Ultra-low doses of methamphetamine suppress 5-hydroxytryptophan-induced head-twitch response in mice during aging.
Journal
Behavioural pharmacology
ISSN: 1473-5849
Titre abrégé: Behav Pharmacol
Pays: England
ID NLM: 9013016
Informations de publication
Date de publication:
05 Aug 2024
05 Aug 2024
Historique:
medline:
31
8
2024
pubmed:
31
8
2024
entrez:
29
8
2024
Statut:
aheadofprint
Résumé
The head-twitch response (HTR) in mice is considered a behavioral assay for activation of 5-HT2A receptors in rodents. It can be evoked by direct-acting 5-HT2A receptor agonists such as (±)-2,5-dimethoxy-4-iodoamphetamine, 5-hydroxytryptamine precursors [e.g. 5-hydroxytryptophan (5-HTP)], and selective 5-hydroxytryptamine releasers (e.g. d-fenfluramine). The nonselective monoamine releaser methamphetamine by itself does not produce the HTR but can suppress both (±)-2,5-dimethoxy-4-iodoamphetamine- and d-fenfluramine-evoked HTRs across ages via concomitant activation of the inhibitory serotonergic 5-HT1A or adrenergic α2 receptors. Currently, we investigated: (1) the ontogenic development of 5-HTP-induced HTR in 20-, 30-, and 60-day-old mice; (2) whether pretreatment with ultra-low doses of methamphetamine (0.1, 0.25, and 0.5 mg/kg, intraperitoneally) can suppress the frequency of 5-HTP-induced HTR at different ages; and (3) whether the inhibitory serotonergic 5-HT1A or adrenergic α2 receptors may account for the potential inhibitory effect of methamphetamine on 5-HTP-induced HTR. In the presence of a peripheral decarboxylase inhibitor (carbidopa), 5-HTP produced maximal frequency of HTRs in 20-day-old mice which rapidly subsided during aging. Methamphetamine dose-dependently suppressed 5-HTP-evoked HTR in 20- and 30-day-old mice. The selective 5-HT1A-receptor antagonist WAY 100635 reversed the inhibitory effect of methamphetamine on 5-HTP-induced HTR in 30-day-old mice, whereas the selective adrenergic α2-receptor antagonist RS 79948 failed to reverse methamphetamine's inhibition at any tested age. These findings suggest an ontogenic rationale for methamphetamine's inhibitory 5-HT1A receptor component of action in its suppressive effect on 5-HTP-induced HTR during development which is not maximally active at a very early age.
Identifiants
pubmed: 39206775
doi: 10.1097/FBP.0000000000000789
pii: 00008877-990000000-00093
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
Copyright © 2024 Wolters Kluwer Health, Inc. All rights reserved.
Références
Amargos-Bosch M, Bortolozzi A, Puig MV, Serrats J, Adell A, Celada P, et al. (2004). Co-expression and in vivo interaction of serotonin1A and serotonin2A receptors in pyramidal neurons of prefrontal cortex. Cereb Cortex 14:281–299.
Andrade R (2011). Serotonergic regulation of neuronal excitability in the prefrontal cortex. Neuropharmacology 61:382–386.
Andrade R, Malenka RC, Nicoll RA (1986). A G protein couples serotonin and GABAB receptors to the same channels in hippocampus. Science 234:1261–1265.
Araneda R, Andrade R (1991). 5-Hydroxytryptamine2 and 5-hydroxytryptamine 1A receptors mediate opposing responses on membrane excitability in rat association cortex. Neuroscience 40:399–412.
Arnt J, Hyttel J (1989). Facilitation of 8-OHDPAT-induced forepaw treading of rats by the 5-HT2 agonist DOI. Eur J Pharmacol 161:45–51.
Arranz B, Eriksson A, Mellerup E, Plenge P, Marcusson J (1993). Effect of aging in human cortical pre- and postsynaptic serotonin binding sites. Brain Res 620:163–166.
