The Korean Journal of Physiology and Pharmacology

The Korean Society of Pharmacology (대한약리학회)
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Predominant $D_1$ Receptors Involvement in the Over-expression of CART Peptides after Repeated Cocaine Administration

  • Hu, Zhenzhen (Department of Pathophysiology, College of Medicine, Nanchang University) ;
  • Oh, Eun-Hye (Department of Pharmacy, College of Pharmacy, Chungbuk National University) ;
  • Chung, Yeon Bok (Department of Pharmacy, College of Pharmacy, Chungbuk National University) ;
  • Hong, Jin Tae (Department of Pharmacy, College of Pharmacy, Chungbuk National University) ;
  • Oh, Ki-Wan (Department of Pharmacy, College of Pharmacy, Chungbuk National University)
  • Received : 2014.09.18
  • Accepted : 2014.12.05
  • Published : 2015.03.30
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Abstract

The aim of this study was to investigate the involvement of dopaminergic receptors (DR) in behavioral sensitization, as measured by locomotor activity, and the over-expression of cocaine- and amphetamine-regulated transcript (CART) peptides after repeated administration of cocaine in mice. Repeated administrations of cocaine induced behavioral sensitization and CART over-expression in mice. The levels of striatal CART mRNA were significantly increased on the $3^{rd}$ day. CART peptides were over-expressed on the $5^{th}$ day in the striata of behaviorally sensitized mice. A higher proportion of $CART^+$ cells in the cocaine-treated mice were present in the nucleus accumbens (NAc) shell than in the dorsolateral (DL) part of caudate putamen (CP). The concomitant administration of both $D_1R$ and $D_2R$ antagonists, SCH 23390 ($D_1R$ selective) and raclopride ($D_2R$ selective), blocked cocaine induced-behavioral sensitization, CART over-expression, and cyclic adenosine 5'-monophosphate (cAMP)/ protein kinase A (PKA)/phospho-cAMP response element-binding protein (pCREB) signal pathways. SCH 23390 more predominantly inhibited the locomotor activity, CART over-expression, pCREB and PKA activity than raclopride. Cocaine induced-behavioral sensitization was also attenuated in the both $D_1R$ and $D_2R$ knockout (KO) mice, respectively. CART over-expression and activated cAMP/PKA/pCREB signal pathways were inhibited in the $D_1R$-KO mice, but not in the $D_2R$-KO mice. It is suggested that behavioral sensitization, CART over-expression and activated cAMP/PKA/pCREB signal pathways induced by repeated administration of cocaine could be more predominantly mediated by $D_1R$.

