Inherent desensitisation-preventing properties of a novel, subtype-selective AMPA receptor agonist, (S)-CPW 399, as a possible explanation for its excitotoxic action in cultured cerebellar granule cells

Neurochemistry International

Volumn 42, Issue 6, 2003, Pages 499-510

  Sinclair, Colin ^a   Reavy, Helen ^a   Grieve, Angus ^a   Schousboe, Arne ^b   Morelli, Elena ^c   Novellino, Ettore ^c   Campiani, Giuseppe ^d   Griffiths, Roger ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d UNIVERSITY OF SIENA   (Italy)

Author keywords

AMPA receptors; Cultured cerebellar granule cells; Desensitisation; Excitotoxicity

Indexed keywords

1 (2 AMINO 2 CARBOXYETHYL) 6,7 DIHYDRO 1H CYCLOPENTAPYRIMIDINE 2,4(1H,3H) DIONE; 1 (4 AMINOPHENYL) 3,4 DIHYDRO 4 METHYL 3 METHYLCARBAMOYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 2 AMINO 5 PHOSPHONOVALERIC ACID; 5 FLUOROWILLARDIINE; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; 6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; AMPA RECEPTOR AGONIST; AMPA RECEPTOR ANTAGONIST; BENZODIAZEPINE DERIVATIVE; CALCIUM CHANNEL L TYPE; CYCLOTHIAZIDE; NIFEDIPINE; PYRIMIDINE DERIVATIVE; QUINOXALINE DERIVATIVE; UNCLASSIFIED DRUG; WILLARDIINE;

ANIMAL CELL; ARTICLE; CELL CULTURE; CEREBELLUM; CONTROLLED STUDY; DESENSITIZATION; DRUG POTENTIATION; DRUG SYNTHESIS; GRANULE CELL; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL;

ALANINE; ANIMALS; CALCIUM; CELLS, CULTURED; CEREBELLUM; CYTOPLASMIC GRANULES; EXCITATORY AMINO ACID AGONISTS; L-LACTATE DEHYDROGENASE; MICE; PYRIMIDINONES; RECEPTORS, AMPA;

EID: 0037401438     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0197-0186(02)00141-9     Document Type: Article

References (62)

