Blockade of nociceptin/orphanin FQ receptor signaling in rat substantia nigra pars reticulata stimulates nigrostriatal dopaminergic transmission and motor behavior

Journal of Neuroscience

Volumn 24, Issue 30, 2004, Pages 6659-6666

  Marti, Matteo ^a   Mela, Flora ^a   Veronesi, Carlo ^a   Guerrini, Remo ^a   Salvadori, Severo ^a   Federici, Mauro ^b   Mercuri, Nicola B ^b   Rizzi, Anna ^a   Franchi, Gianfranco ^a   Beani, Lorenzo ^a   Bianchi, Clementina ^a   Morari, Michele ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b Inst Ricov/Cura Carat S F S L   (Italy)

Author keywords

Dopamine release; J 113397; Microdialysis; Motor activity; N OFQ; Nociceptin orphanin FQ; Substantia nigra; UFP 101

Indexed keywords

1 (1 CYCLOOCTYLMETHYL 3 HYDROXYMETHYL 4 PIPERIDYL) 3 ETHYL 1,3 DIHYDRO 2H BENZIMIDAZOL 2 ONE; [1 N PHENYLALANINE 14 ARGININE 15 LYSINE]NOCICEPTIN[1-13]AMIDE; DOPAMINE; NOCICEPTIN RECEPTOR; OPIATE; PROTEIN INHIBITOR; RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BASAL GANGLION; BRAIN PERFUSION; CONTROLLED STUDY; CORPUS STRIATUM; DENDRITE; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; DOPAMINERGIC TRANSMISSION; ELECTROMYOGRAPHY; ELECTROPHYSIOLOGY; GENE EXPRESSION; HYPERPOLARIZATION; LOCOMOTION; MALE; MOTOR ACTIVITY; MOUSE; MUSCLE CONTRACTION; MUSCLE RELAXATION; MUSCLE TONE; NEUROMODULATION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR GENE; RECEPTOR UPREGULATION; REGULATORY MECHANISM; RETICULAR FORMATION; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; WILD TYPE;

ANIMALS; BENZIMIDAZOLES; CORPUS STRIATUM; DOPAMINE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRODIALYSIS; MICROINJECTIONS; MOTOR ACTIVITY; MUSCLE TONUS; OPIOID PEPTIDES; PIPERIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA;

EID: 3342929522     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0987-04.2004     Document Type: Article

References (65)