Ashby CR Jr, Edwards E, Wang RY (1994). Electrophysiological evidence for a functional interaction between 5-HT1A and 5-HT2A receptors in the rat medial prefrontal cortex: an iontophoretic study. Synapse 17:173–181.
Barnes NM, Ahern GP, Becamel C, Bockaert J, Camilleri M, Chaumont-Dubel S, et al. (2021). International union of basic and clinical pharmacology. CX. Classification of receptors for 5-hydroxytryptamine; pharmacology and function. Pharmacol Rev 73:310–520.
Beakley BD, Kaye AM, Kaye AD (2015). Tramadol, pharmacology, side effects, and serotonin syndrome: a review. Pain Physician 18:395–400.
Beique JC, Campbell B, Perring P, Hamblin MW, Walker P, Mladenovic L, et al. (2004). Serotonergic regulation of membrane potential in developing rat prefrontal cortex: coordinated expression of 5-hydroxytryptamine (5-HT)1A, 5-HT2A, and 5-HT7 receptors. J Neurosci 24:4807–4817.
Canal CE, Morgan D (2012). Head-twitch response in rodents induced by the hallucinogen 2,5-dimethoxy-4-iodoamphetamine: a comprehensive history, a re-evaluation of mechanisms, and its utility as a model. Drug Test Anal 4:556–576.
Canal CE, Booth RG, Morgan D (2013). Support for 5-HT2C receptor functional selectivity in vivo utilizing structurally diverse, selective 5-HT2C receptor ligands and the 2,5-dimethoxy-4-iodoamphetamine elicited head-twitch response model. Neuropharmacology 70:112–121.
Canedo L, Cantu RG, Hernandez RJ (2003). Magnetic field exposure during gestation: pineal and cerebral cortex serotonin in the rat. Int J Dev Neurosci 21:263–266.
Carr DB, Sesack SR (2000). Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J Neurosci 20:3864–3873.
Celada P, Puig MV, Diaz-Mataix L, Artigas F (2008). The hallucinogen DOI reduces low-frequency oscillations in rat prefrontal cortex: reversal by antipsychotic drugs. Biol Psychiatry 64:392–400.
Chemel BR, Roth BL, Armbruster B, Watts VJ, Nichols DE (2006). WAY-100635 is a potent dopamine D4 receptor agonist. Psychopharmacolology (Berl) 188:244–251.
Chiu HY, Chan MH, Lee MY, Chen ST, Zhan ZY, Chen HH (2014). Long-lasting alterations in 5-HT2A receptor after a binge regimen of methamphetamine in mice. Int J Neuropsychopharmacol 17:1647–1658.
Claustre Y, Rouquier L, Scatton B (1988). Pharmacological characterization of serotonin-stimulated phosphoinositide turnover in brain regions of the immature rat. J Pharmacol Exp Ther 244:1051–1056.
Cornea-Hebert V, Riad M, Wu C, Singh SK, Descarries L (1999). Cellular and subcellular distribution of the serotonin 5-HT2A receptor in the central nervous system of adult rat. J Comp Neurol 409:187–209.
Courtney KE, Ray LA (2014). Methamphetamine: an update on epidemiology, pharmacology, clinical phenomenology, and treatment literature. Drug Alcohol Depend 143:11–21.
Cruickshank CC, Dyer KR (2009). A review of the clinical pharmacology of methamphetamine. Addiction 104:1085–1099.
Darmani NA (1993). Role of the inhibitory adrenergic alpha 2 and serotonergic 5-HT1A components of cocaine’s actions on the DOI-induced head-twitch response in 5-HT2-receptor supersensitive mice. Pharmacol Biochem Behav 45:269–274.
Darmani NA (1998). Cocaine and selective monoamine uptake blockers (sertraline, nisoxetine, and GBR 12935) prevent the d-fenfluramine-induced head-twitch response in mice. Pharmacol Biochem Behav 60:83–90.
Darmani NA, Johnson JC (2004). Central and peripheral mechanisms contribute to the antiemetic actions of delta-9-tetrahydrocannabinol against 5-hydroxytryptophan-induced emesis. Eur J Pharmacol 488:201–212.
