Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1990 Jan;420:387–408. doi: 10.1113/jphysiol.1990.sp017919

Evidence for the uptake of neuronally derived choline by glial cells in the leech central nervous system.

W A Wuttke 1, V W Pentreath 1
PMCID: PMC1190056  PMID: 2324991

Abstract

1. With ion-sensitive microelectrodes based on the Corning exchanger 477317, the accumulation of an unidentified interfering substance was monitored in leech neuropile glial cells but not in neurons after a 10-fold increase in extracellular K+ concentration. Evidence is presented which shows that this substance may be choline. 2. The accumulation of interfering ions was not observed in Ca2(+)-free saline and was substantially reduced in the presence of eserine (a blocker of acetylcholinesterase). 3. In neuropile (and also packet) glial cells, extracellularly applied choline (10(-4) M) caused a steady increase in ion signal. This increase was not affected by removal of extracellular calcium, by hemicholinium-3 (a blocker of high-affinity choline uptake) or eserine. Shortly after the removal of choline from the saline the increase in ion signal stopped and the ion signal then decreased slowly to its original level. 4. Extracellular acetylcholine (10(-4) M) caused a similar increase in intracellular ion signal of neuropile glial cells to that caused by choline. This increase was blocked by eserine. 5. Extracellular choline caused a comparatively small increase in ion signal of Retzius neurones which was blocked by hemicholinium-3. In pressure neurones, choline or hemicholinium-3 had no effect on intracellular ion signal. 6. Autoradiographic analysis of [3H]choline uptake showed that most of the choline was taken up by glial cells in a time- and dose-dependent manner. Small but significant amounts of choline were taken up by neurones and connective tissue. 7. It is concluded that the neuropile and packet glial cells possess an effective choline uptake system which is activated by exogenous choline but also by choline that stems from enzymatic inactivation of acetylcholine released by neurones.

