Mechanisms of 1S,3R-ACPD-induced neuroprotection in rat hippocampal slices subjected to oxygen and glucose deprivation

Neuropharmacology

Volumn 35, Issue 8, 1996, Pages 1037-1048

  Small, D L ^a,b   Monette, R ^a   Chakravarthy, B ^a   Durkin, J ^a   Barbe, G ^c   Mealing, G ^a   Morley, P ^a   Buchan, A M ^b  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

cAMP; Confocal microscopy; Hippocampal slice; Ischemia; Metabotropic glutamate receptors; Neuroprotection; Protein kinase C (PKC)

Indexed keywords

1 AMINO 1,3 CYCLOPENTANEDICARBOXYLIC ACID; CYCLIC AMP; FORSKOLIN; GLUCOSE; NEUROPROTECTIVE AGENT; PHORBOL ESTER; PROTEIN KINASE C;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; HIPPOCAMPUS; HYPOXIA; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; CYCLIC AMP; CYCLOLEUCINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHYSIOLOGY; GLUCOSE; HIPPOCAMPUS; HYPOXIA, BRAIN; MALE; MICROSCOPY, CONFOCAL; NEUROPROTECTIVE AGENTS; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

EID: 0030475451     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0028-3908(96)00028-7     Document Type: Article

References (72)