Darmani NA, Reeves SL (1996). The stimulatory and inhibitory components of cocaine’s actions on the 5-HTP-induced 5-HT2A receptor response. Pharmacol Biochem Behav 55:387–396.
Darmani NA, Martin BR, Glennon RA (1990a). Withdrawal from chronic treatment with (±)-DOI causes super-sensitivity to 5-HT2 receptor-induced head-twitch behaviour in mice. Eur J Pharmacol 186:115–118.
Darmani NA, Martin BR, Pandey U, Glennon RA (1990b). Do functional relationships exist between 5-HT1A and 5-HT2 receptors? Pharmacol Biochem Behav 36:901–906.
Darmani NA, Martin BR, Pandey U, Glennon RA (1991). Inhibition of 5-HT2 receptor-mediated head-twitch response by cocaine via indirect stimulation of adrenergic alpha 2 and serotonergic 5-HT1A receptors. Pharmacol Biochem Behav 38:353–357.
Darmani NA, Shaddy J, Gerdes CF (1996). Differential ontogenesis of three DOI-induced behaviors in mice. Physiol Behav 60:1495–1500.
Darmani NA, Shaddy J, Elder EL (1997). Prolonged deficits in presynaptic serotonin function following withdrawal from chronic cocaine exposure as revealed by 5-HTP-induced head-twitch response in mice. J Neural Transm (Vienna) 104:1229–1247.
De Almeida J, Mengod G (2007). Quantitative analysis of glutamatergic and GABAergic neurons expressing 5-HT(2A) receptors in human and monkey prefrontal cortex. J Neurochem 103:475–486.
Dreshfield-Ahmad LJ, Thompson DC, Schaus JM, Wong DT (2000). Enhancement in extracellular serotonin levels by 5-hydroxytryptophan loading after administration of WAY 100635 and fluoxetine. Life Sci 66:2035–2041.
Endo Y (1985). Evidence that the accumulation of 5-hydroxytryptamine in the liver but not in the brain may cause the hypoglycaemia induced by 5-hydroxytryptophan. Br J Pharmacol 85:591–598.
Fagerholm V, Philipp M, Hein L, Scheinin M (2004). [Ethyl-3H]RS-79948-197 alpha2-adrenoceptor autoradiography validation in alpha2-adrenoceptor knockout mice. Eur J Pharmacol 497:301–309.
Fantegrossi WE, Simoneau J, Cohen MS, Zimmerman SM, Henson CM, Rice KC, et al. (2010). Interaction of 5-HT2A and 5-HT2C Receptors in R(−)-2,5-dimethoxy-4-iodoamphetamine-elicited head twitch behavior in mice. J Pharmacol Exp Ther 335:728–734.
Farrell MS, McCorvy JD, Huang X, Urban DJ, White KL, Giguere PM, et al. (2016). In vitro and in vivo characterization of the alkaloid nuciferine. PLoS One 11:e0150602.
Gartside SE, Cowen PJ, Sharp T (1992). Effect of 5-hydroxy-l-tryptophan on the release of 5-HT in rat hypothalamus in vivo as measured by microdialysis. Neuropharmacology 31:9–14.
Gonzalez-Maeso J, Yuen T, Ebersole BJ, Wurmbach E, Lira A, Zhou M, et al. (2003). transcriptome fingerprints distinguish hallucinogenic and nonhallucinogenic 5-hydroxytryptamine 2A receptor agonist effects in mouse somatosensory cortex. J Neurosci 23:8836–8843.
Gonzalez-Maeso J, Weisstaub NV, Zhou M, Chan P, Ivic L, Ang R, et al. (2007). Hallucinogens recruit specific cortical 5-HT(2A) receptor-mediated signaling pathways to affect behavior. Neuron 53:439–452.
Goodfellow NM, Benekareddy M, Vaidya VA, Lambe EK (2009). Layer II/III of the prefrontal cortex: Inhibition by the serotonin 5-HT1A receptor in development and stress. J Neurosci 29:10094–10103.
