Impact of Caffeine on Ethanol-Induced Stimulation and Sensitization: Changes in ERK and DARPP-32 Phosphorylation in Nucleus Accumbens.
Animals
Caffeine
/ administration & dosage
Dopamine and cAMP-Regulated Phosphoprotein 32
/ metabolism
Dose-Response Relationship, Drug
Ethanol
/ administration & dosage
Locomotion
/ drug effects
MAP Kinase Signaling System
/ drug effects
Male
Nucleus Accumbens
/ drug effects
Phosphorylation
/ drug effects
Accumbens
Alcohol
Caffeine
Sensitization
Stimulation
Journal
Alcoholism, clinical and experimental research
ISSN: 1530-0277
Titre abrégé: Alcohol Clin Exp Res
Pays: England
ID NLM: 7707242
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
12
08
2020
accepted:
05
01
2021
pubmed:
21
1
2021
medline:
3
11
2021
entrez:
20
1
2021
Statut:
ppublish
Résumé
Caffeine is frequently consumed with ethanol to reduce the impairing effects induced by ethanol, including psychomotor slowing or incoordination. Both drugs modulate dopamine (DA)-related markers in accumbens (Acb), and Acb DA is involved in voluntary locomotion and locomotor sensitization. The present study determined whether caffeine can affect locomotion induced by acute and repeated ethanol administration in adult male CD-1 mice. Acute administration of caffeine (7.5 to 30.0 mg/kg) was evaluated for its effects on acute ethanol-induced (1.5 to 3.5 g/kg) changes in open-field horizontal locomotion, supported rearing, and rearing not supported by the wall. DA receptor-dependent phosphorylation markers were assessed: extracellular signal-regulated kinase (pERK), and dopamine-and cAMP-regulated phosphoprotein Mr32kDa phosphorylated at threonine 75 site (pDARPP-32-Thr75) in Acb core and shell. Acutely administered caffeine was also evaluated in ethanol-sensitized (1.5 g/kg) mice. Acute ethanol decreased both types of rearing. Caffeine increased supported rearing but did not block ethanol -induced decreases in rearing. Both substances increased horizontal locomotion in a biphasic manner, and caffeine potentiated ethanol-induced locomotion. Although ethanol administered repeatedly induced sensitization of locomotion and unsupported rearing, acute administration of caffeine to ethanol-sensitized mice in an ethanol-free state resulted in blunted stimulant effects compared with those seen in ethanol-naïve mice. Ethanol increased pERK immunoreactivity in both subregions of the Acb, but coadministration with caffeine blunted this increase. There were no effects on pDARPP-32(Thr75) immunoreactivity. The present results demonstrated that, after the first administration, caffeine potentiated the stimulating actions of ethanol, but did not counteract its suppressant or ataxic effects. Moreover, our results show that caffeine has less activating effects in ethanol-sensitized animals.
Sections du résumé
BACKGROUND
Caffeine is frequently consumed with ethanol to reduce the impairing effects induced by ethanol, including psychomotor slowing or incoordination. Both drugs modulate dopamine (DA)-related markers in accumbens (Acb), and Acb DA is involved in voluntary locomotion and locomotor sensitization. The present study determined whether caffeine can affect locomotion induced by acute and repeated ethanol administration in adult male CD-1 mice.
METHODS
Acute administration of caffeine (7.5 to 30.0 mg/kg) was evaluated for its effects on acute ethanol-induced (1.5 to 3.5 g/kg) changes in open-field horizontal locomotion, supported rearing, and rearing not supported by the wall. DA receptor-dependent phosphorylation markers were assessed: extracellular signal-regulated kinase (pERK), and dopamine-and cAMP-regulated phosphoprotein Mr32kDa phosphorylated at threonine 75 site (pDARPP-32-Thr75) in Acb core and shell. Acutely administered caffeine was also evaluated in ethanol-sensitized (1.5 g/kg) mice.
RESULTS
Acute ethanol decreased both types of rearing. Caffeine increased supported rearing but did not block ethanol -induced decreases in rearing. Both substances increased horizontal locomotion in a biphasic manner, and caffeine potentiated ethanol-induced locomotion. Although ethanol administered repeatedly induced sensitization of locomotion and unsupported rearing, acute administration of caffeine to ethanol-sensitized mice in an ethanol-free state resulted in blunted stimulant effects compared with those seen in ethanol-naïve mice. Ethanol increased pERK immunoreactivity in both subregions of the Acb, but coadministration with caffeine blunted this increase. There were no effects on pDARPP-32(Thr75) immunoreactivity.
