Glycogen synthase kinase 3β inhibitor Chir025 reduces neuronal death resulting from oxygen-glucose deprivation, glutamate excitotoxicity, and cerebral ischemia

Experimental Neurology

Volumn 188, Issue 2, 2004, Pages 378-386

  Kelly, Stephen ^a,c   Zhao, Heng ^a   Sun, Guo Hua ^a   Cheng, Danye ^a   Qiao, Yanli ^a   Luo, Jian ^b   Martin, Kathleen ^b   Steinberg, Gary K ^a   Harrison, Stephen D ^b   Yenari, Midori A ^a  

^a STANFORD UNIVERSITY   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Focal cerebral ischemia; Glutamate toxicity; Glycogen kinase synthase 3 ; Neuroprotection; Oxygen glucose deprivation; Stroke

Indexed keywords

CASPASE 3; CASPASE 9; GLUCOSE; GLUTAMIC ACID; GLYCOGEN SYNTHASE KINASE 3BETA; OXYGEN; PROTEIN BCL 2; PROTEIN SERINE KINASE; SERINE; THREONINE;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN INFARCTION; BRAIN ISCHEMIA; CONTROLLED STUDY; CYTOSOL; DECORTICATION; ENZYME ACTIVITY; ENZYME INHIBITION; FETUS; HIPPOCAMPUS; IN VITRO STUDY; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; RAT; STATISTICAL SIGNIFICANCE;

ANIMALS; BRAIN CHEMISTRY; BRAIN ISCHEMIA; CASPASES; CELL DEATH; CELL HYPOXIA; CELLS, CULTURED; CYTOSOL; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; GLUCOSE; GLUTAMIC ACID; GLYCOGEN SYNTHASE KINASE 3; IN SITU NICK-END LABELING; MALE; MICE; NEURONS; NEUROPROTECTIVE AGENTS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY;

EID: 3042749593     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2004.04.004     Document Type: Article

References (49)