Grahame-Smith DG (1971). Studies in vivo on the relationship between brain tryptophan, brain 5-HT synthesis and hyperactivity in rats treated with a monoamine oxidase inhibitor and l-tryptophan. J Neurochem 18:1053–1066.
Halberstadt AL, Heijden I, Ruderman MA, Risbrough VB, Gingrich JA, Geyer MA, et al. (2009). 5-HT(2A) and 5-HT(2C) receptors exert opposing effects on locomotor activity in mice. Neuropsychopharmacology 34:1958–1967.
Halberstadt AL, Chatha M, Klein AK, Wallach J, Brandt SD (2020). Correlation between the potency of hallucinogens in the mouse head-twitch response assay and their behavioral and subjective effects in other species. Neuropharmacology 167:107933.
Hartvig P, Tedroff J, Lindner KJ, Bjurling P, Chang CW, Tsukada H, et al. (1993). Positron emission tomographic studies on aromatic l-amino acid decarboxylase activity in vivo for l-dopa and 5-hydroxy-l-tryptophan in the monkey brain. J Neural Transm Gen Sect 94:127–135.
Heal DJ, Philpot J, O’shaughnessy KM, Davies CL (1986). The influence of central noradrenergic function on 5-HT2-mediated head-twitch responses in mice: possible implications for the actions of antidepressant drugs. Psychopharmacology (Berl) 89:414–420.
Hongyan L, Zhenyang S, Chunyan W, Qingqing P (2017). Lipopolysaccharide aggravated DOI-induced Tourette syndrome: elaboration for recurrence of Tourette syndrome. Metab Brain Dis 32:1929–1934.
Hotchkiss AJ, Morgan ME, Gibb JW (1979). The long-term effects of multiple doses of methamphetamine on neostriatal tryptophan hydroxylase, tyrosine hydroxylase, choline acetyltransferase and glutamate decarboxylase activities. Life Sci 25:1373–1378.
Jakab RL, Goldman-Rakic PS (1998). 5-Hydroxytryptamine2A serotonin receptors in the primate cerebral cortex: possible site of action of hallucinogenic and antipsychotic drugs in pyramidal cell apical dendrites. Proc Natl Acad Sci U S A 95:735–740.
Jodo E, Chiang C, Aston-Jones G (1998). Potent excitatory influence of prefrontal cortex activity on noradrenergic locus coeruleus neurons. Neuroscience 83:63–79.
Jørgensen H, Knigge U, Kjaer A, Warberg J (1999). Adrenocorticotropic hormone secretion in rats induced by stimulation with serotonergic compounds. J Neuroendocrinol 11:283–290.
Kalsner S, Abdali SA (2001). Rate-independent inhibition by norepinephrine of 5-HT release from the somadendritic region of serotonergic neurons. Brain Res Bull 55:761–765.
Kogias G, Zheng F, Kalinichenko LS, Kornhuber J, Alzheimer C, Mielenz D, et al. (2020). Swiprosin1/EFhd2 is involved in the monoaminergic and locomotor responses of psychostimulant drugs. J Neurochem 154:424–440.
Levi G, Raiteri M (1993). Carrier-mediated release of neurotransmitters. Trends Neurosci 16:415–419.
Marcusson JO, Morgan DG, Winblad B, Finch CE (1984). Serotonin-2 binding sites in human frontal cortex and hippocampus. Selective loss of S-2A sites with age. Brain Res 311:51–56.
Martin JR, Bös M, Jenck F, Moreau J, Mutel V, Sleight AJ, et al. (1998). 5-HT2C receptor agonists: pharmacological characteristics and therapeutic potential. J Pharmacol Exp Ther 286:913–924.
Martin-Ruiz R, Puig MV, Celada P, Shapiro DA, Roth BL, Mengod G, et al. (2001). Control of serotonergic function in medial prefrontal cortex by serotonin-2A receptors through a glutamate-dependent mechanism. J Neurosci 21:9856–9866.