1. Aderem A. (1992) The MARCKS brothers: a family of protein kinase C substrates. Cell 71: 713-716.
2. Ambrosini A., Bresciani L., Fracchia S., Brunello N. and Racagni O. (1995) Metabotropic glutamate receptors negatively coupled to adenylate cyclase inhibit N-methyl-D-aspartate receptor activity and prevent neurotoxicity in mesencephalic neurons in vitro. Molec. Pharmacol. 47: 1057-1064.
3. Aronowski J., Waxham M. N. and Grotta J. C. (1993) Neuronal protection and preservation of calcium/calmodulin-dependent protein kinase II and protein kinase C activity by dextrorphan treatment in global ischemia. J. Cerebr. Blood Flow Metab. 13: 550-557.
4. 2+ accumulation. Neuropharmacology 32: 1351-1358.
5. Blackshear P. S. (1993) The MARCKS family of cellular protein kinase C substrates. J. biol. Chem. 269: 29367-29370.
6. Bortolotto Z. A. and Collingridge O. L. (1992) Activation of glutamate metabotropic receptors induces long-term potentiation. Eur. J. Pharmacol. 214: 297-298.
7. Bruno V., Copani A., Battaglia G., Raffaele R., Shinozaki H. and Nicoletti F. (1994) Protective effect of the metabotropic glutamate receptor agonist DCG-IV, against excitotoxic neuronal death. Neuropharmacology 256: 109-112.
8. Buchan A. M., Lesiuk H., Barnes K. A., Li H., Huang Z. -G., Smith K. E. and Xue D. (1993) AMPA anagonists: Do they hold more promise for clinical stroke trials than NMDA antagonists? Stroke 24: 1148-1152.
9. Buchan A. M. and Pulsinelli W. A. (1991) N-methyl-D-aspartate excitotoxicity: Is it important in ischemic neuronal injury? In: Advances in Brain Resuscitation (Takeshita H., Siesjo B., Miller J. D., Eds), pp. 59-75, Springer-Verlag, Tokyo.
10. Busto R., Globus M. Y. -T., Neary J. T. and Ginsberg M. D. (1994) Transient cerebral ischemia: effects of intraischemic brain temperature modulation. J. Neurochem. 63: 1095-1103.
11. Cardell M., Bingren H., Wieloch T., Zivin J. and Saitoh T. (1990) Protein kinase C is translocated to cell membranes during cerebral ischemia. Neurosci. Lett. 119: 228-232.
12. Chakravarthy B., Bussey A., Whitfield J. F., Sikorska M., Williams R. E. and Durkin J. P. (1991) The direct measurement of protein kinase C in isolated membranes using a selective peptide substrate. Analyt. Biochem. 196: 144-150.
13. Chakravarthy B. R., Tremblay R., MacDonald P., Krsmanovic V., Whitfield J. F. and Durkin J. P. (1992) The activation of inactive membrane-associated protein kinase C is associated with DMSO-induced erythroleukemia cell differentiation. Biochim. Biophys. Acta 1136: 83-90.
14. Chakravarthy B. R., Whitfield J. F. and Durkin J. P. (1994) Inactive membrane protein kinase Cs - a possible target for receptor signalling. Biochem. J. 304: 809-816.
15. 2+-induced keratinocyte differentiation. J. biol. Chem. 270: 1362-1368.
16. Chakravarthy B., Wong J. and Durkin J. P. (1995b) Evidence that the modulation of membrane-associated protein kinase C activity by an endogenous inhibitor plays a role in N1E-115 murine neuroblastoma cell differentiation. J. Neurochem. 65: 1569-1579.
17. Chavis P., Shinozald H., Bockaert J. and Fagni L. (1994) The metabotropic glutamate, receptor types 2/3 inhibit L-type calcium channels via a pertussis toxin-sensitive G-protein in cultures cerebellar granule cells. J. Neurosci. 14: 7067-7076.
18. Chiamulera C., Albertini P., Valeric E. and Regglani A. (1992) Activation of metabotropic receptors has a neuroprotective effect in a rodent model of focal ischemia. Eur. J. Pharmacol. 216: 335-336.
19. Crumrine R. C., Dubyak G. and LaManna J. C. (1990) Decreased protein kinase C activity during cerebral ischemia and after reperfusion in the adult rat. J. Neurochem. 55: 2001-2007.
20. Crumrine R. C., Selman W. R., LaManna J. C. and Lust W. D. (1992) Protein kinase C activity in permanent focal cerebral ischemia. Molec. Chem. Neuropathol. 16: 85-93.
21. Domariska-Janik K. and Zalewska T. (1992) Effect of brain ischemia on protein kinase C. J. Neurochem. 58: 1432-1439.
22. Favaron M., Manev H., Siman R., Bertolino M., Szekely A. M., DeErausquin G., Guidotti A. and Costa E. (1990) Down-regulation of protein kinase C protects cerebellar granule neurons in primary culture from glutamate-induced neuronal death. Proc. natn. Acad Sci U.S.A. 87: 1983-1987.
23. Felipo V., Miñana M. D. and Grisolía S. (1993) Inhibitors of protein kinase C prevent the toxicity of glutamate in primary neuronal cultures. Brain Res. 604: 192-196.
24. Fujise A., Mizuno K., Ueda Y., Osada S., Hirai S., Takayanagi A., Shimizu N., Owada M. K., Nakajima H. and Ohno S. (1994) Specificity of the high affinity interaction of protein kinase C with a physiological substrate, myristoylated alanine-rich protein kinase C substrate. J. biol. Chem. 269: 31642-31648.