1. i changes in cultured rat hippocampal neurons. Eur. J. Neurosci. 12:2000;2021-2031.
2. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S.A., Nicotera P. Glutamate-induced neuronal death: a succession of necrosis or apoptosis-dependent on mitochondrial function. Neuron. 15:1995;961-973.
3. Balázs R., Jorgensen O.S., Hack N. N-Methyl-D-aspartate promotes the survival of cerebellar granule cells in culture. Neuroscience. 27:1988;437-451.
4. Banke T.G., Greenwood J.R., Christensen J.K., Liljefors T., Traynelis S.F., Schousboe A., Pickering D.S. Identification of amino acid residues in GluR1 responsible for ligand binding and desensitisation. J. Neurosci. 21:2001;3052-3062.
5. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., Lipton S.A. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. U.S.A. 92:1995;7162-7166.
6. 2+ entry via AMPA/KA receptors and excitotoxicity in cultured cerebellar Purkinje cells. J. Neurosci. 14:1994;187-197.
7. Campiani G., Morelli E., Nacci V., Fattorusso C., Ramunno A., Novellino E., Greenwood J., Liljefors T., Griffiths R., Sinclair C., Reavy H., Kristensen A.S., Pickering D.S., Schousboe A., Cagnotto A., Mennini T. Characterization of the 1H-cyclopentapyrimidine-2,4(1H,3H)-dione derivative (S)-CPW 399, as a novel, potent and subtype-selective AMPA receptor full agonist with partial desensitisation-preventing properties. J. Med. Chem. 44:2001;4501-4504.
8. Cebers G., Zhivotovsky B., Ankarcrona M., Liljequist S. AMPA neurotoxicity in cultured cerebellar granule neurons: mode of cell death. Brain Res. Bull. 43:1997;393-403.
9. Condorelli D.F., Dell' Albani P., Aronica E., Genezzani A.A., Casabona G., Corsaro M., Balázs R., Nicoletti F. Growth conditions differentially regulate the expression of α-amino-3-hydroxy-5-methylisoxazole-4-propionate (AMPA) receptor subunits in cultured neurons. J. Neurochem. 61:1993;2133-2139.
10. Fletcher E.J., Lodge D. New developments in the molecular pharmacology of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate and kainate receptors. Pharmacol. Ther. 70:1996;65-89.
11. Frandsen A., Schousboe A. Time and concentration-dependency of the toxicity of excitatory amino acids on cerebral neurones in primary culture. Neurochem. Int. 10:1987;583-591.
12. Frandsen A., Schousboe A. Excitatory amino acid-mediated cytotoxicity and calcium homeostasis in cultured neurons. J. Neurochem. 60:1993;1202-1211.
13. Frandsen A., Drejer J., Schousboe A. Direct evidence that excitotoxicity in cultured neurons is mediated via N-methyl-D-aspartate (NMDA) as well as non-NMDA receptors. J. Neurochem. 53:1989;297-299.
14. Frerking M., Nicoll R.A. Synaptic kainate receptors. Curr. Opin. Neurobiol. 10:2000;342-351.
15. Gallo V., Upson L.M., Hayes W.P., Vyklicky L., Winters C.A., Buonanno A. Molecular cloning and developmental analysis of a new glutamate receptor subunit isoform in cerebellum. J. Neurosci. 12:1992;1010-1023.
16. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron. 15:1995;193-204.
17. Gibertson T.A., Scobey R., Wilson M. Permeation of calcium ions through non-NMDA glutamate channels in retinal bipolar cells. Science. 251:1991;1613-1615.
18. Gill R., Lodge D. Pharmacology of AMPA antagonists and their role in neuroprotection. Int. Rev. Neurobiol. 40:1997;197-232.
19. Griffiths R., Ritchie L., Lidwell K., Grieve A., Malcolm C.S., Scott M., Meredith C. Calcium influx via L-type voltage-gated channels mediates the delayed, elevated increases in steady-state c-fos mRNA levels in cerebellar granule cells exposed to excitotoxic levels of glutamate. J. Neurosci. Res. 52:1998;641-652.
20. 2+ influx studies. J. Neurochem. 65:1995;1077-1084.
21. Hollman M., Heinemann S. Cloned glutamate receptors. Annu. Rev. Neurosci. 17:1994;31-108.
22. Iino M., Ozawa S., Tsuzuki K. Permeation of calcium through excitatory amino acid channels in cultured rat hippocampal neurones. J. Physiol. (London). 424:1990;151-165.
23. Jane D.E., Hoo K., Deverill M., Bleakman D., Mandelzys A. Synthesis of willardiine and 6-azawillardiine analogues: pharmacological characterization on cloned homomeric human AMPA and kainate receptor subtypes. J. Med. Chem. 40:1997;3645-3650.
24. Janssens N., Lesage A.S.J. Glutamate receptor subunit expression in primary neuronal and secondary glial cultures. J. Neurochem. 77:2001;1457-1474.
25. Jensen J.B., Schousboe A., Pickering D.S. AMPA receptor mediated excitotoxicity in neocortical neurons is developmentally regulated and dependent upon receptor desensitisation. Neurochem. Int. 32:1998a;505-513.
26. Jensen J.B., Schousboe A., Pickering D.S. Development of calcium-permeable α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors in cultured neocortical neurons visualised by cobalt staining. J. Neurosci. Res. 54:1998b;273-281.
27. Jensen J.B., Lund T.M., Timmermann D.B., Schousboe A., Pickering D.S. Role of GluR2 expression in AMPA-induced toxicity in cultured murine cerebral cortical neurons. J. Neurosci. Res. 65:2001;267-277.
28. 2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron. 12:1994;1281-1289.
29. B receptors in regulation of transmitter release in cerebellar granule cells. J. Neurosci. Res. 39:1995;646-655.
30. König N., Poluch S., Estabel J., Durand M., Drain M.-J., Exbrayat J.-M. Synaptic and non-synaptic AMPA receptors permeable to calcium. Jpn. J. Pharmacol. 86:2001;1-17.
