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. 1975 Mar 1;65(3):255–273. doi: 10.1085/jgp.65.3.255

Metabolism of acetylcholine in the nervous system of Aplysia californica. I. Source of choline and its uptake by intact nervous tissue

PMCID: PMC2214879  PMID: 1117282

Abstract

Although acetylcholine is a major neurotransmitter in Aplysia, labeling studies with methionine and serine showed that little choline was synthesized by nervous tissue and indicated that the choline required for the synthesis of acetylcholine must be derived exogenously. Aanglia in the central nervous system (abdominal, cerebral, and pleuropedals) all took up about 0.5 nmol of choline per hour at 9 muM, the concentration of choline we found in hemolymph. This rate was more than two orders of magnitude greater than that of synthesis from the labeled precursors. Ganglia accumulated choline by a process which has two kinetic components, one with a Michaelis constant between 2-8 muM. The other component was not saturated at 420 muM. Presumably the process with the high affinity functions to supply choline for synthesis of transmitter, since the efficiency of conversion to acetylcholine was maximal in the range of external concentrations found in hemolymph.

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Selected References

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  1. APPLETON H. D., LA DU B. N., Jr, LEVY B., STEELE J. M., BRODIE B. B. A chemical method for the determination of free choline in plasma. J Biol Chem. 1953 Dec;205(2):803–813. [PubMed] [Google Scholar]
  2. Ambron R. T., Goldman J. E., Schwartz J. H. Axonal transport of newly synthesized glycoproteins in a single identified neuron of Aplysia californica. J Cell Biol. 1974 Jun;61(3):665–675. doi: 10.1083/jcb.61.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ambron R. T., Pieringer R. A. The metabolism of glyceride glycolipids. V. Identification of the membrane lipid formed from diglucosyl diglyceride in Streptococcus faecalis ATCC 9790 as an acylated derivative of glyceryl phosphoryl diglucosyl glycerol. J Biol Chem. 1971 Jul 10;246(13):4216–4225. [PubMed] [Google Scholar]
  4. Ansell G. B., Spanner S. Studies on the origin of choline in the brain of the rat. Biochem J. 1971 May;122(5):741–750. doi: 10.1042/bj1220741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ansell G. B., Spanner S. The metabolism of [Me-14C]choline in the brain of the rat in vivo. Biochem J. 1968 Nov;110(2):201–206. doi: 10.1042/bj1100201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ansell G. B., Spanner S. The metabolism of labelled ethanolamine in the brain of the rat in vivo. J Neurochem. 1967 Sep;14(9):873–885. doi: 10.1111/j.1471-4159.1967.tb09576.x. [DOI] [PubMed] [Google Scholar]
  7. BLIGH J. The level of free choline in plasma. J Physiol. 1952 Jun;117(2):234–240. doi: 10.1113/jphysiol.1952.sp004743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. BREMER J., GREENBERG D. M. Biosynthesis of choline in vitro. Biochim Biophys Acta. 1960 Jan 1;37:173–175. doi: 10.1016/0006-3002(60)90104-9. [DOI] [PubMed] [Google Scholar]
  9. Bennett J. P., Jr, Logan W. J., Snyder S. H. Amino acids as central nervous transmitters: the influence of ions, amino acid analogues, and ontogeny on transport systems for L-glutamic and L-aspartic acids and glycine into central nervous synaptosomes of the rat. J Neurochem. 1973 Dec;21(6):1533–1550. doi: 10.1111/j.1471-4159.1973.tb06037.x. [DOI] [PubMed] [Google Scholar]
  10. Carew T. J., Pinsker H., Rubinson K., Kandel E. R. Physiological and biochemical properties of neuromuscular transmission between identified motoneurons and gill muscle in Aplysia. J Neurophysiol. 1974 Sep;37(5):1020–1040. doi: 10.1152/jn.1974.37.5.1020. [DOI] [PubMed] [Google Scholar]
  11. Collier B., Lang C. The metabolism of choline by a sympathetic ganglion. Can J Physiol Pharmacol. 1969 Feb;47(2):119–126. doi: 10.1139/y69-022. [DOI] [PubMed] [Google Scholar]
  12. Diamond I., Kennedy E. P. Carrier-mediated transport of choline into synaptic nerve endings. J Biol Chem. 1969 Jun 25;244(12):3258–3263. [PubMed] [Google Scholar]
  13. Dowdall M. J., Simon E. J. Comparative studies on synaptosomes: uptake of (N-Me-3H)choline by synaptosomes from squid optic lobes. J Neurochem. 1973 Oct;21(4):969–982. doi: 10.1111/j.1471-4159.1973.tb07541.x. [DOI] [PubMed] [Google Scholar]
