Activation of PPARγ by pioglitazone potentiates the effects of naltrexone on alcohol drinking and relapse in msP rats

Alcoholism: Clinical and Experimental Research

Volumn 37, Issue 8, 2013, Pages 1351-1360

  Stopponi, Serena ^a   de Guglielmo, Giordano ^a   Somaini, Lorenzo ^b   Cippitelli, Andrea ^a   Cannella, Nazzareno ^a   Kallupi, Marsida ^a   Ubaldi, Massimo ^a   Heilig, Markus ^c   Demopulos, Gregory ^d   Gaitanaris, George ^d   Ciccocioppo, Roberto ^a  

^a UNIVERSITY OF CAMERINO   (Italy)

^b Addiction Treatment Centre   (Italy)

^c NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^d OMEROS CORPORATION   (United States)

Author keywords

Abuse; Addiction; Drug Seeking; Ethanol; Self Administration

Indexed keywords

ALCOHOL; NALTREXONE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; YOHIMBINE;

ALCOHOL CONSUMPTION; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; DRINKING BEHAVIOR; DRUG EFFECT; DRUG EFFICACY; DRUG POTENTIATION; GENETIC ASSOCIATION; NONHUMAN; PRIORITY JOURNAL; RAT; RAT STRAIN; RECURRENT DISEASE;

ABUSE; ADDICTION; DRUG SEEKING; ETHANOL; SELF-ADMINISTRATION;

ALCOHOL DRINKING; ANIMALS; CUES; DRUG EVALUATION, PRECLINICAL; DRUG THERAPY, COMBINATION; HYPOGLYCEMIC AGENTS; MALE; NALTREXONE; NARCOTIC ANTAGONISTS; PPAR GAMMA; RATS; THIAZOLIDINEDIONES; YOHIMBINE;

EID: 84881012336     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/acer.12091     Document Type: Article

References (53)

