A combined pharmacological and genetic approach to investigate the role of orphanin FQ in learning and memory

European Journal of Neuroscience

Volumn 15, Issue 5, 2002, Pages 911-922

  Higgins, Guy A ^a,c   Kew, J N C ^a   Richards, J G ^a   Takeshima, H ^b   Jenck, F ^d   Adam, G ^a   Wichmann, J ^a   Kemp, J A ^d   Grottick, A J ^a  

^a F HOFFMANN LA ROCHE LTD   (Switzerland)

^b KURUME UNIVERSITY   (Japan)

^c MERCK RESEARCH LABORATORIES   (United States)

^d NONE

Author keywords

Delayed match nonmatch to position; Hippocampus; Mouse; OFQ N peptide knockout mouse; ORL1 receptor knockout mouse; Rat

Indexed keywords

NOCICEPTIN; OPIOID RECEPTOR LIKE RECEPTOR; PEPTIDE; RECEPTOR; RO 646198; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BRAIN CORTEX; BRAIN FUNCTION; COGNITION; CONDITIONING; CONTROLLED STUDY; DENTATE GYRUS; ELECTROPHYSIOLOGY; FEAR; GENETICS; HIPPOCAMPUS; KNOCKOUT MOUSE; LEARNING; MALE; MAZE TEST; MEMORY; MEMORY DISORDER; MOUSE; NERVE CELL NETWORK; NEUROLOGIC DISEASE; NONHUMAN; PASSIVE AVOIDANCE; PRIORITY JOURNAL; RAT; SHORT TERM MEMORY; SPATIAL ORIENTATION; SUBICULUM; TASK PERFORMANCE; TEMPORAL LOBE;

ANIMALS; ANTI-ANXIETY AGENTS; AVOIDANCE LEARNING; COGNITION; CONDITIONING (PSYCHOLOGY); DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; IMIDAZOLES; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; OPIOID PEPTIDES; RADIOLIGAND ASSAY; RATS; RATS, INBRED STRAINS; RECEPTORS, OPIOID; SPACE PERCEPTION; SPIRO COMPOUNDS;

EID: 0036456557     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.01926.x     Document Type: Article

References (53)

