Abstract
Anatoxin-a is an important neurotoxin that acts a potent nicotinic acetylcholine receptor agonist. This characteristic makes anatoxin-a an important tool for the study of nicotinic receptors. Anatoxin-a has been used extensively in vitro experiments, however anatoxin-a has never been studied by in vivo microdialysis studies. This study test the effect of anatoxin-a on striatal in vivo dopamine release by microdialysis.
The results of this work show that anatoxin-a evoked dopamine release in a concentration-dependent way. Atropine had not any effect on dopamine release evoked by 3.5 mM anatoxin-a. However, perfusion of nicotinic antagonists mecamylamine and α-bungarotoxin induced a total inhibition of the striatal dopamine release. Perfusion of α7*-receptors antagonists, metillycaconitine or α-bungarotoxin, partially inhibits the release of dopamine stimulated by anatoxin-a. These results show that anatoxin-a can be used as an important nicotinic agonist in the study of nicotinic receptor by in vivo microdialysis technique and also support further in vivo evidences that α7*nicotinic AChRs are implicated in the regulation of striatal dopamine release.
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References
Carmichael WW, Biggs DF, Gorham PR (1975) Toxicology and pharmacological action of anabaena flos-aquae toxin. Science 187:542–544
Biggs DF, Dryden WF (1977) Action of anatoxin-I at neuromuscular junction. Proc West Pharmacol Soc 20: 461–466
Carmichael WW (1989) Freshwater cyanobacteria (blue-green algae) toxins. In: Ownby CL, Odell GV, (Eds). Natural Toxins: Characterization, Pharmacology and Therapeutics. Pergamon Press, Oxford, pp. 3–16
Spivak CE, Witkop B, Albuquerque EX (1980) Anatoxin-a: a novel, potent agonist at the nicotinic receptor. Mol Pharmacol 18: 384–394
Thomas P, Stephens M, Wilkie G, Amar M, Lunt GG, Whiting P, Gallagher T, Pereira E, Alkondon M, Albuquerque EX, Wonnacott S (1993) (+)-Anatoxin-a is a potent agonist at neuronal nicotinic acetylcholine receptors. J Neurochem 60: 2308–2311
Amar M, Thomas P, Johnson C, Lunt GG, Wonnacott S (1993) Agonist pharmacology of the neuronal alpha 7 nicotinic receptor expressed in Xenopus oocytes. FEBS Lett 327: 284–288
Swanson KL, Allen CN, Aronstam RS, Rapoport H, Albuquerque EX (1986) Molecular mechanisms of the potent and stereospecific nicotinic receptor agonist (+)-anatoxin-a. Mol Pharmacol 29: 250–257
Aronstam RS, Witkop B (1981) Anatoxin-a interactions with cholinergic synaptic molecules. Proc Natl Acad Sci USA 78: 4639–4643
Macallan DR, Lunt GG, Wonnacott S, Swanson KL, Rapoport H, Albuquerque EX (1988) Methyllycaconitine and (+)-anatoxin-a differentiate between nAChRs in vertebrate and invertebrate nervous systems. FEBS Lett 226: 357–363
Romanelli MN, Gualtieri F (2003) Cholinergic nAChRs: competitive ligands, allosteric modulators, and their potential applications. Med Res Rev 23: 393–426
Seguela P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW (1993) Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium. J Neurosci 13: 596–604
Zoli M, Lena C, Picciotto MR, Changeux JP (1998) Identification of four classes o f brain nAChRs using beta2 mutant mice. J Neurosci 18: 4461–4472
Zoli M, Moretti M, Zanardi A, McIntosh JM, Clementi F, Gotti C (2002) Identification of the nicotinic receptor subtypes expressed on dopaminergic terminals in the rat striatum. J Neurosci 22: 8785–8789
Dani JA (2001) Overview of nAChRs and their roles in the central nervous system. Biol Psychiatry 49: 166–174
Vizi ES, Lendvai B (1999) Modulatory role of presynaptic nAChRs in synaptic and non-synaptic chemical communication in the central nervous system. Brain Res Rev 30: 219–235
Wonnacott S (1997) Presynaptic nicotinic Ach receptors. Trends Neurosci 20: 92–98
Cao YJ, Surowy CS, Puttfarcken PS (2005) Nicotinic acetylcholine receptor-mediated [3H]dopamine release from hippocampus. J Pharmacol Exp Ther 312: 1298–1304
