Evidence that brain-derived neurotrophic factor neuroprotection is linked to its ability to reverse the NMDA-induced inactivation of protein kinase C in cortical neurons

Journal of Neurochemistry

Volumn 72, Issue 1, 1999, Pages 102-111

  Tremblay, R ^c   Hewitt, K ^c   Lesiuk, H ^a   Mealing, G ^c   Morley, P ^c   Durkin, J P ^b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c NONE

Author keywords

Brain derived neurotrophic factor; Cortical cultures; Glutamate toxicity; Protein kinase C

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; N METHYL DEXTRO ASPARTIC ACID; PROTEIN KINASE C;

ANIMAL CELL; ARTICLE; BRAIN ISCHEMIA; BRAIN PROTECTION; BRAIN TOXICITY; ENZYME ACTIVITY; ENZYME INACTIVATION; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM; CEREBRAL CORTEX; ELECTROPHYSIOLOGY; ENZYME INHIBITORS; EXCITATORY AMINO ACID AGONISTS; FEMALE; GLUTAMIC ACID; INDOLES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALEIMIDES; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; N-METHYLASPARTATE; NEURONS; NEUROPROTECTIVE AGENTS; NEUROTOXINS; PHOSPHORYLATION; PREGNANCY; PROTEIN KINASE C; PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; STAUROSPORINE;

ANIMALIA;

EID: 0032953646     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0720102.x     Document Type: Article

References (61)