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References

  1. McGregor IS, Atrens DM, Jackson DM. Cocaine facilitation of prefrontal cortex self-stimulation: a microstructural and pharmacological analysis. Psychopharmacology (Berl). 1992;106:239-247. https://doi.org/10.1007/BF02801979
  2. Kuribara H. Modification of cocaine sensitization by dopamine D1 and D2 receptor antagonists in terms of ambulation in mice. Pharmacol Biochem Behav. 1995;51:799-805. https://doi.org/10.1016/0091-3057(95)00037-W
  3. Nazarian A, Russo SJ, Festa ED, Kraish M, Quinones-Jenab V. The role of D1 and D2 receptors in the cocaine conditioned place preference of male and female rats. Brain Res Bull. 2004;63:295-299. https://doi.org/10.1016/j.brainresbull.2004.03.004
  4. Woolverton WL, Ranaldi R. Comparison of the reinforcing efficacy of two dopamine D2-like receptor agonists in rhesus monkeys using a progressive-ratio schedule of reinforcement. Pharmacol Biochem Behav. 2002;72:803-809. https://doi.org/10.1016/S0091-3057(02)00749-9
  5. Singh VP, Singh N, Jaggi AS. A review on renal toxicity profile of common abusive drugs. Korean J Physiol Pharmacol. 2013;17: 347-357. https://doi.org/10.4196/kjpp.2013.17.4.347
  6. Bertran-Gonzalez J, Bosch C, Maroteaux M, Matamales M, HerveD, Valjent E, Girault JA. Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J Neurosci. 2008;28:5671-5685. https://doi.org/10.1523/JNEUROSCI.1039-08.2008
  7. Luo Z, Volkow ND, Heintz N, Pan Y, Du C. Acute cocaine induces fast activation of D1 receptor and progressive deactivation of D2 receptor striatal neurons: in vivo optical microprobe $[Ca^{2+}]_i$ imaging. J Neurosci. 2011;31:13180-13190. https://doi.org/10.1523/JNEUROSCI.2369-11.2011
  8. Gao J, Li Y, Zhu N, Brimijoin S, Sui N. Roles of dopaminergic innervation of nucleus accumbens shell and dorsolateral caudate- putamen in cue-induced morphine seeking after prolonged abstinence and the underlying D1- and D2-like receptor mechanisms in rats. J Psychopharmacol. 2013;27:181-191. https://doi.org/10.1177/0269881112466181
  9. Capper-Loup C, Canales JJ, Kadaba N, Graybiel AM. Concurrent activation of dopamine D1 and D2 receptors is required to evoke neural and behavioral phenotypes of cocaine sensitization. J Neurosci. 2002;22:6218-6227. https://doi.org/10.1523/JNEUROSCI.22-14-06218.2002
  10. Drago J, Gerfen CR, Westphal H, Steiner H. D1 dopamine receptor-deficient mouse: cocaine-induced regulation of immediateearly gene and substance P expression in the striatum. Neuroscience. 1996;74:813-823. https://doi.org/10.1016/0306-4522(96)00145-5
  11. Kim S, Shin JK, Yoon HS, Kim JH. Blockade of ERK Phosphorylation in the Nucleus Accumbens Inhibits the Expression of Cocaine-induced Behavioral Sensitization in Rats. Korean J Physiol Pharmacol. 2011;15:389-395. https://doi.org/10.4196/kjpp.2011.15.6.389
  12. Chausmer AL, Katz JL. The role of D2-like dopamine receptors in the locomotor stimulant effects of cocaine in mice. Psychopharmacology (Berl). 2001;155:69-77. https://doi.org/10.1007/s002130000668
  13. Jaworski JN, Jones DC. The role of CART in the reward/ reinforcing properties of psychostimulants. Peptides. 2006;27:1993-2004. https://doi.org/10.1016/j.peptides.2006.03.034
  14. Yoo SB, Lee S, Lee JY, Kim BT, Lee JH, Jahng JW. cAMP/PKA agonist restores the fasting-induced down-regulation of nNOS expression in the paraventricular nucleus. Korean J Physiol Pharmacol. 2012;16:333-337. https://doi.org/10.4196/kjpp.2012.16.5.333
  15. Douglass J, McKinzie AA, Couceyro P. PCR differential display identifies a rat brain mRNA that is transcriptionally regulated by cocaine and amphetamine. J Neurosci. 1995;15:2471-2481. https://doi.org/10.1523/JNEUROSCI.15-03-02471.1995
  16. Moffett MC, Song J, Kuhar MJ. CART peptide inhibits locomotor activity induced by simultaneous stimulation of D1 and D2 receptors, but not by stimulation of individual dopamine receptors. Synapse. 2011;65:1-7. https://doi.org/10.1002/syn.20815
  17. Lee S, Kim Y, Li E, Park S. Ghrelin protects spinal cord motoneurons against chronic glutamate excitotoxicity by inhibiting microglial activation. Korean J Physiol Pharmacol. 2012;16:43-48. https://doi.org/10.4196/kjpp.2012.16.1.43
  18. Hunter RG, Jones D, Vicentic A, Hue G, Rye D, Kuhar MJ. Regulation of CART mRNA in the rat nucleus accumbens via D3 dopamine receptors. Neuropharmacology. 2006;50:858-864. https://doi.org/10.1016/j.neuropharm.2005.12.007
  19. Salinas A, Wilde JD, Maldve RE. Ethanol enhancement of cocaineand amphetamine-regulated transcript mRNA and peptide expression in the nucleus accumbens. J Neurochem. 2006;97:408-415. https://doi.org/10.1111/j.1471-4159.2006.03745.x
  20. Jones DC, Kuhar MJ. Cocaine-amphetamine-regulated transcript expression in the rat nucleus accumbens is regulated by adenylyl cyclase and the cyclic adenosine 5'-monophosphate/protein kinase a second messenger system. J Pharmacol Exp Ther. 2006;317:454-461.
  21. Jones DC, Kuhar MJ. CART receptor binding in primary cell cultures of the rat nucleus accumbens. Synapse. 2008;62:122-127. https://doi.org/10.1002/syn.20476
