Increased extracellular glutamate in the nucleus accumbens promotes excessive ethanol drinking in ethanol dependent mice

Neuropsychopharmacology

Volumn 39, Issue 3, 2014, Pages 707-717

  Griffin Iii, William C ^a   Haun, Harold L ^a   Hazelbaker, Callan L ^a   Ramachandra, Vorani S ^a   Becker, Howard C ^a,b,c  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

dependence; drinking; ethanol; glutamate; microdialysis; mouse

Indexed keywords

4 AMINO 2 OXABICYCLO[3.1.0]HEXANE 4,6 DICARBOXYLIC ACID; ALCOHOL; GLUTAMATE RECEPTOR ANTAGONIST; GLUTAMIC ACID; THREO BETA BENZYLOXYASPARTATE; UNCLASSIFIED DRUG;

ADAPTATION; ALCOHOL CONSUMPTION; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRINKING BEHAVIOR; GLUTAMATERGIC TRANSMISSION; IN VIVO STUDY; MALE; MICRODIALYSIS; MOUSE; NEUROTRANSMISSION; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; REGULATORY MECHANISM; RELAPSE;

ALCOHOL DRINKING; ALCOHOLISM; AMINO ACIDS; ANALYSIS OF VARIANCE; ANIMALS; ASPARTIC ACID; BICYCLO COMPOUNDS, HETEROCYCLIC; EXCITATORY AMINO ACID AGENTS; EXTRACELLULAR FLUID; GLUTAMIC ACID; MALE; MICE; MICE, INBRED C57BL; MICRODIALYSIS; MICROINJECTIONS; NUCLEUS ACCUMBENS;

EID: 84892669236     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2013.256     Document Type: Article

References (67)

