Cocaine self-administration differentially modulates the expression of endogenous cannabinoid system-related proteins in the hippocampus of Lewis vs. Fischer 344 rats

International Journal of Neuropsychopharmacology

Volumn 16, Issue 6, 2013, Pages 1277-1293

  Rivera, Patricia ^a   Miguéns, Miguel ^b   Coria, Santiago M ^b   Rubio, Leticia ^c   Higuera Matas, Alejandro ^b   Bermúdez Silva, Francisco J ^a   De Fonseca, Fernando Rodríguez ^a   Suárez, Juan ^a   Ambrosio, Emilio ^b  

^a HOSPITAL REGIONAL UNIVERSITARIO DE MÁLAGA   (Spain)

^b UNIVERSIDAD NACIONAL DE EDUCACIÓN A DISTANCIA   (Spain)

^c UNIVERSITY OF MÁLAGA   (Spain)

Author keywords

Cannabinoid receptor; cocaine; Fischer rat; hippocampus; Lewis rat

Indexed keywords

4 AMINOBUTYRIC ACID; ACYLGLYCEROL LIPASE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; COCAINE; FATTY ACID AMINO HYDROLASE; GLUTAMIC ACID; HYDROLASE; LIPOPROTEIN LIPASE; N ACYL PHOSPHATIDYLETHANOLAMINE PHOSPHOLIPASE; PHOSPHOLIPASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COCAINE DEPENDENCE; CONTROLLED STUDY; FISCHER 344 RAT; GENOTYPE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LEWIS RAT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SYNAPSE;

AMIDOHYDROLASES; ANIMALS; ARACHIDONIC ACIDS; COCAINE; CONDITIONING, OPERANT; DOPAMINE UPTAKE INHIBITORS; ENDOCANNABINOIDS; GENE EXPRESSION REGULATION; GLYCERIDES; HIPPOCAMPUS; LIPOPROTEIN LIPASE; MONOACYLGLYCEROL LIPASES; PHOSPHOLIPASE D; RATS; RATS, INBRED F344; RATS, INBRED LEW; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; SELF ADMINISTRATION; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; TIME FACTORS;

EID: 84878861794     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145712001186     Document Type: Article

References (74)

