Nociceptin/orphanin FQ blockade of corticotropin-releasing factor-induced gamma-aminobutyric acid release in central amygdala is enhanced after chronic ethanol exposure

Biological Psychiatry

Volumn 71, Issue 8, 2012, Pages 666-676

  Cruz, Maureen T ^a   Herman, Melissa A ^a   Kallupi, Marsida ^a   Roberto, Marisa ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Central nucleus of the amygdala; CRF; electrophysiology; N OFQ; neuroadaptation; nociceptin

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; ALCOHOL; CORTICOTROPIN RELEASING FACTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; NOCICEPTIN;

4 AMINOBUTYRIC ACID RELEASE; ALCOHOLISM; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GABAERGIC TRANSMISSION; IN VITRO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; LONG TERM EXPOSURE; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SENSITIZATION; SIGNAL TRANSDUCTION;

ALCOHOLISM; AMYGDALA; ANIMALS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CORTICOTROPIN-RELEASING HORMONE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ETHANOL; GABA AGENTS; GAMMA-AMINOBUTYRIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; OPIOID PEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC TRANSMISSION;

EID: 84859103753     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2011.10.032     Document Type: Article

References (62)

1. C.R. Neal Jr, A. Mansour, R. Reinscheid, H.P. Nothacker, O. Civelli, S.J. Watson Jr Localization of orphanin FQ (nociceptin) peptide and messenger RNA in the central nervous system of the rat J Comp Neurol 406 1999 503 547 (Pubitemid 29144937)
2. B.J. Everitt, M.E. Wolf Psychomotor stimulant addiction: A neural systems perspective J Neurosci 22 2002 3312 3320 (Pubitemid 37465734)
3. M.J. Eckardt, S.E. File, G.L. Gessa, K.A. Grant, C. Guerri, P.L. Hoffman Effects of moderate alcohol consumption on the central nervous system Alcohol Clin Exp Res 22 1998 998 1040 (Pubitemid 28408991)
4. R.A. Wise Drug-activation of brain reward pathways Drug Alcohol Depend 51 1998 13 22 (Pubitemid 28353753)
5. R. Martin-Fardon, E.P. Zorrilla, R. Ciccocioppo, F. Weiss Role of innate and drug-induced dysregulation of brain stress and arousal systems in addiction: Focus on corticotropin-releasing factor, nociceptin/orphanin FQ, and orexin/hypocretin Brain Res 1314 2010 145 161
6. R. Ciccocioppo, D. Economidou, A. Fedeli, M. Massi The nociceptin/orphanin FQ/NOP receptor system as a target for treatment of alcohol abuse: A review of recent work in alcohol-preferring rats Physiol Behav 79 2003 121 128 (Pubitemid 36734836)
7. R. Ciccocioppo, S. Angeletti, I. Panocka, M. Massi Nociceptin/orphanin FQ and drugs of abuse Peptides 21 2000 1071 1080
8. R. Martin-Fardon, R. Ciccocioppo, M. Massi, F. Weiss Nociceptin prevents stress-induced ethanol- but not cocaine-seeking behavior in rats Neuroreport 11 2000 1939 1943 (Pubitemid 30429139)
9. R. Ciccocioppo, D. Economidou, A. Fedeli, S. Angeletti, F. Weiss, M. Heilig Attenuation of ethanol self-administration and of conditioned reinstatement of alcohol-seeking behaviour by the antiopioid peptide nociceptin/orphanin FQ in alcohol-preferring rats Psychopharmacology (Berl) 172 2004 170 178 (Pubitemid 38388766)
10. R. Ciccocioppo, I. Panocka, C. Polidori, D. Regoli, M. Massi Effect of nociceptin on alcohol intake in alcohol-preferring rats Psychopharmacology (Berl) 141 1999 220 224 (Pubitemid 29200175)