1. Anton, B., Fein, J., To, T., Li, X., Silberstein, L. & Evans, C.J. (1996) Immunohistochemical localisation of ORL-1 in the central nervous system of the rat. J. Comp. Neurol., 368, 229-251.
2. Bannerman, D.M., Good, M.A., Butcher, S.P., Ramsey, M. & Morris, R.G.M. (1995) Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature, 378, 182-186.
3. Beiko, J., Candusso, L. & Cain, D.P. (1997) The effect of nonspatial water maze pretraining in rats subjected to serotonin depletion and muscarinic receptor antagonism: A detailed behavioural assessment of spatial performance. Behav. Brain Res., 88, 201-211.
4. Burwell, R.D., Witter, M.P. & Amaral, D.G. (1995) Perirhinal and postrhinal cortices in the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain. Hippocampus, 5, 390- 408.
5. 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.
6. Darland, T., Heinricher, M.M. & Grandy, D.K. (1998) Orphanin FQ/nociceptin: A role in pain and analgesia, but so much more. Trends Neurosci., 21, 215-221.
7. Deacon, R.M.J. (1991) Pharmacological studies of a rat spatial delayed non-match-to-sample task as an animal model of dementia. Drug Dev. Res., 24, 67-79.
8. Dhawan, B.N., Cesselin, F., Raghubir, R., Reisine, T., Bradley, P.B., Portoghese, P.S. & Hamon, M. (1996) International Union of Pharmacology. XII. Classification of opioid receptors. Pharmacol. Rev., 48, 567-592.
9. Dunnett, S.B. (1985) Comparative effects of cholinergic drugs and lesions of nucleus basalis or fimbria-fornix on delayed matching in rats. Psychopharmacology, 87, 357-363.
10. Dunnett, S.B., Evenden, J.L. & Iversen, S.D. (1988) Delay-dependent short-term memory deficits in aged rats. Psychopharmacology, 96, 174-180.
11. Eichenbaum, H. (2000) A cortical-hippocampal system for declarative memory. Nature Rev., 1, 41-50.
12. 3H]nociceptin binding sites in the rat brain. Brain Res., 880, 11-16.
13. Gerlai, R. (1996) Gene-targetting studies of mammalian behaviour: Is it the mutation or the background genotype? Trends Neurosci., 19, 177-181.
14. Griebel, G., Perrault, G. & Sanger, D.J. (1999) Orphanin FQ a novel neuropeptide with anti-stress-like activity. Brain Res., 836, 221-224.
15. Henderson, G. & McKnight, A.T. (1997) The orphan opioid receptor and its endogenous ligand - Nociceptin/orphanin FQ. Trends Pharmacol. Sci., 18, 293-300.
16. Higgins, G.A., Adam, G., Kapps, M., Kew, J.N.C., Grottick, A.J., Ouagazzal, A.M., Richards, J.G., Takeshima, H., Wichmann, J., Pauly-Evers, M. & Jenck, F. (2000) A combined pharmacological and genetic approach to studying the role of orphanin FQ in cognition. Eur. J. Neurosci., 12 (Suppl. 11), 77.22.
17. Higgins, G.A., Grottick, A.J., Ballard, T.M., Richards, J.G., Messer, J., Takeshima, H., Pauly-Evers, M., Jenck, F., Adam, G. & Wichmann, J. (2001) Influence of the selective ORL1 receptor agonist, Ro64-6198, on rodent neurological function. Neuropharmacology, 41, 97-107.
18. Hiramatsu, M. & Inoue, K. (1999) Effects of nocistatin on nociceptin-induced impairment of learning and memory in mice. Eur. J. Pharmacol., 367, 151- 155.
19. Houtani, T., Nishi, M., Takeshima, H., Sato, K., Sakuma, S., Kakimoto, S., Ueyama, T., Noda, T. & Sugimoto, T. (2000) Distribution of nociceptin/orphaninFQ precursor protein and receptor in brain and spinal cord: A study using in-situ hybridisation and X-gal histochemistry in receptor-deficient mice. J. Comp. Neurol., 424, 489-508.
20. Hunter, A.J. & Roberts, F.F. (1987) The effects of 8-hydroxy-2-(di-n-propylamino) tetralin (8-OH DPAT) on spatial learning in the Morris water maze task. In Dourish, C.T., Ahlenius, S. & Hutson, P.H. (eds), Brain 5-HT1A Receptors. Ellis Horwood Publishers, Chichester, UK.
