Differential Effects of Single Versus Repeated Alcohol Withdrawal on the Expression of Endocannabinoid System-Related Genes in the Rat Amygdala

Alcoholism: Clinical and Experimental Research

Volumn 36, Issue 6, 2012, Pages 984-994

  Serrano, Antonia ^a,b   Rivera, Patricia ^a   Pavon, Francisco J ^a,b   Decara, Juan ^a   Suárez, Juan ^a   Rodriguez de Fonseca, Fernando ^a   Parsons, Loren H ^b  

^a HOSPITAL REGIONAL UNIVERSITARIO DE MÁLAGA   (Spain)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Amygdala; Endocannabinoid System; Ethanol; Withdrawal

Indexed keywords

ALCOHOL; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; ENDOCANNABINOID; FATTY ACID AMIDASE; MESSENGER RNA;

ALCOHOL BLOOD LEVEL; ALCOHOL CONSUMPTION; ALCOHOL WITHDRAWAL; ALCOHOLISM; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

AMIDOHYDROLASES; AMYGDALA; ANIMALS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ENDOCANNABINOIDS; ETHANOL; GENE EXPRESSION; GENE EXPRESSION PROFILING; MALE; MONOACYLGLYCEROL LIPASES; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, CANNABINOID; RNA, MESSENGER; SIGNAL TRANSDUCTION; SUBSTANCE WITHDRAWAL SYNDROME;

RATTUS;

EID: 84861727828     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2011.01686.x     Document Type: Article

References (89)