Millan MJ, Rivet JM, Canton H, Lejeune F, Bervoets K, Brocco M, et al. (1992). S 14671: a naphtylpiperazine 5-hydroxytryptamine1A agonist of exceptional potency and high efficacy possessing antagonist activity at 5-hydroxytryptamine1C/2 receptors. J Pharmacol Exp Ther 262:451–463.
Nabeshima T, Yamada K, Hayashi T, Hasegawa T, Ishihara S, Kameyama T, et al. (1994). Changes in muscarinic cholinergic, PCP, GABAA, D1, and 5-HT2A receptor binding, but not in benzodiazepine receptor binding in the brains of aged rats. Life Sci 55:1585–1593.
Nguyen EC, Mccracken KA, Liu Y, Pouw B, Matsumoto RR (2005). Involvement of sigma (sigma) receptors in the acute actions of methamphetamine: receptor binding and behavioral studies. Neuropharmacology 49:638–645.
Perry KW, Fuller RW (1993). Extracellular 5-hydroxytryptamine concentration in rat hypothalamus after administration of fluoxetine plus l-5-hydroxytryptophan. J Pharm Pharmacol 45:759–761.
Pranzatelli MR, Galvan I, Tailor PT (1996). Human brainstem serotonin receptors: characterization and implications for subcortical myoclonus. Clin Neuropharmacol 19:507–514.
Quinton MS, Yamamoto BK (2006). Causes and consequences of methamphetamine and MDMA toxicity. AAPS J 8:E337–E347.
Reese EA, Bunzow JR, Arttamangkul S, Sonders MS, Grandy DK (2007). Trace amine-associated receptor 1 displays species-dependent stereoselectivity for isomers of methamphetamine, amphetamine, and para-hydroxyamphetamine. J Pharmacol Exp Ther 321:178–186.
Ricaurte GA, Schuster CR, Seiden LS (1980). Long-term effects of repeated methylamphetamine administration on dopamine and serotonin neurons in the rat brain: a regional study. Brain Res 193:153–163.
Riga MS, Soria G, Tudela R, Artigas F, Celada P (2014). The natural hallucinogen 5-MeO-DMT, component of Ayahuasca, disrupts cortical function in rats: reversal by antipsychotic drugs. Int J Neuropsychopharmacol 17:1269–1282.
Roth BL, Hamblin MW, Ciaranello RD (1991). Developmental regulation of 5-HT2 and 5-HT1c mRNA and receptor levels. Brain Res Dev Brain Res 58:51–58.
Rutz S, Riegert C, Rothmaier AK, Jackisch R (2007). Presynaptic modulation of 5-HT release in the rat septal region. Neuroscience 146:643–658.
Santana N, Bortolozzi A, Serrats J, Mengod G, Artigas F (2004). Expression of serotonin1A and serotonin2A receptors in pyramidal and GABAergic neurons of the rat prefrontal cortex. Cereb Cortex 14:1100–1109.
Schreiber R, Brocco M, Audinot V, Gobert A, Veiga S, Millan MJ (1995). (1-(2,5-dimethoxy-4 iodophenyl)-2-aminopropane)-induced head-twitches in the rat are mediated by 5-hydroxytryptamine (5-HT) 2A receptors: modulation by novel 5-HT2A/2C antagonists, D1 antagonists and 5-HT1A agonists. J Pharmacol Exp Ther 273:101–112.
Steinkellner T, Freissmuth M, Sitte HH, Montgomery T (2011). The ugly side of amphetamines: short- and long-term toxicity of 3,4-methylenedioxymethamphetamine (MDMA, ‘Ecstasy’), methamphetamine and D-amphetamine. Biol Chem 392:103–115.
Sulzer D, Sonders MS, Poulsen NW, Galli A (2005). Mechanisms of neurotransmitter release by amphetamines: a review. Prog Neurobiol 75:406–433.
Sun Y, Chebolu S, Henry D, Lankireddy S, Darmani NA (2022). An ontogenic study of receptor mechanisms by which acute administration of low-doses of methamphetamine suppresses DOI-induced 5-HT(2A)-receptor mediated head-twitch response in mice. BMC Neurosci 23:2.
