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Abstract:

Caffeine is the world’s most popular psychostimulant and is frequently used as an active adulterant in many illicit drugs including cocaine. Previous studies have shown that caffeine can potentiate the stimulant effects of cocaine and cocaine-induced drug seeking behavior. However, little is known about the effects of this drug combination on reward-related learning, a key process in the maintenance of addiction and vulnerability to relapse. The goal of the present study was thus to determine caffeine and cocaine combined effects on the Conditioned Place Preference (CPP) test and to determine potential differential mRNA expression in the Nucleus Accumbens (NAc) and medial prefrontal cortex (mPFC) of immediate-early genes (IEGs) as well as dopamine and adenosine receptor subunits. Mice were treated with caffeine (5 mg/kg, CAF), cocaine (10mg/kg, COC), or their combination (caffeine 5 mg/kg +cocaine 10 mg/kg, CAF-COC) and trained in the CPP test or treated with repeated injections inside the home cage. NAc and mPFC tissues were dissected immediately after the CPP test, after a single conditioning session or following psychostimulant injection in the home cage for mRNA expression analysis. CAF-COC induced a marked change of preference to the drug conditioned side of the CPP and a significant increase in locomotion compared to COC. Gene expression analysis after CPP test revealed specific up-regulation in the CAF-COC group of Drd1a, cFos, and FosB in the NAc, and cFos, Egr1, and Npas4 in the mPFC. Importantly, none of these changes were observed when animals received same treatments in their home cage. With a single conditioning session, we found similar effects in both CAF and CAF-COC groups: increased Drd1a and decreased cFos in the NAc, and increased expression of Drd1a and Drd2, in the mPFC. Interestingly, we found that cFos and Npas4 gene expression were increased only in the mPFC of the CAF-COC. Our study provides evidence that caffeine acting as an adulterant could potentiate reward-associated memories elicited by cocaine. This is associated with specific changes in IEGs expression that were observed almost exclusively in mice that received the combination of both psychostimulants in the context of CPP memory encoding and retrieval. Our results highlight the potential relevance of caffeine in the maintenance of cocaine addiction which might be mediated by modifying neural plasticity mechanisms that strengthen learning of the association between drug and environment. © 2017 Muñiz, Prieto, González, Sosa, Cadet, Scorza, Urbano and Bisagno.

Registro:

Documento: Artículo
Título:Cocaine and caffeine effects on the conditioned place preference test: Concomitant changes on early genes within the mouse prefrontal cortex and nucleus accumbens
Autor:Muñiz, J.A.; Prieto, J.P.; González, B.; Sosa, M.H.; Cadet, J.L.; Scorza, C.; Urbano, F.J.; Bisagno, V.
Filiación:Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Investigaciones Farmacológicas, Universidad de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
Departamento de Neurofarmacología Experimental, Instituto de Investigaciones Biológicas Clemente Estable, Montevideo, Uruguay
National Institute on Drug Abuse (NIDA), Molecular Neuropsychiatry Research Branch, Baltimore, MD, United States
Laboratorio de Fisiología y Biología Molecular, Instituto de Fisiología, Biología Molecular y Neurociencias, Universidad de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
Palabras clave:Caffeine; Cocaine; Immediate-early genes; Learning; Nucleus accumbens; Prefrontal cortex; caffeine; cocaine; messenger RNA; animal experiment; animal model; animal tissue; Article; cocaine dependence; conditioned place preference test; controlled study; Drd1a gene; Drd2 gene; Egr1 gene; FosB gene; gene; gene expression; immediate early gene; locomotion; male; medial prefrontal cortex; mouse; nonhuman; Npas4 gene; nucleus accumbens; oncogene c fos; reward; upregulation
Año:2017
Volumen:11
DOI: http://dx.doi.org/10.3389/fnbeh.2017.00200
Título revista:Frontiers in Behavioral Neuroscience
Título revista abreviado:Front. Behav. Neurosci.
ISSN:16625153
CAS:caffeine, 58-08-2; cocaine, 50-36-2, 53-21-4, 5937-29-1
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_16625153_v11_n_p_Muniz

Referencias:

  • Aguilar-Valles, A., Vaissière, T., Griggs, E.M., Mikaelsson, M.A., Takács, I.F., Young, E.J., Methamphetamine-associated memory is regulated by a writer and an eraser of permissive histone methylation (2014) Biol. Psychiatry, 76, pp. 7-65
  • Alibhai, I.N., Green, T.A., Potashkin, J.A., Nestler, E.J., Regulation of fosB and DeltafosB mRNAexpression: In vivo and in vitro studies (2007) Brain Res, 1143, pp. 22-33
  • Bedingfield, J.B., King, D.A., Holloway, F.A., Cocaine and caffeine: Conditioned place preference, locomotor activity, and additivity (1998) Pharmacol. Biochem. Behav., 61, pp. 291-296
  • Bennett, H.J., Semba, K., Immunohistochemical localization of caffeine-induced c-Fos protein expression in the rat brain (1998) J. Comp. Neurol, 401, pp. 89-108
  • Beyer, C.E., Steketee, J.D., Cocaine sensitization: Modulation by dopamine D2 receptors (2002) Cereb. Cortex, 12, pp. 526-535
  • Bisagno, V., González, B., Urbano, F.J., Cognitive enhancers versus addictive psychostimulants: The good and bad side of dopamine on prefrontal cortical circuits (2016) Pharmacol. Res., 109, pp. 108-118
  • Cadet, J.L., Bisagno, V., The primacy of cognition in the manifestations of substance use disorders (2013) Front. Neurol., 4, p. 189
  • Cadet, J.L., Bisagno, V., Neuropsychological consequences of chronic drug use: Relevance to treatment approaches (2016) Front. Psychiatry, 6, p. 189
  • Childs, E., Influence of energy drink ingredients on mood and cognitive performance (2014) Nutr. Rev., 72, pp. 48-59
  • Cole, C., Jones, L., McVeigh, J., Kicman, A., Syed, Q., Bellis, M., Adulterants in illicit drugs: A review of empirical evidence (2011) Drug Test. Anal., 3, pp. 89-96
  • Cruz, F.C., Javier Rubio, F., Hope, B.T., Using c-fos to study neuronal ensembles in corticostriatal circuitry of addiction (2015) Brain Res, 1628, pp. 157-173
  • Cruz, F.C., Koya, E., Guez-Barber, D.H., Bossert, J.M., Lupica, C.R., Shaham, Y., New technologies for examining the role of neuronal ensembles in drug addiction and fear (2013) Nat. Rev. Neurosci., 14, pp. 743-754
  • Dalley, J.W., Cardinal, R.N., Robbins, T.W., Prefrontal executive and cognitive functions in rodents: Neural and neurochemical substrates (2004) Neurosci. Biobehav. Rev., 28, pp. 771-784
  • Daly, J.W., Fredholm, B.B., Caffeine–an atypical drug of dependence (1998) Drug Alcohol Depend, 51, pp. 199-206
  • El Rawas, R., Klement, S., Kummer, K.K., Fritz, M., Dechant, G., Saria, A., Brain regions associated with the acquisition of conditioned place preference for cocaine vs. Social interaction (2012) Front. Behav. Neurosci., 6, p. 63
  • Ferré, S., Lluís, C., Justinova, Z., Quiroz, C., Orru, M., Navarro, G., Adenosine-cannabinoid receptor interactions. Implications for striatal function (2010) Br. J. Pharmacol., 160, pp. 443-453
  • Fritz, M., El Rawas, R., Salti, A., Klement, S., Bardo, M.T., Kemmler, G., Reversal of cocaine-conditioned place preference and mesocorticolimbic Zif268 expression by social interaction in rats (2011) Addict. Biol., 16, pp. 273-284
  • González, C.R., González, B., Matzkin, M.E., Mu-Iz, J.A., Cadet, J.L., Garcia-Rill, E., Psychostimulant-induced testicular toxicity in mice: evidence of cocaine and caffeine effects on the local dopaminergic system (2015) Plos ONE, 10
  • Hyman, S.E., Malenka, R.C., Nestler, E.J., Neural mechanisms of addiction: The role of reward-related learning and memory (2006) Annu. Rev. Neurosci., 29, pp. 565-598
  • Kelz, M.B., Chen, J., Carlezon, W.A., Whisler, K., Gilden, L., Beckmann, A.M., Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine (1999) Nature, 401, pp. 272-276
  • Kendler, K.S., Myers, J., O Gardner, C., Caffeine intake, toxicity and dependence and lifetime risk for psychiatric and substance use disorders: An epidemiologic and co-twin control analysis (2006) Psychol. Med., 36, pp. 1717-1725
  • Khairnar, A., Plumitalloa Frau, L., Schintu, N., Morelli, M., Caffeine enhances astroglia and microglia reactivity induced by 3,4-methylenedioxymethamphetamine (‘ecstasy’) in mouse brain (2010) Neurotox. Res., 17, pp. 435-439
  • Li, Y., Ge, S., Li, N., Chen, L., Zhang, S., Wang, J., NMDA and dopamine D1 receptors within NAc-shell regulate IEG proteins expression in reward circuit during cocaine memory reconsolidation (2016) Neuroscience, 315, pp. 45-69
  • López-Hill, X., Prieto, J.P., Meikle, M.N., Urbanavicius, J., Abin-Carriquiry, J.A., Prunell, G., Coca-paste seized samples characterization: Chemical analysis, stimulating effect in rats and relevance of caffeine as a major adulterant (2011) Behav. Brain Res., 221, pp. 134-141
