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Cellular and Molecular Neurobiology

, Volume 4, Issue 4, pp 319–338 | Cite as

Alteration of calcium conductances and outward current by cyclic adenosine monophosphate (cAMP) in neurons ofLimax maximus

  • Philip Hockberger
  • John A. Connor
Article

Summary

  1. 1.

    Membrane responses to cyclic adenosine monophosphate (cAMP) injections have been studied by means of voltage clamp, Ca-indicator dye, and ion substitution techniques in identified neurons from the abdominal ganglion ofLimax maximus.

     
  2. 2.

    The ventral abdominal giant cell (AGC) displayed a response consisting of a decrease in outward current usually accompanied by a smaller enhancement of voltage-gated Ca2+ influx. Both responses were eliminated by external Cd2+ or Mn2+ and required membrane voltages more positive than −40 mV for expression. The enhanced influx persisted in Ba2+-substituted saline, while the decrease in outward current was blocked.

     
  3. 3.

    A group of dorsal neurons (RD1-3, LD1) showed a mixed Na-Ca influx induced by cAMP that could be activated over a wide range of membrane potentials (< − 100 to > − 20 mV). This flux caused a measurable increase in internal Ca2+. The influx was insensitive to Cd2+ and Mn2+ but was reduced by prolonged exposure to Co2+.

     
  4. 4.

    The relative magnitude of the Na-Ca flux ratio showed considerable variation between specimens. In immature animals the Ca component was absent.

     
  5. 5.

    The results demonstrated that elevation of intracellular cAMP can cause cell-specific changes of membrane conductance within closely associated neurons.

     

Key words

gastropod neurons cyclic adenosine monophosphate (cAMP) membrane conductance calcium voltage clamp arsenazo III 

