Drug-induced GABA transporter currents enhance GABA release to induce opioid withdrawal behaviors

Nature Neuroscience

Volumn 14, Issue 12, 2011, Pages 1548-1554

  Bagley, Elena E ^a   Hacker, Jennifer ^a   Chefer, Vladimir I ^b   Mallet, Christophe ^a   McNally, Gavan P ^c   Chieng, Billy C H ^a   Perroud, Julie ^a   Shippenberg, Toni S ^b   Christie, MacDonald J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

1 [2 (BENZHYDRYLIDENEAMINOOXY)ETHYL] 1,2,5,6 TETRAHYDRO 3 PYRIDINECARBOXYLIC ACID; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID CARRIER; 4 AMINOBUTYRIC ACID CARRIER 1; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; GLUTAMATE RECEPTOR ANTAGONIST; METENKEPHALIN; MORPHINE; NALOXONE; OPIATE; OPIATE AGONIST; TETRODOTOXIN; TIAGABINE; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DIARRHEA; GENE EXPRESSION; JUMPING; MICROINJECTION; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; ONCOGENE C FOS; OPIATE ADDICTION; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAT; TREMOR; WEIGHT REDUCTION; WITHDRAWAL SYNDROME;

ANALYSIS OF VARIANCE; ANIMALS; DISEASE MODELS, ANIMAL; GABA ANTAGONISTS; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION; GLUTAMATE DECARBOXYLASE; GREEN FLUORESCENT PROTEINS; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRODIALYSIS; MORPHINE; NALOXONE; NARCOTIC ANTAGONISTS; NIPECOTIC ACIDS; OXIMES; PERIAQUEDUCTAL GRAY; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANCE WITHDRAWAL SYNDROME; TIME FACTORS;

EID: 82255183147     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.2940     Document Type: Article

References (40)