1. Aderem A. (1992) The MARCKS brothers: a family of protein kinase C substrates. Cell 71, 713-716.
2. Altar C. A., Boylan C. B., Fritsche M., Jones B. E., Jackson C., Wiegand S. J., Lindsay R. M., and Hyman C. (1994) Efficacy of brain-derived neurotrophic factor and neurotrophin-3 on neurochemical and behavioral deficits associated with partial nigrostriatal dopamine lesions. J. Neurochem. 63, 1021-1032.
3. Ballarin M., Ernfors P., Lindefors N., and Persson H. (1991) Hippocampal damage and kainic acid injection induce a rapid increase in mRNA for BDNF and NGF in the rat brain. Exp. Neurol. 114, 35-43.
4. Beck T., Lindholm D., Castren E., and Wree A. (1994) Brain-derived neurotrophic factor protects against ischemic cell damage in rat hippocampus. J. Cereb. Blood Flow Metab. 14, 689-692.
5. Blackshear P. J. (1993) The MARCKS family of cellular protein kinase C substrates. J. Biol. Chem. 268, 1501-1504.
6. Blumberg P. M., Acs G., Acs P., Areces L. B., Kazanietz M. G., Lewin N. E., and Szallasi Z. (1995) Protein kinase C in cell signaling: strategies for the development of selective inhibitors. Agents Actions Suppl. 47, 87-100.
7. Busto R., Globus M. Y.-T., Neary J. T., and Ginsberg M. D. (1994) Regional alterations of protein kinase C activity following transient cerebral ischemia: effects of intraischemic brain temperature modulation. J. Neurochem. 63, 1095-1103.
8. Cardell M. and Wieloch T. (1993) Time course of the translocation and inhibition of protein kinase C during complete cerebral ischemia in the rat. J. Neurochem. 61, 1308-1314.
9. 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.
10. Chakravarthy B. R., Bussey A., Whitfield J. F., Sikorska M., Williams R. E., and Durkin J. P. (1991) The direct measurement of protein kinase C (PKC) activity in isolated membranes using a selective peptide substrate. Anal. Biochem. 196, 144-150.
11. 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.
12. Chakravarthy B. R., Wong J., and Durkin J. P. (1995) Evidence that the modulation of membrane-associated protein kinase C activity by an endogenous inhibitor plays a role in NIE-115 murine neuroblastoma cell differentiation. J. Neurochem. 65, 1569-1579.
13. Chakravarthy B., Wang J., Tremblay R., Atkinson T., Wang F., Li L., Buchan A., and Durkin J. P. (1998) Comparison of the changes in protein kinase C induced by glutamate in primary cortical neurons by in vivo cerebral ischemia. Cell. Signal. 10, 291-295.
14. Cheng B. and Mattson M. P. (1994) NT-3 and BDNF protect CNS neurons against metabolic/excitotoxic insults. Brain Res. 640, 56-67.
15. Comelli M. C., Seren M. S., Guidolin D., Manev R. M., Favaron M., Rimland J. M., Canella R., Negro A., and Manev H. (1992) Photochemical stroke and brain-derived neurotrophic factor (BDNF) mRNA expression. Neuroreport 3, 473-476.
16. 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.
17. Cui Q. and Harvey A. R. (1995) At least two mechanisms are involved in the death of retinal ganglion cells following target ablation in neonatal rats. J. Neurosci. 15, 8143-8155.
18. Cunningham M. E., Stephens R. M., Kaplan D. R., and Greene L. A. (1997) Autophosphorylation of activation loop tyrosines regulates signaling by the TRK nerve growth factor receptor. J. Biol. Chem. 272, 10957-10967.
19. Dessi F., Charriaut-Marlangue C., and Ben-Ari Y. (1992) Anisomycin and cycloheximide protect cerebellar neurons in culture from anoxia. Brain Res. 581, 323-326.
20. Dichter M. A. (1978) Rat cortical neurons in cell culture: culture methods, cell morphology, electrophysiology, and synapse formation. Brain Res. 149, 279-293.
21. Domańska-Janik K. and Zalewska T. (1992) Effect of brain ischemia on protein kinase C. J. Neurochem. 58, 1432-1439.
22. Durkin J. P., Tremblay R., Buchan A., Blosser J., Chakravarthy B., Mealing G., Morley P., and Song D. (1996) An early loss in membrane protein kinase C activity precedes the excitatory amino acid-induced death of primary cortical neurons. J. Neurochem. 66, 951-962.
23. Durkin J. P., Tremblay R., Chakravarthy B., Mealing G., Morley P., Small D., and Song D. (1997) Evidence that the early loss of membrane protein kinase C is a necessary step in the excitatory amino acid-induced death of primary cortical neurons. J. Neurochem. 68, 1400-1412.
24. Ernfors P., Bengzon J., Kokaia Z., Persson H., and Lindvall O. (1991) Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis. Neuron 7, 165-176.
25. Freese A., Finklestein S. P., and DiFiglia M. (1992) Basic fibroblast growth factor protects striatal neurons in vitro from NMDA-receptor mediated excitotoxicity. Brain Res. 575, 351-355.
26. Furukawa K., Estus S., Fu W., Mark R. J., and Mattson M. P. (1997) Neuroprotective action of cycloheximide involves induction of bcl-2 and antioxidant pathways. J. Cell Biol. 136, 1137-1149.
27. Gordge P. C. and Ryves W. J. (1994) Inhibitors of protein kinase C. Cell. Signal. 6, 871-882.
28. Hannun Y. A., Loomis C. R., and Bell R. M. (1985) Activation of protein kinase C by Triton X-100 mixed micelles containing diacylglycerol and phosphatidylserine. J. Biol. Chem. 260, 10039-10043.
29. 160 of MARCKS in rat brain. Biochem. Biophys. Res. Commun. 190, 236-241.
30. Isackson P. J., Huntsman M. M., Murray K. D., and Gall C. M. (1991) BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distant from NGF. Neuron 6, 937-948.
31. Jarvis C. R., Xiong Z. G., Plant J. R., Churchill D., Lu W. Y., MacVicar B. A., and MacDonald J. F. (1997) Neurotrophin modulation of NMDA receptors in cultured murine and isolated rat neurons. J. Neurophysiol. 78, 2363-2371.
32. Jian Z., Nonaka I., Hattori S., and Nakamura S. (1996) Activation of Ras and protection from apoptotic cell death by BDNF in PC12 cells expressing TrkB. Cell. Signal. 8, 365-370.
33. Kaplan D. R. and Miller F. D. (1997) Signal transduction by the neurotrophin receptors. Curr. Opin. Cell Biol. 9, 213-221.
34. Kato H., Kanellopoulos G. K., Matsuo S., Wu Y. J., Jacquin M. F., Hsu C. Y., Choi D. W., and Kouchoukos N. T. (1997) Protection of rat spinal cord from ischemia with dextrorphan and cycloheximide: effects on necrosis and apoptosis. J. Thorac. Cardiovasc. Surg. 114, 609-618.