11. D. Economidou, A.C. Hansson, F. Weiss, A. Terasmaa, W.H. Sommer, A. Cippitelli Dysregulation of nociceptin/orphanin FQ activity in the amygdala is linked to excessive alcohol drinking in the rat Biol Psychiatry 64 2008 211 218
12. D. Economidou, A. Cippitelli, S. Stopponi, S. Braconi, S. Clementi, M. Ubaldi Activation of brain NOP receptors attenuates acute and protracted alcohol withdrawal symptoms in the rat Alcohol Clin Exp Res 35 2011 747 755
13. M. Roberto, G.R. Siggins Nociceptin/orphanin FQ presynaptically decreases GABAergic transmission and blocks the ethanol-induced increase of GABA release in central amygdala Proc Natl Acad Sci U S A 103 2006 9715 9720 (Pubitemid 43955890)
14. S. Lindholm, K. Ploj, J. Franck, I. Nylander Nociceptin/orphanin FQ tissue concentration in the rat brain Effects of repeated ethanol administration at various post-treatment intervals Prog Neuropsychopharmacol Biol Psychiatry 26 2002 303 306 (Pubitemid 34038058)
15. K. Ploj, E. Roman, L. Gustavsson, I. Nylander Basal levels and alcohol-induced changes in nociceptin/orphanin FQ, dynorphin, and enkephalin levels in C57BL/6J mice Brain Res Bull 53 2000 219 226
16. C.J. Heyser, A.J. Roberts, G. Schulteis, G.F. Koob Central administration of an opiate antagonist decreases oral ethanol self-administration in rats Alcohol Clin Exp Res 23 1999 1468 1476 (Pubitemid 29468443)
17. P. Hyytia, G.F. Koob GABAA receptor antagonism in the extended amygdala decreases ethanol self-administration in rats Eur J Pharmacol 283 1995 151 159
18. M. Roberto, S.G. Madamba, S.D. Moore, M.K. Tallent, G.R. Siggins Ethanol increases GABAergic transmission at both pre- and postsynaptic sites in rat central amygdala neurons Proc Natl Acad Sci U S A 100 2003 2053 2058 (Pubitemid 36254572)
19. Z. Nie, P. Schweitzer, A.J. Roberts, S.G. Madamba, S.D. Moore, G.R. Siggins Ethanol augments GABAergic transmission in the central amygdala via CRF1 receptors Science 303 2004 1512 1514 (Pubitemid 38314419)
20. M. Roberto, M.T. Cruz, N.W. Gilpin, V. Sabino, P. Schweitzer, M. Bajo Corticotropin releasing factor-induced amygdala gamma-aminobutyric acid release plays a key role in alcohol dependence Biol Psychiatry 67 2010 831 839
21. M. Roberto, S.G. Madamba, D.G. Stouffer, L.H. Parsons, G.R. Siggins Increased GABA release in the central amygdala of ethanol-dependent rats J Neurosci 24 2004 10159 10166 (Pubitemid 39492041)
22. R. Ciccocioppo, R. Martin-Fardon, F. Weiss, M. Massi Nociceptin/orphanin FQ inhibits stress- and CRF-induced anorexia in rats Neuroreport 12 2001 1145 1149 (Pubitemid 32374733)
23. M.T. Cruz, M. Bajo, E.M. Magnoli, B. Tabakoff, G.R. Siggins, M. Roberto Type 7 adenylyl cyclase is involved in the ethanol and CRF sensitivity of GABAergic synapses in mouse central amygdala Front Neurosci 4 2011 207
24. J.C. Meunier Nociceptin/orphanin FQ and the opioid receptor-like ORL1 receptor Eur J Pharmacol 340 1997 1 15
25. N. Papadopoulou, J. Chen, H.S. Randeva, M.A. Levine, E.W. Hillhouse, D.K. Grammatopoulos Protein kinase A-induced negative regulation of the corticotropin-releasing hormone R1 alpha receptor-extracellularly regulated kinase signal transduction pathway: The critical role of Ser(301) for signaling switch and selectivity Mol Endocrinol 18 2004 624 639 (Pubitemid 38328207)
26. J. Hanoune, N. Defer Regulation and role of adenylyl cyclase isoforms Annu Rev Pharmacol Toxicol 41 2001 145 174 (Pubitemid 32385886)