1. Ahn K, McKinney MK, Cravatt BF (2008) Enzymatic pathways that regulate endocannabinoid signaling in the nervous system. Chem Rev 108:1687-1707.
2. Alvarez-Jaimes L, Stouffer DG, Parsons LH (2009) Chronic ethanol treatment potentiates ethanol-induced increases in interstitial nucleus accumbens endocannabinoid levels in rats. J Neurochem 111:37-48.
3. Arnone M, Maruani J, Chaperon F, Thiebot MH, Poncelet M, Soubrie P, Le Fur G (1997) Selective inhibition of sucrose and ethanol intake by SR 141716, an antagonist of central cannabinoid (CB1) receptors. Psychopharmacology (Berl) 132:104-106.
4. Basavarajappa BS, Cooper TB, Hungund BL (1998) Chronic ethanol administration down-regulates cannabinoid receptors in mouse brain synaptic plasma membrane. Brain Res 793:212-218.
5. Basavarajappa BS, Hungund BL (1999) Chronic ethanol increases the cannabinoid receptor agonist anandamide and its precursor N-arachidonoylphosphatidylethanolamine in SK-N-SH cells. J Neurochem 72:522-528.
6. Basavarajappa BS, Saito M, Cooper TB, Hungund BL (2000) Stimulation of cannabinoid receptor agonist 2-arachidonylglycerol by chronic ethanol and its modulation by specific neuromodulators in cerebellar granule neurons. Biochim Biophys Acta 1535:78-86.
7. Basavarajappa BS, Saito M, Cooper TB, Hungund BL (2003) Chronic ethanol inhibits the anandamide transport and increases extracellular anandamide levels in cerebellar granule neurons. Eur J Pharmacol 466:73-83.
8. Bertotto ME, Maldonado NM, Bignante EA, Gorosito SV, Cambiasso MJ, Molina VA, Martijena ID (in press) Erk activation in the amygdala and hippocampus induced by fear conditioning in ethanol withdrawn rats: modulation by mk-801. Eur Neuropsychopharmacol doi: 10.1016/j.euroneuro.2011.01.001
9. Bisogno T, Howell F, Williams G, Minassi A, Cascio MG, Ligresti A, Matias I, Schiano-Moriello A, Paul P, Williams EJ, Gangadharan U, Hobbs C, Di Marzo V, Doherty P (2003) Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J Cell Biol 163:463-468.
10. Boger DL, Henriksen SJ, Cravatt BF (1998) Oleamide: an endogenous sleep-inducing lipid and prototypical member of a new class of biological signaling molecules. Curr Pharm Des 4:303-314.
11. Bortolato M, Campolongo P, Mangieri RA, Scattoni ML, Frau R, Trezza V, La Rana G, Russo R, Calignano A, Gessa GL, Cuomo V, Piomelli D (2006) Anxiolytic-like properties of the anandamide transport inhibitor AM404. Neuropsychopharmacology 31:2652-2659.
12. Caille S, Alvarez-Jaimes L, Polis I, Stouffer DG, Parsons LH (2007) Specific alterations of extracellular endocannabinoid levels in the nucleus accumbens by ethanol, heroin, and cocaine self-administration. J Neurosci 27:3695-3702.
13. Cippitelli A, Bilbao A, Hansson AC, del Arco I, Sommer W, Heilig M, Massi M, Bermudez-Silva FJ, Navarro M, Ciccocioppo R, de Fonseca FR (2005) Cannabinoid CB1 receptor antagonism reduces conditioned reinstatement of ethanol-seeking behavior in rats. Eur J Neurosci 21:2243-2251.
14. Cippitelli A, Cannella N, Braconi S, Duranti A, Tontini A, Bilbao A, Defonseca FR, Piomelli D, Ciccocioppo R (2008) Increase of brain endocannabinoid anandamide levels by FAAH inhibition and alcohol abuse behaviours in the rat. Psychopharmacology (Berl) 198:449-460.
15. Colombo G, Serra S, Brunetti G, Gomez R, Melis S, Vacca G, Carai MM, Gessa L (2002) Stimulation of voluntary ethanol intake by cannabinoid receptor agonists in ethanol-preferring sP rats. Psychopharmacology (Berl) 159:181-187.
16. Comings DE, Muhleman D, Gade R, Johnson P, Verde R, Saucier G, MacMurray J (1997) Cannabinoid receptor gene (CNR1): association with i.v. drug use. Mol Psychiatry 2:161-168.
17. Cravatt BF, Giang DK, Mayfield SP, Boger DL, Lerner RA, Gilula NB (1996) Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384:83-87.
18. Di Marzo V (2008) Endocannabinoids: synthesis and degradation. Rev Physiol Biochem Pharmacol 160:1-24.
19. Dinh TP, Carpenter D, Leslie FM, Freund TF, Katona I, Sensi SL, Kathuria S, Piomelli D (2002) Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci USA 99:10819-10824.
20. Ferrer B, Bermudez-Silva FJ, Bilbao A, Alvarez-Jaimes L, Sanchez-Vera I, Giuffrida A, Serrano A, Baixeras E, Khaturia S, Navarro M, Parsons LH, Piomelli D, Rodriguez de Fonseca F (2007) Regulation of brain anandamide by acute administration of ethanol. Biochem J 404:97-104.
21. Fowler CJ (2006) The cannabinoid system and its pharmacological manipulation-a review, with emphasis upon the uptake and hydrolysis of anandamide. Fundam Clin Pharmacol 20:549-562.
