Modification of anxiety-like behaviors by nociceptin/orphanin FQ (N/OFQ) and time-dependent changes in N/OFQ-NOP gene expression following ethanol withdrawal

Addiction Biology

Volumn 18, Issue 3, 2013, Pages 467-479

  Aujla, Harinder ^a   Cannarsa, Rosalia ^b   Romualdi, Patrizia ^b   Ciccocioppo, Roberto ^a,c   Martin Fardon, Rémi ^a   Weiss, Friedbert ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSITY OF CAMERINO   (Italy)

Author keywords

Alcohol; defensive burying; elevated plus maze; mRNA; nociceptin; stress

Indexed keywords

ALCOHOL; NOCICEPTIN; NOCICEPTIN RECEPTOR;

ALCOHOL BLOOD LEVEL; ALCOHOL WITHDRAWAL; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; GENE EXPRESSION; LATERAL HYPOTHALAMUS; MALE; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRIA TERMINALIS; TRANQUILIZING ACTIVITY;

ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ETHANOL; GENE EXPRESSION; MALE; MAZE LEARNING; OPIOID PEPTIDES; RATS; RATS, WISTAR; RECEPTORS, OPIOID; SUBSTANCE WITHDRAWAL SYNDROME; TIME FACTORS;

EID: 84876107354     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/j.1369-1600.2012.00466.x     Document Type: Article

References (49)