27. J. Rogers, S.G. Wiener, F.E. Bloom Long-term ethanol administration methods for rats: Advantages of inhalation over intubation or liquid diets Behav Neural Biol 27 1979 466 486 (Pubitemid 10166400)
28. R.S. Zucker Short-term synaptic plasticity Annu Rev Neurosci 12 1989 13 31 (Pubitemid 19085445)
29. A. Bonci, J.T. Williams Increased probability of GABA release during withdrawal from morphine J Neurosci 17 1997 796 803 (Pubitemid 27024591)
30. R. Ciccocioppo, M. Biondini, L. Antonelli, J. Wichmann, F. Jenck, M. Massi Reversal of stress- and CRF-induced anorexia in rats by the synthetic nociceptin/orphanin FQ receptor agonist, Ro 64-6198 Psychopharmacology (Berl) 161 2002 113 119 (Pubitemid 34492655)
31. Y. De Koninck, I. Mody Noise analysis of miniature IPSCs in adult rat brain slices: properties and modulation of synaptic GABAA receptor channels J Neurophysiol 71 1994 1318 1335 (Pubitemid 24121832)
32. T.S. Otis, Y. De Koninck, I. Mody Lasting potentiation of inhibition is associated with an increased number of gamma-aminobutyric acid type A receptors activated during miniature inhibitory postsynaptic currents Proc Natl Acad Sci U S A 91 1994 7698 7702 (Pubitemid 24238252)
33. G. Calo, R. Guerrini, R. Bigoni, A. Rizzi, G. Marzola, H. Okawa Characterization of [Nphe(1)]nociceptin(1-13)NH(2), a new selective nociceptin receptor antagonist Br J Pharmacol 129 2000 1183 1193 (Pubitemid 30153975)
34. S. Florin, I. Leroux-Nicollet, J.C. Meunier, J. Costentin Autoradiographic localization of [3H]nociceptin binding sites from telencephalic to mesencephalic regions of the mouse brain Neurosci Lett 230 1997 33 36 (Pubitemid 27308836)
35. A. Lochner, J.A. Moolman The many faces of H89: A review Cardiovasc Drug Rev 24 2006 261 274 (Pubitemid 46435008)
36. M.G. Chheda, U. Ashery, P. Thakur, J. Rettig, Z.H. Sheng Phosphorylation of Snapin by PKA modulates its interaction with the SNARE complex Nat Cell Biol 3 2001 331 338 (Pubitemid 32288439)
37. S. Seino, T. Shibasaki PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis Physiol Rev 85 2005 1303 1342 (Pubitemid 41362272)
38. L.E. Trudeau, D.G. Emery, P.G. Haydon Direct modulation of the secretory machinery underlies PKA-dependent synaptic facilitation in hippocampal neurons Neuron 17 1996 789 797 (Pubitemid 26365357)
39. M.K. Kelm, H.E. Criswell, G.R. Breese The role of protein kinase A in the ethanol-induced increase in spontaneous GABA release onto cerebellar Purkinje neurons J Neurophysiol 100 2008 3417 3428
40. P. Veinante, M.E. Stoeckel, M.J. Freund-Mercier GABA- and peptide-immunoreactivities co-localize in the rat central extended amygdala Neuroreport 8 1997 2985 2989 (Pubitemid 27394831)
41. H.E. Day, E.J. Curran, S.J. Watson Jr, H. Akil Distinct neurochemical populations in the rat central nucleus of the amygdala and bed nucleus of the stria terminalis: Evidence for their selective activation by interleukin-1beta J Comp Neurol 413 1999 113 128 (Pubitemid 29409755)
42. C. Gianoulakis Endogenous opioids and addiction to alcohol and other drugs of abuse Curr Top Med Chem 4 2004 39 50 (Pubitemid 38849357)
43. D. Rodi, C. Polidori, G. Bregola, S. Zucchini, M. Simonato, M. Massi Pro-nociceptin/orphanin FQ and NOP receptor mRNA levels in the forebrain of food deprived rats Brain Res 957 2002 354 361 (Pubitemid 35356531)
44. B.E. Hawes, M.P. Graziano, D.G. Lambert Cellular actions of nociceptin: Transduction mechanisms Peptides 21 2000 961 967