25. Hajimohammadreza I., Probert A. W., Coughenour L. L., Borosky S. A., Marcoux F. W., Boxer P. A. and Wang K. K. W. (1995) A specific inhibitor of calcium/calmodulin-dependent protein kinase-II provides neuroprotection against NMDA- and hypoxia/hypoglycemia-induced cell death. J. Neurosci. 15: 4093-4101.
26. Hara H., Onodera H., Yoshidomi M., Matsuda Y. and Kogure K. (1990) Staurosporin, a novel protein kinase inhibitor, prevents postischemic neuronal damage in the gerbil and rat. J. Cerebr. Blood Flow Metab. 10: 646-653.
27. Haugland R. P. (1992) Fluorescent dyes for assessing vital cell functions. In: Molecular Probes Handbook of Fluorescent Probes and Research Chemicals: 5th Edition (Larison K. D., Ed.), pp. 172-180. Molecular Probes Inc., Eugene, OR.
28. Heemskerk F. M. L., Cheng H. -C. and Huang F. L. (1993) Protein kinase C phosphorylates Ser152, Ser156 and Ser163 but not Ser160 of MARCKS in rat brain. Biochem. Biophys. Res. Commun. 190: 236-241.
29. Hockberger P., Toselli M., Swandulla D. and Lux H. D. (1989) A diacylglycerol analogue reduces neuronal calcium currents independently of protein kinase C activation. Nature 338: 340-342.
30. Kobayashi E., Nakano H., Morimoto M. and Tamaoki T. (1989) Calphostin C (UCN-1028C), a novel microbial compound, is a highly potent and specific inhibitor of protein kinase C. Biochem. Biophys. Res. Comm. 159: 548-553.
31. Kochhar A., Saitoh T. and Zivin J. (1989) Reduced protein kinase C activity in ischenic spinal cord. J. Neurochem. 53: 946-952.
32. Koh J. Y., Palmer E. and Cotman C. W. (1991) Activation of the metabotropic glutamate receptor attenuates N-methyl-D-aspartate neurotoxicity in cortical cultures. Proc. natn. Acad Sci. U.S.A. 88: 9431-9435.
33. Li H. and Buchan A. M. B. (1993) Treatment with an AMPA antagonist 12 hours following severe normothermic forebrain ischemia prevents CA1 neuronal injury. J. Cerebr. Blood Flow Metab. 13: 933-939.
34. Lipton S. A. and Rosenberg P. A. (1994) Excitatory amino acids as a final common pathway for neurological disorders. New Eng. J. Med. 330: 613-622.
35. Lopez-Molina L., Boddeke H. and Muller D. (1993) Blockade of long-term potentiation and NMDA receptors by the protein kinase C antagonist calphostin C. Naunyn-Schmiedeberg's Arch. Pharmacol. 349: 1-6.
36. Madden K. P., Clark W. M., Kochhar A. and Zivin J. A. (1991) Effect of protein kinase C modulation on outcome of experimental CNS ischemia. Brain Res. 547: 193-198.
37. Maiese K. and Boccone L. (1995) Neuroprotection by peptide growth factors against anoxia and nitric oxide toxicity requires modulation of protein kinase C. J, Cerebr. Blood Flow Metab. 15: 440-149.
38. Maiese K., Boniece I. R., Skurat K. and Wagner J. A. (1993) Protein kinases modulate the sensitivity of hippocampal neurons to nitric oxide toxicity and anoxia. J. Neurosci. Res. 36: 77-87.
39. 2+ homeostasis in glutamate-induced neuronal death. In: Neurotoxicity of Excitatory Amino Acids (Guidotti A., Ed.), pp. 63-77. Raven Press, New York.
40. McDonald M. and Schoepp D. D. (1992) The metabotropic excitatory amino, acid receptor agonist 15,3R-ACDP selectively potentiates N-methyl-D-aspartate-induced brain injury. Eur. J. Pharmacol. 215: 353-354.
41. O'Hara P. L. Sheppard P. O., Thorgersen H., Venezia D., Haldeman B. A., McGrane V., Houamed K. M., Thomsen C., Gilbert T. L. and Mulvihill E. R. (1993) The ligand-binding domain in metabotropic glutamate receptors is related to bacterial periplasmic binding proteins. Neuron 11: 41-52.
42. Olah Z., Ikeda J., Anderson W. B. and Joo F. (1990) Altered protein kinase C activity in different subfields of hippocampus following cerebral ischemia. Neurochem. Res. 15: 515-518.
43. Opitz T. and Reymann K. G. (1991) Blockade of metabotropic glutamate receptors protects rat CA1 neurons from hypoxic injury. NeuroReport 2: 455-457.
44. Opitz T. and Reymann K. G. (1993) (15,3R)-ACDP protects synaptic transmission from hypoxia in hippocampal slices. Neuropharmacology 32: 103-104.
45. Orr J. W., Keranivi L. M. and Newton A. C. (1992) Reversible exposure of the pseudosubstrate domain of protein kinase C by phosphatidylserine and diacylglycerol. J. biol. Chem. 267: 15263-15268.
46. Otani S., Ben-Ari Y. and Roisin-Lallemand M. -P. (1993) Metabotropic receptor stimulation coupled to weak tetanus leads to long-term potentiation and a rapid elevation of cytosolic protein kinase C activity. Brain Res. 613: 1-9.
47. Pizzi M., Concetta F., Arrighi V., Memo M, and Spano P. F. (1993) Attenuation of excitatory amino acid toxicity by metabotropic glutamate receptor agonists and aniracetam in primary cultures of cerebellar granule cells. J. Neurochem. 61: 683-689.
48. Reddoch R. B., Pelletier R. -M., Barbe G. J. and Armstrong D. T. (1986) Lack of ovarian responsiveness to gonadotropic hormones in infantile rats sterilized with busulfan. Endocrinology 119: 879-896.
