Involvement of the neuropeptide nociceptin/orphanin FQ in kainate seizures

Journal of Neuroscience

Volumn 22, Issue 22, 2002, Pages 10030-10038

  Bregola, Gianni ^a   Zucchini, Silvia ^a   Rodi, Donata ^a   Binaschi, Anna ^a   D'Addario, Claudio ^b   Landuzzi, Daniela ^b   Reinscheid, Rainer ^c   Candeletti, Sanzio ^b   Romualdi, Patrizia ^b   Simonato, Michele ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Epilepsy; Kainate; Knock out mice; Nociceptin; Opioid receptor like 1; Seizure

Indexed keywords

1 (1 CYCLOOCTYLMETHYL 3 HYDROXYMETHYL 4 PIPERIDYL) 3 ETHYL 1,3 DIHYDRO 2H BENZIMIDAZOL 2 ONE; KAINIC ACID; MESSENGER RNA; NOCICEPTIN; NOCICEPTIN RECEPTOR ANTAGONIST; OPIATE RECEPTOR;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE PREDISPOSITION; EPILEPSY; GENE EXPRESSION; IN SITU HYBRIDIZATION; KNOCKOUT GENE; MALE; MOUSE; NERVE CELL EXCITABILITY; NEUROMODULATION; NOCICEPTION; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; RECEPTOR DENSITY; SEIZURE;

EID: 0037111839     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-22-10030.2002     Document Type: Article

References (70)