Full text

PDF
387

Images in this article

403Fig. 11
on p.403

Selected References

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

  1. Adamic S. (3H)Choline entry and (3H)acetylcholine formation in leech segmental ganglia. Biochem Pharmacol. 1975 Oct 1;24(19):1763–1766. doi: 10.1016/0006-2952(75)90453-0. [DOI] [PubMed] [Google Scholar]
  2. Adamic S. Accumulation of choline by the segmental ganglia of the leech. Biochem Pharmacol. 1974 Sep 15;23(18):2595–2602. doi: 10.1016/0006-2952(74)90182-8. [DOI] [PubMed] [Google Scholar]
  3. Ballanyi K., Schlue W. R. Direct effects of carbachol on membrane potential and ion activities in leech glial cells. Glia. 1988;1(2):165–167. doi: 10.1002/glia.440010209. [DOI] [PubMed] [Google Scholar]
  4. Bührle C. P., Sonnhof U. Intracellular ion activities and equilibrium potentials in motoneurones and glia cells of the frog spinal cord. Pflugers Arch. 1983 Feb;396(2):144–153. doi: 10.1007/BF00615519. [DOI] [PubMed] [Google Scholar]
  5. Cammelli E., De Bellis A. M., Nistri A. Proceedings: Distribution of acetylcholine and of acetylcholinesterase activity in the nervous tissue of the frog and of the leach. J Physiol. 1974 Oct;242(2):88P–90P. [PubMed] [Google Scholar]
  6. Coles J. A. Bias current modifies the selectivity of liquid membrane ion-selective microelectrodes. Pflugers Arch. 1988 Mar;411(3):339–344. doi: 10.1007/BF00585125. [DOI] [PubMed] [Google Scholar]
  7. Coles J. A., Orkand R. K. Modification of potassium movement through the retina of the drone (Apis mellifera male) by glial uptake. J Physiol. 1983 Jul;340:157–174. doi: 10.1113/jphysiol.1983.sp014756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cooke J. D., Quastel D. M. The specific effect of potassium on transmitter release by motor nerve terminals and its inhibition by calcium. J Physiol. 1973 Jan;228(2):435–458. doi: 10.1113/jphysiol.1973.sp010094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dross K., Kewitz H. Concentration and origin of choline in the rat brain. Naunyn Schmiedebergs Arch Pharmacol. 1972;274(1):91–106. doi: 10.1007/BF00501010. [DOI] [PubMed] [Google Scholar]
  10. Evans P. D. An autoradiographical study of the localization of the uptake of glutamate by the peripheral nerves of the crab, Carcinus maenas (L.). J Cell Sci. 1974 Mar;14(2):351–367. doi: 10.1242/jcs.14.2.351. [DOI] [PubMed] [Google Scholar]
  11. Fisher A., Hanin I. Choline analogs as potential tools in developing selective animal models of central cholinergic hypofunction. Life Sci. 1980 Nov 3;27(18):1615–1634. doi: 10.1016/0024-3205(80)90635-9. [DOI] [PubMed] [Google Scholar]
  12. Francescangeli E., Goracci G., Piccinin G. L., Mozzi R., Woelk H., Porcellati G. The metabolism of labelled choline in neuronal and glial cells of the rabbit in vivo. J Neurochem. 1977 Jan;28(1):171–176. doi: 10.1111/j.1471-4159.1977.tb07723.x. [DOI] [PubMed] [Google Scholar]
  13. Freeman J. J., Jenden D. J. The source of choline for acetylcholine synthesis in brain. Life Sci. 1976 Oct 1;19(7):949–961. doi: 10.1016/0024-3205(76)90285-x. [DOI] [PubMed] [Google Scholar]
  14. Haber B., Hutchison H. T. Uptake of neurotransmitters and precursors by clonal cell lines of neural origin. Adv Exp Med Biol. 1976;69:179–198. doi: 10.1007/978-1-4684-3264-0_14. [DOI] [PubMed] [Google Scholar]
  15. Hansson E., Rönnbäck L., Sellström A. Is there a "dopaminergic glial cell"? Neurochem Res. 1984 May;9(5):679–689. doi: 10.1007/BF00964514. [DOI] [PubMed] [Google Scholar]
  16. Hertz L., Nissen C. Differences between leech and mammalian nervous systems in metabolic reaction to K+ as an indication of differences in potassium homeostasis mechanisms. Brain Res. 1976 Jun 25;110(1):182–188. doi: 10.1016/0006-8993(76)90220-1. [DOI] [PubMed] [Google Scholar]
  17. Kai-Kai M. A., Pentreath V. W. The structure, distribution, and quantitative relationships of the glia in the abdominal ganglia of the horse leech, Haemopis sanguisuga. J Comp Neurol. 1981 Oct 20;202(2):193–210. doi: 10.1002/cne.902020206. [DOI] [PubMed] [Google Scholar]
