Nociceptin/orphanin FQ decreases glutamate transmission and blocks ethanol-induced effects in the central amygdala of naive and ethanol-dependent rats

Neuropsychopharmacology

Volumn 39, Issue 5, 2014, Pages 1081-1092

  Kallupi, Marsida ^a,b   Varodayan, Florence P ^a   Oleata, Christopher S ^a   Correia, Diego ^a,c   Luu, George ^a   Roberto, Marisa ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CAMERINO   (Italy)

^c FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

Author keywords

alcohol; amygdala; electrophysiology; glutamate; nociceptin; NOP receptor

Indexed keywords

6,7 DINITRO 2,3 QUINOXALINEDIONE; ALCOHOL; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; BICUCULLINE; DL AP 5; GLUTAMIC ACID; NOCICEPTIN; NOCICEPTIN RECEPTOR ANTAGONIST; PICROTOXIN; UNCLASSIFIED DRUG; CENTRAL DEPRESSANT AGENT; NOCICEPTIN RECEPTOR; OPIATE PEPTIDE; OPIATE RECEPTOR;

4 AMINOBUTYRIC ACID RELEASE; ADULT; ALCOHOL BLOOD LEVEL; ALCOHOL CONSUMPTION; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; CURRENT CLAMP TECHNIQUE; DOSE RESPONSE; DRUG EFFECT; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; IN VITRO STUDY; INTRACELLULAR RECORDING; MALE; MEMBRANE STEADY POTENTIAL; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; VOLTAGE CLAMP TECHNIQUE; WHOLE CELL PATCH CLAMP; ALCOHOL-RELATED DISORDERS; AMYGDALOID NUCLEUS; ANIMAL; DRUG EFFECTS; ELECTROSTIMULATION; METABOLISM; MICROELECTRODE; NERVE CELL; PATCH CLAMP TECHNIQUE; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNAPSE; SYNAPTIC TRANSMISSION; WISTAR RAT;

ALCOHOL-RELATED DISORDERS; AMYGDALA; ANIMALS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ELECTRIC STIMULATION; ETHANOL; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; IN VITRO TECHNIQUES; MICROELECTRODES; NEURONS; OPIOID PEPTIDES; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, OPIOID; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84896394126     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2013.308     Document Type: Article

References (66)