CONCLUSIONS
The present results demonstrated that, after the first administration, caffeine potentiated the stimulating actions of ethanol, but did not counteract its suppressant or ataxic effects. Moreover, our results show that caffeine has less activating effects in ethanol-sensitized animals.
Substances chimiques
Dopamine and cAMP-Regulated Phosphoprotein 32
0
Ppp1r1b protein, mouse
0
Caffeine
3G6A5W338E
Ethanol
3K9958V90M
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
608-619Informations de copyright
© 2021 by the Research Society on Alcoholism.
Références
Abrahao KP, Goeldner FO, Souza-Formigoni ML (2014) Individual differences in ethanol locomotor sensitization are associated with dopamine D1 receptor intra-cellular signaling of DARPP-32 in the nucleus accumbens. PLoS One 9:e98296.
Acquas E, Tanda G, Di Chiara G (2002) Differential effects of caffeine on dopamine and acetylcholine transmission in brain areas of drug-naive and caffeine-pretreated rats. Neuropsychopharmacology 27:182-193.
Acquas E, Vinci S, Ibba F, Spiga S, De Luca MA, Di Chiara G (2010) Role of dopamine D1 receptors in caffeine-mediated ERK phosphorylation in the rat brain. Synapse 64:341-349.
Agnati LF, Ferré S, Lluis C, Franco R, Fuxe K (2003) Molecular mechanisms and therapeutical implications of intramembrane receptor/receptor interactions among heptahelical receptors with examples from the striatopallidal GABA neurons. Pharmacol Rev 55:509-550.
Arizzi-LaFrance MN, Correa M, Aragon CM, Salamone JD (2006) Motor stimulant effects of ethanol injected into the substantia nigra pars reticulata: importance of catalase-mediated metabolism and the role of acetaldehyde. Neuropsychopharmacology 31:997-1008.
Arria AM, Caldeira KM, Kasperski SJ, Vincent KB, Griffiths RR, O'Grady KE (2011) Energy drink consumption and increased risk for alcohol dependence. Alcohol Clin Exp Res 35:365-375.
Astorino TA, Roberson DW (2010) Efficacy of acute caffeine ingestion for short-term high-intensity exercise performance: a systematic review. J Strength Cond Res 24:257-265.
Attwood AS, Rogers PJ, Ataya AF, Adams S, Munafò MR (2012) Effects of caffeine on alcohol-related changes in behavioural control and perceived intoxication in light caffeine consumers. Psychopharmacology 221:551-560.
Bassareo V, Talani G, Frau R, Porru S, Rosas M, Kasture SB, Peana AT, Loi E, Sanna E, Acquas E (2019) Inhibition of morphine- and ethanol-mediated stimulation of mesolimbic dopamine neurons by Withania somnifera. Front Neurosci. 13:545.
Boehm SL 2nd, Crabbe JC, Phillips TJ (2000) Sensitivity to ethanol-induced motor incoordination in FAST and SLOW selectively bred mice. Pharmacol Biochem Behav. 66:241-247. https://doi.org/10.1016/s0091-3057(00)00264-1
Camarini R, Pautassi RM (2016) Behavioral sensitization to ethanol: neural basis and factors that influence its acquisition and expression. Brain Res Bull 125:53-78.
Carboni E, Silvagni A, Rolando MTP, Di Chiara G (2000) Stimulation of in vivo dopamine transmission in the bed nucleus of stria terminalis by reinforcing drugs. J Neurosci 20:RC102.
Celik E, Uzbay IT, Karakas S (2006) Caffeine and amphetamine produce cross-sensitization to nicotine-induced locomotor activity in mice. Prog Neuro-Psychopharmacology Biol Psychiatry 30:50-55.
Chuck TL, McLaughlin PJ, Arizzi-LaFrance MN, Salamone JD, Correa M (2006) Comparison between multiple behavioral effects of peripheral ethanol administration in rats: sedation, ataxia, and bradykinesia. Life Sci 79:154-161.
Correa M, Arizzi MN, Betz A, Mingote S, Salamone JD (2003a) Locomotor stimulant effects of intraventricular injections of low doses of ethanol in rats: acute and repeated administration. Psychopharmacology 170:368-375.
Correa M, Arizzi MN, Betz A, Mingote S, Salamone JD (2003b) Open field locomotor effects in rats after intraventricular injections of ethanol and the ethanol metabolites acetaldehyde and acetate. Brain Res Bull 62:197-202.