1. Amara SG, Fontana ACK (2002). Excitatory amino acid transporters: keeping up with glutamate. Neurochem Int 41: 313-318.
2. Bauer J, Pedersen A, Scherbaum N, Bening J, Patschke J, Kugel H et al (2013). Craving in alcohol-dependent patients after detoxification is related to glutamatergic dysfunction in the nucleus accumbens and the anterior cingulate cortex. Neuropsychopharmacology 38: 1401-1408.
3. Becker HC (2008). Alcohol dependence, withdrawal, and relapse. Alcohol Res Health 31: 348-361.
4. Becker HC, Lopez MF (2004). Increased ethanol drinking after repeated chronic ethanol exposure and withdrawal experience in C57BL/6 mice. Alcohol Clin Exp Res 28: 1829-1838.
5. Berger L, Fisher M, Brondino M, Bohn M, Gwyther R, Longo L et al (2013). Efficacy of acamprosate for alcohol dependence in a family medicine setting in the United States: a randomized, double-blind, placebo-controlled study. Alcohol Clin Exp Res 37: 668-674.
6. Besheer J, Grondin JJ, Salling MC, Spanos M, Stevenson RA, Hodge CW (2009). Interoceptive effects of alcohol require mGlu5 receptor activity in the nucleus accumbens. J Neurosci 29: 9582-9591.
7. Britt JP, Benaliouad F, McDevitt RA, Stuber GD, Wise RA, Bonci A (2012). Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens. Neuron 76: 790-803.
8. Cartmell J, Schoepp DD (2000). Regulation of neurotransmitter release by metabotropic glutamate receptors. J Neurochem 75: 889-907.
9. Chefer V, Meis J, Wang G, Kuzmin A, Bakalkin G, Shippenberg T (2011). Repeated exposure to moderate doses of ethanol augments hippocampal glutamate neurotransmission by increasing release. Addict Biol 16: 229-237.
10. Cozzoli DK, Courson J, Caruana AL, Miller BW, Greentree DI, Thompson AB et al (2012). Nucleus accumbens mGluR5-associated signaling regulates binge alcohol drinking under drinking-inthe-dark procedures. Alcohol Clin & Exp Res 36: 1623-1633.
11. Dahchour A, De Witte P (1999). Effect of repeated ethanol withdrawal on glutamate microdialysate in the hippocampus. Alcohol Clin Exp Res 23: 1698-1703.
12. Dahchour A, De Witte P (2003). Excitatory and inhibitory amino acid changes during repeated episodes of ethanol withdrawal: an in vivo microdialysis study. Eur J Pharmacol 459: 171-178.
13. Dahchour A, Hoffman A, Deitrich R, de Witte P (2000). Effects of ethanol on extracellular amino acid levels in high-and lowalcohol sensitive rats: a microdialysis study. Alcohol Alcohol 35: 548-553.
14. Danbolt NC (2001). Glutamate uptake. Prog Neurobiol 65: 1-105.
15. De Sousa A (2010). The pharmacotherapy of alcohol dependence: a state of the art review. Mens Sana Monogr 8: 69-82.
16. Dhaher R, Finn D, Snelling C, Hitzemann R (2008). Lesions of the extended amygdala in C57BL/6J mice do not block the intermittent ethanol vapor-induced increase in ethanol consumption. Alcohol Clin Exp Res 32: 197-208.
17. Ding ZM, Rodd ZA, Engleman EA, Bailey JA, Lahiri DK, McBride WJ (2013). Alcohol drinking and deprivation alter basal extracellular glutamate concentrations and clearance in the mesolimbic system of alcohol-preferring (P) rats. Addict Biol 18: 297-306.
18. Finn DA, Snelling C, Fretwell AM, Tanchuck MA, Underwood L, Cole M et al (2007). Increased drinking during withdrawal from intermittent ethanol exposure is blocked by the CRF receptor antagonist d-Phe-CRF(12-41). Alcohol Clin Exp Res 31: 939-949.
19. Gass JT, Olive MF (2008). Glutamatergic substrates of drug addiction and alcoholism. Biochem Pharmacol 75: 218-265.
20. Gass JT, Olive MF (2009). Role of protein kinase C epsilon (PKCvarepsilon) in the reduction of ethanol reinforcement due to mGluR5 antagonism in the nucleus accumbens shell. Psychopharmacology 204: 587-597.
21. Gehlert DR, Cippitelli A, Thorsell A, Le AD, Hipskind PA, Hamdouchi C et al (2007). 3-(4-Chloro-2-morpholin-4-yl-thiazol-5-yl)-8-(1-ethylpropyl)-2,6- dimethyl-imidazo[1,2-b]pyridazine: a novel brain-penetrant, orally available corticotropin-releasing factor receptor 1 antagonist with efficacy in animal models of alcoholism. J Neurosci 27: 2718-2726.
22. Griffin WC 3rd, Lopez MF, Becker HC (2009a). Intensity and duration of chronic ethanol exposure is critical for subsequent escalation of voluntary ethanol drinking in mice. Alcohol Clin Exp Res 33: 1893-1900.
23. Griffin WC 3rd, Lopez MF, Yanke AB, Middaugh LD, Becker HC (2009b). Repeated cycles of chronic intermittent ethanol exposure in mice increases voluntary ethanol drinking and ethanol concentrations in the nucleus accumbens. Psychopharmacol 201: 569-580.