22. Freedland CS, Sharpe AL, Samson HH, Porrino LJ (2001) Effects of SR141716A on ethanol and sucrose self-administration. Alcohol Clin Exp Res 25:277-282.
23. Gaetani S, Oveisi F, Piomelli D (2003) Modulation of meal pattern in the rat by the anorexic lipid mediator oleoylethanolamide. Neuropsychopharmacology 28:1311-1316.
24. Glaser ST, Kaczocha M (2009) Temporal changes in mouse brain fatty acid amide hydrolase activity. Neuroscience 163:594-600.
25. Godlewski G, Offertaler L, Wagner JA, Kunos G (2009) Receptors for acylethanolamides-GPR55 and GPR119. Prostaglandins Other Lipid Mediat 89:105-111.
26. Gonzalez S, Cascio MG, Fernandez-Ruiz J, Fezza F, Di Marzo V, Ramos JA (2002) Changes in endocannabinoid contents in the brain of rats chronically exposed to nicotine, ethanol or cocaine. Brain Res 954:73-81.
27. Gonzalez S, Valenti M, de Miguel R, Fezza F, Fernandez-Ruiz J, Di Marzo V, Ramos JA (2004) Changes in endocannabinoid contents in reward-related brain regions of alcohol-exposed rats, and their possible relevance to alcohol relapse. Br J Pharmacol 143:455-464.
28. Gulyas AI, Cravatt BF, Bracey MH, Dinh TP, Piomelli D, Boscia F, Freund TF (2004) Segregation of two endocannabinoid-hydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur J Neurosci 20:441-458.
29. Haller J, Bakos N, Szirmay M, Ledent C, Freund TF (2002) The effects of genetic and pharmacological blockade of the CB1 cannabinoid receptor on anxiety. Eur J Neurosci 16:1395-1398.
30. Hansson AC, Bermudez-Silva FJ, Malinen H, Hyytia P, Sanchez-Vera I, Rimondini R, Rodriguez de Fonseca F, Kunos G, Sommer WH, Heilig M (2007) Genetic impairment of frontocortical endocannabinoid degradation and high alcohol preference. Neuropsychopharmacology 32:117-126.
31. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563-583.
32. Hill MN, Gorzalka BB (2009) The endocannabinoid system and the treatment of mood and anxiety disorders. CNS Neurol Disord Drug Targets 8:451-458.
33. Holter SM, Engelmann M, Kirschke C, Liebsch G, Landgraf R, Spanagel R (1998) Long-term ethanol self-administration with repeated ethanol deprivation episodes changes ethanol drinking pattern and increases anxiety-related behaviour during ethanol deprivation in rats. Behav Pharmacol 9:41-48.
34. Huang MM, Overstreet DH, Knapp DJ, Angel R, Wills TA, Navarro M, Rivier J, Vale W, Breese GR (2010) Corticotropin-releasing factor (CRF) sensitization of ethanol withdrawal-induced anxiety-like behavior is brain site specific and mediated by CRF-1 receptors: relation to stress-induced sensitization. J Pharmacol Exp Ther 332:298-307.
35. Hungund BL, Szakall I, Adam A, Basavarajappa BS, Vadasz C (2003) Cannabinoid CB1 receptor knockout mice exhibit markedly reduced voluntary alcohol consumption and lack alcohol-induced dopamine release in the nucleus accumbens. J Neurochem 84:698-704.
36. Kamprath K, Romo-Parra H, Haring M, Gaburro S, Doengi M, Lutz B, Pape HC (2011) Short-term adaptation of conditioned fear responses through endocannabinoid signaling in the central amygdala. Neuropsychopharmacology 36:652-663.
37. Kathuria S, Gaetani S, Fegley D, Valino F, Duranti A, Tontini A, Mor M, Tarzia G, La Rana G, Calignano A, Giustino A, Tattoli M, Palmery M, Cuomo V, Piomelli D (2003) Modulation of anxiety through blockade of anandamide hydrolysis. Nat Med 9:76-81.
38. Katona I, Rancz EA, Acsady L, Ledent C, Mackie K, Hajos N, Freund TF (2001) Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 21:9506-9518.
39. Koob GF (2009) Brain stress systems in the amygdala and addiction. Brain Res 1293:61-75.
40. Koob GF, Roberts AJ, Schulteis G, Parsons LH, Heyser CJ, Hyytia P, Merlo-Pich E, Weiss F (1998) Neurocircuitry targets in ethanol reward and dependence. Alcohol Clin Exp Res 22:3-9.
41. Labar G, Michaux C (2007) Fatty acid amide hydrolase: from characterization to therapeutics. Chem Biodivers 4:1882-1902.
42. Landolt HP, Gillin JC (2001) Sleep abnormalities during abstinence in alcohol-dependent patients. Aetiology and management. CNS Drugs 15:413-425.
43. 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.
44. Little HJ, Croft AP, O'Callaghan MJ, Brooks SP, Wang G, Shaw SG (2008) Selective increases in regional brain glucocorticoid: a novel effect of chronic alcohol. Neuroscience 156:1017-1027.