21. Ikeda, K., Kobayashi, K., Kobayashi, T., Ichikawa, T., Kumanishi, T., Kishida, H., Yano, R. & Manabe, T. (1997) Functional coupling of the nociceptin/orphanin FQ receptor with the G-protein-activated K+ (GIRK) channel. Mol. Brain Res., 45, 117-126.
22. Jenck, F., Moreau, J.-L., Borroni, E., Pauly-Evers, M., Ouagazzal, A.M., Reinscheid, R., Nothacker, H.-P., Civelli, O. & Kilpatrick, G.J. (1999) Orphanin-FQ: Role as a neuromodulator of mood/anxiety-like states in rodents. Eur. Neuropsychopharmacol., 9 (S5), 139-140.
23. Jenck, F., Moreau, J.-L., Martin, J.R., Kilpatrick, G.J., Reinscheid, R.K., Monsma, F.J., Nothacker, H.-P. & Civelli, O. (1997) Orphanin FQ acts as an anxiolytic to attenuate behavioural responses to stress. Proc. Natl. Acad. Sci., 94, 14854-14858.
24. Jenck, F., Wichmann, J., Dautzenberg, F.M., Moreau, J.-L., Ouagazzal, A.M., Martin, J.R., Lundstrom, K., Cesura, A.M., Poli, S.M., Roever, S., Kolczewski, S., Adam, G. & Kilpatrick, G.J. (2000) A synthetic agonist at the orphanin FQ/nociceptin receptor ORL1: Anxiolytic profile in the rat. Proc. Natl. Acad. Sci., 97, 4938-4943.
25. Kirkby, D.L. & Higgins, G.A. (1998) Characterization of perforant path lesions in rodent models of memory and attention. Eur. J. Neurosci., 10, 823-838.
26. Knoflach, F., Reinscheid, R.K., Civelli, O. & Kemp, J.A. (1996) Modulation of voltage-gated calcium channels by orphanin FQ in freshly dissociated hippocampal neurons. J. Neurosci., 16, 6657-6664.
27. Koester, A., Montkowski, A., Schulz, S., Stube, E.-M., Knaudt, K., Jenck, F., Moreau, J.-L., Nothacker, H.-P., Civelli, O. & Reinscheid, R.K. (1999) Targetted disruption of the orphanin FQ/nociceptin gene increases stress susceptibility and impairs stress adaptation in mice. Proc. Natl. Acad. Sci., 96, 10444-10449.
28. Madamba, G.S., Schweitzer, P. & Siggins, G.R. (1999) Nociceptin augments K+ currents in hippocampal CA1 neurons by both ORL-1 and opiate receptor mechanisms. J. Neurophysiol., 82, 1776-1785.
29. Mamiya, T., Noda, Y., Nishi, M., Takeshima, H. & Nabeshima, T. (1998) Enhancement of spatial attention in nociceptin/orphanin FQ receptor-knockout mice. Brain Res., 783, 236-240.
30. 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.
31. Meunier, J.-C., Mollereau, C., Toll, L., Suaudeneau, C., Moisand, C., Alvinerie, P., Butour, J.-L., Guillemot, J.C., 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.
32. Milner, B., Squire, L.R. & Kandel, E.R. (1998) Cognitive neuroscience and the study of memory. Neuron, 20, 445-468.
33. Morris, R.G.M., Garrud, P., Rawlins, J.N.P. & O'Keefe, J. (1982) Place navigation impaired in rats with hippocampal lesions. Nature, 297, 681- 683.
34. Nabeshima, T., Noda, Y. & Mamiya, T. (1999) The role of nociceptin in cognition. Brain Res., 848, 167-173.
35. Neal, C.R., Mansour, A., Reinscheid, R., Nothacker, H.-P., Civelli, O. & Watson, S.J. (1999) Localization of orphanin FQ (nociceptin) peptide and messenger RNA in the central nervous system of the rat. J. Comp. Neurol., 406, 503-547.
36. Nishi, M., Houtani, T., Noda, Y., Mamiya, T., Sato, K., Doi, T., Kuno, J., Takeshima, H., Nukuda, T., Nabeshima, T., Yamashita, T., Noda, T. & Sugimoto, T. (1997) Unrestrained nociceptive response and disregulation of hearing ability in mice lacking the nociceptin/orphanin FQ receptor. EMBO J., 16, 1858-1864.
37. Noble, F. & Roques, B.P. (1997) Association of aminopeptidase N and endopeptidase 24.15 inhibitors potentiate behavioural effects mediated by nociceptin/orphanin FQ in mice. FEBS Lett., 401, 227-229.