Sun Y, Chebolu S, Skegrud S, Kamali S, Darmani NA (2023). Effects of low-doses of methamphetamine on d-fenfluramine-induced head-twitch response (HTR) in mice during ageing and c-fos expression in the prefrontal cortex. BMC Neurosci 24:2.
Tang AH, Franklin SR, Himes CS, Smith MW, Tenbrink RE (1997). PNU-96415E, a potential antipsychotic agent with clozapine-like pharmacological properties. J Pharmacol Exp Ther 281:440–447.
Tizabi Y, Russell LT, Johnson M, Darmani NA (2001). Nicotine attenuates DOI-induced head-twitch response in mice: implications for Tourette syndrome. Prog Neuropsychopharmacol Biol Psychiatry 25:1445–1457.
Turner EH, Loftis JM, Blackwell AD (2006). Serotonin a la carte: supplementation with the serotonin precursor 5-hydroxytryptophan. Pharmacol Ther 109:325–338.
Uphouse L, Andrade M, Caldarola-Pastuszka M, Maswood S (1994). Hypothalamic infusion of the 5-HT2/1C agonist, DOI, prevents the inhibitory actions of the 5-HT1A agonist, 8-OH-DPAT, on lordosis behavior. Pharmacol Biochem Behav 47:467–470.
Vickers SP, Easton N, Malcolm CS, Allen NH, Porter RH, Bickerdike MJ, et al. (2001). Modulation of 5-HT2A receptor-mediated head-twitch behaviour in the rat by 5-HT2C receptor agonists. Pharmacol Biochem Behav 69:643–652.
Vollenweider FX, Vollenweider-Scherpenhuyzen MF, Babler A, Vogel H, Hell D (1998). Psilocybin induces schizophrenia-like psychosis in humans via a serotonin-2 agonist action. Neuroreport 9:3897–3902.
Wagner GC, Ricaurte GA, Seiden LS, Schuster CR, Miller RJ, Westley J (1980). Long-lasting depletions of striatal dopamine and loss of dopamine uptake sites following repeated administration of methamphetamine. Brain Res 181:151–160.
Wallace J, Jackson RK, Shotton TL, Munjal I, Mcquade R, Gartside SE (2014). Characterization of electrically evoked field potentials in the medial prefrontal cortex and orbitofrontal cortex of the rat: modulation by monoamines. Eur Neuropsychopharmacol 24:321–332.
Warden MR, Selimbeyoglu A, Mirzabekov JJ, Lo M, Thompson KR, Kim SY, et al. (2012). A prefrontal cortex-brainstem neuronal projection that controls response to behavioural challenge. Nature 492:428–432.
Williams GV, Rao SG, Goldman-Rakic PS (2002). The physiological role of 5-HT2A receptors in working memory. J Neurosci 22:2843–2854.
Willins DL, Meltzer HY (1997). Direct injection of 5-HT2A receptor agonists into the medial prefrontal cortex produces a head-twitch response in rats. J Pharmacol Exp Ther 282:699–706.
Willins DL, Deutch AY, Roth BL (1997). Serotonin 5-HT2A receptors are expressed on pyramidal cells and interneurons in the rat cortex. Synapse 27:79–82.
World Drug Report (2019). Stimulants. The United Nations Office on Drugs and Crime (UNODC). Sales No. E.19.XI.8, June: United Nations publication.
Xu T, Pandey SC (2000). Cellular localization of serotonin(2A) (5HT(2A)) receptors in the rat brain. Brain Res Bull 51:499–505.
Yan QS, Jobe PC, Dailey JW (1994). Evidence that a serotonergic mechanism is involved in the anticonvulsant effect of fluoxetine in genetically epilepsy-prone rats. Eur J Pharmacol 252:105–112.
Zhang ZW, Arsenault D (2005). Gain modulation by serotonin in pyramidal neurones of the rat prefrontal cortex. J Physiol 566:379–394.