1. Albrecht D, Bluhdorn R, Siegmund H, Berger H, Calò G (2001) Inhibitory action of nociceptin/orphanin FQ on functionally different thalamic neurons in urethane-anaesthetized rats. Br J Pharmacol 134:333-342.
2. Bregola G, Candeletti S, Romualdi P, Simonato M (1999) Limbic seizures increase pronociceptin mRNA levels in the thalamic reticular nucleus. NeuroReport 10:541-546.
3. Bunzow JR, Saez C, Mortrud M, Bouvier C, Williams JT, Low M, Grandy DK (1994) Molecular cloning and tissue distribution of a putative member of the rat opioid receptor gene family that is not a μ, δ or κ opioid receptor type. FEBS Lett 347:284-288.
4. 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.
5. Chen Y, Fan Y, Liu J, Mestak A, Tian M, Kozak CA, Yu L (1994) Molecular cloning tissue distribution and chromosomal localization of a novel member of the opioid receptor gene family. FEBS Lett 347:279-283.
6. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
7. Cox BM, Chavkin C, Christie MJ, Civelli O, Evans C, Hamon MD, Hollt 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.
8. Dautzenberg FM, Wichmann J, Higelin J, Py-Lang G, Kratzeisen C, Malherbe P, Kilpatrick GJ, Jenck F (2001) Pharmacological characterization of the novel nonpeptide orphanin FQ/nociceptin receptor agonist Ro 64-6198: rapid and reversible desensitization of the ORL1 receptor in vitro and lack of tolerance in vivo. J Pharmacol Exp Ther 298:812-819.
9. De Risi C, Pollini GP, 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-benzimidazol-2-one (J-113397), the first non-peptide ORL-1 receptor antagonist. Bioorg Med Chem 9:1871-1877.
10. Dingledine R, McBain CJ, McNamara JO (1990) Excitatory amino acid receptors in epilepsy. Trends Pharmacol Sci 11:334-338.
11. Fukuda K, Kato S, Mori K, Nishi M, Takeshima H, Iwabe N, Miyata T, Houtani T, Sugimoto T (1994) cDNA cloning and regional distribution of a novel member of the opioid receptor family. FEBS Lett 343:42-46.
12. Grisel JE, Mogil JS (2000) Effects of supraspinal orphanin FQ/nociceptin. Peptides 21:1037-1045.
13. Guillery RW, Feig SL, Lozsadi DA (1998) Paying attention to the thalamic reticular nucleus. Trends Neurosci 21:28-32.
14. Gunning P, Ponte P, Okayama H, Engel J, Blau H, Kedes L (1983) Isolation and characterization of full-length cDNA clones for human alpha-, beta-, and gamma-actin mRNAs: Skeletal but not cytoplasmic actins have an amino-terminal cysteine that is subsequently removed. Mol Cell Biol 3:787-795.
15. Gutierrez R, Leff P, Romo-Parra H, Acevedo R, Anton B (2001) Orphanin-FQ/nociceptin inhibits kindling epileptogenesis and enhances hippocampal feed-forward inhibition. Neuroscience 105:325-333.
16. Hokfelt T (1991) Neuropeptides in perspective: The last ten years. Neuron 7:867-879.
17. Hosford DA, Simonato M, Cao Z, Garcia-Cairasco N, Silver JM, Butler L, Shin C, McNamara JO (1995) Differences in the anatomic distribution of immediate-early gene expression in amygdala and angular bundle kindling development. J Neurosci 15:2513-2523.
18. Janumpalli S, Butler LS, MacMillan LB, Limbird LE, McNamara JO (1998) A point mutation (D79N) of the α2A adrenergic receptor abolishes the anti-epileptogenic action of endogenous norepinephrine. J Neurosci 18:2004-2008.
19. Jenck F, Moreau JL, Martin JR, Kilpatrick GJ, Reinscheid RK, Monsma FJ, Nothacker HP, Civelli O (1997) Orphanin FQ acts as an anxiolytic to attenuate behavioral responses to stress. Proc Natl Acad Sci USA 94:14854-14858.
20. 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 ORL1: Anxiolytic profile in the rat. Proc Natl Acad Sci USA 97:4938-4943.
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. Köster A, Montkowski A, Schulz S, Stube EM, Knaudt K, Jenck F, Moreau JL, Nothacker HP, Civelli O, Reinscheid RK (1999) Targeted disruption of the orphanin FQ/nociceptin gene increases stress susceptibility and impairs stress adaptation in mice. Proc Natl Acad Sci USA 96:10444-10449.
23. Lachowicz JE, Shen Y, Monsma FJ, Sibley DR (1995) Molecular cloning of a novel G protein-coupled receptor related to the opiate receptor family. J Neurochem 64:34-40.