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References

  1. Adams, D. J., Smith, S. J., and Thompson, S. H. (1980). Ionic currents in molluscan soma.Ann. Rev. Neurosci. 3141–167.Google Scholar
  2. Ahmed, Z., and Connor, J. A. (1979). Measurement of calcium influx under voltage clamp in molluscan neurons using the metallochromic dye Arsenazo III.J. Physiol. (Lond.) 28661–82.Google Scholar
  3. Aldenhoff, J. B., Hofmeier, G., Lux, H. D., and Swandulla, D. (1983). Stimulation of a sodium influx by cAMP inHelix neurons.Brain Res. 276289–296.Google Scholar
  4. Brinley, F., and Scarpa, A. (1975). Ionized magnesium concentration in axoplasm of dialyzed squid axons.FEBS Lett. 5082–85.Google Scholar
  5. Brown, A. M., Tsuda, Y., and Wilson, D. L. (1983). A description of activation and conduction in calcium channels based on tail and turn-on current measurements in the snail.J. Physiol. (Lond.) 344549–583.Google Scholar
  6. Chang, J., Gelperin, A., and Johnson, F. (1974). Intracellularly injected aequorin detects transmembrane calcium flux during action potentials in an identified neuron from the terrestrial slug,Limax maximus.Brain Res. 77431–442.Google Scholar
  7. Connor, J. A., and Ahmed, Z. (1984). Diffusion of ions and indicator dyes in neural cytoplasm.Cell. Mol. Neurobiol. 453–66.Google Scholar
  8. Connor, J. A., and Alkon, D. (1984). Light and voltage-dependent increases of calcium ion concentration in molluscan photoreceptors.J. Neurophysiol. 51745–752.Google Scholar
  9. Connor, J. A., and Hockberger, P. E. (1982). Direct measurements of cAMP effects on membrane conductance, intracellular Ca2+ and pH in molluscan neurons. InConditioning: Representation of Involved Neural Functions (Woody, C., Ed.), Plenum, New York, pp. 179–196.Google Scholar
  10. Connor, J. A., and Hockberger, P. E. (1983). Changes in membrane current and internal calcium of molluscan neurons induced by injected cAMP.Soc. Neurosci. Abstr. 91189.Google Scholar
  11. Connor, J. A., and Hockberger, P. (1984a). A novel membrane sodium current induced by injection of cyclic nucleotides into gastropod neurones.J. Physiol. (Lond.) 354139–162.Google Scholar
  12. Connor, J. A., and Hockberger, P. (1984b). Intracellular pH changes induced by injection of cyclic nucleotides into gastropod neurones.J. Physiol. (Lond.) 354163–172.Google Scholar
  13. Connor, J. A., and Nikolakopoulou, G. (1982). Calcium diffusion and buffering in nerve cytoplasm.Lect. Math. Life Sci 1579–101.Google Scholar
  14. Deterre, P., Paupardin-Tritsch, D., Bockaert, J., and Gerschenfeld, H. (1981). Role of cyclic AMP in a serotonin-evoked slow inward current in snail neurons.Nature 290783–785.Google Scholar
  15. Deterre, P., Paupardin-Tritsch, D., Bockaert, J., and Gerschenfeld, M. (1982). cAMP-mediated decrease in K+ conductance evoked by serotonin and dopamine in the same neuron: A biochemical and physiological single-cell study.Proc. Natl. Acad. Sci USA 797934–7938.Google Scholar
  16. Drummond, A., Benson, J., and Levitan, I. (1980). Serotonin-induced hyperpolarization of an identifiedAplysia neuron is mediated by cyclic AMP.Proc. Natl. Acad. Sci. USA 775013–5017.Google Scholar
  17. Ewald, D., and Eckert, R. (1983). Cyclic AMP enhances calcium-dependent potassium current inAplysia neurons.Cell. Mol. Neurobiol. 3345–353.Google Scholar
  18. Green, D. J., and Gillette, R. (1983). Patch- and voltage-clamp analysis of cyclic AMP-stimulated inward current underlying neuron bursting.Nature 306784–785.Google Scholar
  19. Hockberger, P., and Connor, J. A. (1983). Intracellular calcium measurements with arsenazo III during cyclic AMP injections into molluscan neurons.Sciences 219869–871.Google Scholar
  20. Kaczmarek, L. K., and Strumwasser, F. (1984). A voltage clamp analysis of currents underlying cyclic-AMP induced membrane modulation in isolated peptidergic neurons ofAplysia.J. Neurophysiol. 52340–349.Google Scholar
  21. Kendrick, N. C., Ratzlaff, R. W., and Blaustein, M. P. (1977). Arsenazo III as an indicator for ionized calcium in physiological salt solutions: Its use for determinations of the CaATP dissociation constant.Anal. Biochem 83433–450.Google Scholar
  22. Klein, M., Camardo, J., and Kandel, E. (1982). Serotonin modulates a specific potassium current in the sensory neurons that show presynaptic facilitation inAplysia.Proc. Natl. Acad. Sci. USA 795713–5717.Google Scholar
  23. Klein, M., and Kandel, E. R. (1978). Presynaptic modulation of voltage-dependent Ca current: Mechanism for behavioral sensitization in Aplysia californica.Proc. Natl. Acad. Sci. USA 753512–3516.Google Scholar
  24. Klein, M., and Kandel, E. R. (1980). Mechanism of calcium current modulation underlying presynaptic facilitation and behavioral sensitization inAplysia.Proc. Natl. Acad. Sci. USA 776912–6916.Google Scholar
  25. Kononenko, N. I., and Mironov, S. L. (1980). Effect of intracellular injection of cyclic AMP on electrical characteristics of identified neurons inHelix pomatia.Neurophysiology (USSR) 12517–525.Google Scholar
  26. Kononenko, N. I., Kostyuk, P. G., and Shcherbatko, A. D. (1983). The effect of intracellular cAMP injections on stationary membrane conductance and voltage- and time-dependent ionic currents in identified snail neurons.Brain Res. 268321–338.Google Scholar
  27. Libet, B. (1979). Which postsynaptic action of dopamine is mediated by cyclic AMP?Life Sci. 241043–1057.Google Scholar
  28. MacKay, A. R., and Gelperin, A. (1972). Pharmacology and reflex responsiveness of the heart in the giant garden slug,Limax maximus.Comp. Biochem. Physiol. 43A877–896.Google Scholar
  29. McAfee, D. and Greengard, P. (1971). Adenosine 3′,5′-monophosphate: Electrophysiological evidence for a role in sympathetic transmission.Science 178310–312.Google Scholar
  30. Paupardin-Tritsch, D., Deterre, P., and Gerscheufeld, H. (1981). Relationship between two voltagedependent serotonin responses of molluscan neurones.Brain Res. 217201–206.Google Scholar
  31. Pellmar, T. C. (1981). Ionic mechanism of a voltage-dependent current elicited by cyclic AMP.Cell. Mol. Neurobiol. 187–97.Google Scholar
  32. Reuter, H., Stevens, C. F., Tsien, R. W., and Yellen, G. (1982). Properties of single calcium channels in cardiac cell culture.Nature 297501–504.Google Scholar
  33. Smith, S. J., and Zucker, R. S. (1980). Aequorin response facilitation and intracellular calcium accumulation in molluscan neurons.J. Physiol. (Lond.) 300167–196.Google Scholar
  34. Tillotson, D. L., and Gorman, A. L. F. (1983). Localization of neuronal Ca2+ buffering near plasma membrane studied with different divalent cations.Cell. Mol. Neurobiol. 4297–310.Google Scholar
  35. Trautwein, W., Taniguchi, J., and Noma, A. (1982). The effect of intracellular cyclic nucleotides and calcium on the action potential and acetylcholine response of isolated cardiac cells.Pflugers Arch. 392307–314.Google Scholar
  36. Treistman, S. N. (1981). Effect of adenosine 3', 5'-monophosphate on neuronal pacemaker activity: A voltage clamp analysis.Science 21159–61.Google Scholar
  37. Tsien, R. W. (1983). Calcium channels in excitable cell membranes.Annu. Rev. Physiol. 4541–58.Google Scholar
  38. van Minnen, J., and Sokolove, P. (1984). Galactogen synthesis-stimulating factor in the slug,Limax maximus: Cellular localization and partial purification.Gen. Comp. Endorinal. 54114–122.Google Scholar
  39. Weight, F. (1983). Synaptic mechanisms in amphibian sympathetic ganglia. InAntonomic Ganglia (Elfvin, L., ed.), John Wiley and Sons, New York, pp. 309–344.Google Scholar

Copyright information

© Plenum Publishing Corporation 1984

Authors and Affiliations

  • Philip Hockberger
    • 1
    • 2
  • John A. Connor
    • 1
    • 2
  1. 1.Department of Molecular BiophysicsAT&T Bell LaboratoriesMurray HillUSA
  2. 2.Department of Physiology and BiophysicsUniversity of IllinoisUrbanaUSA

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