  • Mattson, B.J., Koya, E., Simmons, D.E., Mitchell, T.B., Berkow, A., Crombag, H.S., Context-specific sensitization of cocaine-induced locomotor activity and associated neuronal ensembles in rat nucleus accumbens (2008) Eur. J. Neurosci., 27, pp. 202-212
  • Maya-Vetencourt, J.F., Tiraboschi, E., Greco, D., Restani, L., Cerri, C., Auvinen, P., Experience-dependent expression of NPAS4 regulates plasticity in adult visual cortex (2012) J. Physiol., 590, pp. 4777-4787
  • Miller, K.E., Energy drinks, race, and problem behaviors among college students (2008) J. Adolesc. Health., 43, pp. 490-497
  • Muñiz, J.A., Gomez, G., González, B., Rivero-Echeto, M.C., Cadet, J.L., García-Rill, E., Combined effects of simultaneous exposure to caffeine and cocaine in the mouse striatum (2016) Neurotox. Res., 29, pp. 525-538
  • (2003) Guidelines for the Care and Use of Mammals in Neuroscience and Behavioral Research, , Washington, DC: National Academies Press
  • Prast, J.M., Schardl, A., Schwarzer, C., Dechant, G., Saria, A., Zernig, G., Reacquisition of cocaine conditioned place preference and its inhibition by previous social interaction preferentially affect D1-medium spiny neurons in the accumbens corridor (2014) Front. Behav. Neurosci., 8, p. 317
  • Prieto, J.P., Galvalisi, M., López-Hill, X., Meikle, M.N., Abin-Carriquiry, J.A., Scorza, C., Caffeine enhances and accelerates the expression of sensitization induced by coca paste indicating its relevance as a main adulterant (2015) Am. J. Addict., 24, pp. 475-481
  • Prieto, J.P., Scorza, C., Serra, G.P., Perra, V., Galvalisi, M., Abin-Carriquiry, J.A., Caffeine, a common active adulterant of cocaine, enhances the reinforcing effect of cocaine and its motivational value (2016) Psychopharmacology, 233, pp. 2879-2889
  • Qiu, J., Dunbar, D.R., Noble, J., Cairns, C., Carter, R., Kelly, V., Decreased Npas4 and Arc mRNA levels in the hippocampus of aged memory-impaired wild-type but not memory preserved 11β-HSD1 deficient mice (2016) J. Neuroendocrinol, 28
  • Risinger, R.C., Salmeron, B.J., Ross, T.J., Amen, S.L., Sanfilipo, M., Hoffmann, R.G., Neural correlates of high and craving during cocaine self-administration using BOLD fMRI (2005) Neuroimage, 26, pp. 1097-1108
  • Robins, M.T., Lu, J., Van Rijn, R.M., Unique behavioral and neurochemical effects induced by repeated adolescent consumption of caffeine-mixed alcohol in C57BL/6 Mice (2016) Plos ONE, 11
  • Sena, L.C., Matos, H.R., Dórea, H.S., Pimentel, M.F., De Santana, D.C., De Santana, F.J., Dispersive liquid-liquid microextraction based on solidification of floating organic drop and high-performance liquid chromatography to the analysis of cocaine’s major adulterants in human urine (2017) Toxicology, 376, pp. 102-112
  • Slaker, M., Churchill, L., Todd, R.P., Blacktop, J.M., Zuloaga, D.G., Raber, J., Removal of perineuronal nets in the medial prefrontal cortex impairs the acquisition and reconsolidation of a cocaine-induced conditioned place preference memory (2015) J. Neurosci., 35, pp. 4190-4202
  • Spiegel, I., Mardinly, A.R., Gabel, H.W., Bazinet, J.E., Couch, C.H., Tzeng, C.P., Npas4 regulates excitatory-inhibitory balance within neural circuits through cell-type-specific gene programs (2014) Cell, 157, pp. 1216-1229
  • Tzschentke, T.M., Schmidt, W.J., Functional heterogeneity of the rat medial prefrontal cortex: Effects of discrete subarea-specific lesions on drug-induced conditioned place preference and behavioural sensitization (1999) Eur. J. Neurosci., 11, pp. 4099-4109
  • Veyrac, A., Besnard, A., Caboche, J., Davis, S., Laroche, S., The transcription factor Zif268/Egr1, brain plasticity, and memory (2014) Prog. Mol. Biol. Transl. Sci., 122, pp. 89-129
  • Volkow, N.D., Wang, G.-J., Fowler, J.S., Tomasi, D., Addiction circuitry in the human brain (2012) Ann. Rev. Pharmacol. Toxicol., 52, pp. 321-336
  • Volkow, N.D., Wang, G.J., Logan, J., Alexoff, D., Fowler, J.S., Thanos, P.K., Caffeine increases striatal dopamine D2/D3 receptor availability in the human brain (2015) Transl. Psychiatry, 5
  • Volkow, N.D., Wang, G.J., Ma, Y., Fowler, J.S., Wong, C., Ding, Y.S., Activation of orbital and medial prefrontal cortex by methylphenidate in cocaine-addicted subjects but not in controls: Relevance to addiction (2005) J. Neurosci., 25, pp. 3932-3939
  • Ye, L., Allen, W.E., Thompson, K.R., Tian, Q., Hsueh, B., Ramakrishnan, C., Wiring and molecular features of prefrontal ensembles representing distinct experiences (2016) Cell, 165, pp. 1776-1788