24. Laursen SE, Belknap JK (1986) Intracerebroventricular injections in mice. Some methodological refinements. J Pharmacol Methods 16:355-357.
25. Leventhal L, Mathis JP, Rossi GC, Pasternak GW, Bodnar RJ (1998) Orphan opioid receptor antisense probes block orphanin FQ-induced hyperphagia. Eur J Pharmacol 349:R1-3.
26. Lowry OH, Rosebrough NJ, Farr A, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275.
27. Ma L, Cheng ZJ, Fan GH, Cai YC, Jiang LZ, Pei G (1997) Functional expression, activation and desensitization of opioid receptor-like receptor ORL1 in neuroblastoma x glioma NG108-15 hybrid cells. FEBS Lett 403:91-94.
28. Madamba SG, Schweitzer P, Siggins GR (1999) Nociceptin augments K(+) currents in hippocampal CA1 neurons by both ORL-1 and opiate receptor mechanisms. J Neurophysiol 82:1776-1785.
29. 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.
30. Mathis JP, Goldberg IE, Rossi GC, Leventhal L, Pasternak GW (1998) Antinociceptive analogs of orphanin FQ/nociceptin(1-11). Life Sci 63:161-166.
31. McNamara JO (1988) Pursuit of the mechanism of kindling. Trends Neurosci 11:33-36.
32. Meis S, Pape HC (2001) Control of glutamate and GABA release by nociceptin/orphanin FQ in the rat lateral amygdala. J Physiol (Lond) 532:701-712.
33. Meunier JC, Mollereau C, Toll L, Suaudeau C, Moisand C, Alvinerie P, Butour JL, Guillemot JC, Ferrara P, Monsarrat B, Mazarguil H, Vassart G, Parmentier M, Costentin J (1995) Isolation and structure of the endogenous agonist of opioid receptor-like ORL1 receptor. Nature 377:532-535.
34. Mollereau C, Parmentier M, Mailleux P, Butour JL, Moisand C, Chalon P, Caput D, Vassart G, Meunier JC (1994) ORL1, a novel member of the opioid receptor family. Cloning, functional expression and localization. FEBS Lett 341:33-38.
35. Moran TD, Abdulla FA, Smith PA (2000) Cellular neurophysiological actions of nociceptin/orphanin FQ. Peptides 21:969-976.
36. Mulle C, Sailer A, Perez-Otano I, Dickinson-Anson H, Castillo PE, Bureau I, Maron C, Gage FH, Mann JR, Bettler B, Heinemann SF (1998) Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392:601-605.
37. Neal Jr CR, Mansour A, Reinscheid R, Nothacker HP, Civelli O, Watson Jr SJ (1999a) Localization of orphanin FQ (nociceptin) peptide and messenger RNA in the central nervous system of the rat. J Comp Neurol 406:503-547.
38. 14Tyr]-orphanin FQ binding. J Comp Neurol 412:563-605.
39. Nicol B, Lambert DG, Rowbotham DJ, Smart D, McKnight AT (1996) Nociceptin induced inhibition of K+ evoked glutamate release from rat cerebrocortical slices. Br J Pharmacol 119:1081-1083.
40. Okuda-Ashitaka E, Minami T, Tachibana S, Yoshihara Y, Nishiuchi Y, Kimura T, Ito S (1998) Nocistatin, a peptide that blocks nociceptin action in pain transmission. Nature 392:286-289.
41. Ozaki S, Kawamoto H, Itoh Y, Miyaji M, Azuma T, Ichikawa D, Nambu H, Iguchi T, Iwasawa Y, Ohta H (2000) In vitro and in vivo pharmacological characterization of J-113397, a potent and selective nonpeptidyl ORL1 receptor antagonist. Eur J Pharmacol 402:45-53.
42. S-related opioid receptor. Mol Pharmacol 47:1180-1188.
43. Pasternak GW (1993) Pharmacological mechanisms of opioid analgesics. Clin Neuropharmacol 16:1-18.
44. Pasternak GW, Standifer KM (1995) Mapping of opioid receptors using antisense oligodeoxynucleotides: Correlating their molecular biology and pharmacology. Trends Pharmacol Sci 16:344-350.
45. Pellegrino LJ, Pellegrino AS, Cushman AJ (1979) A Stereotaxic Atlas of the Rat Brain. New York: Plenum.
46. Reinscheid RK, Nothacker HP, Bourson A, Ardati A, Henningsen RA, Bunzow JR, Grandy DK, Langen H, Monsma FJ Jr, Civelli O (1995) Orphanin FQ: A neuropeptide that activates an opioidlike G proteincoupled receptor. Science 270:792-794.
47. Rocha LL, Evans CJ, Maidment NT (1997) Amygdala kindling modifies extracellular opioid peptide content in rat hippocampus measured by microdialysis. J Neurochem 68:616-624.