35. Kikkawa U., Takai Y., Minakuchi R., Inohara S., and Nishizuki Y. (1982) Calcium-activated, phospholipid-dependent protein kinase from rat brain. Subcellular distribution, purification, and properties. J. Biol. Chem. 257, 13341-13348.
36. Kishimoto A. (1990) Limited proteolysis of protein kinase C by calpain, its possible implication. Adv. Second Messenger Phosphoprotein Res. 24, 472-477.
37. Klein R., Nanduri V., Jing S. A., Lamballe F., Tapley P., Bryant S., Cordon-Cardo C., Jones K. R., Reichardt L. F., and Barcacid M. (1991) The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell 66, 395-403.
38. Kokaia Z., Othberg A., Kokaia M., and Lindvall O. (1994) BDNF makes cultured dentate granule cells more resistant to hypoglycaemic damage. Neuroreport 5, 1241-1244.
39. Kokaia Z., Zhao Q., Kokaia M., Elmer E., Metsis M., Smith M. L., Siesjo B. K., and Lindvall O. (1995) Regulation of brain-derived neurotrophic factor gene expression after transient middle cerebral artery occlusion with and without brain damage. Exp. Neurol. 136, 73-88.
40. Koketsu N., Berlove D. J., Moskowitz M. A., Kowall N. W., Caday C. G., and Finklestein S. P. (1994) Pretreatment with intraventricular basic fibroblast growth factor decreases infarct size following focal cerebral ischemia in rats. Ann. Neurol. 35, 451-457.
41. Lewin G. R. and Barde Y. A. (1996) Physiology of the neurotrophins. Annu. Rev. Neurosci. 19, 289-317.
42. Lindefors N., Ballarin M., Emfors P., Falkenberg T., and Persson H. (1992) Stimulation of glutamate receptors increases expression of brain-derived neurotrophic factor mRNA in rat hippocampus. Ann. NY Acad. Sci. 648, 296-299.
43. Lindholm D., Dechant G., Heisenberg C. P., and Thoenen H. (1993) Brain-derived neurotrophic factor is a survival factor for cultured rat cerebellar granule neurons and protects them against glutamate-induced neurotoxicity. Eur. J. Neurosci. 5, 1455-1464.
44. Louis J. C., Magal E., Brixi A., Steinberg R., Yavin E., and Vincedon G. (1991) Reduction of protein kinase C activity in the adult rat brain following transient forebrain ischemia. Brain Res. 541, 171-174.
45. Mattson M. P., Murrain M., Guthrie P. B., and Kater S. B. (1989) Fibroblast growth factor and glutamate: opposing roles in the generation and degeneration of hippocampal neuroarchitecture. J. Neurosci. 9, 3728-3740.
46. Mudo G., Persson H., Timmusk T., Funakoshi H., Bindoni M., and Belluardo N. (1993) Increased expression of trkB and trkC messenger RNAs in the rat forebrain after focal mechanical injury. Neuroscience 57, 901-912.
47. Nozaki K., Finklestein S. P., and Beal M. F. (1993) Delayed administration of basic fibroblast growth factor protects against N-methyl-D-aspartate neurotoxicity in neonatal rats. Eur. J. Pharmacol. 232, 295-297.
48. Pang L., Sawada T., Decker S. J., and Saltiel A. R. (1995) Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J. Biol. Chem. 270, 13585-13588.
49. Robinson P. J., Liu J. P., Chen W., and Wenzel T. (1993) Activation of protein kinase C in vitro and in intact cells or synaptosomes determined by acetic acid extraction of MARCKS. Anal. Biochem. 210, 172-178.
50. Schreiber S. S., Tocco G., Najm I., Thompson R. F., and Baudry M. (1993) Cycloheximide prevents kainate-induced neuronal death and c-fos expression in adult rat brain. J. Mol. Neurosci. 4, 149-159.
51. Segal R. and Greenberg M. E. (1996) Intracellular signalling pathways activated by neurotrophic factors. Annu. Rev. Neurosci. 19, 463-489.
52. Senger D. L. and Campenot R. B. (1997) Rapid retrograde tyrosine phosphorylation of trkA and other proteins in rat sympathetic neurons in compartmented cultures. J. Cell Biol. 138, 411-421.
53. Shimohama S., Tamura Y., Akaike A., Tsukahara T., Ohara O., Watanabe S., and Kimura J. (1993) Brain-derived neurotrophic factor pretreatment exerts a partially protective effect against glutamate-induced neurotoxicity in cultured rat cortical neurons. Neurosci. Lett. 164, 55-58.
54. Small D. L., Monette R., Chakravarthy B., Durkin J., Barbe G., Mealing G., Morley P., and Buchan A. M. (1996) Mechanisms of 1S,3R-ACPD-induced neuroprotection in rat hippocampal slices subjected to oxygen and glucose deprivation. Neuropharmacology 35, 1037-1048.
55. Small D. L., Murray C. L., Mealing G. A. R., Poulter M. O., Buchan A. M., and Morley P. (1998) Brain derived neurotrophic factor induction of N-methyl-D-aspartate receptor subunit NR2A expression in cultured rat cortical neurons. Neurosci. Lett. 252, 211-214.
56. Spina M. B., Squinto S. P., Miller J., Lindsay R. M., and Hyman C. (1992) Brain-derived neurotrophic factor protects dopamine neurons against 6-hydroxydopamine and N-methyl-4-phenylpyridinium ion toxicity: involvement of the glutathione system. J. Neurochem. 59, 99-106.
57. Stephens R. M., Loeb D. M., Copeland T. D., Pawson T., Greene L. A., and Kaplan D. R. (1994) Trk receptors use redundant signal transduction pathways involving SHC and PLC-gamma 1 to mediate NGF responses. Neuron 12, 691-705.
58. Williams R. E., Chakravarthy B. R., Sikorska M., Whitfield J. F., and Durkin J. P. (1991) A protein kinase C substrate peptide derived from MARCKS protein in Chemistry, Structure and Biology (Rivier J. and Smilli J. A., eds). pp. 903-927. ESCOM, Amsterdam.
59. Yamashita K., Wiessner C., Lindholm D., Thoenen H., and Hossmann K. A. (1997) Post-occlusion treatment with BDNF reduces infarct size in a model of permanent occlusion of the middle cerebral artery in rat. Metab. Brain Dis. 12, 271-280.
60. Yu O. and Chuang D. M. (1997) Neurotrophin protection against toxicity induced by low potassium and nitroprusside in cultured cerebellar granule neurons. J. Neurochem. 68, 68-77.
61. Zirrgiebel U., Ohga Y., Carter B., Berninger B., Inagaki N., Thoenen H., and Lindholm D. (1995) Characterization of TrkB receptor-mediated signaling pathways in rat cerebellar granule neurons: involvement of protein kinase C in neuronal survival. J. Neurochem. 65, 2241-2250.