  14. Eisenstadt M. L., Schwartz J. H. Metabolism of acetylcholine in the nervous system of Aplysia californica. III. Studies of an indentified cholinergic neuron. J Gen Physiol. 1975 Mar;65(3):293–213. doi: 10.1085/jgp.65.3.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Eisenstadt M. L., Treistman S. N., Schwartz J. H. Metabolism of acetylcholine in the nervous system of Aplysia californica. II. Reginal localization and characterization of choline uptake. J Gen Physiol. 1975 Mar;65(3):275–291. doi: 10.1085/jgp.65.3.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Eisenstadt M., Goldman J. E., Kandel E. R., Koike H., Koester J., Schwartz J. H. Intrasomatic injection of radioactive precursors for studying transmitter synthesis in identified neurons of Aplysia californica. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3371–3375. doi: 10.1073/pnas.70.12.3371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. FOLCH J., LEES M., SLOANE STANLEY G. H. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957 May;226(1):497–509. [PubMed] [Google Scholar]
  18. Giller E., Jr, Schwartz J. H. Acetylcholinesterase in identified neurons of abdominal ganglion of Aplysia californica. J Neurophysiol. 1971 Jan;34(1):108–115. doi: 10.1152/jn.1971.34.1.108. [DOI] [PubMed] [Google Scholar]
  19. Haga T., Noda H. Choline uptake systems of rat brain synaptosomes. Biochim Biophys Acta. 1973 Jan 26;291(2):564–575. doi: 10.1016/0005-2736(73)90508-7. [DOI] [PubMed] [Google Scholar]
  20. Hille B. The permeability of the sodium channel to organic cations in myelinated nerve. J Gen Physiol. 1971 Dec;58(6):599–619. doi: 10.1085/jgp.58.6.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Illingworth D. R., Portman O. W. The uptake and metabolism of plasma lysophosphatidylcholine in vivo by the brain of squirrel monkeys. Biochem J. 1972 Nov;130(2):557–567. doi: 10.1042/bj1300557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Koike H., Eisenstadt M., Schwartz J. H. Axonal transport of newly synthesized acetylcholine in an identified neuron of Aplysia. Brain Res. 1972 Feb 11;37(1):152–159. doi: 10.1016/0006-8993(72)90359-9. [DOI] [PubMed] [Google Scholar]
  23. Komai Y., Matsukawa S., Satake M. Lipid composition of the nervous tissue of the invertebrates Aplysia kurodai (gastropod) and Cambarus clarki (arthropod). Biochim Biophys Acta. 1973 Sep 25;316(3):271–281. [PubMed] [Google Scholar]
  24. Kuhar M. J., Sethy V. H., Roth R. H., Aghajanian G. K. Choline: selective accumulation by central cholinergic neurons. J Neurochem. 1973 Feb;20(2):581–593. doi: 10.1111/j.1471-4159.1973.tb12157.x. [DOI] [PubMed] [Google Scholar]
  25. MARINETTI G. V., ERBLAND J., KOCHEN J. Quantitative chromatography of phosphatides. Fed Proc. 1957 Sep;16(3):837–844. [PubMed] [Google Scholar]
  26. Martin K. Concentrative accumulation of choline by human erythrocytes. J Gen Physiol. 1968 Apr;51(4):497–516. doi: 10.1085/jgp.51.4.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McCaman R. E., Weinreich D., Borys H. Endogenous levels of acetylcholine and choline in individual neurons of Aplysia. J Neurochem. 1973 Aug;21(2):473–476. doi: 10.1111/j.1471-4159.1973.tb04267.x. [DOI] [PubMed] [Google Scholar]
  28. Neal J. L. Analysis of Michaelis kinetics for two independent, saturable membrane transport functions. J Theor Biol. 1972 Apr;35(1):113–118. doi: 10.1016/0022-5193(72)90196-8. [DOI] [PubMed] [Google Scholar]
  29. Schwartz J. H., Castellucci V. F., Kandel E. R. Functioning of identified neurons and synapses in abdominal ganglion of Aplysia in absence of protein synthesis. J Neurophysiol. 1971 Nov;34(6):939–953. doi: 10.1152/jn.1971.34.6.939. [DOI] [PubMed] [Google Scholar]
  30. Shaskan E. G., Snyder S. H. Kinetics of serotonin accumulation into slices from rat brain: relationship to catecholamine uptake. J Pharmacol Exp Ther. 1970 Nov;175(2):404–418. [PubMed] [Google Scholar]
  31. Shaw F. H. The estimation of choline and acetylcholine. Biochem J. 1938 Jun;32(6):1002–1007. doi: 10.1042/bj0321002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Toru M., Aprison M. H. Brain acetylcholine studies: a new extraction procedure. J Neurochem. 1966 Dec;13(12):1533–1544. doi: 10.1111/j.1471-4159.1966.tb04318.x. [DOI] [PubMed] [Google Scholar]
  33. Yamamura H. I., Snyder S. H. Choline: high-affinity uptake by rat brain synaptosomes. Science. 1972 Nov 10;178(4061):626–628. doi: 10.1126/science.178.4061.626. [DOI] [PubMed] [Google Scholar]

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