Action Potential Bursts in Central Snail Neurons Elicited by Procaine: Roles of Ionic Currents

10.4077/CJP.2010.AMK072

Chia-Hsien Lin；Pei-Lin Lin；Ming-Cheng Tsai；Hui-Yu Hsu；Han-Yin Yang；Chieh-Min Chuang；Yi-Hung Chen

procaine ； snail ； central neuron ； bursts of action potentials ； Ca(superscript 2+) current ； Na(superscript +) current ； phospholipase C ； fast-inactivating K(superscript +) current ； delayed rectifying K(superscript +) current ； ionic currents

The Chinese Journal of Physiology

53卷5期（2010 / 10 / 31）

271 - 284

英文

The role of ionic currents on procaine-elicited action potential bursts was studied in an identifiable RP1 neuron of the African snail, Achatina fulica Ferussac, using the two-electrode voltage clamp method. The RP1 neuron generated spontaneous action potentials and bath application of procaine at 10 mM reversibly elicited action potential bursts in a concentration-dependent manner. Voltage clamp studies revealed that procaine at 10 mM decreased [1] the Ca(superscript 2+) current, [2] the Na(superscript +) current, [3] the delayed rectifying K(superscript +) current I(subscript KD), and [4] the fast-inactivating K(superscript +) current (I(subscript A)). Action potential bursts were not elicited by 4-aminopyridine (4-AP), an inhibitor of IA, whereas they were seen after application of tetraethylammonium chloride (TEA), a blocker of the I(subscript K(Ca)) and IKD currents, and tacrine, an inhibitor of I(subscript KD). Pretreatment with U73122, a phospholipase C inhibitor, blocked the action potential bursts elicited by procaine. U73122 did not affect the I(subscript KD) of the RP1 neuron; however, U73122 decreased the inhibitory effect of procaine on the I(subscript KD). Tacrine decreased the TEA-sensitive I(subscript KD) of RP1 neuron but did not significantly affect the I(subscript A). Tacrine also successfully induced action potential bursts in the RP1 neuron. It is concluded that the inhibition on the I(subscript KD) is responsible for the generation of action potential bursts in the central snail RP1 neuron. Further, phospholipase C activity is involved in the procaine-elicited I(subscript KD) inhibition and action potential bursts.