Clarke PB, Reuben M (1996) Release of [3H]-noradrenaline from rat hippocampal synaptosomes by nicotine: mediation by different nicotinic receptor subtypes from striatal [3H]-dopamine release. Br J Pharmacol 117: 595–606
Sershen H, Balla A, Lajtha A, Vizi ES (1997) Characterization of nAChRs involved in the release of noradrenaline from the hippocampus. Neuroscience 77: 121–130
Wilkie GI, Hutson P, Sullivan JP, Wonnacott S (1996) Pharmacological characterization of a nicotinic autoreceptor in rat hippocampal synaptosomes. Neurochem Res 21: 1141–1148
Marchi M, Lupinacci M, Bernero E, Bergaglia F, Raiteri M (1999) nAChRs modulating ACh release in rat cortical synaptosomes: role of Ca2+ ions in their function and desensitization. Neurochem Int 34: 319–328
Marchi M, Risso F, Viola C, Cavazzani P, Raiteri M (2002) Direct evidence that release-stimulating alpha7* nicotinic cholinergic receptors are localized on human and rat brain glutamatergic axon terminals. J Neurochem 80: 1071–1078
Anderson DJ, Puttfarcken PS, Jacobs I, Faltynek C (2000) Assessment of nicotinic acetylcholine receptor-mediated release of [(3)H]-norepinephrine from rat brain slices using a new 96-well format assay. Neuropharmacology 39: 2663–2672
Kaiser SA, Soliakov L, Harvey SC, Luetje CW, Wonnacott S (1998) Differential inhibition by alpha-conotoxin-MII of the nicotinic stimulation of [3H] dopamine release from rat striatal synaptosomes and slices. J Neurochem 70: 1069–1076
Kaiser S, Wonnacott S (2000) α-Bungarotoxin-Sensitive nAChRs indirectly modulate [3H]dopamine release in rat striatal slices via glutamate release. Mol Pharmacol 58: 312–318
Soliakov L, Gallagher T, Wonnacott S (1995) Anatoxin-a-evoked 3[H]dopamine release from rat striatal synaptosomes. Neuropharmacology 34: 1535–1541
Soliakov L, Wonnacott S (1996) Voltage-sensitive Ca2+ channels involved in nicotinic receptor-mediated [3H]dopamine release from rat striatal synaptosomes. J Pharmacol 35: 163–170
Soliakov L., Wonnacott S (2001) Involvement of protein kinase C in the presynaptic nicotinic modulation of [(3)H]-dopamine release from rat striatal synaptosomes. Br J Pharmacol 132: 785–791
Wonnacott S, Kaiser S, Mogg A, Soliakov L, Jones IW (2000) Presynaptic nAChRs modulating dopamine release in the rat striatum. Eur J Pharmacol 393: 51–58
Björklund A, Lindvall, O (1984) In: Björklund A, Hökfelt, T (eds), Classical Transmitters in the CNS Part I. Elsevier, Amsterdam, pp 55–122
Butcher LL, Woolf NJ (1982) Monoaminergic-cholinergic relationships and the chemical communication matrix of the substantia nigra and neostriatum. Brain Res Bull 9: 475–492
Zhou FM, Liang Y, Dani JA (2001) Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat Neurosci 4: 1224–1229
Alfonso M, Duran R, Campos F, Perez-Vences D, Faro LR, Arias B (2003) Mechanisms underlying domoic acid-induced dopamine release from striatum: an in vivo microdialysis study. Neurochemistry Res 10: 1487–1493
Paxinos G, Watson C (1986) The rat brain: In Stereotaxic Coordinates, (4Th edition). Academic Press, New York
Fu Y, Matta SG, Gao W, Sharp BM (2000) Local alpha-bungarotoxin-sensitive nAChRs in the nucleus accumbens modulate nicotine-stimulated dopamine secretion in vivo. Neuroscience 101: 369–375
Marshall D, Soliakov L, Redfern P, Wonnacott S (1996) Tetrodotoxin-sensitivity of nicotine-evoked dopamine release from rat striatum. Neuropharmacology 35: 1531–1536
Marshall DL, Redfern PH, Wonnacott S (1997) Presynaptic nicotinic modulation of dopamine release in the three ascending pathways studied by in vivo microdialysis: comparison of naive and chronic nicotine-treated rats. J Neurochem 68: 1511–1519
Nisell M, Nomikos GG, Svensson TH (1994) Infusion of nicotine in the ventral tegmental area or the nucleus accumbens of the rat differentially affects accumbal dopamine release. Pharmacol Toxicol 75: 348–352
Rahman S, McBride WJ (2002) Involvement of GABA and cholinergic receptors in the nucleus accumbens on feedback control of somatodendritic dopamine release in the ventral tegmental area. J Neurochem 80: 646–654
Rahman S, Zhang J, Corrigall WA (2004) Local perfusion of nicotine differentially modulates somatodendritic dopamine release in the rat ventral tegmental area after nicotine preexposure. Neurochem Res 29: 1687–1693
Reid RT, Lloyd GK, Rao TS (1999) Pharmacological characterization of nicotine-induced acetylcholine release in the rat hippocampus in vivo: evidence for a permissive dopamine synapse. Br J Pharmacol 127: 1486–1494
Rossi S, Singer S, Shearman E, Sershen H, Lajtha A (2005) The effects of cholinergic and dopaminergic antagonists on nicotine-induced cerebral neurotransmitter changes. Neurochem Res 30: 541–558
Whitehead KJ, Rose S, Jenner P (2001) Involvement of intrinsic cholinergic and GABAergic innervation in the effect of NMDA on striatal dopamine efflux and metabolism as assessed by microdialysis studies in freely moving rats. Eur J Neurosci 14: 851–860
Durán R, Alfonso M, Arias B (1998) Determination of biogenic amines in rat brain dialysates by High Performance Liquid Chromatography. J Liq Chromatogr Rel Technol 21: 2799–2811
Gago-Martinez A, Rellan S, Campos F, Alfonso M, Durán R (2003) HPLC determination of anatoxin-a An application for the evaluation of this Diffusion rate through the microdialysis probe. The 117th AOAC International Annual Meeting and Exposition. Atlanta
Varanda WA, Aracava Y, Sherby SM, VanMeter WG, Eldefrawi ME, Albuquerque EX (1985) The acetylcholine receptor of the neuromuscular junction recognizes mecamylamine as a noncompetitive antagonist. Mol Pharmacol 28: 128–137
Chen D, Patrick JW (1997) The alpha-bungarotoxin-binding nicotinic acetylcholine receptor from rat brain contains only the alpha7 subunit. J Biol Chem 272: 24024–24029
Role LW, Berg DK (1996) nAChRs in the development and modulation of CNS synapses. Neuron 16: 1077–1085
Champtiaux N, Han ZY, Bessis A, Rossi FM, Zoli M, Marubio L, McIntosh JM, Changeux JP (2002) Distribution and pharmacology of alpha 6-containing nicotinic acetylcholine receptors analyzed with mutant mice. J Neurosci 22: 1208–1217
el-Bizri H, Clarke PB (1994) Blockade of nicotinic receptor-mediated release of dopamine from striatal synaptosomes by chlorisondamine administered in vivo. Br J Pharmacol 111: 414–418
Grady S, Marks MJ, Wonnacott S, Collins AC (1992) Characterization of nicotinic receptor-mediated [3H]dopamine release from synaptosomes prepared from mouse striatum. J Neurochem 59: 848–856
Marubio LM, Gardier AM, Durier S, David D, Klink R, Arroyo-Jimenez MM, McIntosh JM, Rossi F, Champtiaux N, Zoli M, Changeux JP (2003) Effects of nicotine in the DAergic system of mice lacking the alpha4 subunit of neuronal nicotinic acetylcholinereceptors. Eur J Neurosci 17: 1329–1337
Rapier C, Lunt GG, Wonnacott S (1988) Stereoselective nicotine-induced release of dopamine from striatal synaptosomes: concentration dependence and repetitive stimulation. J Neurochem 50: 1123–1130
Nicke A, Wonnacott S, Lewis RJ (2004) Alpha-conotoxins as tools for the elucidation of structure and function of neuronal nicotinic acetylcholine receptor subtypes. Eur J Biochem 271: 2305–2319
Miller DK, Crooks PA, Dwoskin LP (2000) Lobeline inhibits nicotine-evoked [(3)H]dopamine overflow from rat striatal slices and nicotine-evoked (86)Rb(+) efflux from thalamic synaptosomes. Neuropharmacology 39: 2654–2662
Miller DK, Harrod SB, Green TA, Wong MY, Bardo MT, Dwoskin LP (2003) Lobeline attenuates locomotor stimulation induced by repeated nicotine administration in rats. Pharmacol Biochem Be 74: 279–286
Sacaan AI, Menzaghi F, Dunlop JL, Correa LD, Whelan KT, Lloyd GK (1996) Epibatidine: a nicotinic acetylcholine receptor agonist releases monoaminergic neurotransmitters: in vitro and in vivo evidence in rats. J Pharmacol Exp Ther 276: 509–515
Sacaan AI, Dunlop JL, Lloyd GK (1995) Pharmacological characterization of neuronal acetylcholine gated ion channel receptor-mediated hippocampal norepinephrine and striatal dopamine release from rat brain slices. J Pharmacol Exp Ther 274: 224–230
Grilli M, Parodi M, Raiteri M, Marchi M (2005) Chronic nicotine differentially affects the function of nicotinic receptor subtypes regulating neurotransmitter release. J Neurochem 93: 1353–1560
Risso F, Parodi M, Grilli M, Molfino F, Raiteri M, Marchi M (2004) Chronic nicotine causes functional upregulation of ionotropic glutamate receptors mediating hippocampal noradrenaline and striatal dopamine release. Neurochem Int 44: 293–301
Sakurai Y, Takano Y, Kohjimoto Y, Honda K, Kamiya HO (1982) Enhancement of [3H]dopamine release and its [3H]metabolites in rat striatum by nicotinic drugs. Brain Res 242: 99–106
Salminen O, Murphy KL, McIntosh JM, Drago J, Marks MJ, Collins AC, Grady SR (2004) Subunit composition and pharmacology of two classes of striatal presynaptic nicotinic acetylcholine receptors mediating dopamine release in mice. Mol Pharmacol 65: 1526–1535
Carboni E, Silvagni A, Rolando MT, Di Chiara G (2000) Stimulation of in vivo dopamine transmission in the bed nucleus of stria terminalis by reinforcing drugs. J Neurosci 2000 20: 1–5
Janhunen S, Ahtee L (2004) Comparison of the effects of nicotine and epibatidine on the striatal extracellular dopamine. Eur J Pharmacol 494: 167–177
Lecca D, Shim I, Costa E, Javaid JI (2000) Striatal application of nicotine, but not of lobeline, attenuates dopamine release in freely moving rats. Neuropharmacology 39: 88–98
Tani Y, Saito K, Imoto M, Ohno T (1998) Pharmacological characterization of nicotinic receptor-mediated acetylcholine release in rat brain—an in vivo microdialysis study. Eur J Pharmacol 351: 181–188
Sacaan AI, Reid RT, Santori EM, Adams P, Correa LD, Mahaffy LS, Bleicher L, Cosford ND, Stauderman KA, McDonald IA, Rao TS, Lloyd GK (1997) Pharmacological characterization of SIB-1765F: a novel cholinergic ion channel agonist. J Pharmacol Exp Ther 280: 373–383
Chavez-Noriega LE, Crona JH, Washburn MS, Urrutia A, Elliott KJ, Johnson EC (1997) Pharmacological characterization of recombinant human neuronal nicotinic acetylcholine receptors h alpha 2 beta 2, h alpha 2 beta 4, h alpha 3 beta 2, h alpha 3 beta 4, h alpha 4 beta 2, h alpha 4 beta 4 and h alpha 7 expressed in Xenopus oocytes. J Pharmacol Exp Ther 280: 346–356
Shimosato K, Nagao N, Watanabe S, Kitayama S (2003) Suppressive effects of trihexyphenidyl on methamphetamine-induced dopamine release as measured by in vivo microdialysis. Synapse 49: 47–54
Smolders I, Bogaert L, Ebinger G, Michotte Y (1997) Muscarinic modulation of striatal dopamine, glutamate, and GABA release, as measured with in vivo microdialysis. J Neurochem 68: 1942–1948
Mogg AJ, Whiteaker P, McIntosh JM, Marks M, Collins AC, Wonnacott S (2002) Methyllycaconitine is a potent antagonist of alpha-conotoxin-MII-sensitive presynaptic nicotinic acetylcholine receptors in rat striatum. J Pharmacol Exp Ther 302: 197–204
Cao YJ, Surowy CS, Puttfarcken PS (2005) Different nicotinic acetylcholine receptor subtypes mediating striatal and prefrontal cortical [3H]dopamine release. Neuropharmacology 48: 72–79
Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383: 713–716
Hamada M, Higashi H, Nairn AC, Greengard P, Nishi A (2004) Differential regulation of dopamine D1 and D2 signaling by nicotine in neostriatal neurons. J Neurochem 90: 1094–1103
Acknowledgements
This research was supported by grants from the Direction General de Investigación-Ministerio de Ciencia y Tecnología (BQU2002–00083) and the Xunta de Galicia (PGIDT02PXIB30101PR).
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Campos, F., Durán, R., Vidal, L. et al. In vivo Effects of the Anatoxin-a on Striatal Dopamine Release. Neurochem Res 31, 491–501 (2006). https://doi.org/10.1007/s11064-006-9042-x
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DOI: https://doi.org/10.1007/s11064-006-9042-x