1. Abush H, Akirav I (2010). Cannabinoids modulate hippocampal memory and plasticity. Hippocampus 20: 1126-1138.
2. Aracil-Fernández A, Trigo JM, García-Gutiérrez MS, Ortega-Á lvaro A, et al. (2012). Decreased cocaine motor sensitization and self-administration in mice overexpressing cannabinoid CB2 receptors. Neuropsychopharmacology 37: 1749-1763.
3. Arnold JC (2005). The role of endocannabinoid transmission in cocaine addiction. Pharmacol Biochem Behav 81: 396-406.
4. Beitner-Johnson D, Guitart X, Nestler EJ (1993). Glial fibrillary acidic protein and the mesolimbic dopamine system: Regulation by chronic morphine and Lewis-Fischer strain differences in the rat ventral tegmental area. J Neurochem 61: 1766-1773.
5. Blankman JL, Simon GM, Cravatt BF (2007). A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol. Chem Biol 14: 1347-1356.
6. Brown SM, Wager-Miller J, Mackie K (2002). Cloning and molecular characterization of the rat CB2 cannabinoid receptor. Biochim Biophys Acta 1576: 255-264.
7. Cabral GA, Raborn ES, Griffin L, Dennis J, et al. (2008). CB2 receptors in the brain : Role in central immune function. Br J Pharmacol 153: 240-251.
8. Cadoni C, Di Chiara G (2007). Differences in dopamine responsiveness to drugs of abuse in the nucleus accumbens shell and core of Lewis and Fischer 344 rats. J Neurochem 103: 487-499.
9. Caille S, Alvarez-Jaimes L, Polis I, Stouffer DG, et al. (2007). Specific alterations of extracellular endocannabinoid levels in the nucleus accumbens by ethanol, heroin, and cocaine self-administration. J Neurosci 27: 3695-3702.
10. Camp DM, Browman KE, Robinson TE (1994). The effects of metamphetamine and cocaine on motor behavior and extracellular dopamine in the ventralstriatum of Lewis versus Fischer 344 rats. Brain Res 668: 180-193.
11. Cossu G, Ledent C, Fattore L, Imperato A, et al. (2001). Cannabinoid CB1 receptor knockout mice fail to selfadminister morphine but not other drugs of abuse. Behav Brain Res 118: 61-65.
12. Crespo JA, Manzanares J, Oliva JM, Corchero J, et al. (2001). Extinction of cocaine self-administration produces a differential time-related regulation of proenkephalin gene expression in rat brain. Neuropsychopharmacology 25: 185-194.
13. Chambers RA, Sentir AM, Conroy SK, Truitt WA, et al. (2010). Cortical-striatal integration of cocaine history and prefrontal dysfunction in animal modeling of dual diagnosis. Biol Psychiatry 67: 788-792.
14. de Vries TJ, Shaham Y, Homberg JR, Crombag H, et al. (2001). A cannabinoid mechanism in relapse to cocaine seeking. Nat Med 7 : 1151-1154.
15. del Olmo N, Higuera-Matas A, Miguens M, Garcia-Lecumberri C, et al. (2006a). Hippocampal synaptic plasticity and water maze learning in cocaine self-administered rats. Ann N Y Acad Sci 1074: 427-437.
16. del Olmo N, Higuera-Matas A, Miguens M, Garcia-Lecumberri C, et al. (2007). Cocaine self-administration improves performance in a highly demanding water maze task. Psychopharmacology (Berl) 195: 19-25.
17. del Olmo N, Miguens M, Higuera-Matas A, Torres I, et al. (2006b). Enhancement of hippocampal long-term potentiation induced by cocaine self-administration is maintained during the extinction of this behavior. Brain Res 1116: 120-126.
18. Fattore L, Martellotta MC, Cossu G, Mascia MS, et al. (1999). CB1 cannabinoid receptor agonist WIN 55,212-2 decreases intravenous cocaine self-administration in rats. Behav Brain Res 104: 141-146.
19. Fole A, Gonzalez-Martin C, Huarte C, Alguacil LF, et al. (2011). Effects of chronic cocaine administration on spatial learning and hippocampal spine density in two genetically different strains of rats. Neurobiol Learn Mem 95: 491-497.
20. Freeman KB, Kearns DN, Kohut SJ, Riley AL (2009). Strain differences in patterns of drug-intake during prolonged access to cocaine self-administration. Behav Neurosci 123: 156-164.
21. Gao Y, Vasilyev DV, Goncalves MB, Howell FV, et al. (2010). Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. J Neurosci 30: 2017-2024.
22. Giuffrida A, Parsons LH, Kerr TM, Rodriguez de Fonseca F, et al. (1999). Dopamine activation of endogenous cannabinoid signaling in dorsal striatum. Nat Neurosci 2 : 358-363.
23. Glowa JR, Shaw AE, Riley AL (1994). Cocaine-induced conditioned taste aversions : Comparisons between effects in LEW/N and F344/N rat strains. Psychopharmacology (Berl) 114: 229-232.
24. Gonzalez S, Cascio MG, Fernandez-Ruiz J, Fezza F, et al. (2002). Changes in endocannabinoid contents in the brain of rats chronically exposed to nicotine, ethanol or cocaine. Brain Res 954: 73-81.