45. Liu J, Wang L, Harvey-White J, Huang BX, Kim HY, Luquet S, Palmiter RD, Krystal G, Rai R, Mahadevan A, Razdan RK, Kunos G (2008) Multiple pathways involved in the biosynthesis of anandamide. Neuropharmacology 54:1-7.
46. Liu J, Wang L, Harvey-White J, Osei-Hyiaman D, Razdan R, Gong Q, Chan AC, Zhou Z, Huang BX, Kim HY, Kunos G (2006) A biosynthetic pathway for anandamide. Proc Natl Acad Sci USA 103:13345-13350.
47. Lopez MF, Becker HC (2005) Effect of pattern and number of chronic ethanol exposures on subsequent voluntary ethanol intake in C57BL/6J mice. Psychopharmacology (Berl) 181:688-696.
48. Lutz B (2009) Endocannabinoid signals in the control of emotion. Curr Opin Pharmacol 9:46-52.
49. Malinen H, Lehtonen M, Hyytia P (2009) Modulation of brain endocannabinoid levels by voluntary alcohol consumption in alcohol-preferring AA rats. Alcohol Clin Exp Res 33:1711-1720.
50. McDonald AJ, Mascagni F (2001) Localization of the CB1 type cannabinoid receptor in the rat basolateral amygdala: high concentrations in a subpopulation of cholecystokinin-containing interneurons. Neuroscience 107:641-652.
51. Merlo Pich E, Lorang M, Yeganeh M, Rodriguez de Fonseca F, Raber J, Koob GF, Weiss F (1995) Increase of extracellular corticotropin-releasing factor-like immunoreactivity levels in the amygdala of awake rats during restraint stress and ethanol withdrawal as measured by microdialysis. J Neurosci 15:5439-5447.
52. Moonat S, Sakharkar AJ, Zhang H, Pandey SC (2011) The role of amygdaloid brain-derived neurotrophic factor, activity-regulated cytoskeleton-associated protein and dendritic spines in anxiety and alcoholism. Addict Biol 16:238-250.
53. Moreira FA, Wotjak CT (2010) Cannabinoids and anxiety. Curr Top Behav Neurosci 2:429-450.
54. Naassila M, Pierrefiche O, Ledent C, Daoust M (2004) Decreased alcohol self-administration and increased alcohol sensitivity and withdrawal in CB1 receptor knockout mice. Neuropharmacology 46:243-253.
55. Okamoto Y, Morishita J, Tsuboi K, Tonai T, Ueda N (2004) Molecular characterization of a phospholipase D generating anandamide and its congeners. J Biol Chem 279:5298-5305.
56. Orio L, Edwards S, George O, Parsons LH, Koob GF (2009) A role for the endocannabinoid system in the increased motivation for cocaine in extended-access conditions. J Neurosci 29:4846-4857.
57. Overstreet DH, Knapp DJ, Breese GR (2002) Accentuated decrease in social interaction in rats subjected to repeated ethanol withdrawals. Alcohol Clin Exp Res 26:1259-1268.
58. Overstreet DH, Knapp DJ, Breese GR (2004) Similar anxiety-like responses in male and female rats exposed to repeated withdrawals from ethanol. Pharmacol Biochem Behav 78:459-464.
59. Pandey SC, Zhang H, Ugale R, Prakash A, Xu T, Misra K (2008) Effector immediate-early gene arc in the amygdala plays a critical role in alcoholism. J Neurosci 28:2589-2600.
60. Patel S, Cravatt BF, Hillard CJ (2005a) Synergistic interactions between cannabinoids and environmental stress in the activation of the central amygdala. Neuropsychopharmacology 30:497-507.
61. Patel S, Roelke CT, Rademacher DJ, Cullinan WE, Hillard CJ (2004) Endocannabinoid signaling negatively modulates stress-induced activation of the hypothalamic-pituitary-adrenal axis. Endocrinology 145:5431-5438.
62. Patel S, Roelke CT, Rademacher DJ, Hillard CJ (2005b) Inhibition of restraint stress-induced neural and behavioural activation by endogenous cannabinoid signalling. Eur J Neurosci 21:1057-1069.
63. Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York.
64. Radwanska K, Wrobel E, Korkosz A, Rogowski A, Kostowski W, Bienkowski P, Kaczmarek L (2008) Alcohol relapse induced by discrete cues activates components of AP-1 transcription factor and ERK pathway in the rat basolateral and central amygdala. Neuropsychopharmacology 33:1835-1846.
65. Rimondini R, Arlinde C, Sommer W, Heilig M (2002) Long-lasting increase in voluntary ethanol consumption and transcriptional regulation in the rat brain after intermittent exposure to alcohol. FASEB J 16:27-35.
66. Roberto M, Cruz M, Bajo M, Siggins GR, Parsons LH, Schweitzer P (2010) The endocannabinoid system tonically regulates inhibitory transmission and depresses the effect of ethanol in central amygdala. Neuropsychopharmacology 35:1962-1972.
67. Rodriguez de Fonseca F, Carrera MR, Navarro M, Koob GF, Weiss F (1997) Activation of corticotropin-releasing factor in the limbic system during cannabinoid withdrawal. Science 276:2050-2054.