  18. Karwoski C. J., Newman E. A., Shimazaki H., Proenza L. M. Light-evoked increases in extracellular K+ in the plexiform layers of amphibian retinas. J Gen Physiol. 1985 Aug;86(2):189–213. doi: 10.1085/jgp.86.2.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kimelberg H. K., Katz D. M. High-affinity uptake of serotonin into immunocytochemically identified astrocytes. Science. 1985 May 17;228(4701):889–891. doi: 10.1126/science.3890180. [DOI] [PubMed] [Google Scholar]
  20. Kuramoto T., Haber B. The K+ liquid ion exchange electrode system: responses to drugs and neurotransmitters. J Neurosci Res. 1981;6(1):37–48. doi: 10.1002/jnr.490060105. [DOI] [PubMed] [Google Scholar]
  21. Massarelli R., Sensenbrenner M., Ebel A., Mandel P. Kinetics of choline uptake in mixed neuronal-glial, and exclusively glial cultures. Neurobiology. 1974;4(6):414–418. [PubMed] [Google Scholar]
  22. McCaman M. W., Weinreich D., McCaman R. E. The determination of picomole levels of 5-hydroxytryptamine and dopamine in Aplysia, Tritonia and leech nervous tissues. Brain Res. 1973 Apr 13;53(1):129–137. doi: 10.1016/0006-8993(73)90772-5. [DOI] [PubMed] [Google Scholar]
  23. Orkand R. K., Dietzel I., Coles J. A. Light-induced changes in extracellular volume in the retina of the drone, Apis mellifera. Neurosci Lett. 1984 Apr 6;45(3):273–278. doi: 10.1016/0304-3940(84)90238-6. [DOI] [PubMed] [Google Scholar]
  24. Pentreath V. W., Kai-Kai M. A. Significance of the potassium signal from neurones to glial cells. Nature. 1982 Jan 7;295(5844):59–61. doi: 10.1038/295059a0. [DOI] [PubMed] [Google Scholar]
  25. Reynolds R., Herschkowitz N. Uptake of [3H]GABA by oligodendrocytes in dissociated brain cell culture: a combined autoradiographic and immunocytochemical study. Brain Res. 1984 Nov 19;322(1):17–31. doi: 10.1016/0006-8993(84)91176-4. [DOI] [PubMed] [Google Scholar]
  26. Richelson E., Thompson E. J. Transport of neurotransmitter precursors into cultured cells. Nat New Biol. 1973 Feb 14;241(111):201–204. doi: 10.1038/newbio241201a0. [DOI] [PubMed] [Google Scholar]
  27. Richter J. A. Characteristics of acetylcholine release by superfused slices of rat brain. J Neurochem. 1976 Apr;26(4):791–797. doi: 10.1111/j.1471-4159.1976.tb04453.x. [DOI] [PubMed] [Google Scholar]
  28. Sargent P. B. Synthesis of acetylcholine by excitatory motoneurons in central nervous system of the leech. J Neurophysiol. 1977 Mar;40(2):453–460. doi: 10.1152/jn.1977.40.2.453. [DOI] [PubMed] [Google Scholar]
  29. Schlue W. R., Deitmer J. W. Extracellular potassium in neuropile and nerve cell body region of the leech central nervous system. J Exp Biol. 1980 Aug;87:23–43. doi: 10.1242/jeb.87.1.23. [DOI] [PubMed] [Google Scholar]
  30. Schlue W. R., Schliep A., Walz W. Fluorescence marking of neuropile glial cells in the central nervous system of the leech Hirudo medicinalis. Cell Tissue Res. 1980;209(2):257–269. doi: 10.1007/BF00237630. [DOI] [PubMed] [Google Scholar]
  31. Schlue W. R., Wuttke W. Potassium activity in leech neuropile glial cells changes with external potassium concentration. Brain Res. 1983 Jul 4;270(2):368–372. doi: 10.1016/0006-8993(83)90616-9. [DOI] [PubMed] [Google Scholar]
  32. Sellström A., Hamberger A. Potassium-stimulated gamma-aminobutyric acid release from neurons and glia. Brain Res. 1977 Jan 1;119(1):189–198. doi: 10.1016/0006-8993(77)90099-3. [DOI] [PubMed] [Google Scholar]
  33. Serve G., Endres W., Grafe P. Continuous electrophysiological measurements of changes in cell volume of motoneurons in the isolated frog spinal cord. Pflugers Arch. 1988 Apr;411(4):410–415. doi: 10.1007/BF00587720. [DOI] [PubMed] [Google Scholar]
  34. Wallace B. G., Gillon J. W. Characterization of acetylcholinesterase in individual neurons in the leech central nervous system. J Neurosci. 1982 Aug;2(8):1108–1118. doi: 10.1523/JNEUROSCI.02-08-01108.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Walz W., Schlue W. R. Ionic mechanism of a hyperpolarizing 5-hydroxytryptamine effect on leech neuropile glial cells. Brain Res. 1982 Oct 28;250(1):111–121. doi: 10.1016/0006-8993(82)90957-x. [DOI] [PubMed] [Google Scholar]
  36. Wuhrmann P., Ineichen H., Riesen-Willi U., Lezzi M. Change in nuclear potassium electrochemical activity and puffing of potassium-sensitive salivary chromosome regions during Chironomus development. Proc Natl Acad Sci U S A. 1979 Feb;76(2):806–808. doi: 10.1073/pnas.76.2.806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES