Abstract
Methamphetamine (METH) abuse and addiction present a major problem in the United States and globally. Oxidative stress associated with exposure to METH mediates to the large extent METH-evoked neurotoxicity. While there are currently no medications approved for treating METH addiction, its pharmacology provides opportunities for potential pharmacotherapeutic adjuncts to behavioral therapy in the treatment of METH addiction. Opioid receptor agonists can modulate the activity of dopamine neurons and could, therefore, modify the pharmacodynamic effects of METH in the dopaminergic system. Efficacy of the adjunctive medication with buprenorphine has been demonstrated in the treatment of cocaine addiction extending beyond opiate addiction. We investigated the interactions of morphine (10 mg/kg) and buprenorphine (0.01 and 10 mg/kg) with METH (2 mg/kg) affecting striatal dopaminergic transmission. The extracellular concentration of dopamine (DA) and its metabolite 3,4-dihydroxyphenylacetic acid (DOPAC) were determined using brain microdialysis coupled with high performance liquid chromatography with electrochemical detection (HPLC-ED) in the caudate nucleus of adult, awake, male Sprague–Dawley rats. Compared to METH alone, extracellular DA release was prolonged for 140 min without changes in DA peak-effect by combined treatment with morphine/METH. Morphine did not change DOPAC efflux evoked by METH. On the other hand, both buprenorphine doses attenuated the METH-induced DA peak-effect. However, whereas high buprenorphine dose extended DA outflow for 190 min, the low-dose abbreviated DA release. High buprenorphine dose also shortened METH-induced decrease in DOPAC efflux. Data confirm that opiates modulate dopaminergic neurotransmission evoked by METH. Alteration of dopaminergic response to METH challenge under buprenorphine may suggest effectiveness of buprenorphine treatment in METH addiction.
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References
Attila LM, Ahtee L (1984) Retardation of cerebral dopamine turnover after morphine withdrawal and its enhanced acceleration by acute morphine administration in rats. Naunyn Schmiedebergs Arch Pharmacol 327:201–207
Bloms-Funke P, Gillen C, Schuettler AJ, Wnendt S (2000) Agonistic effects of the opioid buprenorphine on the nociceptin/OFQ receptor. Peptides 21:1141–1146
Brown EE, Finlay JM, Wong JT, Damsma G, Fibiger HC (1991) Behavioral and neurochemical interactions between cocaine and buprenorphine: implications for the pharmacotherapy of cocaine abuse. J Pharmacol Exp Ther 256:119–126
Cadet JL, Krasnova IN, Jayanthi S, Lyles J (2007) Neurotoxicity of substituted amphetamines: molecular and cellular mechanisms. Neurotox Res 11:183–202
Ciccocioppo R, Angeletti S, Sanna PP, Weiss F, Massi M (2000) Effect of nociceptin/orphanin FQ on the rewarding properties of morphine. Eur J Pharmacol 404:153–159
Cowan A (2003) Buprenorphine: new pharmacological aspects. Int J Clin Pract Suppl 133:3–8
Di Chiara G, North RA (1992) Neurobiology of opiate abuse. Trends Pharmacol Sci 13:185–193
Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481–1489
Fleckenstein AE, Volz TJ, Riddle EL, Gibb JW, Hanson GR (2007) New insights into the mechanism of action of amphetamines. Ann Rev Pharmacol Toxicol 47:681–698
Foltin R, Fischman MW (1996) Effects of methadone or buprenorphine maintenance on the subjective and reinforcing effects of intravenous cocaine in humans. J Pharmacol Exp Ther 278:1153–1164
Gonzalez G, Oliveto A, Kosten TR (2004) Combating opiate dependence: a comparison among the available pharmacological options. Expert Opin Pharmacother 5:713–725
Hedenqvist P, Hellebrekers LJ (2003) Laboratory animal analgesia, anaesthesia, and euthanasia. In: Hau J, Van Hoosier GL Jr (eds) Handbook of laboratory animal science. CRC Press, Boca Raton, pp 413–455
Hood S, Sorge RE, Stewart J (2007) Chronic buprenorphine reduces the response to sucrose-associated cues in non food-deprived rats. Pharmacol Biochem Behav 86:566–575
Jones SR, Gainetdinov RR, Wightman RM, Caron MG (1998) Mechanisms of amphetamine action revealed in mice lacking the dopamine transporter. J Neurosci 18:1979–1986
Kimmel HL, Justice JB Jr, Holtzman SG (1998) Dissociation of morphine-induced potentiation of turning and striatal dopamine release by amphetamine in the nigrally-lesioned rat. Eur J Pharmacol 346:203–208
Kish SJ (2008) Pharmacologic mechanisms of crystal meth. CMAJ 178:1679–1682
Kosten TR, Kleber HD, Morgan C (1989) Treatment of cocaine abuse with buprenorphine. Biol Psychiatry 26:637–639
Li X, Wang H, Qiu P, Luo H (2008) Proteomic profiling of proteins associated with methamphetamine-induced neurotoxicity in different regions of rat brain. Neurochem Int 52:256–264
Lutfy K, Do T, Maidment NT (2001) Orphanin FQ/nociceptin attenuates motor stimulation and changes in nucleus accumbens extracellular dopamine induced by cocaine in rats. Psychopharmacology 154:1–7
Mello NK, Mendelson JH, Bree MP, Lukas SE (1989) Buprenorphine suppresses cocaine self-administration by rhesus monkeys. Science 245:859–862
Mello NK, Lukas SE, Kamien JB, Mendelson JH, Drieze J, Cone EJ (1992) The effects of chronic buprenorphine treatment on cocaine and food self-administration by rhesus monkeys. J Pharmacol Exp Ther 260:1185–1193
Montoya ID, Gorelick DA, Preston KL, Schroeder JR, Umbricht A, Cheskin LJ, Lange WR, Contoreggi C, Johnson RE, Fudala PJ (2004) Randomized trial of buprenorphine for treatment of concurrent opiate and cocaine dependence. Clin Pharmacol Ther 75:34–48
Mori T, Ito S, Kita T, Narita M, Suzuki T, Sawaguchi T (2006) Effects of mu-, delta- and kappa-opioid receptor agonists on methamphetamine-induced self-injurious behavior in mice. Eur J Pharmacol 532:81–87
Olianas MC, Dedoni S, Boi M, Onali P (2008) Activation of nociceptin/orphanin FQ-NOP receptor system inhibits tyrosine hydroxylase phosphorylation, dopamine synthesis, and dopamine D(1) receptor signaling in rat nucleus accumbens and dorsal striatum. J Neurochem 107:544–556
Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press Limited, London
Pereira FC, Imam SZ, Gough B, Newport GD, Ribeiro CF, Slikker W Jr, Macedo TR, Ali SF (2002) Acute changes in dopamine release and turnover in rat caudate nucleus following a single dose of methamphetamine. J Neural Transm 109:1151–1158
Pereira FC, Macedo TR, Imam SZ, Ribeiro CF, Ali SF (2004) Lack of hydroxyl radical generation upon central administration of methamphetamine in rat caudate nucleus: a microdialysis study. Neurotox Res 6:149–152
Pereira FC, Lourenço ES, Borges F, Morgadinho T, Ribeiro CF, Macedo TR, Ali SF (2006a) Single or multiple injections of methamphetamine increased dopamine turnover but did not decrease tyrosine hydroxylase levels or cleave caspase-3 in caudate-putamen. Synapse 60:185–193
Pereira FC, Lourenço E, Morgadinho T, Milhazes N, Ribeiro CF, Ali SF, Macedo TR (2006b) Methamphetamine, morphine and their combination: acute changes in striatal dopaminergic transmission evaluated by microdialysis in awake rats. Ann NY Acad Sci 1074:160–173
Sakoori K, Murphy NP (2004) Central administration of nociceptin/orphanin FQ blocks the acquisition of conditioned place preference to morphine and cocaine, but not conditioned place aversion to naloxone in mice. Psychopharmacology 172:129–136
Schottenfeld RS, Pakes J, Ziedonis D, Kosten TR (1993) Buprenorphine: dose-related effects on cocaine and opioid use in cocaine-abusing opioid-dependent humans. Biol Psychiatry 34:66–74
Sorge RE, Stewart J (2006) The effects of chronic buprenorphine on intake of heroin and cocaine in rats and its effects on nucleus accumbens dopamine levels during self-administration. Psychopharmacology 188:28–41
Vocci FJ, Appel NM (2007) Approaches to the development of medications for the treatment of methamphetamine dependence. Addiction 102:96–106
Volkow ND, Wang GJ, Telang F, Fowler JS, Logan J, Childress AR, Jayne M, Ma Y, Wong C (2006) Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. J Neurosci 26:6583–6588
Volkow ND, Fowler JS, Wang GJ, Swanson JM, Telang F (2007) Dopamine in drug abuse and addiction: results of imaging studies and treatment implications. Arch Neurol 64:1575–1579
Walsh SL, Preston KL, Stitzer ML, Cone EJ, Bigelow GE (1994) Clinical pharmacology of buprenorphine: ceiling effects at high doses. Clin Pharmacol Ther 55:569–580
Wood PL (1983) Opioid regulation of CNS dopaminergic pathways: a review of methodology, receptor types, regional variations and species differences. Peptides 4:595–601
Wood PL, Rao TS (1991) Morphine stimulation of mesolimbic and mesocortical but not nigrostriatal dopamine release in the rat as reflected by changes in 3-methoxytyramine levels. Neuropharmacology 30:399–401
Zhang Z, Schulteis G (2008) Withdrawal from acute morphine dependence is accompanied by increased anxiety-like behavior in the elevated plus maze. Pharmacol Biochem Behav 89:392–403
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We would like to acknowledge Mr. João Silva from Center for Bioavailability Studies, AIBILI, Coimbra, Portugal for valuable expert technical assistance in HPLC measurements.
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This document has been reviewed in accordance with United States Food and Drug Administration (FDA) policy and approved for publication. Approval does not signify that the contents necessarily reflect the position or opinions of the FDA nor does mention of trade names or commercial products constitute endorsement or recommendation for use. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the FDA.
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Pereira, F.C., Gough, B., Macedo, T.R. et al. Buprenorphine Modulates Methamphetamine-Induced Dopamine Dynamics in the Rat Caudate Nucleus. Neurotox Res 19, 94–101 (2011). https://doi.org/10.1007/s12640-009-9143-9
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DOI: https://doi.org/10.1007/s12640-009-9143-9