Summary
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1.
We have investigated the effect of the volatile anesthetic sevoflurane on acetylcholine (ACh) release from rat brain cortical slices.
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2.
The release of [3H]-ACh into the incubation fluid was studied after labeling the tissue ACh with [methyl-3H]-choline chloride.
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3.
We observed that sevoflurane induced an increase on the release of ACh that was dependent on incubation time and anesthetic concentration. The sevoflurane-induced ACh release was not blocked by tetrodotoxin (TTX) and therefore was independent of sodium channels. In addition, the sevoflurane effect was not blocked by ethylene glycol-bis(β-aminoethyl ether (EGTA) or cadmium (Cd2+), thus independent of extracellular calcium.
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4.
The sevoflurane-induced ACh release was inhibited by 1,2-bis (2-aminophenoxy) ethane-N,N,N’,N’-tetra-acetic acid (BAPTA-AM), suggestingthe involvement of intracellular calcium-sensitive stores in the process. Dantrolene, an inhibitor of ryanodine receptors, had no effect but 2-aminoethoxydiphenylborate (2-APB), a membrane-permeable inhibitor of inositol 1,4,5-triphosphate receptor inhibited the sevoflurane-induced release of ACh.
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5.
It is concluded that sevoflurane-induced release of ACh in brain cortical slices involves the mobilization of calcium from IP_{3}-sensitive calcium stores.
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References
Adachi, M., Ikemoto, Y., Kubo, K., and Takuma, C. (1992) Seizure-like movements during induction of anaesthesia with sevoflurane. Br. J. Anaesth. 68:214–215
Adachi, Y. U., Watanabe, H., Higuchi, T., Satoh, T., and Zsilla, G. (2001). Halothane enhances acetylcholine release by decreasing dopaminergic activity in rat striatal slices. Neurochem. Int. 40:189–193.
Adler, E. M., Augustine, G. J., Duffy S. N., and Chariton M. P. (1991). Alien intracellular calcium chelator attenuate neurotransmitter release at the squid giant synapse. J. Neurosci. 11:1496–1507.
Bazil, C. W., and Minneman, K. P. (1989a). Effects of clinically effective concentrations of halothane on adrenergic and cholinergic synapses in rat brain in vitro, J. Pharmacol. Exp. Ther. 248:143–148.
Bazil, C. W., and Minneman, K. P. (1989b). Clinical concentrations of volatile anesthetics reduce depolarization-evoked release of [3H]-norepinephrine, but not [3H]-acetylcholine, from rat cerebral cortex. J. Neurochem. 53:962–965.
Bertorelli, A., Hallstrom, A., Hurd, Y. L., Karlsson, S., Consolo, S., and Ungerstedt, U. (1990). Anaesthesia effects on in vivo acetylcholine transmission: Comparison of radioenzymatic and HPLC assays. Eur. J. Pharmacol. 175:79–83.
Casali, T. A. A., Gomez, R. S., Moraes-Santos, T., Romano-Silva, M. A., Prado, M. A. M., and Gomez, M. V. (1997). Different effects of reducing agents on ω –conotoxin GVIA inhibition of [3H]-acetylcholine release from cortical slices and guinea-pig myenteric plexus. Br. J. Pharmacol. 120:88–92.
Fox, A. P., Nowycky, M. C., and Tsien R. W. (1987). Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurons. J. Physiol. (Lond.) 394:149–172.
Goldberg, A. M., and McCaman, R. E. (1973). The determination of picomole amounts of acetylcholine in mammalian brain. J. Neurochem. 20:1–8.
Gomez, R. S., Gomez, M. V., and Prado, M. A. M. (1996) Inhibition of Na+, K+,-ATPase by ouabain opens calcium channles coupled to acetylcholine release in guinea pig myenteric plexus. J. Neurochem. 66:1440–1447.
Gomez, R. S., Prado, M. A. M., Carazza, F., and Gomez, M. V. (1999). Halothane enhances exocytosis of [3H]-acetylcholine without increasing calcium influx in rat brain cortical slices. Br. J. Pharmacol. 127:679–684.
Gomez, R. S., Gomez, M. V., and Prado, M. A. M. (2000). The effect of isoflurane on the release of [3H]-acetylcholine from rat brain cortical slices. Brain Res. Bull. 52:263–267.
Gomez, R. S., Guatimosim, C., Barbosa, Jr. J., Massensini, A. R., Gomez, M. V., and Prado, M. A. M. (2001). Halothane induced intracellular calcium release in cholinergic cells. Brain Res. 921:106–114.
Griffiths, R., Greiff, J. M. C., Haycock, J., Elton, C. D., Rowbotham, D. J., and Norman, R. I. (1995). Inhibition by halothane of potassium-stimulated acetylcholine release from rat cortical slices. Br. J. Pharmacol. 116:2310–2314.
Griffiths, R., and Norman, R. I. (1993). Effects of anaesthetics on uptake, synthesis and release of transmitters. Br. J. Anaesth. 71:96–107.
Hossain, M. D., and Evers, A. S. (1994). Volatile anesthetic-induced efflux of calcium from IP3-gated stores in clonal (GH3) pituitary cells. Anesthesiology 80:1379–1389.
Johnson, G. V. W., and Hartzell, C. R. (1985). Choline uptake, acetylcholine synthesis and release, and halothane effects in sinaptosomes. Anesth. Analg. 64:395–399.
Katsuoka, M., and Ohnishi, S. T. (1989). Inhalation anaesthetics decrease calcium content of cardiac sarcoplasmic reticulum. Br. J. Anaesth. 62:669–673.