  22. Lakatos A, Dominguez G,Kuhar MJ. CART promoter CRE site binds phosphorylated CREB. Brain Res Mol Brain Res. 2002;104:81-85. https://doi.org/10.1016/S0169-328X(02)00321-2
  23. Tadokoro S, Kuribara H. Reverse tolerance to the ambulation-increasing effect of methamphetamine in mice as an animal model of amphetamine-psychosis. Psychopharmacol Bull. 1986;22:757-762.
  24. Hu Z, Park KS, Han JY, Jang CG, Oh S, Kim HC , Yang CH, Kim EJ, Oh KW. Markers in morphine- and cocaine-addicted animals. Biomol Ther. 2011;19:45-51. https://doi.org/10.4062/biomolther.2011.19.1.045
  25. Franklin KB, Paxinos G. The mouse brain in stereotaxic coordinates. San Diego: Academic Press; 1997.
  26. Tanegashima K, Okamoto S, Nakayama Y, Taya C, Shitara H, Ishii R, Yonekawa H, MinokoshiY, Hara T. CXCL14 deficiency in mice attenuates obesity and inhibits feeding behavior in a novel environment. PLoS One. 2010;5:e10321. https://doi.org/10.1371/journal.pone.0010321
  27. Morio A, Ujike H, Nomura A, Tanaka Y, Morita Y, Otani K, Kishimoto M, Harano M, Inada T, Komiyama T, Yamada M, Sekine Y, Iwata N, Iyo M, Sora I, Ozaki N, Kuroda S. No association between CART (cocaine- and amphetamine-regulated transcript) gene and methamphetamine dependence. Ann N Y Acad Sci. 2006;1074:411-417. https://doi.org/10.1196/annals.1369.041
  28. Marie-Claire C, Laurendeau I, Canestrelli C, Courtin C, Vidaud M, Roques B, Noble F. Fos but not Cart (cocaine and amphetamine regulated transcript) is overexpressed by several drugs of abuse: a comparative study using real-time quantitative polymerase chain reaction in rat brain. Neurosci Lett. 2003;345:77-80. https://doi.org/10.1016/S0304-3940(03)00307-0
  29. Roh MS, Cui FJ, Ahn YM, Kang UG. Up-regulation of cocaine- and amphetamine-regulated transcript (CART) in the rat nucleus accumbens after repeated electroconvulsive shock. Neurosci Res. 2009;65:210-213. https://doi.org/10.1016/j.neures.2009.06.013
  30. Germano CM, de Castro M, Rorato R, Laguna MT, Antunes-Rodrigues J, Elias CF, Elias LL. Time course effects of adrenalectomy and food intake on cocaine- and amphetamine-regulated transcript expression in the hypothalamus. Brain Res. 2007;1166:55-64. https://doi.org/10.1016/j.brainres.2007.05.077
  31. Jang HS, Kim JY, Kim SH, Lee MG. Role of dopamine receptors on electroencephalographic changes produced by repetitive apomorphine treatments in rats. Korean J Physiol Pharmacol. 2009;13:147-151. https://doi.org/10.4196/kjpp.2009.13.3.147
  32. Hubert GW, Kuhar MJ. Colocalization of CART peptide with prodynorphin and dopamine D1 receptors in the rat nucleus accumbens. Neuropeptides. 2006;40:409-415. https://doi.org/10.1016/j.npep.2006.09.001
  33. Jaworski JN, Vicentic A, Hunter RG, Kimmel HL, Kuhar MJ. CART peptides are modulators of mesolimbic dopamine and psychostimulants. Life Sci. 2003;73:741-747. https://doi.org/10.1016/S0024-3205(03)00394-1
  34. Couceyro PR, Evans C, McKinzie A, Mitchell D, Dube M, Hagshenas L, White FJ, Douglass J, Richards WG, Bannon AW. Cocaine- and amphetamine-regulated transcript (CART) peptides modulate the locomotor and motivational properties of psychostimulants. J Pharmacol Exp Ther. 2005;315:1091-1100. https://doi.org/10.1124/jpet.105.091678
  35. Valjent E, Corvol JC, Pages C, Besson MJ, Maldonado R, Caboche J. Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties. J Neurosci. 2000;20:8701-8709. https://doi.org/10.1523/JNEUROSCI.20-23-08701.2000
  36. Rogge GA, Jones DC, Green T, Nestler E, Kuhar MJ. Regulation of CART peptide expression by CREB in the rat nucleus accumbens in vivo. Brain Res. 2009;1251:42-52. https://doi.org/10.1016/j.brainres.2008.11.011
  37. Shi X, McGinty JF. D1 and D2 dopamine receptors differentially mediate the activation of phosphoproteins in the striatum of amphetamine-sensitized rats. Psychopharmacology (Berl). 2011;214:653-663. https://doi.org/10.1007/s00213-010-2068-4
  38. Guan X, Tao J, Li S. Dopamine D1 receptor, but not dopamine D2 receptor, is a critical regulator for acute cocaine-enhanced gene expression. Neurol Res. 2009;31:17-22. https://doi.org/10.1179/174313208X332986
  39. Welter M, Vallone D, Samad TA, Meziane H, Usiello A, Borrelli E. Absence of dopamine D2 receptors unmasks an inhibitory control over the brain circuitries activated by cocaine. Proc Natl Acad Sci U S A. 2007;104:6840-6845. https://doi.org/10.1073/pnas.0610790104
  40. Rouge-Pont F, Usiello A, Benoit-Marand M, Gonon F, Piazza PV, Borrelli E. Changes in extracellular dopamine induced by morphine and cocaine: crucial control by D2 receptors. J Neurosci. 2002;22:3293-3301. https://doi.org/10.1523/JNEUROSCI.22-08-03293.2002
  41. Kelly MA, Rubinstein M, Asa SL, Zhang G, Saez C, Bunzow JR, Allen RG, Hnasko R, Ben-Jonathan N, Grandy DK, Low MJ. Pituitary lactotroph hyperplasia and chronic hyperprolactinemia in dopamine D2receptor-deficient mice. Neuron. 1997;19:103-113. https://doi.org/10.1016/S0896-6273(00)80351-7
  42. Fekete C, Lechan RM. Neuroendocrine implications for the association between cocaine- and amphetamine regulated transcript (CART) and hypophysiotropic thyrotropin-releasing hormone (TRH). Peptides. 2006;27:2012-2018. https://doi.org/10.1016/j.peptides.2005.11.029

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