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. 1993 Mar;462:229–242. doi: 10.1113/jphysiol.1993.sp019552

Cyclic AMP mediates inhibition of the Na(+)-K+ electrogenic pump by serotonin in tactile sensory neurones of the leech.

S Catarsi 1, R Scuri 1, M Brunelli 1
PMCID: PMC1175298  PMID: 7687293

Abstract

1. Serotonin (5-HT) reduced the after-hyperpolarization (AHP) amplitude in tactile sensory neurones (T) but not in pressor (P) or nociceptive (N) cells of the leech. 2. Adenylate cyclase activators, phosphodiesterase inhibitors and membrane permeant analogues of cyclic adenosine monophosphate (cyclic AMP) mimicked the effect of 5-HT in reducing the AHP amplitude in T neurones. 3. Ionophoretic injection of cyclic AMP in T cells reduced the AHP amplitude, while cyclic guanosine monophosphate (cyclic GMP) or adenosine-5'-monophosphate (AMP) were without effect. 4. Inhibition of adenylate cyclase by the drug RMI 12330A (also known as MDL 12330A) suggested that 5-HT reduced the AHP amplitude through cyclic AMP. 5. 8-Bromoadenosine-3'-5'-cyclic monophosphate (8-Br-cyclic AMP) was still able to reduce the AHP amplitude after blocking the Ca(2+)-activated K+ conductance with CdCl2 and converted the normal hyperpolarization which follows the intracellular injection of Na+ into a depolarization. In addition, the cyclic AMP analogue slowed down and reduced the repolarization usually induced by CsCl after perfusion with K(+)-free solution. It is proposed that, in T sensory neurones, cyclic AMP mediates the inhibition of the Na(+)-K+ electrogenic pump induced by 5-HT application.