24. Griffin WC 3rd, Middaugh LD, Becker HC (2007). Voluntary ethanol drinking in mice and ethanol concentrations in the nucleus accumbens. Brain Res 1138: 208-213.
25. Gu M, Zahr NM, Spielman DM, Sullivan EV, Pfefferbaum A, Mayer D (2013). Quantification of glutamate and glutamine using constant-time point-resolved spectroscopy at 3 T. NMR Biomed 26: 164-172.
26. Guglielmo R, Martinotti G, Clerici M, Janiri L (2012). Pregabalin for alcohol dependence: a critical review of the literature. Adv Ther 29: 947-957.
27. Hansson AC, Rimondini R, Neznanova O, Sommer WH, Heilig M (2008). Neuroplasticity in brain reward circuitry following a history of ethanol dependence. Eur J Neurosci 27: 1912-1922.
28. Heilig M, Egli M, Crabbe JC, Becker HC (2010). Acute withdrawal, protracted abstinence and negative affect in alcoholism: are they linked? Addict Biol 15: 169-184.
29. Hermann D, Weber-Fahr W, Sartorius A, Hoerst M, Frischknecht U, Tunc-Skarka N et al (2012). Translational magnetic resonance spectroscopy reveals excessive central glutamate levels during alcohol withdrawal in humans and rats. Biol Psychiatry 71: 1015-1021.
30. Hodge CW, Grant KA, Becker HC, Besheer J, Crissman AM, Platt DM et al (2006). Understanding how the brain perceives alcohol: neurobiological basis of ethanol discrimination. Alcohol Clin Exp Res 30: 203-213.
31. Johnson BA, Ait-Daoud N (2010). Topiramate in the new generation of drugs: efficacy in the treatment of alcoholic patients. Curr Pharm Des 16: 2103-2112.
32. Kalivas PW (2009). The glutamate homeostasis hypothesis of addiction. Nature Rev Neuro 10: 561-572.
33. Kapasova Z, Szumlinski KK (2008). Strain differences in alcoholinduced neurochemical plasticity: a role for accumbens glutamate in alcohol intake. Alcohol Clin Exp Res 32: 617-631.
34. Koob GF, Le Moal M (2008). Addiction and the brain antireward system. Annu Rev Psychol 59: 29-53.
35. Krystal JH, Petrakis IL, Mason G, Trevisan L, D'Souza DC (2003). N-methyl-D-aspartate glutamate receptors and alcoholism: reward, dependence, treatment, and vulnerability. Pharmacol Ther 99: 79-94.
36. Kufahl PR, Martin-Fardon R, Weiss F (2011). Enhanced sensitivity to attenuation of conditioned reinstatement by the mGluR 2/3 agonist LY379268 and increased functional activity of mGluR 2/3 in rats with a history of ethanol dependence. Neuropsychopharmacol 36: 2762-2773.
37. Lominac KD, Kapasova Z, Hannun RA, Patterson C, Middaugh LD, Szumlinski KK (2006). Behavioral and neurochemical interactions between Group 1 mGluR antagonists and ethanol: Potential insight into their anti-addictive properties. Drug Alcohol Depend 85: 142-156.
38. Lopez MF, Becker HC (2005). Effect of pattern and number of chronic ethanol exposures on subsequent voluntary ethanol intake in C57BL/6J mice. Psychopharmacology 181: 688-696.
39. Lovinger DM, McCool BA (1995). Metabotropic glutamate receptor-mediated presynaptic depression at corticostriatal synapses involves mGLuR2 or 3. J Neurophysiol 73: 1076-1083.
40. Mason BJ, Lehert P (2012). Acamprosate for alcohol dependence: a sex-specific meta-analysis based on individual patient data. Alcohol Clin Exp Res 36: 497-508.
41. Mann K, Lemenager T, Hoffmann S, Reinhard I, Hermann D, Batra A et al The PREDICT Study Team (2012). Results of a doubleblind, placebo-controlled pharmacotherapy trial in alcoholism conducted in Germany and comparison with the US COMBINE study. Addict Biol; doi:10.1111/adb.12012 (e-pub ahead of print).
42. Melendez RI, Hicks MP, Cagle SS, Kalivas PW (2005). Ethanol exposure decreases glutamate uptake in the nucleus accumbens. Alcohol Clin Exp Res 29: 326-333.
43. Moghaddam B, Bolinao ML (1994). Biphasic effect of ethanol on extracellular accumulation of glutamate in the hippocampus and the nucleus accumbens. Neurosci Lett 178: 99-102.
44. Ohishi H, Neki A, Mizuno N (1998). Distribution of a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat and mouse: an immunohistochemical study with a monoclonal antibody. Neurosci Res 30: 65-82.
45. Paxinos G, Franklin KBJ (2001). The Mouse Brain in Stereotaxic Coordinates 2ndAcademic Press: San Diego, CA, USA.
46. Piepponen TP, Kiianmaa K, Ahtee L (2002). Effects of ethanol on the accumbal output of dopamine, GABA and glutamate in alcohol-tolerant and alcohol-nontolerant rats. Pharmacol Biochem Behav 74: 21-30.