25. Gorriti MA, Rodriguez de Fonseca F, Navarro M, Palomo T (1999). Chronic (-)-delta9-tetrahydrocannabinol treatment induces sensitization to the psychomotor effects of amphetamine in rats. Eur J Pharmacol 365: 133-142.
26. Grabus SD, Glowa JR, Riley AL (2004). Morphine- and cocaine-induced c-Fos levels in Lewis and Fischer rat strains. Brain Res 998: 20-28.
27. Green AI, Brown ES (2006). Comorbid schizophrenia and substance abuse. J Clin Psychiatry 67: E088
28. Haile CN, Kosten TA (2001). Differential effects of D1- and D2-like compounds on cocaine self-administration in Lewis and Fischer 344 inbred rats. J Pharmacol Exp Ther 299: 509-518.
29. Hajos N, Katona I, Naiem SS, Mackie K, et al. (2000). Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12: 3239-3249.
30. Katona I, Sperlagh B, Magloczky Z, Santha E, et al. (2000). GABAergic interneurons are the targets of cannabinoid actions in the human hippocampus. Neuroscience 100: 797-804.
31. Kim DJ, Thayer SA (2000). Activation of CB1 cannabinoid receptors inhibits neurotransmitter release from identified synaptic sites in rat hippocampal cultures. Brain Res 852: 398-405.
32. Koob GF, Volkow ND (2010). Neurocircuitry of addiction. Neuropsychopharmacology 35: 217-238.
33. Kosten TA, Ambrosio E (2002). HPA axis function and drug addictive behaviors : Insights from studies with Lewis and Fischer 344 inbred rats. Psychoneuroendocrinology 27: 35-69.
34. Kosten TA, Miserendino MJ, Chi S, Nestler EJ (1994). Fischer and Lewis rat strains show differential cocaine effects in conditioned place preference and behavioral sensitization but not in locomotor activity or conditioned taste aversion. J Pharmacol Exp Ther 269: 137-144.
35. Kosten TA, Miserendino MJ, Haile CN, DeCaprio JL, et al. (1997). Acquisition and maintenance of intravenous cocaine self-administration in Lewis and Fischer inbred rat strains. Brain Res 778: 418-429.
36. Kruzich PJ, Xi J (2006). Different patterns of pharmacological reinstatement of cocaine-seeking behavior between Fischer 344 and Lewis rats. Psychopharmacology (Berl) 187: 22-29.
37. Lepore M, Liu X, Savage V, Matalon D, et al. (1996). Genetic differences in delta 9-tetrahydrocannabinol-induced facilitation of brain stimulation reward as measured by a rate-frequency curve-shift electrical brain stimulation paradigm in three different rat strains. Life Sci 58: PL365-PL372.
38. Leung D, Saghatelian A, Simon GM, Cravatt BF (2006). Inactivation of N-acyl phosphatidylethanolamine phospholipase D reveals multiple mechanisms for the biosynthesis of endocannabinoids. Biochemistry 45: 4720-4726.
39. Liu J, Wang L, Harvey-White J, Huang BX, et al. (2008). Multiple pathways involved in the biosynthesis of anandamide. Neuropharmacology 54: 1-7.
40. Lopez-Moreno JA, Gonzalez-Cuevas G, Moreno G, Navarro M (2008). The pharmacology of the endocannabinoid system: Functional and structural interactions with other neurotransmitter systems and their repercussions in behavioral addiction. Addict Biol 13: 160-187.
41. Malenka RC, Bear MF (2004). LTP and LTD: an embarrassment of riches. Neuron 44: 5-21.
42. Miguens M, Botreau F, Olías O, Del Olmo N, et al. (2011a). Genetic differences in the modulation of accumbal glutamate and g-amino butyric acid levels after cocaine-induced reinstatement. Addict Biol. Published online 18 October 2011. doi :10.1111/j.1369-1600.2011.00404.xx
43. Miguens M, Coria SM, Higuera-Matas A, Fole A, et al. (2011b). Depotentiation of hippocampal long-term potentiation depends on genetic background and is modulated by cocaine self-administration. Neuroscience 187: 36-42.
44. Miguens M, Crespo JA, Del Olmo N, Higuera-Matas A, et al. (2008). Differential cocaine-induced modulation of glutamate and dopamine transporters after contingent and non-contingent administration. Neuropharmacology 55: 771-779.
45. Munn NA (2000). Microglia dysfunction in schizophrenia : An integrative theory. Med Hypotheses 54: 198-202.
46. Onaivi ES, Ishiguro H, Gong JP, Patel S, et al. (2008). Functional expression of brain neuronal CB2 cannabinoid receptors are involved in the effects of drugs of abuse and in depression. Ann N Y Acad Sci 1139: 434-449.
47. Orio L, Edwards S, George O, Parsons LH, et al. (2009). A role for the endocannabinoid system in the increased motivation for cocaine in extended-access conditions. J Neurosci 29: 4846-4857.
48. Ortega-Alvaro A, Aracil-Fernandez A, Garcia-Gutierrez MS, Navarrete F, et al. (2011). Deletion of CB(2) cannabinoid receptor induces schizophrenia- related behaviors in mice. Neuropsychopharmacology 37: 1489-1504.
49. Ortiz J, Fitzgerald LW, Lane S, Terwilliger R, et al. (1996). Biochemical adaptations in the mesolimbic dopamine system in response to repeated stress. Neuropsychopharmacology 14: 443-452.