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Selected References

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  1. Aperia A., Fryckstedt J., Svensson L., Hemmings H. C., Jr, Nairn A. C., Greengard P. Phosphorylated Mr 32,000 dopamine- and cAMP-regulated phosphoprotein inhibits Na+,K(+)-ATPase activity in renal tubule cells. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2798–2801. doi: 10.1073/pnas.88.7.2798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baylor D. A., Nicholls J. G. After-effects of nerve impulses on signalling in the central nervous system of the leech. J Physiol. 1969 Aug;203(3):571–589. doi: 10.1113/jphysiol.1969.sp008880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beavo J. A., Rogers N. L., Crofford O. B., Hardman J. G., Sutherland E. W., Newman E. V. Effects of xanthine derivatives on lipolysis and on adenosine 3',5'-monophosphate phosphodiesterase activity. Mol Pharmacol. 1970 Nov;6(6):597–603. [PubMed] [Google Scholar]
  4. Belardetti F., Biondi C., Brunelli M., Fabri M., Trevisani A. Heterosynaptic facilitation and behavioral sensitization are inhibited by lowering endogenous cAMP in Aplysia. Brain Res. 1983 Dec 12;288(1-2):95–104. doi: 10.1016/0006-8993(83)90084-7. [DOI] [PubMed] [Google Scholar]
  5. Belardetti F., Biondi C., Colombaioni L., Brunelli M., Trevisani A. Role of serotonin and cyclic AMP on facilitation of the fast conducting system activity in the leech Hirudo medicinalis. Brain Res. 1982 Aug 19;246(1):89–103. doi: 10.1016/0006-8993(82)90145-7. [DOI] [PubMed] [Google Scholar]
  6. Belardetti F., Brunelli M., Demontis G., Sonetti D. Serotonin and Retzius cell depress the hyperpolarization following impulses of leech touch cell. Brain Res. 1984 May 21;300(1):91–102. doi: 10.1016/0006-8993(84)91343-x. [DOI] [PubMed] [Google Scholar]
  7. Bertorello A. M., Hopfield J. F., Aperia A., Greengard P. Inhibition by dopamine of (Na(+)+K+)ATPase activity in neostriatal neurons through D1 and D2 dopamine receptor synergism. Nature. 1990 Sep 27;347(6291):386–388. doi: 10.1038/347386a0. [DOI] [PubMed] [Google Scholar]
  8. Biondi C., Campi A. L., Pareschi M. C., Portolan A., Ferretti M. E. RMI 12330A, an inhibitor of adenylate cyclase and cyclic AMP-phosphodiesterase activities in the segmental ganglia of the leech Hirudo medicinalis. Neurosci Lett. 1990 Jun 8;113(3):322–327. doi: 10.1016/0304-3940(90)90605-9. [DOI] [PubMed] [Google Scholar]
  9. Brunelli M., Castellucci V., Kandel E. R. Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP. Science. 1976 Dec 10;194(4270):1178–1181. doi: 10.1126/science.186870. [DOI] [PubMed] [Google Scholar]
  10. Catarsi S., Brunelli M. Serotonin depresses the after-hyperpolarization through the inhibition of the Na+/K+ electrogenic pump in T sensory neurones of the leech. J Exp Biol. 1991 Jan;155:261–273. doi: 10.1242/jeb.155.1.261. [DOI] [PubMed] [Google Scholar]
  11. Catarsi S., Garcia-Gil M., Traina G., Brunelli M. Seasonal variation of serotonin content and nonassociative learning of swim induction in the leech Hirudo medicinalis. J Comp Physiol A. 1990 Sep;167(4):469–474. doi: 10.1007/BF00190817. [DOI] [PubMed] [Google Scholar]
  12. Colombaioni L., Brunelli M. Neurotransmitter-induced modulation of an electrotonic synapse in the CNS of Hirudo medicinalis. Exp Biol. 1988;47(3):139–144. [PubMed] [Google Scholar]
  13. Garcia-Gil M., Berton F., Tongiorgi E., Brunelli M. Effects of cyclic nucleotides and calcium/calmodulin on protein phosphorylation in the CNS of Hirudo medicinalis. J Neurochem. 1989 Mar;52(3):699–704. doi: 10.1111/j.1471-4159.1989.tb02511.x. [DOI] [PubMed] [Google Scholar]
  14. Gu X. N. Effect of conduction block at axon bifurcations on synaptic transmission to different postsynaptic neurones in the leech. J Physiol. 1991 Sep;441:755–778. doi: 10.1113/jphysiol.1991.sp018777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hagiwara S., Byerly L. Calcium channel. Annu Rev Neurosci. 1981;4:69–125. doi: 10.1146/annurev.ne.04.030181.000441. [DOI] [PubMed] [Google Scholar]
  16. Jansen J. K., Nicholls J. G. Conductance changes, an electrogenic pump and the hyperpolarization of leech neurones following impulses. J Physiol. 1973 Mar;229(3):635–655. doi: 10.1113/jphysiol.1973.sp010158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kandel E. R., Schwartz J. H. Molecular biology of learning: modulation of transmitter release. Science. 1982 Oct 29;218(4571):433–443. doi: 10.1126/science.6289442. [DOI] [PubMed] [Google Scholar]
  18. Madison D. V., Nicoll R. A. Noradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus. Nature. 1982 Oct 14;299(5884):636–638. doi: 10.1038/299636a0. [DOI] [PubMed] [Google Scholar]
  19. Meech R. W. Calcium-dependent potassium activation in nervous tissues. Annu Rev Biophys Bioeng. 1978;7:1–18. doi: 10.1146/annurev.bb.07.060178.000245. [DOI] [PubMed] [Google Scholar]
  20. Mourek J. Arachidonic acid-induced inhibition of (Na+K+)-stimulated ATPase in the cerebral cortex and medulla oblongata of young and adult rats. Physiol Bohemoslov. 1988;37(5):427–431. [PubMed] [Google Scholar]
  21. Pareschi M. C., Portolan A., Ferretti M. E., Biondi C. Gli enzimi del metabolismo dell'AMP ciclico nel SNC della sanguisuga Hirudo m. Boll Soc Ital Biol Sper. 1987 Aug 31;63(8):701–707. [PubMed] [Google Scholar]
  22. Phillis J. W., Wu P. H. Catecholamines and the sodium pump in excitable cells. Prog Neurobiol. 1981;17(3):141–184. doi: 10.1016/0301-0082(81)90012-5. [DOI] [PubMed] [Google Scholar]
  23. SKOU J. C. ENZYMATIC BASIS FOR ACTIVE TRANSPORT OF NA+ AND K+ ACROSS CELL MEMBRANE. Physiol Rev. 1965 Jul;45:596–617. doi: 10.1152/physrev.1965.45.3.596. [DOI] [PubMed] [Google Scholar]
  24. Sanchez-Armass S., Merz D. C., Drapeau P. Distinct receptors, second messengers and conductances underlying the dual responses to serotonin in an identified leech neurone. J Exp Biol. 1991 Jan;155:531–547. doi: 10.1242/jeb.155.1.531. [DOI] [PubMed] [Google Scholar]
  25. Schlue W. R., Deitmer J. W. Potassium distribution and membrane potential of sensory neurons in the leech nervous system. J Neurophysiol. 1984 Apr;51(4):689–704. doi: 10.1152/jn.1984.51.4.689. [DOI] [PubMed] [Google Scholar]
  26. Stewart R. R., Nicholls J. G., Adams W. B. Na+, K+ and Ca2+ currents in identified leech neurones in culture. J Exp Biol. 1989 Jan;141:1–20. doi: 10.1242/jeb.141.1.1. [DOI] [PubMed] [Google Scholar]
  27. Thomas R. C. Electrogenic sodium pump in nerve and muscle cells. Physiol Rev. 1972 Jul;52(3):563–594. doi: 10.1152/physrev.1972.52.3.563. [DOI] [PubMed] [Google Scholar]
  28. Van Essen D. C. The contribution of membrane hyperpolarization to adaptation and conduction block in sensory neurones of the leech. J Physiol. 1973 May;230(3):509–534. doi: 10.1113/jphysiol.1973.sp010201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Walsh J. P., Byrne J. H. Modulation of a steady-state Ca2+-activated, K+ current in tail sensory neurons of Aplysia: role of serotonin and cAMP. J Neurophysiol. 1989 Jan;61(1):32–44. doi: 10.1152/jn.1989.61.1.32. [DOI] [PubMed] [Google Scholar]
  30. Yau K. W. Receptive fields, geometry and conduction block of sensory neurones in the central nervous system of the leech. J Physiol. 1976 Dec;263(3):513–538. doi: 10.1113/jphysiol.1976.sp011643. [DOI] [PMC free article] [PubMed] [Google Scholar]

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