1. Anton RF, O'Malley SS, Ciraulo DA, Cisler RA, Couper D, Donovan DM, Gastfriend DR, Hosking JD, Johnson BA, LoCastro JS, Longabaugh R, Mason BJ, Mattson ME, Miller WR, Pettinati HM, Randall CL, Swift R, Weiss RD, Williams LD, Zweben A, COMBINE Study Research Group (2006) Combined pharmacotherapies and behavioral interventions for alcohol dependence: the COMBINE study: a randomized controlled trial. JAMA 295:2003-2017.
2. Anton RF, Oroszi G, O'Malley S, Couper D, Swift R, Pettinati H, Goldman D (2008) An evaluation of mu-opioid receptor (OPRM1) as a predictor of naltrexone response in the treatment of alcohol dependence: results from the Combined Pharmacotherapies and Behavioral Interventions for Alcohol Dependence (COMBINE) study. Arch Gen Psychiatry 65:135-144.
3. Berger J, Moller DE (2002) The mechanisms of action of PPARs. Annu Rev Med 53:409-435.
4. Boettcher E, Csako G, Pucino F, Wesley R, Loomba R (2012) Meta-analysis: pioglitazone improves liver histology and fibrosis in patients with non-alcoholic steatohepatitis. Aliment Pharmacol Ther 35:66-75.
5. Breese GR, Knapp DJ, Overstreet DH, Navarro M, Wills TA, Angel RA (2008) Repeated lipopolysaccharide (LPS) or cytokine treatments sensitize ethanol withdrawal-induced anxiety-like behavior. Neuropsychopharmacology 33:867-876.
6. Breidert T, Callebert J, Heneka MT, Landreth G, Launay JM, Hirsch EC (2002) Protective action of the peroxisome proliferator-activated receptor-gamma agonist pioglitazone in a mouse model of Parkinson's disease. J Neurochem 82:615-624.
7. Chang F, Jaber LA, Berlie HD, O'Connell MB (2007) Evolution of peroxisome proliferator-activated receptor agonists. Ann Pharmacother 41:973-983.
8. Charney DS, Heninger GR, Redmond DE Jr (1983) Yohimbine induced anxiety and increased noradrenergic function in humans: effects of diazepam and clonidine. Life Sci 33:19-29.
9. Ciccocioppo R, Angeletti S, Weiss F (2001a) Long-lasting resistance to extinction of response reinstatement induced by ethanol-related stimuli: role of genetic ethanol preference. Alcohol Clin Exp Res 25:1414-1419.
10. Ciccocioppo R, Economidou D, Cippitelli A, Cucculelli M, Ubaldi M, Soverchia L, Lourdusamy A, Massi M (2006) Genetically selected Marchigian Sardinian alcohol-preferring (msP) rats: an animal model to study the neurobiology of alcoholism. Addict Biol 11:339-355.
11. Ciccocioppo R, Martin-Fardon R, Weiss F (2002) Effect of selective blockade of mu(1) or delta opioid receptors on reinstatement of alcohol-seeking behavior by drug-associated stimuli in rats. Neuropsychopharmacology 27:391-399.
12. Ciccocioppo R, Sanna PP, Weiss F (2001b) Cocaine-predictive stimulus induces drug-seeking behavior and neural activation in limbic brain regions after multiple months of abstinence: reversal by D(1) antagonists. Proc Natl Acad Sci USA 98:1976-1981.
13. 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 198:449-460.
14. Devine DP, Leone P, Wise RA (1993) Mesolimbic dopamine neurotransmission is increased by administration of mu-opioid receptor antagonists. Eur J Pharmacol 243:55-64.
15. Di Chiara G, North RA (1992) Neurobiology of opiate abuse. Trends Pharmacol Sci 13:185-193.
16. Economidou D, Mattioli L, Cifani C, Perfumi M, Massi M, Cuomo V, Trabace L, Ciccocioppo R (2006) Effect of the cannabinoid CB1 receptor antagonist SR-141716A on ethanol self-administration and ethanol-seeking behaviour in rats. Psychopharmacology 183:394-403.
17. Garcia-Bueno B, Madrigal JL, Lizasoain I, Moro MA, Lorenzo P, Leza JC (2005) Peroxisome proliferator-activated receptor gamma activation decreases neuroinflammation in brain after stress in rats. Biol Psychiatry 57:885-894.
18. Gofflot F, Chartoire N, Vasseur L, Heikkinen S, Dembele D, Le Merrer J, Auwerx J (2007) Systematic gene expression mapping clusters nuclear receptors according to their function in the brain. Cell 131:405-418.
19. Gupta AK, Smith SR, Greenway FL, Bray GA (2009) Pioglitazone treatment in type 2 diabetes mellitus when combined with portion control diet modifies the metabolic syndrome. Diabetes Obes Metab 11:330-337.
20. Hansson AC, Cippitelli A, Sommer WH, Fedeli A, Bjork K, Soverchia L, Terasmaa A, Massi M, Heilig M, Ciccocioppo R (2006) Variation at the rat Crhr1 locus and sensitivity to relapse into alcohol seeking induced by environmental stress. Proc Natl Acad Sci USA 103:15236-15241.
21. He DY, McGough NN, Ravindranathan A, Jeanblanc J, Logrip ML, Phamluong K, Janak PH, Ron D (2005) Glial cell line-derived neurotrophic factor mediates the desirable actions of the anti-addiction drug ibogaine against alcohol consumption. J Neurosci 25:619-628.
22. Heilig M, Goldman D, Berrettini W, O'Brien CP (2011) Pharmacogenetic approaches to the treatment of alcohol addiction. Nat Rev Neurosci 12:670-684.
23. Ladenheim B, Krasnova IN, Deng X, Oyler JM, Polettini A, Moran TH, Huestis MA, Cadet JL (2000) Methamphetamine-induced neurotoxicity is attenuated in transgenic mice with a null mutation for interleukin-6. Mol Pharmacol 58:1247-1256.
24. Landreth GE, Heneka MT (2001) Anti-inflammatory actions of peroxisome proliferator-activated receptor gamma agonists in Alzheimer's disease. Neurobiol Aging 22:937-944.
25. Le AD, Harding S, Juzytsch W, Funk D, Shaham Y (2005) Role of alpha-2 adrenoceptors in stress-induced reinstatement of alcohol seeking and alcohol self-administration in rats. Psychopharmacology 179:366-373.
26. Le AD, Harding S, Juzytsch W, Watchus J, Shalev U, Shaham Y (2000) The role of corticotrophin-releasing factor in stress-induced relapse to alcohol-seeking behavior in rats. Psychopharmacology 150:317-324.