1. Adamec, R. E.,Stark-Adamec, C.,Burnham, W. M.,Bruun-Meyer, S.,Perrin, R.,Livingston, K. E.(1981).Power spectral analysis of EEG drug response in the kindled rat brain.Electroencephalogr. Clin. Neurophysiol.,52,451-460.
2. Adams, D. J.,Gage, P. W.(1979).Ionic currents in response to membrane depolarization in an Aplysia neurone.J. Physiol.,289,115-141.
3. Adams, D. J.,Gage, P. W.(1979).Characteristics of sodium and calcium conductance changes produced by membrane depolarization in an Aplysia neurone.J. Physiol.,289,143-161.
4. Arvanov, V. L.,Liou, H. H.,Chang, Y. C.,Chen, R. C.,Peng, F. C.,Ling, K. H.,Tsai, M. C.(1994).Interactions of anticholinesterases with Achatina fulica acetylcholine responses and electrogenic sodium pump.Neuroscience,62,581-586.
5. Babb, T. L.,Perryman, K. M.,Lieb, J. P.,Finch, D. M.,Crandall, P. H.(1979).Procaine-induced seizures in epileptic monkeys with bilateral hippocampal foci.Electroencephalogr. Clin. Neurophysiol.,47,725-737.
6. Barker, J. L.,Smith, T. G. Jr.(1976).Peptide regulation of neuronal membrane properties.Brain Res.,103,167-170.
7. Berridge, M. J.(1998).Neuronal calcium signaling.Neuron,21,13-26.
8. Bilia, A. R.,Braca, A.,Mendez, J.,Morelli, I.(2000).Molluscicidal and piscicidal activities of Venezuelan Chrysobalanaceae plants.Life Sci.,66,L53-L59.
9. Bukanova, J. V.,Solntseva, E. I.,Skrebitsky, V. G.(2002).Selective suppression of the slow-inactivating potassium currents by nootropics in molluscan neurons.Int. J. Neuropsychopharmacol.,5,229-237.
10. Chen, Y. H.,Lin, C. H.,Lin, P. L.,Tsai, M. C.(2006).Cocaine elicits action potential bursts in a central snail neuron: The role of delayed rectifying K(+) current.Neuroscience,138,257-280.
11. Chen, Y. H.,Lu, K. L.,Hsiao, R. W.,Lee, Y. L.,Tsai, H. C.,Lin, C. H.,Tsai, M. C.(2008).Effects of penicillin on procaine-elicited bursts of potential in central neuron of snail, Achatina fulica.Comp. Biochem. Physiol. C,148,128-135.
12. Chen, Y. H.,Tsai, M. C.(1997).Bursting firing of action potentials in central snail neurons elicited by d-amphetamine: role of cytoplasmic second messengers.Neurosci. Res.,27,295-304.
13. Chen, Y. H.,Tsai, M. C.(1996).Bursting firing of action potential in central snail neuron elicited by d-amphetamine: role of the intracellular calcium ions.Comp. Biochem. Physiol. A,115,195-205.
14. Chen, Y. H.,Tsai, M. C.(2000).Action potential bursts in central snail neurons elicited by d-amphetamine: roles of ionic currents.Neuroscience,96,237-248.
15. Ellershaw, D. C.,Greenwood, I. A.,Large, W. A.(2002).Modulation of volume-sensitive chloride current by noradrenaline in rabbit portal vein myocytes.J. Physiol.,542,537-547.
16. Feldman, H. S.,Arthur, G. R.,Covino, B. G.(1989).Comparative systemic toxicity of convulsant and supraconvulsant doses of intravenous ropivacaine, bupivacaine, and lidocaine in the conscious dog.Anesth. Analg.,69,794-801.
17. Ferrendelli, J. A.,Kinscherf, D. A.(1977).Cyclic nucleotides in epileptic brain: effects of pentylenetetrazol on regional cyclic AMP and cyclic GMP levels in vivo.Epilepsia,18,525-531.
18. Flood, J. F.,Smith, G. E.,Cherkin, A.(1985).Memory enhancement: supra-additive effect of subcutaneous cholinergic drug combinations in mice.Psychopharmacology (Berl),86,61-67.
19. Funase, K.(1990).Oxytocin-induced sodium current is mediated by cAMP-dependent protein phosphorylation in an identified snail neuron.Brain Res.,517,263-268.
20. Ichinose, M.,McAdoo, D. J.(1988).The voltage-dependent, slow inward current induced by the neuropeptide FMRFamide in Aplysia neuron R14.J. Neurosci.,8,3891-3900.
21. Kerkut, G. A.,Lambert, J. D.,Gayton, R. J.,Loker, J. E.,Walder, R. J.(1975).Mapping of nerve cells in the suboesophageal ganglia of Helix aspersa.Comp. Biochem. Physiol. A,50,1-25.
22. Komai, H.,McDowell, T. S.(2001).Local anesthetic inhibition of voltage-activated potassium currents in rat dorsal root ganglion neurons.Anesthesiology,94,1089-1095.
23. Kraliz, D.,Singh, S.(1997).Selective blockade of the delayed rectifier potassium current by tacrine in Drosophila.J. Neurobiol.,32,1-10.
24. Lin, C. H.,Tsai, M. C.(2003).D-amphetamine-elicited action potential bursts in central snail neurons: role of second messenger systems.J. Formos. Med. Assoc.,102,394-403.
25. Lin, C. H.,Tsai, M. C.(2005).Effects of procaine on a central neuron of the snail, Achatina fulica Ferussac.Life Sci.,76,1641-1666.
26. Liou, H. H.,Wang, C. R.,Chou, H. C.,Arvanov, V. L.,Chen, R. C.,Chang, Y. C.,Chuang, C. Y.,Chen, C. Y.,Tsai, M. C.(1994).Anticardiolipin antisera from lupus patients with seizures reduce a GABA receptor-mediated chloride current in snail neurons.Life Sci.,54,1119-1125.
27. Milesi, V.,Aiello, E. A.,Rebolledo, A.,Gomez, A. A.,Grassi de Gende, A.O.(1999).Role of a Ca²⁺-activated K⁺ current in the maintenance of resting membrane potential of isolated, human, saphenous vein smooth muscle cells.Pflugers Arch.,437,455-461.
28. Muller, M.,Litz, R. J.,Huler, M.,Albrecht, D. M.(2001).Grand mal convulsion and plasma concentrations after intravascular injection of ropivacaine for axillary brachial plexus blockade.Br. J. Anaesth.,87,784-787.