1. Albrecht D, Bluhdorn R, Siegmund H, Berger H, Calò G (2001) Inhibitory action of nociceptinforphanin FQ on functionally different thalamic neurons in urethane-anaesthetized rats. Br J Pharmacol 134:333-342.
2. Bergquist F, Shahabi HN, Nissbrandt H (2003) Somatodendritic dopamine release in rat substantia nigra influences motor performance on the accelerating rod. Brain Res 973:81-91.
3. Bertorelli R, Bastia E, Citterio F, Corradini L, Forlani A, Ongini E (2002) Lack of the nociceptin receptor does not affect acute or chronic nociception in mice. Peptides 23:1589-1596.
4. Bontempi B, Sharp FR (1997) Systemic morphine-induced Fos protein in the rat striatum and nucleus accumbens is regulated by μ opioid receptors in the substantia nigra and ventral tegmental area. J Neurosci 17:8596-8612.
5. Buchthal F, Kuhl V (1979) Nerve conduction, tactile sensibility, and the electromyogram after suture or compression of peripheral nerve: a longitudinal study in man. J Neurol Neurosurg Psychiatry 42:436-451.
6. Calò 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.
7. 2, a novel potent and selective antagonist of the nociceptin/orphanin FQ receptor. Br J Pharmacol 136:303-311.
8. Candeletti S, Ferri S (2000) Effects of an antisense oligonucleotide to pronociceptin and long-term prevention of morphine actions by nociceptin. Peptides 21:1119-1124.
9. Chiodo L, Bunney B (1984) Effects of dopamine antagonists on midbrain dopamine cell activity. In: Catecholamines: neuropharmacology and central nervous system-theoretical aspects (Usdin E, ed), pp 369-391. New York: Liss.
10. Cox BM, Chavkin C, Christie MJ, Civelli O, Evans C, Hamon MD, Hoellt V, Kieffer B, Kitchen I, Mcknight AT, Meunier JC, Portoghese PS (2000) Opioid receptors. In: The IUPHAR compendium of receptor characterization and classification (Girdlestone D, ed), pp 321-333. London: IUPHAR Media.
11. Devine DP, Taylor L, Reinscheid RK, Monsma Jr FJ, 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.
12. De Risi C, Piero Pollini G, Trapella C, Peretto I, Ronzoni S, Giardina GA (2001) A new synthetic approach to 1-[3R, 4R)-1-cyclooctylmethyl-3- hydroxymethyl-4-piperidyl]-3-ethyl-1,3-dihydro-2H-benzimidazol-2-one (J-113397), the first non-peptide ORL-1 receptor antagonist. Bioorg Med Chem 9:1871-1877.
13. Di Giannuario A, Pieretti S (2000) Nociceptin differentially affects morphine-induced dopamine release from the nucleus accumbens and nucleus caudate in rats. Peptides 21:1125-1130.
14. Di Giannuario A, Pieretti S, Catalani A, Loizzo A (1999) Orphanin FQ reduces morphine-induced dopamine release in the nucleus accumbens: a microdialysis study in rats. Neurosci Lett 272:183-186.
15. Flau K, Redmer A, Liedtke S, Kathmann M, Schlicker E (2002) Inhibition of striatal and retinal dopamine release via nociceptin/orphanin FQ receptors. Br J Pharmacol 137:1355-1361.
16. Gavioli EC, Marzola G, Guerrini R, Bertorelli R, Zucchini S, De Lima TC, Rae GA, Salvadori S, Regoli D, Calò G (2003) Blockade of nociceptin/orphanin FQ-NOP receptor signalling produces antidepressant-like effects: pharmacological and genetic evidences from the mouse forced swimming test. Eur J Neurosci 17:1987-1990.
17. Guerrini R, Calò G, Bigoni R, Rizzi A, Varani K, Toth G, Gessi S, Hashiba E, Hashimoto Y, Lambert DG, Borea PA, Tomatis R, Salvadori S, Regoli D (2000) Further studies on nociceptin-related peptides: discovery of a new chemical template with antagonist activity on the nociceptin receptor. J Med Chem 43:2805-2813.
18. Iwamoto ET, Way EL (1977) Circling behavior and stereotypy induced by intranigral opiate microinjections. J Pharmacol Exp Ther 203:347-359.
19. Jenck F, Wichmann J, Dautzenberg FM, Moreau JL, Ouagazzal AM, Martin JR, Lundstrom K, Cesura AM, Poli SM, Roever S, Kolczewski S, Adam G, Kilpatrick G (2000) A synthetic agonist at the orphanin FQ/nociceptin receptor ORLI: anxiolytic profile in the rat. Proc Natl Acad Sci USA 97:4938-4943.
20. Kawahara Y, Hesselink MB, van Scharrenburg G, Westerink BH (2004) Tonic inhibition by orphanin FQ/nociceptin of noradrenaline neurotransmission in the amygdala. Eur J Pharmacol 485:197-200.
21. Kawamoto H, Ozaki S, Itoh Y, Miyaji M, Arai S, Nakashima H, Kato T, Ohta H, Iwasawa Y (1999) Discovery of the first potent and selective small molecule opioid receptor-like (ORL1) antagonist: 1-[(3R, 4R)-1-cyclooctylmethyl-3- hydroxymethyl-4-piperidyl]-3-ethyl-1,3-dihydro-2H-benzimidazol-2-one (J-113397). J Med Chem 42:5061-5063.