47. Roberto M, Schweitzer P, Madamba SG, Stouffer DG, Parsons LH, Siggins GR (2004). Acute and chronic ethanol alter glutamatergic transmission in rat central amygdala: an in vitro and in vivo analysis. J Neurosci 24: 1594-1603.
48. Roberts AJ, Cole M, Koob GF (1996). Intra-amygdala muscimol decreases operant ethanol self-administration in dependent rats. Alcohol Clin Exp Res 20: 1289-1298.
49. Roberts AJ, Heyser CJ, Cole M, Griffin P, Koob GF (2000). Excessive ethanol drinking following a history of dependence: animal model of allostasis. Neuropsychopharmacology 22: 581-594.
50. Rossetti ZL, Carboni S (1995). Ethanol withdrawal is associated with increased extracellular glutamate in the rat striatum. Eur J Pharmacol 283: 177-183.
51. Schoepp DD (2001). Unveiling the functions of presynaptic metabotropic glutamate receptors in the central nervous system. J Pharmacol Exp Ther 299: 12-20.
52. Selim M, Bradberry CW (1996). Effect of ethanol on extracellular 5-HT and glutamate in the nucleus accumbens and prefrontal cortex: comparison between the Lewis and Fischer 344 rat strains. Brain Res 716: 157-164.
53. Shimamoto K, Lebrun B, Yasuda-Kamatani Y, Sakaitani M, Shigeri Y, Yumoto N et al (1998). DL-threo-beta-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol Pharmacol 53: 195-201.
54. Shimamoto K, Shigeri Y, Yasuda-Kamatani Y, Lebrun B, Yumoto N, Nakajima T (2000). Syntheses of optically pure beta-hydroxyaspartate derivatives as glutamate transporter blockers. Bioorg Med Chem Lett 10: 2407-2410.
55. Sidhpura N, Weiss F, Martin-Fardon R (2010). Effects of the mGlu2/3 agonist LY379268 and the mGlu5 antagonist MTEP on ethanol seeking and reinforcement are differentially altered in rats with a history of ethanol dependence. Biol Psychiatry 67: 804-811.
56. Smith A, Watson CJ, Frantz KJ, Eppler B, Kennedy RT, Peris J (2004). Differential increase in taurine levels by low-dose ethanol in the dorsal and ventral striatum revealed by microdialysis with on-line capillary electrophoresis. Alcohol Clin & Exp Res 28: 1028-1038.
57. Spanagel R (2009). Alcoholism: a systems approach from molecular physiology to addictive behavior. Physiol Rev 89: 649-705.
58. Sommer WH, Rimondini R, Hansson AC, Hipskind PA, Gehlert DR, Barr CS et al (2008). Upregulation of voluntary alcohol intake, behavioral sensitivity to stress, and amygdala crhr1 expression following a history of dependence. Biol Psychiatry 63: 139-145.
59. Szumlinski KK, Ary AW, Lominac KD, Klugmann M, Kippin TE (2008). Accumbens Homer2 overexpression facilitates alcoholinduced neuroplasticity in C57BL/6J mice. Neuropsychopharmacology 33: 1365-1378.
60. Tamaru Y, Nomura S, Mizuno N, Shigemoto R (2001). Distribution of metabotropic glutamate receptor mGluR3 in the mouse CNS: differential location relative to pre-and postsynaptic sites. Neurosci 106: 481-503.
61. Tzingounis AV, Wadiche JI (2007). Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nature Rev Neurosci 8: 935-947.
62. Umhau JC, Momenan R, Schwandt ML, Singley E, Lifshitz M, Doty L et al (2010). Effect of acamprosate on magnetic resonance spectroscopy measures of central glutamate in detoxified alcohol-dependent individuals: a randomized controlled experimental medicine study. Arch Gen Psychiatry 67: 1069-1077.
63. Vengeliene V, Celerier E, Chaskiel L, Penzo F, Spanagel R (2009). Compulsive alcohol drinking in rodents. Addict Biol 14: 384-396.
64. Vivian JA, Waters CA, Szeliga KT, Jordan K, Grant KA (2002). Characterization of the discriminative stimulus effects of N-methyl-D-aspartate ligands under different ethanol training conditions in the cynomolgus monkey (Macaca fascicularis). Psychopharmacology (Berl) 162: 273-281.
65. Yan QS, Reith ME, Yan SG, Jobe PC (1998). Effect of systemic ethanol on basal and stimulated glutamate releases in the nucleus accumbens of freely moving Sprague-Dawley rats: a microdialysis study. Neurosci Lett 258: 29-32.
66. Yahn SL, Watterson LR, Olive MF (2013). Safety and efficacy of acamprosate for the treatment of alcohol dependence. Subst Abuse 6: 1-12.
67. Zahr NM, Mayer D, Vinco S, Orduna J, Luong R, Sullivan EV et al (2009). In vivo evidence for alcohol-induced neurochemical changes in rat brain without protracted withdrawal, pronounced thiamine deficiency, or severe liver damage. Neuropsychopharmacology 34: 1427-1442.