29. Muraki, S.,Tohse, N.,Seki, S.,Nagashima, M.,Yamada, Y.,Abe, T.,Yabu, H.(2001).Decrease in the Ca²⁺-activated K⁺ current of pulmonary arterial smooth muscle in pulmonary hypertension rats.Naunyn Schmiedebergs Arch. Pharmacol.,364,183-192.
30. Naguib, M.,Magboul, A.,Samarkandi, A. H.,Attia, M.(1998).Adverse effects and drug interactions associated with local and regional anaesthesia.Drug Saf.,18,221-250.
31. Onizuka, S.,Kasaba, T.,Hamakawa, T.,Takasaki, M.(2005).Lidocaine excites both pre-and postsynaptic neurons of reconstructed respiratory pattern generator in Lymnaea stagnalis.Anesth. Analg.,100,175-182.
32. Onizuka, S.,Kasaba, T.,Takasaki, M.(2008).The effect of lidocaine on cholinergic neurotransmission in an identified reconstructed synapse.Anesth. Analg.,107,1236-1242.
33. Onozuka, M.,Imai, S.,Furuichi, H.,Ozono, S.(1991).A specific 70K protein found in epileptic rat cortex: induction of bursting activity and negative resistance by its intracellular application in Euhadra neurons.J. Neurobiol.,22,287-297.
34. Onozuka, M.,Imai, S.,Sugaya, E.(1986).Pentylenetetrazole-induced bursting activity and cellular protein phosphorylation in snail neurons.Brain Res.,362,33-39.
35. Onozuka, M.,Kishii, K.,Furuichi, H.,Sugaya, E.(1983).Behavior of intracellular cyclic nucleotide and calcium in pentylenetetrazoleinduced bursting activity in snail neurons.Brain Res.,269,277-286.
36. Onozuka, M.,Kubo, K. Y.,Ozono, S.(1991).The molecular mechanism underlying pentylenetetrazole-induced bursting activity in Euhadra neurons: involvement of protein phosphorylation.Comp. Biochem. Physiol. C,100,423-432.
37. Roy, M. L.,Saal, D.,Perney, T.,Sontheimer, H.,Waxman, S. G.,Kaczmarek, L. K.(1996).Manipulation of the delayed rectifier Kv1.5 potassium channel in glial cells by antisense oligodeoxynucleotides.Glia,18,177-184.
38. Ruetsch, Y. A.,Boni, T.,Borgeat, A.(2001).From cocaine to ropivacaine: the history of local anesthetic drugs.Curr. Top. Med. Chem.,1,175-182.
39. Smith, T. G., Jr.,Barker, J. L.,Gainer, H.(1975).Requirements for bursting pacemaker potential activity in molluscan neurones.Nature,253,450-452.
40. Staras, K.,Gyori, J.,Kemenes, G.(2002).Voltage-gated ionic currents in an identified modulatory cell type controlling molluscan feeding.Eur. J. Neurosci.,15,109-119.
41. Sugaya, E.,Furuichi, H.,Takagi, T.,Kajiwara, K.,Komatsubara, J.(1987).Intracellular calcium concentration during pentylenetetrazolinduced bursting activity in snail neurons.Brain Res.,416,183-186.
42. Sugaya, E.,Goldring, S.,O''leary, J. L.(1964).Intracellular potentials associated with direct cortical response and seizure discharge in cat.Electroencephalogr. Clin. Neurophysiol.,17,661-669.
43. Sugaya, E.,Onozuka, M.(1978).Intracellular calcium: its release from granules during bursting activity in snail neurons.Science,202,1195-1197.
44. Sugaya, E.,Onozuka, M.(1978).Intracellular calcium: its movement during pentylenetetrazole-induced bursting activity.Science,200,797-799.
45. Sugimoto, M.,Uchida, I.,Mashimo, T.(2003).Local anaesthetics have different mechanisms and sites of action at the recombinant Nmethyl-D-aspartate (NMDA) receptors.Br. J. Pharmacol.,138,876-882.
46. Summers, W. K.,Kaufman, K. R.,Altman, F.,Fischer, J. M., Jr.(1980).THA-a review of the literature and its use in treatment of five overdose patients.Clin. Toxicol.,16,269-281.
47. Sun, X. P.,Funase, K.,Takeuchi, H.(1987).Ionic current of an identifiable giant neurone, d-RPLN, of an African giant snail (Achatina fulica Ferussac), measured under voltage clamping-II Outward currents.Comp. Biochem. Physiol. A,88,707-714.
48. Sun, X. P.,Funase, K.,Takeuchi, H.(1987).Ionic current of an identifiable giant neurone, d-RPLN, of an African giant snail (Achatina fulica Férussac), measured under voltage clamping-I Intward currents.Comp. Biochem. Physiol. A,88,317-324.
49. Takeuchi, H.,Araki, Y.,Emaduddin, M.,Zhang, W.,Han, X. Y.,Salunga, T. L.,Wong, S. M.(1996).Identifiable Achatina giant neurones: their localizations in ganglia, axonal pathways and pharmacological features.Gen. Pharmacol.,27,3-32.
50. Thompson, S. H.(1977).Three pharmacologically distinct potassium channels in molluscan neurones.J. Physiol.,265,465-488.
51. Tsai, M. C.,Chen, Y. H.(1995).Bursting firing of action potentials in central snail neurons elicited by d-amphetamine: role of the electrogenic sodium pump.Comp. Biochem. Physiol. C,111,131-141.
52. Vaur, S.,Bresson-Bepoldin, L.,Dufy, B.,Tuffet, S.,Dufy-Barbe, L.(1998).Potassium channel inhibition reduces cell proliferation in the GH3 pituitary cell line.J. Cell. Physiol.,177,402-410.
53. Wilson, W. A.,Wachtel, H.(1978).Prolonged inhibition in burst firing neurons: synaptic inactivation of the slow regenerative inward current.Science,202,772-775.
54. Zhao, M. L.,Wu, C. F.(1997).Alterations in frequency coding and activity dependence of excitability in cultured neurons of Drosophila memory mutants.J. Neurosci.,17,2187-2199.
55. Zhou, W.,Arrabit, C.,Choe, S.,Slesinger, P. A.(2001).Mechanism underlying bupivacaine inhibition of G protein-gated inwardly rectifying K⁺ channels.Proc. Natl. Acad. Sci. U.S.A.,98,6482-6487.