22. Koizumi M, Midorikawa N, Takeshima H, Murphy NP (2004) Exogenous, but not endogenous nociceptin modulates mesolimbic dopamine release in mice. J Neurochem 89:257-263.
23. Kuzmin A, Sandin J, Terenius L, Ogren SO (2004) Evidence in locomotion test for the functional heterogeneity of ORL-1 receptors. Br J Pharmacol 141:132-140.
24. Lacey MG, Mercuri NB, North RA (1987) Dopamine acts on D2 receptors to increase potassium conductance in neurones of the rat substantia nigra zona compacta. J Physiol (Lond) 392:397-416.
25. Lutfy K, Do T, Maidment NT (2001) Orphanin FQ/nociceptin attenuates motor stimulation and changes in nucleus accumbens extracellular dopamine induced by cocaine in rats. Psychopharmacology (Berl) 154:1-7.
26. Lutfy K, Khaliq I, Carroll FI, Maidment NT (2002) Orphanin FQ/nociceptin blocks cocaine-induced behavioral sensitization in rats. Psychopharmacology (Berl) 164:168-176.
27. Maidment NT, Chen Y, Tan AM, Murphy NP, Leslie FM (2002) Rat ventral midbrain dopamine neurons express the orphanin FQ/nociceptin receptor ORL-1. NeuroReport 13:1137-1140.
28. Manabe T, Noda Y, Mamiya T, Katagiri H, Houtani T, Nishi M, Noda T, Takahashi T, Sugimoto T, Nabeshima T, Takeshima H (1998) Facilitation of long-term potentiation and memory in mice lacking nociceptin receptors. Nature 394:577-581.
29. Mansour A, Fox CA, Akil H, Watson SJ (1995) Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci 18:22-29.
30. Marti M, Guerrini R, Beani L, Bianchi C, Morari M (2002a) Nociceptin/ orphanin FQ receptors modulate glutamate extracellular levels in the substantia nigra pars reticulata. A microdialysis study in the awake freely moving rat. Neuroscience 112:153-160.
31. Marti M, Mela F, Bianchi C, Beani L, Morari M (2002b) Striatal dopamine-NMDA receptor interactions in the modulation of glutamate release in the substantia nigra pars reticulata in vivo: opposite role for D1 and D2 receptors. J Neurochem 83:635-644.
32. Marti M, Mela F, Ulazzi E, Vaccari E, Beani L, Bianchi C, Morari M (2003a) Nigral NOP receptor stimulation inhibits dopamine release in the dorsolateral striatum and motor behavior in rats. In: Monitoring molecules in neuroscience (Kehr J, Fuke K, Ungerstedt U, Svensson T, eds), pp 327-329. Stockholm: Karolinska UP.
33. Marti M, Stocchi S, Paganini F, Mela F, De Risi C, Calò G, Guerrini R, Barnes TA, Lambert DG, Beani L, Bianchi C, Morari M (2003b) Pharmacological profiles of presynaptic nociceptin/orphanin FQ receptors modulating 5-hydroxytryptamine and noradrenaline release in the rat neocortex. Br J Pharmacol 138:91-98.
34. Matsumoto RR, Brinsfield KH, Patrick RL, Walker JM (1988) Rotational behavior mediated by dopaminergic and nondopaminergic mechanisms after intranigral microinjection of specific mu, delta and kappa opioid agonists. J Pharmacol Exp Ther 246:196-203.
35. McLeod RL, Parra LE, Mutter JC, Erickson CH, Carey GJ, Tulshian DB, Fawzi AB, Smith-Torhan A, Egan RW, Cuss FM, Hey JA (2001) Nociceptin inhibits cough in the guinea-pig by activation of ORL(1) receptors. Br J Pharmacol 132:1175-1178.
36. Mercuri NB, Calabresi P, Bernardi G (1990) Effects of glycine on neurons in the rat substantia nigra zona compacta: in vitro electrophysiological study. Synapse 5:190-200.
37. Mercuri NB, Bonci A, Calabresi P, Stefani A, Bernardi G (1995) Properties of the hyperpolarization-activated cation current Ih in rat midbrain dopaminergic neurones. Eur J Neurosci 7:462-469.
38. 1 receptor. Nature 377:532-535.
39. Mogil JS, Pasternak GW (2001) The molecular and behavioral pharmacology of the orphanin FQ/nociceptin peptide and receptor family. Pharmacol Rev 53:381-415.
40. Morelli M, Di Chiara G (1985) Non-dopaminergic mechanisms in the turning behavior evoked by intranigral opiates. Brain Res 341:350-359.
41. Murphy NP, Maidment NT (1999) Orphanin FQ/nociceptin modulation of mesolimbic dopamine transmission determined by microdialysis. J Neurochem 73:179-186.
42. Murphy NP, Ly HT, Maidment NT (1996) Intracerebroventricular orphanin FQ/nociceptin suppresses dopamine release in the nucleus accumbens of anaesthetized rats. Neuroscience 75:1-4.
43. Murphy NP, Lam HA, Chen Z, Pintar JE, Maidment NT (2002) Heroin-induced locomotion and mesolimbic dopamine release is unchanged in mice lacking the ORL.1 receptor gene. Brain Res 953:276-280.