38. Noda, Y., Mamiya, T., Manabe, T., Nishi, M., Takeshima, H. & Nabeshima, T. (2000) Role of nociceptin systems in learning and memory. Peptides, 21, 1063-1069.
39. Phillips, R.G. & Le Doux, J.E. (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci., 106, 274-285.
40. Pomonis, J.D., Billington, C.J. & Levine, A.S. (1996) Orphanin FQ, agonist of orphan receptor ORL1, stimulates feeding in rats. Neuroreport, 8, 369-371.
41. 2, a nociceptin receptor antagonist, reverses nociceptin-induced spatial memory impairments in the Morris water maze task in rats. Br. J. Pharmacol., 131, 1379-1384.
42. Reinscheid, R.K., Koster, A., Knaudt, K., Montkowski, A. & Civelli, O. (1999) Increased stress susceptibility and fear in orphanin FQ/nociceptin knockout mice is dependent on chronic social stress. Soc. Neurosci. Abstr., 25, 1473.
43. Reinscheid, R.K., Nothacker, H.-P., Bourson, A., Ardati, A., Hinningsen, R.A., Bunzow, J.R., Grandy, D.K., Langen, H., Monsma, F.J. & Civelli, O. (1995) OrphaninFQ: A neuropeptide that activates an opioidlike G proein-coupled receptor. Science, 270, 792-794.
44. Rizzi, A., Bigoni, R., Marzola, G., Guerrini, R., Salvadori, S., Regoli, D. & Calo, G. (2001) Characterisation of the locomotor activity-inhibiting effect of nociceptin/orphanin FQ in mice. Naunyn-Schmiedeberg's Arch. Pharmacol., 363, 161-165.
45. Sahgal, A., Keith, A.B. & Lloyd, S. (1990) Opposing effects of vasopressin on matching versus non-matching to position: Further evidence for response, not memory, modulation. Psychopharmacology, 102, 130-135.
46. Sandin, J., Georgieva, J., Schott, P.A., Ogren, S.O. & Terenius, L. (1997) Nociceptin orphanin FQ microinjected into hippocampus impairs spatial learning in rats. Eur. J. Neurosci., 9, 194-197.
47. Saucier, D., Hargreaves, E.L., Boon, F., Vanderwolf, C.H. & Cain, D.P. (1996) Detailed behavioral analysis of water maze acquisition under systemic NMDA or muscarinic antagonism: Nonspatial pretraining eliminates spatial learning deficits. Behav. Neurosci., 110, 103-116.
48. Silva, A.J., Simpson, E.M., Takahashi, J.S., Lipp, H-P, Nakanishi, S., Wehner, J.M., Giese, K.P., Tully, T., Abel, T., Chapman, P.F., Fox, K., Grant, S., Itohara, S., Lathe, R., Mayford, M., McNamara, J.O., Morris, R.J., Picciotto, M., Roder, J., Shin, H-S., Slesinger, P.A., Storm, D.R., Stryker, M.P., Tonegawa, S., Wang, Y., Wolfer, D.P. (1997) Mutant mice and Neuroscience: Recommendations concerning genetic background. [Banbury Conference on Genetic Background in Mice]. Neuron, 19, 755- 759.
49. Stanhope, K.J., McLenachan, A.P. & Dourish, C.T. (1995) Dissociation between cognitive and motor/motivational deficits in the delayed matching to position test: Effects of scopolamine, 8-OH DPAT and EAA antagonists. Psychopharmacology, 122, 268-280.
50. Stratford, T.R., Holahan, M.R. & Kelley, A.E. (1997) Injections of nociceptin into nucleus accumbens shell or ventromedial hypothalamic nucleus increase food intake. Neuroreport, 8, 423-426.
51. Wichmann, J., Adam, G., Rover, S., Hinnig, M., Scalone, M., Cesura, A.M., Dautzenberg, F.M. & Jenck, F. (2000) Synthesis of (1S,3aS)-8-(2,3,3a,4, 5,6-hexahydro-1H-phenalen-1-yl)-1-phenyl-1,3,8-triazo-spiro[4.5]decan-4-one, a potent and selective orphanin FQ (OFQ) receptor agonist with anxiolytic-like properties. Eur. J. Med. Chem. 35, 839-851.
52. Yu, T.-P., Fein, J., Phan, T., Evans, C. & Xie, C.-W. (1997) Orphanin FQ inhibits synaptic transmission and long-term potentiation in rat hippocampus. Hippocampus, 7, 88-94.
53. Yu, T.-P. & Xie, C.-W. (1998) Orphanin FQ/nociceptin inhibits synaptic transmission and long-term potentiation in rat dentate gyrus through postsynaptic mechanisms. J. Neurophysiol., 80, 1277-1284.