1. Aujla H, Martin-Fardon R, Weiss F, (2008) Rats with extended access to cocaine exhibit increased stress reactivity and sensitivity to the anxiolytic-like effects of the mGluR 2/3 agonist LY379268 during abstinence. Neuropsychopharmacology 33: 1818-1826.
2. Braconi S, Sidhpura N, Aujla H, Martin-Fardon R, Weiss F, Ciccocioppo R, (2009) Revisiting intragastric ethanol intubation as a dependence induction method for studies of ethanol reward and motivation in rats. Alcohol Clin Exp Res 34: 538-544.
3. Ciccocioppo R, Biondini M, Antonelli L, Wichmann J, Jenck F, Massi M, (2002) Reversal of stress- and CRF-induced anorexia in rats by the synthetic nociceptin/orphanin FQ receptor agonist, Ro 64-6198. Psychopharmacology 161: 113-119.
4. Ciccocioppo R, Cippitelli A, Economidou D, Fedeli A, Massi M, (2004a) Nociceptin/orphanin FQ acts as a functional antagonist of corticotropin- releasing factor to inhibit its anorectic effect. Physiol Behav 82: 63-68.
5. Ciccocioppo R, Economidou D, Fedeli A, Angeletti S, Weiss F, Heilig M, Massi M, (2004b) 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 172: 170-178.
6. Ciccocioppo R, Fedeli A, Economidou D, Policani F, Weiss F, Massi M, (2003) The bed nucleus is a neuroanatomical substrate for the anorectic effect of corticotropin-releasing factor and for its reversal by nociceptin/orphanin FQ. J Neurosci 23: 9445-9451.
7. Ciccocioppo R, Panocka I, Polidori C, Regoli D, Massi M, (1999) Effect of nociceptin on alcohol intake in alcohol-preferring rats. Psychopharmacology 141: 220-224.
8. D'Addario C, Caputi FF, Rimondini R, Gandolfi O, Del Borrello E, Candeletti S, Romualdi P, (2011) Different alcohol exposures induce selective alterations on the expression of dynorphin and nociceptin systems related genes in rat brain. Addict Biol. doi: 10.1111/j.1369-1600.2011.00326.x.
9. Dayas C, McGranahan T, Martin-Fardon R, Weiss F, (2008) Stimuli linked to ethanol availability activate hypothalamic CART and orexin neurons in a reinstatement model of relapse. Biol Psychiatry 63: 152-157.
10. Devine DP, Taylor L, Reinscheid RK, Monsma FJ Jr, Civelli O, Akil H, (1996) Rats rapidly develop tolerance to the locomotor-inhibiting effects of the novel neuropeptide orphanin FQ. Neurochem Res 21: 1387-1396.
11. Economidou D, Cippitelli A, Stopponi S, Braconi S, Clementi S, Ubaldi M, Martin-Fardon R, Weiss F, Massi M, Ciccocioppo R, (2011) Activation of brain NOP receptors attenuates acute and protracted alcohol withdrawal. Alcohol Clin Exp Res 35: 747-755.
12. Economidou D, Hansson AC, Weiss F, Terasmaa A, Sommer WH, Cippitelli A, Fedeli A, Martin-Fardon R, Massi M, Ciccocioppo R, Heilig M, (2008) Dysregulation of nociceptin/orphanin FQ activity in the amygdala is linked to excessive alcohol drinking in the rat. Biol Psychiatry 64: 211-218.
13. Fernandez F, Misilmeri MA, Felger JC, Devine DP, (2004) Nociceptin/orphanin FQ increases anxiety-related behavior and circulating levels of corticosterone during neophobic tests of anxiety. Neuropsychopharmacology 29: 59-71.
14. Florin S, Suaudeau C, Meunier JC, Costentin J, (1996) Nociceptin stimulates locomotion and exploratory behaviour in mice. Eur J Pharmacol 317: 9-13.
15. Gerashchenko D, Horvath TL, Xie X, (2011) Direct inhibition of hypocretin/orexin neurons in the lateral hypothalamus by nociceptin/orphanin FQ blocks stress-induced analgesia in rats. Neuropharmacology 60: 543-549.
16. Green MK, Devine DP, (2009) Nociceptin/orphanin FQ and NOP receptor gene regulation after acute or repeated social defeat stress. Neuropeptides 43: 507-514.
17. Heinz A, Beck A, Wrase J, Mohr J, Obermayer K, Gallinat J, Puls I, (2009) Neurotransmitter systems in alcohol dependence. Pharmacopsychiatry 42 (Suppl 1): S95-S101.
18. Huang J, Young B, Pletcher MT, Heilig M, Wahlestedt C, (2008) Association between the nociceptin receptor gene (OPRL1) single nucleotide polymorphisms and alcohol dependence. Addict Biol 13: 88-94.
19. Jenck F, Moreau J-L, Martin JR, Kilpatrick GJ, Reinscheid RK, Monsma FJ, (1997) Orphanin FQ acts as an anxiolytic to attenuate behavioral responses to stress. Proc Natl Acad Sci U S A 94: 14854-14858.
20. Kamei J, Matsunawa Y, Miyata S, Tanaka S, Saitoh A, (2004) Effects of nociceptin on the exploratory behavior of mice in the hole-board test. Eur J Pharmacol 489: 77-87.
21. Kauer JA, Malenka RC, (2007) Synaptic plasticity and addiction. Nat Rev Neurosci 8: 844-858.
22. Koob G, Kreek MJ, (2007) Stress, dysregulation of drug reward pathways, and the transition to drug dependence. Am J Psychiatry 164: 1149-1159.
23. Koob GF, (2008) A role for brain stress systems in addiction. Neuron 59: 11-34.
24. Koob GF, (2009) Neurobiological substrates for the dark side of compulsivity in addiction. Neuropharmacology 56 (Suppl 1): 18-31.