Correa M, Sanchis-Segura C, Aragon CM (2001a) Brain catalase activity is highly correlated with ethanol-induced locomotor activity in mice. Physiol Behav 73:641-647.
Correa M, Sanchis-Segura C, Aragon CM (2001b) Influence of brain catalase on ethanol-induced loss of righting reflex in mice. Drug Alcohol Depend 65:9-15.
Correa M, Sanchis-Segura C, Pastor R, Aragon CMG (2004) Ethanol intake and motor sensitization: the role of brain catalase activity in mice with different genotypes. Physiol Behav 82:231-240.
Dar MS (1988) The biphasic effects of centrally and peripherally administered caffeine on ethanol-induced motor incoordination in mice. J Pharm Pharmacol 40:482-487.
Dar MS (2006) Co-modulation of acute ethanol-induced motor impairment by mouse cerebellar adenosinergic A1 and GABA(A) receptor systems. Brain Res Bull. 71:287-295.
Dar MS (2014) Functional interaction and cross-tolerance between ethanol and delta9-THC: possible modulation by mouse cerebellar adenosinergic A1/GABAergic-A receptors. Behav Brain Res 270:287-294.
De Luca MA, Bassareo V, Bauer A, Di Chiara G (2007) Caffeine and accumbens shell dopamine. J Neurochem. 103:157-163. https://doi.org/10.1111/j.1471-4159.2007.04754.x
Di Chiara G, Imperato A (1988) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats (amphetamine/cocaine/ethanol/nicotine/opiates). Proc Natl Acad Sci USA 85:5274-5278.
Drake CL, Roehrs T, Turner L, Scofield HM, Roth T (2003) Caffeine reversal of ethanol effects on the multiple sleep latency test, memory, and psychomotor performance. Neuropsychopharmacology 28:371-378.
Duncan MJ, Smith M, Cook K, James RS (2012) The acute effect of a caffeine-containing energy drink on mood state, readiness to invest effort, and resistance exercise to failure. J Strength Cond Res 26:2858-2865.
Duncan MJ, Stanley M, Parkhouse N, Cook K, Smith M (2013) Acute caffeine ingestion enhances strength performance and reduces perceived exertion and muscle pain perception during resistance exercise. Eur J Sport Sci 13:392-399.
El Yacoubi M, Ledent C, Parmentier M, Costentin J, Vaugeois JM (2003) Caffeine reduces hypnotic effects of alcohol through adenosine A 2A receptor blockade. Neuropharmacology 45:977-985.
Ferré S (2008) An update on the mechanisms of the psychostimulant effects of caffeine. J Neurochem 105:1067-1079.
Ferré S, Ciruela F, Borycz J, Solinas M, Quarta D, Antoniou K, Quiroz C, Justinova Z, Lluis C, Franco R, Goldberg SR (2008) Adenosine A1-A2A receptor heteromers: new targets for caffeine in the brain. Front Biosci 13:2391-2399.
Ferreira SE, de Mello MT, Pompéia S, de Souza-Formigoni ML (2006) Effects of energy drink ingestion on alcohol intoxication. Alcohol Clin Exp Res 30:598-605.
Fritz BM, Companion M, Boehm SL (2014) "Wired," yet intoxicated: modeling binge caffeine and alcohol co-consumption in the mouse. Alcohol Clin Exp Res 38:2269-2278.
Fritz BM, Quoilin C, Kasten CR, Smoker M, Boehm SL 2nd (2016) Concomitant caffeine increases binge consumption of ethanol in adolescent and adult mice, but produces additive motor stimulation only in adolescent animals. Alcohol Clin Exp Res 40:1351-1360.
Fuxe K, Agnati LF, Jacobsen K, Hillion J, Canals M, Torvinen M, Tinner-Staines B, Staines W, Rosin D, Terasmaa A, Popoli P, Leo G, Vergoni V, Lluis C, Ciruela F, Franco R, Ferre S (2003) Receptor heteromerization in adenosine A2A receptor signaling: Relevance for striatal function and Parkinson’s disease. Neurology 61:S19-S23.
Gessa GL, Muntoni F, Collu M, Vargiu L, Mereu G (1985) Low doses of ethanol activate dopaminergic neurons in the ventral tegmental area. Brain Res 348:201-203.
Hasenfratz M, Bunge A, Dal Prá G, Bättig K (1993) Antagonistic effects of caffeine and alcohol on mental performance parameters. Pharmacol Biochem Behav 46:463-465.