45. B. Buzas, J. Rosenberger, B.M. Cox Activity and cyclic AMP-dependent regulation of nociceptin/orphanin FQ gene expression in primary neuronal and astrocyte cultures J Neurochem 71 1998 556 563 (Pubitemid 28480402)
46. J.C. Meunier, C. Mollereau, L. Toll, C. Suaudeau, C. Moisand, P. Alvinerie Isolation and structure of the endogenous agonist of opioid receptor- like ORL1 receptor Nature 377 1995 532 535
47. E. Merlo Pich, M. Lorang, M. Yeganeh, F. Rodriguez de Fonseca, J. Raber, G.F. Koob 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 1995 5439 5447
48. M.F. Olive, H.N. Koenig, M.A. Nannini, C.W. Hodge Elevated extracellular CRF levels in the bed nucleus of the stria terminalis during ethanol withdrawal and reduction by subsequent ethanol intake Pharmacol Biochem Behav 72 2002 213 220 (Pubitemid 34251330)
49. M. Roberto, M. Bajo, E. Crawford, S.G. Madamba, G.R. Siggins Chronic ethanol exposure and protracted abstinence alter NMDA receptors in central amygdala Neuropsychopharmacology 31 2006 988 996
50. M. Roberto, P. Schweitzer, S.G. Madamba, D.G. Stouffer, L.H. Parsons, G.R. Siggins Acute and chronic ethanol alter glutamatergic transmission in rat central amygdala: An in vitro and in vivo analysis J Neurosci 24 2004 1594 1603 (Pubitemid 38240954)
51. W. Haubensak, P.S. Kunwar, H. Cai, S. Ciocchi, N.R. Wall, R. Ponnusamy Genetic dissection of an amygdala microcircuit that gates conditioned fear Nature 468 2010 270 276
52. M. Lopez de Armentia, P. Sah Firing properties and connectivity of neurons in the rat lateral central nucleus of the amygdala J Neurophysiol 92 2004 1285 1294 (Pubitemid 39100631)
53. E.J. Lang, D. Pare Synaptic responsiveness of interneurons of the cat lateral amygdaloid nucleus Neuroscience 83 1998 877 889 (Pubitemid 28068908)
54. M.D. Cassell, L.J. Freedman, C. Shi The intrinsic organization of the central extended amygdala Ann N Y Acad Sci 877 1999 217 241 (Pubitemid 29351860)
55. M. Roberto, N.W. Gilpin, L.E. O'Dell, M.T. Cruz, A.C. Morse, G.R. Siggins Cellular and behavioral interactions of gabapentin with alcohol dependence J Neurosci 28 2008 5762 5771
56. M. Roberto, M. Cruz, M. Bajo, G.R. Siggins, L.H. Parsons, P. Schweitzer The endocannabinoid system tonically regulates inhibitory transmission and depresses the effect of ethanol in central amygdala Neuropsychopharmacology 35 2010 1962 1972
57. N.W. Gilpin, K. Misra, M.A. Herman, M.T. Cruz, G.F. Koob, M. Roberto Neuropeptide Y opposes alcohol effects on gamma-aminobutyric acid release in amygdala and blocks the transition to alcohol dependence Biol Psychiatry 69 2011 1091 1099
58. J.H. Krystal, J.A. Cramer, W.F. Krol, G.F. Kirk, R.A. Rosenheck Naltrexone in the treatment of alcohol dependence N Engl J Med 345 2001 1734 1739
59. S.S. O'Malley, S. Krishnan-Sarin, C. Farren, R. Sinha, M.J. Kreek Naltrexone decreases craving and alcohol self-administration in alcohol-dependent subjects and activates the hypothalamo-pituitary- adrenocortical axis Psychopharmacology (Berl) 160 2002 19 29 (Pubitemid 34169822)
60. C.P. O'Brien The mosaic of addiction Am J Psychiatry 161 2004 1741 1742 (Pubitemid 39314661)
61. J.R. Volpicelli, A.I. Alterman, M. Hayashida, C.P. O'Brien Naltrexone in the treatment of alcohol dependence Arch Gen Psychiatry 49 1992 876 880
62. D.P. Devine, S.J. Watson, H. Akil Nociceptin/orphanin FQ regulates neuroendocrine function of the limbic-hypothalamic-pituitary-adrenal axis Neuroscience 102 2001 541 553 (Pubitemid 32171875)