25. Lawrence AJ, Cowen MS, Yang HJ, Chen F, Oldfield B, (2006) The orexin system regulates alcohol-seeking in rats. Br J Pharmacol 148: 752-759.
26. de Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE, Fukuhara C, Battenberg EL, Gautvik VT, Bartlett FS 2nd, Frankel WN, van den, Pol AN, Bloom FE, Gautvik KM, Sutcliffe JG, (1998) The hypocretins: hypothalamus- specific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A 95: 322-327.
27. Liu EH, Lee TL, Nishiuchi Y, Kimura T, Tachibana S, (2007) Nocistatin and its derivatives antagonize the impairment of short-term acquisition induced by nociceptin. Neurosci Lett 416: 155-159.
28. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
29. Macey DJ, Schulteis G, Heinrichs SC, Koob GF, (1996) Time-dependent quantifiable withdrawal from ethanol in the rat: effect of method of dependence induction. Alcohol 13: 163-170.
30. Martin-Fardon R, Ciccocioppo R, Massi M, Weiss F, (2000) Nociceptin prevents stress-induced ethanol- but not cocaine-seeking behavior in rats. Neuroreport 11: 1939-1943.
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, N/OFQ/orphanin FQ, and orexin/hypocretin. Brain Res 1314: 145-161.
32. Neal CR Jr, Mansour A, Reinscheid R, Nothacker HP, Civelli O, Watson SJ Jr, (1999) Localization of orphanin FQ (nociceptin) peptide and messenger RNA in the central nervous system of the rat. J Comp Neurol 406: 503-547.
33. Paxinos G, Watson C, (1998) The Rat Brain in Stereotaxic Coordinates, 4th edn. London: Academic Press.
34. Pesold C, Treit D, (1992) Excitotoxic lesions of the septum produce anxiolytic effects in the elevated plus-maze and the shock-probe burying tests. Physiol Behav 52: 37-47.
35. 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.
36. Reinscheid RK, Higelin J, Henningsen RA, Monsma FJ Jr, Civelli O, (1998) Structures that delineate orphanin FQ and dynorphin A pharmacological selectivities. J Biol Chem 273: 1490-1495.
37. Reinscheid RK, Nothacker H, Civelli O, (2001) The orphanin FQ/nociceptin gene: structure, tissue distribution of expression and functional implications obtained from knockout mice. Peptides 21: 901-906.
38. Roberto M, Siggins GR, (2006) 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: 9715-9720.
39. Rodi D, Zucchini S, Simonato M, Cifani C, Massi M, Polidori C, (2008) Functional antagonism between nociceptin/orphanin FQ (N/OFQ) and corticotropin-releasing factor (CRF) in the rat brain: evidence for involvement of the bed nucleus of the stria terminalis. Psychopharmacology 196: 523-531.
40. Sandin J, Ogren SO, Terenius L, (2004) Nociceptin/orphanin FQ modulates spatial learning via ORL-1 receptors in the dorsal hippocampus of the rat. Brain Res 997: 222-233.
41. 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.
42. Valdez GR, Roberts AJ, Chan K, Davis H, Brennan M, Zorrilla EP, Koob GF, (2002) Increased ethanol self-administration and anxiety-like behavior during acute ethanol withdrawal and protracted abstinence: regulation by corticotropin-releasing factor. Alcohol Clin Exp Res 26: 1494-1501.
43. Valdez GR, Zorrilla EP, Roberts AJ, Koob GF, (2003) Antagonism of corticotropin-releasing factor attenuates the enhanced responsiveness to stress observed during protracted ethanol abstinence. Alcohol 29: 55-60.
44. Vale W, Spiess J, Rivier C, Rivier J, (1981) Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotrophin and beta-endorphin. Science 213: 1394-1397.
45. Winsky-Sommerer R, Yamanaka A, Diano S, Borok E, Roberts AJ, Sakurai T, Kilduff TS, Horvath TL, De Lecea L, (2004) Interaction between the corticotropin-releasing factor system and hypocretins (orexins): a novel circuit mediating stress response. J Neurosci 24: 11439-11448.
46. Xuei X, Flury-Wetherill L, Almasy L, Bierut L, Tischfield J, Schuckit M, Nurnberger JI Jr, Foroud T, Edenberg HJ, (2008) Association analysis of genes encoding the nociceptin receptor (OPRL1) and its endogenous ligand (PNOC) with alcohol or illicit drug dependence. Addict Biol 13: 80-87.
47. Zhao Y, Valdez GR, Fekete EM, Rivier JE, Vale WW, Rice KC, Weiss F, Zorrilla EP, (2007a) Subtype-selective corticotropin-releasing factor receptor agonists exert contrasting, but not opposite, effects on anxiety-related behavior in rats. J Pharmacol Exp Ther 323: 846-854.
48. Zhao Y, Weiss F, Zorrilla EP, (2007b) Remission and resurgence of anxiety-like behavior across protracted withdrawal stages in ethanol-dependent rats. Alcohol Clin Exp Res 31: 1505-1515.
49. Zorrilla EP, Valdez GR, Weiss F, (2001) Changes in levels of regional CRF-like-immunoreactivity and plasma corticosterone during protracted drug withdrawal in dependent rats. Psychopharmacology 158: 374-381.