Citas:

---------- APA ----------
Muñiz, J.A., Prieto, J.P., González, B., Sosa, M.H., Cadet, J.L., Scorza, C., Urbano, F.J.,..., Bisagno, V. (2017) . Cocaine and caffeine effects on the conditioned place preference test: Concomitant changes on early genes within the mouse prefrontal cortex and nucleus accumbens. Frontiers in Behavioral Neuroscience, 11.
http://dx.doi.org/10.3389/fnbeh.2017.00200
---------- CHICAGO ----------
Muñiz, J.A., Prieto, J.P., González, B., Sosa, M.H., Cadet, J.L., Scorza, C., et al. "Cocaine and caffeine effects on the conditioned place preference test: Concomitant changes on early genes within the mouse prefrontal cortex and nucleus accumbens" . Frontiers in Behavioral Neuroscience 11 (2017).
http://dx.doi.org/10.3389/fnbeh.2017.00200
---------- MLA ----------
Muñiz, J.A., Prieto, J.P., González, B., Sosa, M.H., Cadet, J.L., Scorza, C., et al. "Cocaine and caffeine effects on the conditioned place preference test: Concomitant changes on early genes within the mouse prefrontal cortex and nucleus accumbens" . Frontiers in Behavioral Neuroscience, vol. 11, 2017.
http://dx.doi.org/10.3389/fnbeh.2017.00200
---------- VANCOUVER ----------
Muñiz, J.A., Prieto, J.P., González, B., Sosa, M.H., Cadet, J.L., Scorza, C., et al. Cocaine and caffeine effects on the conditioned place preference test: Concomitant changes on early genes within the mouse prefrontal cortex and nucleus accumbens. Front. Behav. Neurosci. 2017;11.
http://dx.doi.org/10.3389/fnbeh.2017.00200