68. Rodriguez de Fonseca F, Del Arco I, Bermudez-Silva FJ, Bilbao A, Cippitelli A, Navarro M (2005) The endocannabinoid system: physiology and pharmacology. Alcohol Alcohol 40:2-14.
69. Rodriguez de Fonseca F, Navarro M (1998) Role of the limbic system in dependence on drugs. Ann Med 30:397-405.
70. Rodriguez de Fonseca F, Roberts AJ, Bilbao A, Koob GF, Navarro M (1999) Cannabinoid receptor antagonist SR141716A decreases operant ethanol self administration in rats exposed to ethanol-vapor chambers. Zhongguo Yao Li Xue Bao 20:1109-1114.
71. Rubio M, Fernandez-Ruiz J, de Miguel R, Maestro B, Michael Walker J, Ramos JA (2008) CB1 receptor blockade reduces the anxiogenic-like response and ameliorates the neurochemical imbalances associated with alcohol withdrawal in rats. Neuropharmacology 54:976-988.
72. Rubio M, McHugh D, Fernandez-Ruiz J, Bradshaw H, Walker JM (2007) Short-term exposure to alcohol in rats affects brain levels of anandamide, other N-acylethanolamines and 2-arachidonoyl-glycerol. Neurosci Lett 421:270-274.
73. Ruggeri B, Braconi S, Cannella N, Kallupi M, Soverchia L, Ciccocioppo R, Ubaldi M (2010) Neuropeptide S receptor gene expression in alcohol withdrawal and protracted abstinence in postdependent rats. Alcohol Clin Exp Res 34:90-97.
74. Rutkowska M, Jamontt J, Gliniak H (2006) Effects of cannabinoids on the anxiety-like response in mice. Pharmacol Rep 58:200-206.
75. Schlosburg JE, Blankman JL, Long JZ, Nomura DK, Pan B, Kinsey SG, Nguyen PT, Ramesh D, Booker L, Burston JJ, Thomas EA, Selley DE, Sim-Selley LJ, Liu QS, Lichtman AH, Cravatt BF (2010) Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system. Nat Neurosci 13:1113-1119.
76. Schmidt K, Krishnan B, Xia Y, Sun A, Orozco-Cabal L, Pollandt S, Centeno M, Genzer K, Gallagher JP, Shinnick-Gallagher P, Liu J (2011) Cocaine withdrawal reduces group I mGluR-mediated long-term potentiation via decreased GABAergic transmission in the amygdala. Eur J Neurosci 34:177-189.
77. Schmidt LG, Samochowiec J, Finckh U, Fiszer-Piosik E, Horodnicki J, Wendel B, Rommelspacher H, Hoehe MR (2002) Association of a CB1 cannabinoid receptor gene (CNR1) polymorphism with severe alcohol dependence. Drug Alcohol Depend 65:221-224.
78. Sciolino NR, Zhou W, Hohmann AG (2011) Enhancement of endocannabinoid signaling with JZL184, an inhibitor of the 2-arachidonoylglycerol hydrolyzing enzyme monoacylglycerol lipase, produces anxiolytic effects under conditions of high environmental aversiveness in rats. Pharmacol Res 64:226-234.
79. Simon GM, Cravatt BF (2006) Endocannabinoid biosynthesis proceeding through glycerophospho-N-acyl ethanolamine and a role for alpha/beta-hydrolase 4 in this pathway. J Biol Chem 281:26465-26472.
80. Simon GM, Cravatt BF (2008) Anandamide biosynthesis catalyzed by the phosphodiesterase GDE1 and detection of glycerophospho-N-acyl ethanolamine precursors in mouse brain. J Biol Chem 283:9341-9349.
81. Sipe JC, Chiang K, Gerber AL, Beutler E, Cravatt BF (2002) A missense mutation in human fatty acid amide hydrolase associated with problem drug use. Proc Natl Acad Sci USA 99:8394-8399.
82. Thanos PK, Dimitrakakis ES, Rice O, Gifford A, Volkow ND (2005) Ethanol self-administration and ethanol conditioned place preference are reduced in mice lacking cannabinoid CB1 receptors. Behav Brain Res 164:206-213.
83. Trevisan LA, Boutros N, Petrakis IL, Krystal JH (1998) Complications of alcohol withdrawal: pathophysiological insights. Alcohol Health Res World 22:61-66.
84. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83:393-411.
85. Valenti M, Vigano D, Casico MG, Rubino T, Steardo L, Parolaro D, Di Marzo V (2004) Differential diurnal variations of anandamide and 2-arachidonoyl-glycerol levels in rat brain. Cell Mol Life Sci 61:945-950.
86. Vinod KY, Yalamanchili R, Xie S, Cooper TB, Hungund BL (2006) Effect of chronic ethanol exposure and its withdrawal on the endocannabinoid system. Neurochem Int 49:619-625.
87. Waleh NS, Cravatt BF, Apte-Deshpande A, Terao A, Kilduff TS (2002) Transcriptional regulation of the mouse fatty acid amide hydrolase gene. Gene 291:203-210.
88. Wang L, Liu J, Harvey-White J, Zimmer A, Kunos G (2003) Endocannabinoid signaling via cannabinoid receptor 1 is involved in ethanol preference and its age-dependent decline in mice. Proc Natl Acad Sci USA 100:1393-1398.
89. Zhang H, Pandey SC (2003) Effects of PKA modulation on the expression of neuropeptide Y in rat amygdaloid structures during ethanol withdrawal. Peptides 24:1397-1402.