44. Nishi M, Houtani T, Noda Y, Mamiya T, Sato K, Doi T, Kuno J, Takeshima H, Nukada T, Nabeshima T, Yamashita T, Noda T, Sugimoto T (1997) Unrestrained nociceptive response and dysregulation of hearing ability in mice lacking the nociceptin/orphanin FQ receptor. EMBO J 16:1858-1864.
45. Noda Y, Mamiya T, Nabeshima T, Nishi M, Higashioka M, Takeshima H (1998) Loss of antinociception induced by naloxone benzoylhydrazone in nociceptin receptor-knockout mice. J Biol Chem 273:18047-18051.
46. Norton CS, Neal CR, Kumar S, Akil H, Watson SJ (2002) Nociceptin/orphanin FQ and opioid receptor-like receptor mRNA expression in dopamine systems. J Comp Neurol 444:358-368.
47. Ozaki S, Kawamoto H, Itoh Y, Miyaji M, Iwasawa Y, Ohta H (2000) A potent and highly selective nonpeptidyl nociceptin/orphanin FQ receptor (ORL1) antagonist: J-113397. Eur J Pharmacol 387:R17-R18.
48. Paladini CA, Tepper JM (1999) GABA(A) and GABA(B) antagonists differentially affect the firing pattern of substantia nigra dopaminergic neurons in vivo. Synapse 32:165-176.
49. Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Sydney: Academic.
50. Pinnock RD (1984) The actions of antipsychotic drugs on dopamine receptors in the rat substantia nigra. Br J Pharmacol 8:631-635.
51. Polidori C, Calò G, Ciccocioppo R, Guerrini R, Regoli D, Massi M (2000) Pharmacological characterization of the nociceptin receptor mediating hyperphagia: identification of selective antagonist. Psychopharmacology (Berl) 148:430-437.
52. Pucak ML, Grace AA (1996) Effects of haloperidol on the activity and membrane physiology of substantia nigra dopamine neurons recorded in vitro. Brain Res 713:44-52.
53. Redrobe JP, Calò G, Regoli D, Quirion R (2002) Nociceptin receptor antagonists display antidepressant-like properties in the mouse forced swimming test. Naunyn Schmiedebergs Arch Pharmacol 365:164-167.
54. Reinscheid RK, Nothacker HP, Bourson A, Ardati A, Henningsen RA, Bunzow JR, Grandy DK, Langen H, Monsma Jr FJ, Civelli O (1995) Orphanin FQ: a neuropeptide that activates an opioid-like G protein-coupled receptor. Science 270:792-794.
55. Rizzi A, Bigoni R, Marzola G, Guerrini R, Salvadori S, Regoli D, Calò G (2001) Characterization of the locomotor activity-inhibiting effect of nociceptin/orphanin FQ in mice. Naunyn Schmiedebergs Arch Pharmacol 363:161-165.
56. Rozas G, Guerra MJ, Labandeira-Garcia JL (1997) An automated rotarod method for quantitative drug-free evaluation of overall motor deficits in rat models of parkinsonism. Brain Res Brain Res Protoc 2:75-84.
57. Rustay NR, Wahlsten D, Crabbe JC (2003) Influence of task parameters on rotarod performance and sensitivity to ethanol in mice. Behav Brain Res 141:237-249.
58. Shepard PD, Connelly ST (1999) Pertussis toxin lesions of the rat substantia nigra block the inhibitory effects of the gamma-hydroxybutyrate agent, S(-)HA-966 without affecting the basal firing properties of dopamine neurons. Neuropsychopharmacology 21:650-661.
59. Shieh K, Pan J (1998) Ontogeny of the diurnal rhythm of tuberoinfundibular dopaminergic neuronal activity in peripubertal female rats: possible involvement of cholinergic and opioidergic systems. Neuroendocrinology 68:395-402.
60. Turski L, Havemann U, Schwarz M, Kuschinsky K (1982) Disinhibition of nigral GABA output neurons mediates muscular rigidity elicited by striatal opioid receptor stimulation. Life Sci 31:2327-2330.
61. Turski L, Havemann U, Kuschinsky K (1983) The role of the substantia nigra in motility of the rat. Muscular rigidity, body asymmetry and catalepsy after injection of morphine into the nigra. Neuropharmacology 22:1039-1048.
62. Ueda H, Inoue M, Takeshima H, Iwasawa Y (2000) Enhanced spinal nociceptin receptor expression develops morphine tolerance and dependence. J Neurosci 20:7640-7647.
63. Zaratin PF, Petrone G, Sbacchi M, Garnier M, Fossati C, Petrillo P, Ronzoni S, Giardina GA, Scheideler MA (2004) Modification of nociception and morphine tolerance by the selective opiate receptor-like orphan receptor antagonist (-)-cis-1-methyl-7-[[4-(2,6-dichlorophenyl)piperidin-1-yl]methyl]-6, 7,8,9-tetrahydro-5H-benzocyclohepten-5-ol (SB-612111). J Pharmacol Exp Ther 308:454-461.
64. Zaveri N (2003) Peptide and nonpeptide ligands for the nociceptin/orphanin FQ receptor ORL1: research tools and potential therapeutic agents. Life Sci 73:663-678.
65. Zheng F, Grandy DK, Johnson SW (2002) Actions of orphanin FQ/nociceptin on rat ventral tegmental area neurons in vitro. Br J Pharmacol 136:1065-1071.