1. Veruki, M.L., Morkve, S.H. & Hartveit, E. Activation of a presynaptic glutamate transporter regulates synaptic transmission through electrical signaling. Nat. Neurosci. 9, 1388-1396 (2006). (Pubitemid 44646211)
2. Bagley, E.E., Gerke, M.B., Vaughan, C.W., Hack, S.P. & Christie, M.J. GABA transporter currents activated by protein kinase A excite midbrain neurons during opioid withdrawal. Neuron 45, 433-445 (2005). (Pubitemid 40188210)
3. Ingram, S.L., Prasad, B.M. & Amara, S.G. Dopamine transporter-mediated conductances increase excitability of midbrain dopamine neurons. Nat. Neurosci. 5, 971-978 (2002).
4. Mann, J.J. The medical management of depression. N. Engl. J. Med. 353, 1819-1834 (2005).
5. Cushman, P. & Dole, V.P. Detoxification of rehabilitated methadone-maintained patients. J. Am. Med. Assoc. 226, 747-752 (1973).
6. Bozarth, M.A. & Wise, R.A. Anatomically distinct opiate receptor fields mediate reward and physical dependence. Science 224, 516-517 (1984). (Pubitemid 14134746)
7. Laschka, E., Teschemacher, H., Mehraein, P. & Herz, A. Sites of action of morphine involved in the development of physical dependence in rats. II. Morphine withdrawal precipitated by application of morphine antagonists into restricted parts of the ventricular system and by microinjection into various brain areas. Psychopharmacologia 46, 141-147 (1976).
8. Williams, J.T., Christie, M.J. & Manzoni, O. Cellular and synaptic adaptations mediating opioid dependence. Physiol. Rev. 81, 299-343 (2001). (Pubitemid 32096178)
9. Chieng, B. & Christie, M.J. Local opioid withdrawal in rat single periaqueductal gray neurons in vitro. J. Neurosci. 16, 7128-7136 (1996). (Pubitemid 26382890)
10. Ingram, S.L., Vaughan, C.W., Bagley, E.E., Connor, M. & Christie, M.J. Enhanced opioid efficacy in opioid dependence is caused by an altered signal transduction pathway. J. Neurosci. 18, 10269-10276 (1998). (Pubitemid 29016546)
11. Chieng, B.C., Hallberg, C., Nyberg, F.J. & Christie, M.J. Enhanced c-Fos in periaqueductal grey GABAergic neurons during opioid withdrawal. Neuroreport 16, 1279-1283 (2005). (Pubitemid 41225196)
12. Hacker, J., Pedersen, N.P., Chieng, B.C., Keay, K.A. & Christie, M.J. Enhanced Fos expression in glutamic acid decarboxylase immunoreactive neurons of the mouse periaqueductal grey during opioid withdrawal. Neuroscience 137, 1389-1396 (2006). (Pubitemid 43133162)
13. Tamamaki, N. et al. Green fluorescent protein expression and colocalization with calretinin, parvalbumin and somatostatin in the GAD67-GFP knock-in mouse. J. Comp. Neurol. 467, 60-79 (2003). (Pubitemid 37339758)
14. Cherubini, E. & Conti, F. Generating diversity at GABAergic synapses. Trends Neurosci. 24, 155-162 (2001). (Pubitemid 32166820)
15. Barbaresi, P., Gazzanelli, G. & Malatesta, M. γ-Aminobutyric acid transporters in the cat periaqueductal gray: a light and electron microscopic immunocytochemical study. J. Comp. Neurol. 429, 337-354 (2001).
16. Hack, S.P., Vaughan, C.W. & Christie, M.J. Modulation of GABA release during morphine withdrawal in midbrain neurons in vitro. Neuropharmacology 45, 575-584 (2003). (Pubitemid 36980814)
17. Jensen, K., Chiu, C.S., Sokolova, I., Lester, H.A. & Mody, I. GABA transporter-1 (GAT1)-deficient mice: differential tonic activation of GABAA versus GABAB receptors in the hippocampus. J. Neurophysiol. 90, 2690-2701 (2003). (Pubitemid 37266533)
18. Vaughan, C.W., Ingram, S.L., Connor, M.A. & Christie, M.J. How opioids inhibit GABA-mediated neurotransmission. Nature 390, 611-614 (1997). (Pubitemid 28016195)
19. Kullmann, D.M. et al. Presynaptic, extrasynaptic and axonal GABAA receptors in the CNS: where and why? Prog. Biophys. Mol. Biol. 87, 33-46 (2005). (Pubitemid 39308540)
20. Chiu, C.S. et al. GABA transporter deficiency causes tremor, ataxia, nervousness and increased GABA-induced tonic conductance in cerebellum. J. Neurosci. 25, 3234-3245 (2005).
21. Koob, G.F., Maldonado, R. & Stinus, L. Neural substrates of opiate withdrawal. Trends Neurosci. 15, 186-191 (1992).
22. DiStefano, P.S. & Brown, O.M. Biochemical correlates of morphine withdrawal. 2. Effects of clonidine. J. Pharmacol. Exp. Ther. 233, 339-344 (1985). (Pubitemid 15122030)
23. Itouji, A., Sakai, N., Tanaka, C. & Saito, N. Neuronal and glial localization of two GABA transporters (GAT1 and GAT3) in the rat cerebellum. Brain Res. Mol. Brain Res. 37, 309-316 (1996). (Pubitemid 26148005)
24. Overstreet, L.S. & Westbrook, G. Synapse density regulates independence at unitary inhibitory synapses. J. Neurosci. 23, 2618-2626 (2003). (Pubitemid 36418596)
25. Belelli, D. et al. Extrasynaptic GABAA receptors: form, pharmacology and function. J. Neurosci. 29, 12757-12763 (2009).
26. Yang, K., Furue, H., Kumamoto, E., Dong, Y.X. & Yoshimura, M. Pre-and postsynaptic inhibition mediated by GABAB receptors in rat ventrolateral periaqueductal gray neurons. Biochem. Biophys. Res. Commun. 302, 233-237 (2003). (Pubitemid 36397911)
27. Luer, M.S. & Rhoney, D.H. Tiagabine: a novel antiepileptic drug. Ann. Pharmacother. 32, 1173-1180 (1998). (Pubitemid 28543464)
28. González, G. et al. Clinical efficacy of gabapentin versus tiagabine for reducing cocaine use among cocaine-dependent methadone-treated patients. Drug Alcohol Depend. 87, 1-9 (2007). (Pubitemid 46074378)
29. Minozzi, S. et al. Anticonvulsants for cocaine dependence. Cochrane Database Syst. Rev. 16, CD006754 (2008).
30. Sofuoglu, M., Mouratidis, M., Yoo, S., Culligan, K. & Kosten, T. Effects of tiagabine in combination with intravenous nicotine in overnight abstinent smokers. Psychopharmacology (Berl.) 181, 504-510 (2005). (Pubitemid 41480899)
31. Myrick, H. et al. A retrospective chart review comparing tiagabine and benzodiazepines for the treatment of alcohol withdrawal. J. Psychoactive Drugs 37, 409-414 (2005). (Pubitemid 43152745)
32. Nestler, E.J. Historical review: molecular and cellular mechanisms of opiate and cocaine addiction. Trends Pharmacol. Sci. 25, 210-218 (2004). (Pubitemid 38519912)
33. Hanoune, J. & Defer, N. Regulation and role of adenylyl cyclase isoforms. Annu. Rev. Pharmacol. Toxicol. 41, 145-174 (2001). (Pubitemid 32385886)
34. Tzavara, E.T., Monory, K., Hanoune, J. & Nomikos, G.G. Nicotine withdrawal syndrome: behavioral distress and selective up-regulation of the cyclic AMP pathway in the amygdala. Eur. J. Neurosci. 16, 149-153 (2002). (Pubitemid 35463606)
35. Chieng, B. & Williams, J.T. Increased opioid inhibition of GABA release in nucleus accumbens during morphine withdrawal. J. Neurosci. 18, 7033-7039 (1998). (Pubitemid 28388032)
36. Bonci, A. & Williams, J.T. Increased probability of GABA release during withdrawal from morphine. J. Neurosci. 17, 796-803 (1997). (Pubitemid 27024591)
37. Paxinos, G. & Franklin, K.B.J. The Mouse Brain in Stereotaxic Co-ordinates, 2nd edn. (Academic Press, Sydney, 2001).
38. Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Co-ordinates, 4th edn. (Academic Press, Sydney, 1998).
39. Chefer, V.I., Denoroy, L., Zapata, A. & Shippenberg, T.S. Mu opioid receptor modulation of somatodendritic dopamine overflow: GABAergic and glutamatergic mechanisms. Eur. J. Neurosci. 30, 272-278 (2009).
40. McNally, G.P., Pigg, M. & Weidemann, G. Opioid receptors in the midbrain periaqueductal gray regulate extinction of pavlovian fear conditioning. J. Neurosci. 24, 6912-6919 (2004). (Pubitemid 39045448)