Hilbert MLT, May CE, Griffin WC (2013) Conditioned reinforcement and locomotor activating effects of caffeine and ethanol combinations in mice. Pharmacol Biochem Behav 110:168-173.
Howland J, Rohsenow DJ, Bliss CA, Almeida AB, Calise TV, Heeren T, Winter M (2010) Hangover predicts residual alcohol effects on psychomotor vigilance the morning after intoxication. J Addict Res Ther 1:1000101.
Ibba F, Vinci S, Spiga S, Peana AT, Assaretti AR, Spina L, Longoni R, Acquas E (2009) Ethanol-induced extracellular signal regulated kinase: Role of dopamine D 1 receptors. Alcohol Clin Exp Res 33:858-867.
Karlsson O, Roman E (2016) Dose-dependent effects of alcohol administration on behavioral profiles in the MCSF test. Alcohol 50:51-56.
Kawa AB, Robinson TE (2019) Sex differences in incentive-sensitization produced by intermittent access cocaine self-administration. Psychopharmacology 236:625-639.
Keppel G (1991) Design and Analysis: A Researcher’s Handbook. Prentice-Hall, Englewood.
Kuribara H, Asahi T, Tadokoro S (1992) Ethanol enhances, but diazepam and pentobarbital reduce the ambulation-increasing effect of caffeine in mice. Arukoru Kenkyuto Yakubutsu Ison 27:528-539.
López-Cruz L, Pardo M, Salamone JD, Correa M (2014) Differences between the nonselective adenosine receptor antagonists caffeine and theophylline in motor and mood effects: Studies using medium to high doses in animal models. Behav Brain Res 270:213-222.
López-Cruz L, Salamone JD, Correa M (2013) The impact of caffeine on the behavioral effects of ethanol related to abuse and addiction: a review of animal studies. J Caffeine Res 3:9-21.
López-Cruz L, Salamone JD, Correa M (2018) Caffeine and selective adenosine receptor antagonists as new therapeutic tools for the motivational symptoms of depression. Front Pharmacol 9:526.
López-Cruz L, San-Miguel N, Bayarri P, Baqi Y, Müller CE, Salamone JD, Correa M (2016) Ethanol and caffeine effects on social interaction and recognition in mice: involvement of adenosine A2A and A1 receptors. Front Behav Neurosci 10:206.
Mackus M, van de Loo AJAE, Benson S, Scholey A, Verster JC (2016) Consumption of caffeinated beverages and the awareness of their caffeine content among Dutch students. Appetite 103:353-357.
Marczinski CA, Fillmore MT (2006) Clubgoers and their trendy cocktails: implications of mixing caffeine into alcohol on information processing and subjective reports of intoxication. Exp Clin Psychopharmacol 14:450-458.
May CE, Haun HL, Iii WCG (2015) Sensitization and tolerance following repeated exposure to caffeine and alcohol in mice. Alcohol Clin Exp Res 39:1443-1452.
Melis M, Enrico P, Peana AT, Diana M (2007) Acetaldehyde mediates alcohol activation of the mesolimbic dopamine system. Eur J Neurosci 26:2824-2833.
Nunes EJ, Randall PA, Hart EE, Freeland C, Yohn SE, Baqi Y, Muller CE, Lopez-Cruz L, Correa M, Salamone JD (2013) Effort-related motivational effects of the VMAT-2 inhibitor tetrabenazine: implications for animal models of the motivational symptoms of depression. J Neurosci 33:19120-19130.
Nuutinen S, Kiianmaa K, Panula P (2011) DARPP-32 and Akt regulation in ethanol-preferring AA and ethanol-avoiding ANA rats. Neurosci Lett 503:31-36.
O'Neill CE, Levis SC, Schreiner DC, Amat J, Maier SF, Bachtell RK (2015) Effects of adolescent caffeine consumption on cocaine sensitivity. Neuropsychopharmacology 40:813-821.
Pavón FJ, Serrano A, Stouffer DG, Polis I, Roberto M, Cravatt BF, Martin-Fardon R, Rodríguez de Fonseca F, Parsons LH (2019) Ethanol-induced alterations in endocannabinoids and relevant neurotransmitters in the nucleus accumbens of fatty acid amide hydrolase knockout mice. Addict Biol. 24:1204-1215.
Paxinos G, Franklin K. (2001) The mouse brain in stereotaxic coordinates, 2nd editio. Academic (ed). Sydney.
Peacock A, Pennay A, Droste N, Bruno R, Lubman DI (2014) 'High' risk? A systematic review of the acute outcomes of mixing alcohol with energy drinks. Addiction 109:1612-1633.