31. Kristensen, A.S., Greenwood, J.R., Liljefors, T., Campiani, G., Morelli, E., Novellino, E., Fattorusso, C., Schousboe, A., Pickering, D.S., 2001. Pharmacology and molecular modelling of a novel willardiine analog at AMPA receptors. Soc. Neurosci. Abstr. 27, Program No. 572.14.
32. Larm J.A., Cheung N.S., Beart P.M. (S)-5-Fluorowillardiine-mediated neurotoxicity in cultured murine cortical neurones occurs via AMPA and kainate receptors. Eur. J. Pharmacol. 314:1996;249-254.
33. Lipton S.A., Nicotera P. Excitotoxicity, free radicals, necrosis, and apoptosis. Neuroscientist. 4:1998;345-352.
34. Lipton S.A., Rosenberg P.A. Excitatory amino acids as a final common pathway for neurologic disorders. N. Engl. J. Med. 330:1994;613-622.
35. 2+ entry. NeuroReport. 6:1995;1089-1092.
36. Malcolm C.S., Ritchie L., Grieve A., Griffiths R. Glutamate toxicity in primary cerebellar cultures from mouse brain is unaffected by changes in cGMP levels. Neuroreport. 7:1996;1650-1654.
37. May P.C., Robison P.M. Cyclothiazide treatment unmasks AMPA excitotoxicity in rat primary hippocampal cultures. J. Neurochem. 60:1993;1171-1174.
38. Michaelis E.K. Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog. Neurobiol. 54:1998;369-415.
39. Minta A., Kao J.P.Y., Tsien R.Y. Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. J. Biol. Chem. 264:1989;8171-8178.
40. 2+ release. Trends Pharmacol. Sci. 16:1995;356-359.
41. Monaghan D.T., Bridges R.J., Cotman C.W. The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Ann. Rev. Pharmacol. Toxicol. 29:1989;365-402.
42. Moudy A.M., Yamada K.A., Rothman S.M. Rapid desensitisation determines the pharmacology of glutamate neurotoxicity. Neuropharmacology. 33:1994;953-962.
43. Nicotera P., Bellomo G., Orrenius S. Calcium-mediated mechanisms in chemically induced cell death. Ann. Rev. Pharmacol. Toxicol. 32:1992;449-470.
44. Obrenovitch T.P., Urenjak J. Altered glutamatergic transmission in neurological disorders: from high extracellular glutamate to excessive synaptic efficacy. Prog. Neurobiol. 51:1997;39-87.
45. Paternain A.V., Morales M., Lerma J. Selective antagonism of AMPA receptors unmasks kainate-receptor-mediated responses in hippocampal neurons. Neuron. 14:1995;185-189.
46. Patneau D.K., Mayer M.L., Jane D.E., Watkins J.C. Activation and desensitisation of AMPA/kainate receptors by novel derivatives of willardiine. J. Neurosci. 12:1992;595-606.
47. Resink A., Hack N., Boer G.J., Balázs R. Growth conditions differentially modulate the vulnerability of developing cerebellar granule cells to excitatory amino acids. Brain Res. 655:1994;222-232.
48. Rothman S.M., Olney J.W. Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann. Neurol. 19:1986;105-111.
49. Sattler R., Charlton M.P., Hafner M., Tymianski M. Distinct influx pathways, not calcium load, determine neuronal vulnerability to calcium neurotoxicity. J. Neurochem. 71:1998;2349-2364.
50. Schousboe, A., Meier, E., Drejer, J., Hertz, L., 1989. Preparation of cultures of mouse (rat) cerebellar granule cells. In: Shahar, A., De Vellis, J.A., Vernadakis, A., Haber, B. (Eds.), A Dissection and Tissue Culture Manual for the Nervous System. Alan R. Liss, New York, pp. 203-206.
51. Siesjö B.K. Basis for the application of calcium antagonists in neurology: calcium in the brain under physiological and pathological conditions. Eur. Neurol. 30:1990;3-9.
52. Sommer B., Keinänen K., Verdoorn T.A., Wisden W., Burnashev N., Herb A., Köhler M., Takagi T., Sakmann B., Seeburg P.H. Flip and flop: a cell-specific functional switch in glutamate operated channels of the CNS. Science. 249:1990;1580-1585.
53. Sun G., Uretsky N.J., Wallace L.J., Shams G., Weinstein D.M., Miller D.D. Synthesis of chiral 1-(2′ amino-2′-carboxyethyl)-1,4-dihydro-6,7-quinoxaline-2,3-diones: α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptor agonists and antagonists. J. Med. Chem. 39:1996;4430-4438.
54. Thomas N.K., Hawkins L.M., Miller J.C., Troop H.M., Roberts P.J., Jane D.E. Pharmacological differentiation of kainate receptors on neonatal rat spinal motoneurones and dorsal roots. Neuropharmacology. 37:1998;1223-1237.
55. 2+ in cerebral cortex neurons is transient in immature cells but permanent in mature cells. J. Neurochem. 53:1989;1316-1319.
56. 2+ permeable AMPA or kainate receptors: possible key factors in selective neurodegeneration. Trends Neurosci. 23:2000;365-371.
57. Wilding T.J., Huettner J.E. Differential antagonism of alpha-amino-3-hydroxy-5-methyl-4-isoxazoleproprionic acid-preferring and kainate-preferring receptors by 2,3 benzodiazepines. Mol. Pharmacol. 47:1995;582-587.
58. 2+ concentration and subsequent loss of neuronal function in individual neocortical neurons in culture. Proc. Natl. Acad. Sci. U.S.A. 91:1994;12303-12307.
59. Wong L.A., Mayer M.L., Jane D.E., Watkins J.C. Willardiines differentiate agonist binding sites for kainate- versus AMPA-preferring glutamate receptors in DRG and hippocampal neurons. J. Neurosci. 14:1994;3881-3897.
60. Yamada K.A., Tang C.-M. Benzothiazides inhibit rapid glutamate receptor desensitisation and enhance glutamatergic synaptic currents. J. Neurosci. 13:1993;3904-3915.
61. Zorumski C.F., Thio L.L., Clifford D.B. Effects of bromowillardiine on non-N-methyl-D-aspartate receptors in postnatal rat hippocampal neurons. Mol. Pharmacol. 40:1991;45-51.
62. Zorumski C.F., Yamada K.A., Proce M.T., Olney J.W.A. A benzodiazepine recognition site associated with the non-NMDA glutamate receptor. Neuron. 10:1993;61-67.