1. Bhat R.V., Shanley J., Correll M.P., Fieles W.E., Keith R.A., Scott C.W., Lee C.M. Regulation and localization of tyrosine216 phosphorylation of glycogen synthase kinase-3beta in cellular and animal models of neuronal degeneration. Proc. Natl. Acad. Sci. U. S. A. 97:2000;11074-11079
2. Bijur G.N., De Sarno P., Jope R.S. Glycogen synthase kinase-3beta facilitates staurosporine- and heat shock-induced apoptosis Protection by lithium. J. Biol. Chem. 275:2000;7583-7590
3. Bijur G.N., Jope R.S. Opposing actions of phosphatidylinositol 3-kinase and glycogen synthase kinase-3beta in the regulation of HSF-1 activity. J. Neurochem. 75:2000;2401-2408
4. Brownlees J., Irving N.G., Brion J.P., Gibb B.J., Wagner U., Woodgett J., Miller C.C. Tau phosphorylation in transgenic mice expressing glycogen synthase kinase-3beta transgenes. Neuroreport. 8:1997;3251-3255
5. Chao D.T., Korsmeyer S.J. BCL-2 family: regulators of cell death. Annu. Rev. Immunol. 16:1998;395-419
6. Chuang D.M., Chen R.W., Chalecka-Franaszek E., Ren M., Hashimoto R., Senatorov V., Kanai H., Hough C., Hiroi T., Leeds P. Neuroprotective effects of lithium in cultured cells and animal models of diseases. Bipolar Disord. 4:2002;129-136
7. Cross D.A., Culbert A.A., Chalmers K.A., Facci L., Skaper S.D., Reith A.D. Selective small-molecule inhibitors of glycogen synthase kinase-3 activity protect primary neurones from death. J. Neurochem. 77:2001;94-102
8. Dugan L.L., Bruno V.M., Amagasu S.M., Giffard R.G. Glia modulate the response of murine cortical neurons to excitotoxicity: glia exacerbate AMPA neurotoxicity. J. Neurosci. 15:1995;4545-4555
9. Embi N., Rylatt D.B., Cohen P. Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase. Eur. J. Biochem. 107:1980;519-527
10. Frame S., Cohen P. GSK3 takes centre stage more than 20 years after its discovery. Biochem. J. 359:2001;1-16
11. Grabb M.C., Choi D.W. Ischemic tolerance in murine cortical cell culture: critical role for NMDA receptors. J. Neurosci. 19:1999;1657-1662
12. Graham S.H., Chen J. Programmed cell death in cerebral ischemia. J. Cereb. Blood Flow Metab. 21:2001;99-109
13. Gross A., McDonnell J.M., Korsmeyer S.J. BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13:1999;1899-1911
14. Hanger D.P., Betts J.C., Loviny T.L., Blackstock W.P., Anderton B.H. New phosphorylation sites identified in hyperphosphorylated tau (paired helical filament-tau) from Alzheimer's disease brain using nanoelectrospray mass spectrometry. J. Neurochem. 71:1998;2465-2476
15. Hanger D.P., Hughes K., Woodgett J.R., Brion J.P., Anderton B.H. Glycogen synthase kinase-3 induces Alzheimer's disease-like phosphorylation of tau: generation of paired helical filament epitopes and neuronal localisation of the kinase. Neurosci. Lett. 147:1992;58-62
16. Hemmings B.A., Yellowlees D., Kernohan J.C., Cohen P. Purification of glycogen synthase kinase 3 from rabbit skeletal muscle. Copurification with the activating factor (FA) of the (Mg-ATP) dependent protein phosphatase. Eur. J. Biochem. 119:1981;443-451
17. Hetman M., Cavanaugh J.E., Kimelman D., Xia Z. Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 20:2000;2567-2574
18. Hoehn B., Ringer T.M., Xu L., Giffard R.G., Sapolsky R.M., Steinberg G.K., Yenari M.A. Overexpression of HSP72 after induction of experimental stroke protects neurons from ischemic damage. J. Cereb. Blood Flow Metab. 21:2001;1303-1309
19. Ishiguro K., Shiratsuchi A., Sato S., Omori A., Arioka M., Kobayashi S., Uchida T., Imahori K. Glycogen synthase kinase 3 beta is identical to tau protein kinase I generating several epitopes of paired helical filaments. FEBS. Lett. 325:1993;167-172
20. Johnson J.A., Mochly-Rosen D. Inhibition of the spontaneous rate of contraction of neonatal cardiac myocytes by protein kinase C isozymes. A putative role for the epsilon isozyme. Circ. Res. 76:1995;654-663
21. Kane D.J., Ord T., Anton R., Bredesen D.E. Expression of bcl-2 inhibits necrotic neural cell death. J. Neurosci. Res. 40:1995;269-275
22. Kaytor M.D., Orr H.T. The GSK3 beta signaling cascade and neurodegenerative disease. Curr. Opin. Neurobiol. 12:2002;275-278
23. Kelly S., Bieneman A., Horsburgh K., Hughes D., Sofroniew M.V., McCulloch J., Uney J.B. Targeting expression of hsp70i to discrete neuronal populations using the Lmo-1 promoter: assessment of the neuroprotective effects of hsp70i in vivo and in vitro. J. Cereb. Blood Flow Metab. 21:2001;972-981
24. Kelly S., Yenari M.A. Neuroprotection: heat shock proteins. Curr. Med. Res. Opin. 18(Suppl. 2):2002;s55-s60
25. Kelly S., Zhang Z.J., Zhao H., Xu L., Giffard R.G., Sapolsky R.M., Yenari M.A., Steinberg G.K. Gene transfer of HSP72 protects cornu ammonis 1 region of the hippocampus neurons from global ischemia: influence of Bcl-2. Ann. Neurol. 52:2002;160-167
26. Koh J.Y., Choi D.W. Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J. Neurosci. Methods. 20:1987;83-90