Phillips TJ, Shen EH (1996) Neurochemical bases of locomotion and ethanol stimulant effects. Int Rev Neurobiol 39:243-282.
Porru S, Maccioni R, Bassareo V, Peana AT, Salamone JD, Acquas E, Correa M (2020) Effects of Caffeine on Ethanol-elicited place preference, place aversion and ERK phosphorylation in CD-1 mice. J Psychopharmacol 34:1357-1370.
Reagan-Shaw S, Nihal M, Ahmad N (2008) Dose translation from animal to human studies revisited. FASEB J 22:659-661.
Robins MT, Lu J, van Rijn RM (2016) Unique behavioral and neurochemical effects induced by repeated adolescent consumption of caffeine-mixed alcohol in c57bl/6 mice. PLoS One 11:e0158189.
Robinson TE, Berridge KC (2000) The psychology and neurobiology of addiction: an incentive-sensitization view. Addiction 95(Suppl 2):S91-117.
Salamone JD, Correa M (2012) The mysterious motivational functions of mesolimbic dopamine. Neuron 76:471-480.
Salamone JD, Pardo M, Yohn SE, López-Cruz L, Sanmiguel N, Correa M (2016) Mesolimbic dopamine and the regulation of motivated behavior. Curr Top Behav Neurosci 27:231-257.
Smirmaul BPC, de Moraes AC, Angius L, Marcora SM (2017) Effects of caffeine on neuromuscular fatigue and performance during high-intensity cycling exercise in moderate hypoxia. Eur J Appl Physiol 117:27-38.
Solinas M, Ferré S, You ZB, Karcz-Kubicha M, Popoli P, Goldberg SR (2002) Caffeine induces dopamine and glutamate release in the shell of the nucleus accumbens. J Neurosci 22:6321-6324.
Spanos M, Besheer J, Hodge CW (2012) Increased sensitivity to alcohol induced changes in ERK Map kinase phosphorylation and memory disruption in adolescent as compared to adult C57BL/6J mice. Behav Brain Res 230:158-166.
Steketee JD, Kalivas PW (2011) Drug wanting: behavioral sensitization and relapse to drug-seeking behavior. Pharmacol Rev 63:348-365.
Svenningsson P, Le Moine C, Fisone G, Fredholm BB (1999) Distribution, biochemistry and function of striatal adenosine A(2A) receptors. Prog Neurogibol 59:355-396.
Temple JL, Bernard C, Lipshultz SE, Czachor JD, Westphal JA, Mestre MA (2017) The safety of ingested caffeine: a comprehensive review. Front Psychiatry 8:1-19.
Ulbrich A, Hemberger SH, Loidl A, Dufek S, Pablik E, Fodor S, Herle M, Aufricht C (2013) Effects of alcohol mixed with energy drink and alcohol alone on subjective intoxication. Amino Acids 45:1385-1393.
Ulenius L, Adermark L, Söderpalm B, Ericson M (2019) Energy drink constituents (caffeine and taurine) selectively potentiate ethanol-induced locomotion in mice. Pharmacol Biochem Behav. 187:172795.
Valjent E, Pagès C, Hervé D, Girault JA, Caboche J (2004) Addictive and non-addictive drugs induce distinct and specific patterns of ERK activation in mouse brain. Eur J Neurosci 19:1826-1836.
Valjent E, Pascoli V, Corvol J, Svenningsson P, Paul S, Stipanovich A, Caboche J, Lombroso PJ, Nairn AC, Greengard P, Herve D, Girault J (2005) Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. PNAS 102:491-496.
Vena AA, Mangieri R, Gonzales RA (2016) Regional analysis of the pharmacological effects of acute ethanol on extracellular striatal dopamine activity. Alcohol Clin Exp Res. 40:2528-2536.
Waldeck B (1974) Ethanol and caffeine: a complex interaction with respect to locomotor activity and central catecholamines. Psychopharmacologia 36:209-220.
Weldy DL (2010) Risks of alcoholic energy drinks for youth. J Am Board Fam Med 23:555-558.
Xu S, Kang UG (2017) Characteristics of ethanol-induced behavioral sensitization in rats: molecular mediators and cross-sensitization between ethanol and cocaine. Pharmacol Biochem Behav 160:47-54.
Zhang Q, Yu YP, Ye YL, Zhang JT, Zhang WP, Wei EQ (2011) Spatiotemporal properties of locomotor activity after administration of central nervous stimulants and sedatives in mice. Pharmacol Biochem Behav 97:577-585.