1. Andero R, Brothers SP, Jovanovic T, Chen YT, Salah-Uddin H, Cameron M et al (2013). Amygdala-dependent fear is regulated by Oprl1 in mice and humans with PTSD. Sci Transl Med 5: 173-188.
2. Andreasen M, Hablitz JJ (1994). Paired-pulse facilitation in the dentate gyrus: a patch-clamp study in rat hippocampus in vitro. J Neurophysiol 72: 326-336. (Pubitemid 24233654)
3. Calo G, Guerrini R, Rizzi A, Salvadori S, Regoli D (2000). Pharmacology of nociceptin and its receptor: a novel therapeutic target. Br J Pharmacol 129: 1261-1283. (Pubitemid 30175697)
4. Ciccocioppo R, Angeletti S, Panocka I, Massi M (2000). Nociceptin/orphanin FQ and drugs of abuse. Peptides 21: 1071-1080.
5. Ciccocioppo R, Economidou D, Fedeli A, Angeletti S, Weiss F, Heilig M et al (2004). Attenuation of ethanol self-administration and of conditioned reinstatement of alcohol-seeking behaviour by the antiopioid peptide nociceptin/orphanin FQ in alcoholpreferring rats. Psychopharmacology (Berl) 172: 170-178. (Pubitemid 38388766)
6. Ciccocioppo R, Economidou D, Fedeli A, Massi M (2003). The nociceptin/orphanin FQ/NOP receptor system as a target for treatment of alcohol abuse: a review of recent work in alcoholpreferring rats. Physiol Behav 79: 121-128. (Pubitemid 36734836)
7. Cruz MT, Herman MA, Kallupi M, Roberto M (2012). Nociceptin/orphanin FQ blockade of corticotropin-releasing factor-induced gamma-aminobutyric acid release in central amygdala is enhanced after chronic ethanol exposure. Biol Psychiatry 71: 666-676.
8. Darland T, Heinricher MM, Grandy DK (1998). Orphanin FQ/nociceptin: a role in pain and analgesia, but so much more. Trends Neurosci 21: 215-221. (Pubitemid 28191816)
9. De Koninck Y, Mody I (1994). Noise analysis of miniature IPSCs in adult rat brain slices: properties and modulation of synaptic GABAA receptor channels. J Neurophysiol 71: 1318-1335. (Pubitemid 24121832)
10. De Witte P, Littleton J, Parot P, Koob G (2005). Neuroprotective and abstinence-promoting effects of acamprosate: elucidating the mechanism of action. CNS Drugs 19: 517-537. (Pubitemid 41058377)
11. Eckardt MJ, File SE, Gessa GL, Grant KA, Guerri C, Hoffman PL et al (1998). Effects of moderate alcohol consumption on the central nervous system. Alcohol Clin Exp Res 22: 998-1040. (Pubitemid 28408991)
12. Emmerson PJ, Miller RJ (1999). Pre-and postsynaptic actions of opioid and orphan opioid agonists in the rat arcuate nucleus and ventromedial hypothalamus in vitro. J Physiol (Lond) 517(Part 2): 431-445. (Pubitemid 29294888)
13. Gompf HS, Moldavan MG, Irwin RP, Allen CN (2005). Nociceptin/orphanin FQ (N/OFQ) inhibits excitatory and inhibitory synaptic signaling in the suprachiasmatic nucleus (SCN). Neuroscience 132: 955-965. (Pubitemid 40602531)
14. Henderson G, McKnight AT (1997). The orphan opioid receptor and its endogenous ligand-nociceptin/orphanin FQ. Trends Pharmacol Sci 18: 293-300. (Pubitemid 27353247)
15. Herman MA, Contet C, Justice NJ, Vale W, Roberto M (2013). Novel subunit-specific tonic GABA currents and differential effects of ethanol in the central amygdala of CRF receptor-1 reporter mice. J Neurosci 33: 3284-3298.
16. Jenck F, Moreau JL, Martin JR, Kilpatrick GJ, Reinscheid RK, Monsma FJ Jr. et al (1997). Orphanin FQ acts as an anxiolytic to attenuate behavioral responses to stress. Proc Natl Acad Sci USA 94: 14854-14858. (Pubitemid 28041464)
17. Koob GF (2008). A role for brain stress systems in addiction. Neuron 59: 11-34. (Pubitemid 351905857)
18. Koob GF, Le Moal M (2001). Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24: 97-129.
19. Koob GF, Le Moal M (2008). Addiction and the brain antireward system. Annu Rev Psychol 59: 29-53.
20. Koob GF, Mason BJ, De Witte P, Littleton J, Siggins GR (2002). Potential neuroprotective effects of acamprosate. Alcohol Clin Exp Res 26: 586-592. (Pubitemid 34408726)
21. Koob GF, Roberts AJ, Schulteis G, Parsons LH, Heyser CJ, Hyytia P et al (1998). Neurocircuitry targets in ethanol reward and dependence. Alcohol Clin Exp Res 22: 3-9. (Pubitemid 28139190)
22. Krettek JE, Price JL (1978). A description of the amygdaloid complex in the rat and cat with observations on intra-amygdaloid axonal connections. J Comp Neurol 178: 255-280.