Keifer, J. C., Baghdoyan, H. A., Becker, L., and Lydic, R. (1994). Halothane decreases pontine acetylcholine release and increased EEG spindles. Neuroreport 31:577–580.
Kindler, C. H., Eilers, P., Donohoe, S., Ozer, S., and Bickler, P. E. (1999). Volatile anesthetics increase intracellular calcium in cerebrocortical and hippocampal neuron. Anesthesiology 90:1137–1145.
Komatsu, H., Taie, S., Endo, S., Fukuda, K., Ueki, M., Nogaya, J., and Ogli, K. (1994). Electrical seizures during sevoflurane anesthesia in two pediatric patients with epilepsy. Anesthesiology 81:1535–1537.
Kudoh, A., and Matsuki, A. (2000). Sevoflurane stimulates inositol 1,4,5-triphosphate in skeletal muscle. An esth. Analg. 91:440–445.
Lynch, C., and Frazer, M. J. (1994). Anesthetic alteration of ryanodine binding by cardiac calcium release channels. Biochim. Biophys. Acta. 1194:109–117.
Maruyama, S., Nakade, T., Kann, T., and Mikoshiba, K. (1997). 2-APB, 2- aminoethoxydiphenylborate, a membrane penetrable modulator of Ins(1,4,5)P3-induced Ca2+ release. J. Biochem. 122:495–505.
Miller, M. S., and Gandolfi, A. J. (1979). A rapid, sensitive method for quantifying enflurane in whole blood. Anesthesiology 51:542–544.
Modica, P. A., Tempelhoff, R., and White, P. F. (1990). Pro- and anticonvulsant effects of anesthetics (part I). Anesth. Analg. 70:303–315.
Moe, M. C., Berg-Johnsen, J., Larsen, G. A., Kampenhaug, E. B., and Vinje, M. L. (2003). The effect of isoflurane and sevoflurane on cerebrocortical presynaptic Ca2+ and protein kinase C activity. J. Neurosurg. Anesthesiol. 15:209–214.
Narahashi, J., Moore, J., and Scott, W. R. (1964). Tetrodotoxin blockage of sodium conductance increase in lobster giant axon. J. Gen. Phsyiol. 147:965–974.
Ohta, T., Ito, S., and Ohga, A. (1990). Inhibitory action of dantrolene on Ca-induced Ca2+ release from sarcoplasmic reticulum in guinea pig skeletal muscle. Eur. J. Pharmacol. 178:11–19.
Peppiatt, C. M., Collins, T. J., Mackenzie, I., Conway, S. J., Holmes, A. B., Bootman, M. D., Berridge, M. J., Seo, J. T., and Roderick, H. L. (2003). 2-Aminoethoxydephenylborate (2-APB) antagonizes inositol 1,4,5-triphosphate-induced calcium release, inhibits calcium pumps and has a use-dependent and slowly reversible action on store-operated calcium entry channel. Cell Calcium 34:97–108.
Pocock, G., and Richards, C. D. (1996). Excitatory and inhibitory synaptic mechanism in anaesthesia. Br. J. Anaesth. 71:134–147.
Prado, M. A. M., Gomez, M. V., and Collier, B. (1993). Mobilization of a vesamicol-insensitive pool of acetylcholine from a sympathetic ganglion by ouabain. J. Neurochem. 61:45–56.
Shichino, M. Murakawa, T., Adachi, T., Arai, Y., Miyazaki, Y., and Mori, K. (1998). Effects of inhalation anaesthetics on the release of acetylcholine in the rat cerebral cortex in vivo. Br. J. Anaesth. 80:365–370.
Shichino, T., Murakawa, T., Adachi, T., Arai, S., Nakao, T., Shinomura, J., Kurata, J., and Mori, K. (1997) Effects of isoflurane on in vivo release of acetylcholine in the rat cerebral cortex and striatum. Acta. Anaesthesiol. Scand. 41:1335–1340.
Shichino, M., Murakawa, T., Adachi, T., Arai, Y., Miyazaki, H., Segawa, H., Fukuda, K., and Mori, K. (2002). Effects of xenon on acetylcholine release in the rat cerebral cortex in vivo. Br. J. Anaesth. 88:866–868.
Schotten, M., Greiser, V., Braun, V., Karlein, F., Schoendube, P., and Hanrath, P. (2001). Effect of volatile anesthetics on the force-frequency relation in human ventricular myocardium. Anesthesiology 95:1160–1168.
Taguchi, K., Andresen, M. J., and Hentall, I. D. (1991). Acetylcholine release from the midbrain interpeduncular nucleous during anesthesia. Neuroreport 2:789–792.
Weldon, B. C., Bell, M., and Craddock, T. (2004). The effect of caudal analgesia on emergence agitation in children after sevoflurane versus halothane anesthesia. Anesth. Analg. 98:321–326.
Wells, L. T., and Rasch, D. K. (1999). Emergence “delirium” after sevoflurane anesthesia: A paranoid delusion? Anesth. Analg. 88:1308–1310.
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Silva, J.H., Gomez, R.S., Pinheiro, A.C.N. et al. Acetylcholine Release Induced by the Volatile Anesthetic Sevoflurane in Rat Brain Cortical Slices. Cell Mol Neurobiol 25, 807–818 (2005). https://doi.org/10.1007/s10571-005-4934-x
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DOI: https://doi.org/10.1007/s10571-005-4934-x