27. Le AD, Poulos CX, Harding S, Watchus J, Juzytsch W, Shaham Y (1999) Effects of naltrexone and fluoxetine on alcohol self-administration and reinstatement of alcohol seeking induced by priming injections of alcohol and exposure to stress. Neuropsychopharmacology 21:435-444.
28. Lee B, Tiefenbacher S, Platt DM, Spealman RD (2004) Pharmacological blockade of alpha2-adrenoceptors induces reinstatement of cocaine-seeking behavior in squirrel monkeys. Neuropsychopharmacology 29:686-693.
29. Lin SL, Tsai RY, Tai YH, Cherng CH, Wu CT, Yeh CC, Wong CS (2010) Ultra-low dose naloxone upregulates interleukin-10 expression and suppresses neuroinflammation in morphine-tolerant rat spinal cords. Behav Brain Res 207:30-36.
30. Liu X, Weiss F (2002a) Additive effect of stress and drug cues on reinstatement of ethanol seeking: exacerbation by history of dependence and role of concurrent activation of corticotropin-releasing factor and opioid mechanisms. J Neurosci 22:7856-7861.
31. Liu X, Weiss F (2002b) Reversal of ethanol-seeking behavior by D1 and D2 antagonists in an animal model of relapse: differences in antagonist potency in previously ethanol-dependent versus nondependent rats. J Pharmacol Exp Ther 300:882-889.
32. Maeda T, Kiguchi N, Fukazawa Y, Yamamoto A, Ozaki M, Kishioka S (2007) Peroxisome proliferator-activated receptor gamma activation relieves expression of behavioral sensitization to methamphetamine in mice. Neuropsychopharmacology 32:1133-1140.
33. Mann K, Kiefer F, Smolka M, Gann H, Wellek S, Heinz A (2009) Searching for responders to acamprosate and naltrexone in alcoholism treatment: rationale and design of the PREDICT study. Alcohol Clin Exp Res 33:674-683.
34. Marinelli PW, Funk D, Juzytsch W, Harding S, Rice KC, Shaham Y, Lê AD (2007) The CRF1 receptor antagonist antalarmin attenuates yohimbine-induced increases in operant alcohol self-administration and reinstatement of alcohol seeking in rats. Psychopharmacology 195:345-355.
35. McCusker CG, Brown K (1990) Alcohol-predictive cues enhance tolerance to and precipitate "craving" for alcohol in social drinkers. J Stud Alcohol 51:494-499.
36. Messer CJ, Eisch AJ, Carlezon WA Jr, Whisler K, Shen L, Wolf DH, Westphal H, Collins F, Russell DS, Nestler EJ (2000) Role for GDNF in biochemical and behavioral adaptations to drugs of abuse. Neuron 26:247-257.
37. Mika J (2008) Modulation of microglia can attenuate neuropathic pain symptoms and enhance morphine effectiveness. Pharmacol Rep 60:297-307.
38. Monti PM, Rohsenow DJ, Hutchison KE, Swift RM, Mueller TI, Colby SM, Brown RA, Gulliver SB, Gordon A, Abrams DB (1999) Naltrexone's effect on cue-elicited craving among alcoholics in treatment. Alcohol Clin Exp Res 23:1386-1394.
39. Monti PM, Rohsenow DJ, Rubonis AV, Niaura RS, Sirota AD, Colby SM, Abrams DB (1993) Alcohol cue reactivity: effects of detoxification and extended exposure. J Stud Alcohol 54:235-245.
40. Moreno S, Farioli-Vecchioli S, Ceru MP (2004) Immunolocalization of peroxisome proliferator-activated receptors and retinoid X receptors in the adult rat CNS. Neuroscience 123:131-145.
41. O'Brien CP (1996) Drug Addiction and Drug Abuse. Goodman and Gilman's The Pharmacological Basis of Therapeutics. 9th ed. McGraw-Hill, New York.
42. O'Brien CP, Childress AR, Ehrman R, Robbins SJ (1998) Conditioning factors in drug abuse: can they explain compulsion? J Psychopharmacol 12:15-22.
43. O'Brien CP, Volpicelli LA, Volpicelli JR (1996) Naltrexone in the treatment of alcoholism: a clinical review. Alcohol 13:35-39.
44. O'Malley SS, Jaffe AJ, Chang G, Schottenfeld RS, Meyer RE, Rounsaville B (1992) Naltrexone and coping skills therapy for alcohol dependence. Arch Gen Psychiatry 49:881-888.
45. Rohsenow DJ, Monti PM, Hutchison KE, Swift RM, Colby SM, Kaplan GB (2000) Naltrexone's effects on reactivity to alcohol cues among alcoholic men. J Abnorm Psychol 109:738-742.
46. Sarruf DA, Yu F, Nguyen HT, Williams DL, Printz RL, Niswender KD, Schwartz MW (2009) Expression of peroxisome proliferator-activated receptor-gamma in key neuronal subsets regulating glucose metabolism and energy homeostasis. Endocrinology 150:707-712.
47. Sass H, Soyka M, Mann K, Zieglgansberger W (1996) Relapse prevention by acamprosate. Results from a placebo-controlled study on alcohol dependence. Arch Gen Psychiatry 53:673-680.
48. Stopponi S, Somaini L, Cippitelli A, Cannella N, Braconi S, Kallupi M, Ruggeri B, Heilig M, Demopulos G, Gaitanaris G, Massi M, Ciccocioppo R (2011) Activation of nuclear PPARgamma receptors by the antidiabetic agent pioglitazone suppresses alcohol drinking and relapse to alcohol seeking. Biol Psychiatry 69:642-649.
49. Tontonoz P, Spiegelman BM (2008) Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem 77:289-312.
50. Umhau JC, Schwandt ML, Usala J, Geyer C, Singley E, George DT, Heilig M (2011) Pharmacologically induced alcohol craving in treatment seeking alcoholics correlates with alcoholism severity, but is insensitive to acamprosate. Neuropsychopharmacology 36:1178-1186.
51. Volpicelli JR, Alterman AI, Hayashida M, O'Brien CP (1992) Naltrexone in the treatment of alcohol dependence. Arch Gen Psychiatry 49:876-880.
52. Woods JW, Tanen M, Figueroa DJ, Biswas C, Zycband E, Moller DE, Austin CP, Berger JP (2003) Localization of PPARdelta in murine central nervous system: expression in oligodendrocytes and neurons. Brain Res 975:10-21.
53. Zalcman S, Savina I, Wise RA (1999) Interleukin-6 increases sensitivity to the locomotor-stimulating effects of amphetamine in rats. Brain Res 847:276-283.