23. Kuzmin A, Kreek MJ, Bakalkin G, Liljequist S (2007). The nociceptin/orphanin FQ receptor agonist Ro 64-6198 reduces alcohol self-administration and prevents relapse-like alcohol drinking. Neuropsychopharmacology 32: 902-910. (Pubitemid 46426176)
24. Kuzmin A, Sandin J, Terenius L, Ogren SO (2003). Acquisition, expression, and reinstatement of ethanol-induced conditioned place preference in mice: effects of opioid receptor-like 1 receptor agonists and naloxone. J Pharmacol Exp Ther 304: 310-318. (Pubitemid 36008943)
25. Lambert DG (2008). The nociceptin/orphanin FQ receptor: a target with broad therapeutic potential. Nat Rev Drug Discov 7: 694-710.
26. Liebel JT, Swandulla D, Zeilhofer HU (1997). Modulation of excitatory synaptic transmission by nociceptin in superficial dorsal horn neurones of the neonatal rat spinal cord. Br J Pharmacol 121: 425-432. (Pubitemid 27226294)
27. Lovinger DM, Roberto M (2013). Synaptic effects induced by alcohol. In: Sommer WHSpanagel R (eds) Current Topics in Behavioral Neurosciences Vol. 13 (Springer: Berlin-Heidelberg), pp 31-86.
28. Manabe T, Wyllie D, Perkel DJ, Nicoll RA (1993). Modulation of synaptic transmission and long-term potentiation in the CA1 region of the hippocampus. J Neurophysiol 70: 1451-1459.
29. Mann K, Kiefer F, Spanagel R, Littleton J (2008). Acamprosate: recent findings and future research directions. Alcohol Clin Exp Res 32: 1105-1110.
30. Martin-Fardon R, Ciccocioppo R, Massi M, Weiss F (2000). Nociceptin prevents stress-induced ethanol-but not cocaineseeking behavior in rats. NeuroReport 11: 1939-1943. (Pubitemid 30429139)
31. Martin-Fardon R, Zorrilla EP, Ciccocioppo R, Weiss F (2010). 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: 145-161.
32. Meis S, Munsch T, Pape HC (2002). Antioscillatory effects of nociceptin/orphanin FQ in synaptic networks of the rat thalamus. J Neurosci 22: 718-727. (Pubitemid 34141752)
33. Meis S, Pape HC (2001). Control of glutamate and GABA release by nociceptin/orphanin FQ in the rat lateral amygdala. J Physiol 532(Part 3): 701-712. (Pubitemid 32427885)
34. Mennerick S, Zorumski CF (1995). Paired-pulse modulation of fast excitatory synaptic currents in microcultures of rat hippocampal neurons. J Physiol 488(Part 1): 85-101.
35. Meunier JC (1997). Nociceptin/orphanin FQ and the opioid receptor-like ORL1 receptor. Eur J Pharmacol 340: 1-15.
36. Miller RJ (1998). Presynaptic receptors. Annu Rev Pharmacol Toxicol 38: 201-227. (Pubitemid 28231494)
37. Mogil JS, Pasternak GW (2001). The molecular and behavioral pharmacology of the orphanin FQ/nociceptin peptide and receptor family. Pharmacol Rev 53: 381-415. (Pubitemid 32852018)
38. Neal CR Jr., Mansour A, Reinscheid R, Nothacker HP, Civelli O, Akil H et al (1999). Opioid receptor-like (ORL1) receptor distribution in the rat central nervous system: comparison of ORL1 receptor mRNA expression with (125)I-[(14)Tyr]-orphanin FQ binding. J Comp Neurol 412: 563-605. (Pubitemid 29409672)
39. Otis TS, De Koninck Y, Mody I (1994). Lasting potentiation of inhibition is associated with an increased number of gammaaminobutyric acid type A receptors activated during miniature inhibitory postsynaptic currents. Proc Natl Acad Sci USA 91: 7698-7702. (Pubitemid 24238252)
40. Pich EM, Lorang M, Yeganeh M, Rodriguez de Fonseca F, Raber J, Koob GF et al (1995). Increase of extracellular corticotropinreleasing 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.
41. Pitkanen A, Stefanacci L, Farb CR, Go GG, LeDoux JE, Amaral DG (1995). Intrinsic connections of the rat amygdaloid complex: projections originating in the lateral nucleus. J Comp Neurol 356: 288-310.
42. Rassnick S, Heinrichs SC, Britton KT, Koob GF (1993). Microinjection of a corticotropin-releasing factor antagonist into the central nucleus of the amygdala reverses anxiogenic-like effects of ethanol withdrawal. Brain Res 605: 25-32. (Pubitemid 23083057)
43. Reinscheid RK, Nothacker HP, Bourson A, Ardati A, Henningsen RA, Bunzow JR et al (1995). Orphanin FQ: a neuropeptide that activates an opioidlike G protein-coupled receptor. Science 270: 792-794.