50. Panlilio LV, Solinas M, Matthews SA, Goldberg SR (2007). Previous exposure to THC alters the reinforcing efficacy and anxiety-related effects of cocaine in rats. Neuropsychopharmacology 32: 646-657.
51. Paxinos G, Watson C (1998). The rat brain in stereotaxic coordinates. 4th edn. San Diego: Academic Press.
52. Picetti R, Ho A, Butelman ER, Kreek MJ (2010). Dose preference and dose escalation in extended-access cocaine selfadministration in Fischer and Lewis rats. Psychopharmacology (Berl) 211: 313-323.
53. Prakash S, Ambrosio E, Alguacil LF, Del Olmo N (2009). Genetic differences in hippocampal synaptic plasticity. Neuroscience 161: 342-346.
54. Puighermanal E, Marsicano G, Busquets-Garcia A, Lutz B, et al. (2009). Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling. Nat Neurosci 12: 1152-1158.
55. Rodriguez de Fonseca F, Navarro M (1998). Role of the limbic system in dependence on drugs. Ann Med 30: 397-405.
56. Rogers JL, See RE (2007). Selective inactivation of the ventral hippocampus attenuates cue-induced and cocaine-primed reinstatement of drug-seeking in rats. Neurobiol Learn Mem 87: 688-692.
57. Roohbakhsh A, Keshavarz S, Hasanein P, Rezvani ME, et al. (2009). Role of endocannabinoid system in the ventral hippocampus of rats in the modulation of anxiety-like behaviours. Basic Clin Pharmacol Toxicol 105: 333-338.
58. Ruiz A, Campanac E, Scott RS, Rusakov DA, et al. (2010). Presynaptic GABAA receptors enhance transmission and LTP induction at hippocampal mossy fiber synapses. Nat Neurosci 13: 431-438.
59. Sanchez-Cardoso P, Higuera-Matas A, Martin S, del Olmo N, et al. (2007). Modulation of the endogenous opioid system after morphine self-administration and during its extinction : A study in Lewis and Fischer 344 rats. Neuropharmacology 52: 931-948.
60. Soria G, Mendizabal V, Tourino C, Robledo P, et al. (2005). Lack of CB1 cannabinoid receptor impairs cocaine self-administration. Neuropsychopharmacology 30: 1670-1680.
61. Stefań ski R, Ziółkowska B, Kuśmider M, Mierzejewski P, et al. (2007). Active vs. passive cocaine administration: Differences in the neuroadaptive changes in the brain dopaminergic system. Brain Res 1157: 1-10.
62. Stella N, Schweitzer P, Piomelli D (1997). A second endogenous cannabinoid that modulates long-term potentiation. Nature 388: 773-778.
63. Suárez J, Bermú dez-Silva FJ, Mackie K, Ledent C, et al. (2008). Immunohistochemical description of the endogenous cannabinoid system in the rat cerebellum and functionally related nuclei. J Comp Neurol 509: 400-421.
64. Suárez J, Llorente R, Romero-Zerbo SY, Mateos B, et al. (2009). Early maternal deprivation induces gender-dependent changes on the expression of hippocampal CB(1) and CB(2) cannabinoid receptors of neonatal rats. Hippocampus 19: 623-632.
65. Suárez J, Ortíz O, Puente N, Bermú dez-Silva FJ, et al. (2011). Distribution of diacylglycerol lipase alpha, an endocannabinoid synthesizing enzyme, in the rat forebrain. Neuroscience 192: 112-131.
66. Suárez J, Romero-Zerbo SY, Rivera P, Bermudez-Silva FJ, et al. (2010). Endocannabinoid system in the adult rat circumventricular areas : An immunohistochemical study. J Comp Neurol 518: 3065-3085.
67. Sugiura T, Kondo S, Sukagawa A, Nakane S, et al. (1995). 2-Arachidonoylglycerol : A possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 215: 89-97.
68. Sullivan JM (1999). Mechanisms of cannabinoid-receptormediated inhibition of synaptic transmission in cultured hippocampal pyramidal neurons. J Neurophysiol 82: 1286-1294.
69. Tanda G, Munzar P, Goldberg SR (2000). Self-administration behavior is maintained by the psychoactive ingredient of marijuana in squirrel monkeys. Nat Neurosci 3: 1073-1074.
70. Terranova JP, Michaud JC, Le Fur G, Soubrie P (1995). Inhibition of long-term potentiation in rat hippocampal slices by anandamide and WIN55212-2: Reversal by SR141716 A, a selective antagonist of CB1 cannabinoid receptors. Naunyn Schmiedebergs Arch Pharmacol 352: 576-579.
71. Thompson AM, Swant J, Gosnell BA, Wagner JJ (2004). Modulation of long-term potentiation in the rat hippocampus following cocaine self-administration. Neuroscience 127: 177-185.
72. Vorel SR, Liu X, Hayes RJ, Spector JA, et al. (2001). Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science 292: 1175-1178.
73. Wager-Miller J, Westenbroek R, Mackie K (2002). Dimerization of G protein-coupled receptors : CB1 cannabinoid receptors as an example. Chem Phys Lipids 121: 83-89.
74. Xi ZX, Peng XQ, Li X, Song R, et al. (2011). Brain cannabinoid CB2 receptors modulate cocaine's actions in mice. Nat Neurosci 14: 1160-1166.