27. Lee J.E., Yenari M.A., Sun G.H., Xu L., Emond M.R., Cheng D., Steinberg G.K., Giffard R.G. Differential neuroprotection from human heat shock protein 70 overexpression in in vitro and in vivo models of ischemia and ischemia-like conditions. Exp. Neurol. 170:2001;129-139
28. Leroy K., Brion J.P. Developmental expression and localization of glycogen synthase kinase-3beta in rat brain. J. Chem. Neuroanat. 16:1999;279-293
29. Lovestone S., Reynolds C.H., Latimer D., Davis D.R., Anderton B.H., Gallo J.M., Hanger D., Mulot S., Marquardt B., Stabel S., et al. Alzheimer's disease-like phosphorylation of the microtubule-associated protein tau by glycogen synthase kinase-3 in transfected mammalian cells. Curr. Biol. 4:1994;1077-1086
30. Lucas J.J., Hernandez F., Gomez-Ramos P., Moran M.A., Hen R., Avila J. Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. Embo. J. 20:2001;27-39
31. Mandelkow E.M., Drewes G., Biernat J., Gustke N., Van Lint J., Vandenheede J.R., Mandelkow E. Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS. Lett. 314:1992;315-321
32. Manji H.K., Moore G.J., Chen G. Lithium at 50: have the neuroprotective effects of this unique cation been overlooked? Biol. Psychiatry. 46:1999;929-940
33. Mukai F., Ishiguro K., Sano Y., Fujita S.C. Alternative splicing isoform of tau protein kinase I/glycogen synthase kinase 3beta. J. Neurochem. 81:2002;1073-1083
34. Namura S., Zhu J., Fink K., Endres M., Srinivasan A., Tomaselli K.J., Yuan J., Moskowitz M.A. Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J. Neurosci. 18:1998;3659-3668
35. Nonaka S., Chuang D.M. Neuroprotective effects of chronic lithium on focal cerebral ischemia in rats. Neuroreport. 9:1998;2081-2084
36. Pap M., Cooper G.M. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway. J. Biol. Chem. 273:1998;19929-19932
37. Ring D.B., Johnson K.W., Henriksen E.J., Nuss J.M., Goff D., Kinnick T.R., Ma S.T., Reeder J.W., Samuels I., Slabiak T., Wagman A.S., Hammond M.E., Harrison S.D. Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes. 52:2003;588-595
38. Rylatt D.B., Aitken A., Bilham T., Condon G.D., Embi N., Cohen P. Glycogen synthase from rabbit skeletal muscle. Amino acid sequence at the sites phosphorylated by glycogen synthase kinase-3, and extension of the N-terminal sequence containing the site phosphorylated by phosphorylase kinase. Eur. J. Biochem. 107:1980;529-537
39. Sasaki C., Hayashi T., Zhang W.R., Warita H., Manabe Y., Sakai K., Abe K. Different expression of glycogen synthase kinase-3beta between young and old rat brains after transient middle cerebral artery occlusion. Neurol. Res. 23:2001;588-592
40. Takashima A., Noguchi K., Michel G., Mercken M., Hoshi M., Ishiguro K., Imahori K. Exposure of rat hippocampal neurons to amyloid beta peptide (25-35) induces the inactivation of phosphatidyl inositol-3 kinase and the activation of tau protein kinase I/glycogen synthase kinase-3 beta. Neurosci. Lett. 203:1996;33-36
41. Takashima A., Honda T., Yasutake K., Michel G., Murayama O., Murayama M., Ishiguro K., Yamaguchi H. Activation of tau protein kinase I/glycogen synthase kinase-3beta by amyloid beta peptide (25-35) enhances phosphorylation of tau in hippocampal neurons. Neurosci. Res. 31:1998;317-323
42. Wang J.M., Hayashi T., Zhang W.R., Sakai K., Shiro Y., Abe K. Reduction of ischemic brain injury by topical application of insulin-like growth factor-I after transient middle cerebral artery occlusion in rats. Brain Res. 859:2000;381-385
43. Woodgett J.R. Molecular cloning and expression of glycogen synthase kinase-3/factor A. Embo. J. 9:1990;2431-2438
44. Woodgett J.R. Judging a protein by more than its name: GSK-3. Sci. STKE. RE12:2001;1-11
45. Yenari M.A., Fink S.L., Sun G.H., Chang L.K., Patel M.K., Kunis D.M., Onley D., Ho D.Y., Sapolsky R.M., Steinberg G.K. Gene therapy with HSP72 is neuroprotective in rat models of stroke and epilepsy. Ann. Neurol. 44:1998;584-591
46. Yenari M.A., Onley D., Hedehus M., deCrespigny A., Sun G.H., Moseley M.E., Steinberg G.K. Diffusion- and perfusion-weighted magnetic resonance imaging of focal cerebral ischemia and cortical spreading depression under conditions of mild hypothermia. Brain Res. 885:2000;208-219
47. Yenari M.A., Palmer J.T., Sun G.H., de Crespigny A., Mosely M.E., Steinberg G.K. Time-course and treatment response with SNX-111, an N-type calcium channel blocker, in a rodent model of focal cerebral ischemia using diffusion-weighted MRI. Brain Res. 739:1996;36-45
48. Zhang Z., Sobel R.A., Cheng D., Steinberg G.K., Yenari M.A. Mild hypothermia increases Bcl-2 protein expression following global cerebral ischemia. Brain Res. Mol. Brain Res. 95:2001;75-85
49. Zhao H., Yenari M.A., Cheng D., Sapolsky R.M., Steinberg G.K. Bcl-2 overexpression protects against neuron loss within the ischemic margin following experimental stroke and inhibits cytochrome c translocation and caspase-3 activity. J. Neurochem. 85:2003;1026-1036