44. Roberto M, Bajo M, Crawford E, Madamba SG, Siggins GR (2006a). Chronic ethanol exposure and protracted abstinence alter NMDA receptors in central amygdala. Neuropsychopharmacology 31: 988-996.
45. Roberto M, Cruz MT, Gilpin NW, Sabino V, Schweitzer P, Bajo M et al (2010). Corticotropin releasing factor-induced amygdala gamma-aminobutyric acid release plays a key role in alcohol dependence. Biol Psychiatry 67: 831-839.
46. Roberto M, Gilpin NW, Siggins GR (2012). The central amygdala and alcohol: role of gamma-aminobutyric acid, glutamate, and neuropeptides. Cold Spring Harb Perspect Med 2: a012195.
47. Roberto M, Madamba SG, Moore SD, Tallent MK, Siggins GR (2003). Ethanol increases GABAergic transmission at both pre-and postsynaptic sites in rat central amygdala neurons. Proc Natl Acad Sci USA 100: 2053-2058. (Pubitemid 36254572)
48. Roberto M, Madamba SG, Stouffer DG, Parsons LH, Siggins GR (2004a). Increased GABA release in the central amygdala of ethanol-dependent rats. J Neurosci 24: 10159-10166. (Pubitemid 39492041)
49. Roberto M, Schweitzer P, Madamba SG, Stouffer DG, Parsons LH, Siggins GR (2004b). Acute and chronic ethanol alter glutamatergic transmission in rat central amygdala: an in vitro and in vivo analysis. J Neurosci 24: 1594-1603. (Pubitemid 38240954)
50. Roberto M, Siggins GR (2006b). Nociceptin/orphanin FQ presynaptically decreases GABAergic transmission and blocks the ethanol-induced increase of GABA release in central amygdala. Proc Natl Acad Sci USA 103: 9715-9720. (Pubitemid 43955890)
51. 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. (Pubitemid 26357034)
52. Rogers J, Wiener SG, Bloom FE (1979). Long-term ethanol administration methods for rats: advantages of inhalation over intubation or liquid diets. Behav Neural Biol 27: 466-486. (Pubitemid 10166400)
53. Salin PA, Scanziani M, Malenka RC, Nicoll RA (1996). Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc Natl Acad Sci USA 93: 13304-13309. (Pubitemid 26382811)
54. Savander V, Go CG, LeDoux JE, Pitkanen A (1995). Intrinsic connections of the rat amygdaloid complex: projections originating in the basal nucleus. J Comp Neurol 361: 345-368.
55. Schank JR, Ryabinin AE, Giardino WJ, Ciccocioppo R, Heilig M (2012). Stress-related neuropeptides and addictive behaviors: beyond the usual suspects. Neuron 76: 192-208.
56. Tallent MK (2008). Presynaptic inhibition of glutamate release by neuropeptides: use-dependent synaptic modification. Inhibit Regul Excit Neurotransm 44: 177-200.
57. Tallent MK, Madamba SG, Siggins GR (2001). Nociceptin reduces epileptiform events in CA3 hippocampus via presynaptic and postsynaptic mechanisms. J Neurosci 21: 6940-6948. (Pubitemid 32781136)
58. Ubaldi M, Bifone A, Ciccocioppo R (2013). Translational approach to develop novel medications on alcohol addiction: focus on neuropeptides. Curr Opin Neurobiol 23: 684-691.
59. Van der Kloot W (1991). The regulation of quantal size. Prog Neurobiol 36: 93-130.
60. Vaughan CW, Ingram SL, Connor MA, Christie MJ (1997). How opioids inhibit GABA-mediated neurotransmission (see comments). Nature 390: 611-614. (Pubitemid 28016195)
61. Wang JH, Kelly PT (1997). Attenuation of paired-pulse facilitation associated with synaptic potentiation mediated by postsynaptic mechanisms. J Neurophysiol 78: 2707-2716. (Pubitemid 27495496)
62. Wu LG, Saggau P (1994). Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus. J Neurosci 14: 645-654. (Pubitemid 24043921)
63. Wu LG, Saggau P (1997). Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci 20: 204-212. (Pubitemid 27158049)
64. Yu B, Shinnick-Gallagher P (1998). Corticotropin-releasing factor increases dihydropyridine-and neurotoxin-resistant calcium currents in neurons of the central amygdala. J Pharmacol Exp Ther 284: 170-179. (Pubitemid 28109543)
65. Yu TP, Fein J, Phan T, Evans CJ, Xie CW (1997). Orphanin FQ inhibits synaptic transmission and long-term potentiation in rat hippocampus. Hippocampus 7: 88-94. (Pubitemid 27107633)
66. Zeilhofer HU, Selbach UM, Guhring H, Erb K, Ahmadi S (2000). Selective suppression of inhibitory synaptic transmission by nocistatin in the rat spinal cord dorsal horn. J Neurosci 20: 4922-4929. (Pubitemid 30421696)