49. Reymann K. G. and Opitz T. (1995) Metabotropic glutamate receptor subtypes differentially influence neuronal recovery from in vitro hypoxia/hypoglycemia in rat hippocampal slices. J. Cerebr. Blood Flow Metab. 15: S259.
50. Sacaan A. I. and Schoepp D. D. (1992) Activation of hippocampal metabotropic excitatory amino acid receptors leads to seizures and neuronal damage. Neurosci. Lett. 139: 77-82.
51. Schoepp D. D. (1994) Novel functions for subtypes of metabotropic glutamate receptors. Neurochem. Int. 24: 439-449.
52. Schoepp D. D. and Johnson B. G. (1994a) Metabotropic glutamate receptor modulation of cAMP accumulation in the neonatal rat hippocampus. Neuropharmacology 32: 1359-1365.
53. Schoepp D. D. and Johnson B. G. (1994b) Pharmacology of metabotropic glutamate receptor inhibition of cyclic AMP formation in the adult rat hippocampus. Neurochem. Int. 22: 277-283.
54. Schoepp D. D., Johnson B. G. and Monn J. A. (1992) Inhibition of cyclic AMP formation by a selective metabotropic glutamate receptor agonist. J. Neurochem. 58: 1184-1186.
55. Schoepp D. D., Tizzano J. P., Wright R. A. and Fix A. S. (1995) Reversible and irreversible neuronal injury induced by intrahippocampal infusion of the mGluR agonist 1S,3R-ACDP in the rat. Neurodegeneration 4: 71-80.
56. Schurr A. and Rigor B. M. (1989) Cerebral ischemia revisited: New insights as revealed using in vitro brain slice preparations. Experimentia 45: 684-695.
57. Shinozaki H. (1994) Neuron damage induced by some potent kainoids and neuroprotective action of new agonists for metabotropic glutamate receptors. Eur. Neuro. 34: 2-9.
58. Small D. L., Monette R., Mealing G., Buchan A. M. and Morley P. (1995) Neuroprotective effects of ω-AGA-IVA against in vitro ischaemia in the rat hippocampal slice. NeuroReport 6: 1617-1620.
59. Small D. L. and Buchan A. M. (1996) Mechanisms of cerebral ischemia. intracellular cascades and therapeutic interventions. J. Cardiothoracic. Vascular. Anesth. 10: 139-146.
60. Snell L. D., Iorio K. R., Tabakoff B. and Hoffman P. L. (1994) Protein kinase C activation attenuates N-methyl-D-aspartate-induced increases in intracellular calcium in cerebellar granule cells. J. Neurochem. 62: 1783-1789.
61. Sommer B. and Seeburg P. (1992) Glutamate receptor channels: novel properties and new clones. Trends Pharmacol. Sci. 13: 291-296.
62. Stefani A., Pisani A., Mercuri N. B., Bernadi G. and Calabresi P. (1994) Activation of metabotropic glutamate receptors inhibits calcium currents and GABA-mediated synaptic potentials in striatal neurons. J. Neurosci. 14: 6134-6143.
63. Suyama K., Saito K., Chen G., Pan B.-S., Manji H. K. and Potter W. Z. (1995) Alterations in cyclic AMP generation and G protein subunits following transient ischemia in gerbil hippocampus. J. Cerebr. Blood Flow Metab. 15: 877-885.
64. 2+ dependent protein kinase. Biochem. Biophys. Res. Comm. 135: 397-402.
65. Thomsen C., Frandsen A., Suzdak P. D., Andersen C. F. and Schousboe A. (1993) Effects of t-ACPD on neural survival in cultured cerebral cortical neurons. NeuroReport 4: 1255-1258.
66. Towbin H., Staehelin T. and Gordon J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. natn. Acad. Sci. U.S.A. 76: 4350-4354.
67. Wang L. -Y., Dudek E. M., Browning M. D. and MacDonald S. F. (1994) Modulation of AMPA/kainate receptors in cultured murine hippocampal neurons by protein kinase C. J. Physiol. 475: 431-437.
68. Whitfield J. F., Chakravarthy B. R., Durkin J. P., Isaacs R. J., Jouishomme H., Sikorska M., Williams R. E. and Rixon R. H. (1992) C-terminal fragment of parathyroid hormone-related protein, PTHrP(107-111) and (107-139), and the N-terminal PTHrP(1-40) fragment stimulate membrane associated protein kinase C activity in rat spleen lymphocytes. J. Cell Physiol. 150: 299-303.
69. Whittingham T. S., Lust W. D. and Passonneau J. V. (1984) An in vitro model of ischemia: metabolic and electrical alterations in the hippocampal slice. J. Neurosci. 4: 793-802.
70. Wieloch T., Cardell M., Bingren H., Zivin J. and Saitoh T. (1991) Changes in activity of protein kinase C and the differential subcellular redistribution of its isozymes in the rat striatum during and following transient forebrain ischemia. J. Neurochem. 56: 1227-1235.
71. Williams R. E., Chakravarthy B. R., Sikorska M., Whitfield J. F. and Durkin J. P. (1992) A protein kinase C substrate derived from MARCKS protein. In Peptides: Chemistry and Biology (Smith J. A. and River J. E., Eds.), pp. 923-924, ESCOM, Leiden.
72. Yokota M., Peterson J. W., Kaotitzanis M. and Kowall N. W. (1992) Immunohistochemical distribution of protein kinase C isozymes is differentially altered in ischemic gerbil hippocampus. Brain Res. 587: 123-129.