48. Romualdi P, Donatini A, Bregola G, Bianchi C, Beani L, Ferri S, Simonato M (1995) Early changes in prodynorphin mRNA and irdynorphin A levels after kindled seizures in the rat. Eur J Neurosci 7:1850-1856.
49. Sandin J, Georgieva J, Schott PA, Ogren SO, Terenius L (1997) Nociceptin/orphanin FQ microinjected into hippocampus impairs spatial learning in rats. Eur J Neurosci 9:194-197.
50. Sbrenna S, Marti M, Morari M, Calò G, Guerrini R, Beani L, Bianchi C (1999) L-glutamate and gamma-aminobutyric acid efflux from rat cerebrocortical synaptosomes: Modulation by kappa- and mu- but not delta- and opioid-receptor like-1 receptors. J Pharmacol Exp Ther 291:1365-1371.
51. Schlicker E, Morari M (2000) Nociceptin/orphanin FQ and neurotransmitter release in the central nervous system. Peptides 21:1023-1029.
52. Schlicker E, Werthwein S, Kathmann M, Bauer U (1998) Nociceptin inhibits noradrenaline release in the mouse brain cortex via presynaptic ORL1 receptors. Naunyn Schmiedebergs Arch Pharmacol 358:418-422.
53. Schmued LC, Hopkins KJ (2000) Fluoro-Jade B: A high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874:123-130.
54. Simonato M, Romualdi P (1996) Dynorphin and epilepsy. Prog Neurobiol 50:557-583.
55. Simonato M, Bregola G, Donatini A, Bianchi C, Beani L, Ferri S, Romualdi P (1996) Kindled seizure-induced c-fos and prodynorphin mRNA expressions are unrelated in the rat brain. Eur J Neurosci 8:2064-2067.
56. 3H]-5-HT release from rat cerebral cortex slices. Br J Pharmacol 128:119-123.
57. Spampinato S, Di Toro R, Qasem AR (2001) Nociceptin-induced internalization of the ORL1 receptor in human neuroblastoma cells. NeuroReport 12:3159-3163.
58. Tallent MK, Madamba SG, Siggins GR (2001) Nociceptin reduces epileptiform events in CA3 hippocampus via presynaptic and postsynaptic mechanisms. J Neurosci 21:6940-6948.
59. Tian JH, Zhang W, Fang Y, Xu W, Grandy DK, Han JS (1998) Endogenous orphanin FQ: Evidence for a role in the modulation of electroacupuncture analgesia and the development of tolerance to analgesia produced by morphine and electroacupuncture. Br J Pharmacol 124:21-26.
60. Treiman DM (2001) GABAergic mechanisms in epilepsy. Epilepsia 42(S3):8-12.
61. Wang J-B, Johnson PS, Imai Y, Persico AM, Ozenberger BA, Eppler CM, Uhl G (1994) cDNA cloning of an orphan opiate receptor gene family member and its splice variant. FEBS Lett 348:75-79.
62. Weinshenker D, Szot P, Miller NS, Rust NC, Hohmann JG, Pyati U, White SS, Palmiter RD (2001) Genetic comparison of seizure control by norepinephrine and neuropeptide Y. J Neurosci 21:7764-7769.
63. Werthwein S, Bauer U, Nakazi M, Kathmann M, Schlicker E (1999) Further characterization of the ORL1 receptor-mediated inhibition of noradrenaline release in the mouse brain in vitro. Br J Pharmacol 127:300-308.
64. White LE, Price JL (1993) The functional anatomy of limbic status epilepticus in the rat. I. Patterns of 14C-2-deoxyglucose uptake and Fos immunocytochemistry. J Neurosci 13:4787-4809.
65. Wick MJ, Minnerath SR, Lin X, Elde R, Law PY, Loh HH (1994) Isolation of a novel cDNA encoding a putative membrane receptor with high homology to the cloned mu, delta, and kappa opioid receptors. Mol Brain Res 27:37-44.
66. Wick MJ, Minnerath SR, Roy S, Ramakrishnan S, Loh HH (1995) Expression of alternate forms of brain opioid orphan receptor mRNA in activated human peripheral blood lymphocytes and lymphocytic cell lines. Mol Brain Res 32:342-347.
67. Wisden W, Seeburg PH (1993) A complex mosaic of high-affinity kainate receptors in rat brain. J Neurosci 13:3582-3598.
68. Xie GX, Meuser T, Pietruck C, Sharma M, Palmer PP (1999) Presence of opioid receptor-like (ORL1) receptor mRNA splice variants in peripheral sensory and sympathetic neuronal ganglia. Life Sci 64:2029-2037.
69. Yu TP, Xie CW (1998) Orphanin FQ/nociceptin inhibits synaptic transmission and long-term potentiation in rat dentate gyrus through postsynaptic mechanisms. J Neurophysiol 80:1277-1284.
70. Zhang X, Le Gal La Salle G, Ridoux V, Yu PH, Ju G (1997) Protection of kainic acid-induced limbic seizures and Fos expression by the GABA-A receptor agonist muscimol. Eur J Neurosci 9:29-40.