acetylcholinesterase from Torpedo marmorata and Electrophorus electricus. Eur J Biochem. 1984 Dec 17;145(3):519–524. doi: 10.1111/j.1432-1033.1984.tb08587.x. [DOI] [PubMed] [Google Scholar]

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