Activation of phosphatidylinositol 3-kinase/protein kinase B pathway by a vanadyl compound mediates its neuroprotective effect in mouse brain ischemia

Neuroscience

Volumn 148, Issue 1, 2007, Pages 221-229

  Shioda, N ^a   Ishigami, T ^a   Han, F ^a   Moriguchi, S ^a   Shibuya, M ^a   Iwabuchi, Y ^a   Fukunaga, K ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

Akt; brain ischemia; Fas ligand; FOXO; neuronal death; vanadyl compound

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BIM PROTEIN; BIS(1 OXY 2 PYRIDINETHIOLATO)OXOVANADIUM; CASPASE 3; FAS LIGAND; ORTHOVANADIC ACID; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN AFX; PROTEIN KINASE B; PROTEIN TYROSINE PHOSPHATASE; SERINE; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG; VANADATE SODIUM; VANADIC ACID; VANADYL DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; DIARRHEA; DOSE RESPONSE; DRUG CYTOTOXICITY; DRUG DOSE INCREASE; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS REGULATORY PROTEINS; BRAIN; BRAIN INFARCTION; BRAIN ISCHEMIA; CASPASE 3; CELL DEATH; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; FAS LIGAND PROTEIN; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; VANADATES;

EID: 34547663611     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.05.040     Document Type: Article

References (44)

1. Biggs III W.H., Meisenhelder J., Hunter T., Cavenee W.K., and Arden K.C. Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc Natl Acad Sci U S A 96 (1999) 7421-7426
2. Bouillet P., Metcalf D., Huang D.C., Tarlinton D.M., Kay T.W., Kontgen F., Adams J.M., and Strasser A. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286 (1999) 1735-1738
3. Brunet A., Bonni A., Zigmond M.J., Lin M.Z., Juo P., Hu L.S., Anderson M.J., Arden K.C., Blenis J., and Greenberg M.E. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96 (1999) 857-868
4. Cantley Jr. L.C., Josephson L., Warner R., Yanagisawa M., Lechene C., and Guidotti G. Vanadate is a potent (Na,K)-ATPase inhibitor found in ATP derived from muscle. J Biol Chem 252 (1977) 7421-7423
5. Cantley Jr. L.C., and Aisen P. The fate of cytoplasmic vanadium. Implications on (NA,K)-ATPase inhibition J. Biol Chem 254 (1979) 1781-1784
6. Cardone M.H., Roy N., Stennicke H.R., Salvesen G.S., Franke T.F., Stanbridge E., Frisch S., and Reed J.C. Regulation of cell death protease caspase-9 by phosphorylation. Science 282 (1998) 1318-1321
7. Ciechomska I., Pyrzynska B., Kazmierczak P., and Kaminska B. Inhibition of Akt kinase signalling and activation of Forkhead are indispensable for upregulation of FasL expression in apoptosis of glioma cells. Oncogene 22 (2003) 7617-7627
8. Cohen N., Halberstam M., Shlimovich P., Chang C.J., Shamoon H., and Rossetti L. Oral vanadyl sulfate improves hepatic and peripheral insulin sensitivity in patients with non-insulin-dependent diabetes mellitus. J Clin Invest 95 (1995) 2501-2509
9. Datta S.R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y., and Greenberg M.E. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91 (1997) 231-241
10. Dijkers P.F., Medema R.H., Lammers J.W., Koenderman L., and Coffer P.J. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr Biol 10 (2000) 1201-1204
11. Essafi A., Fernandez de Mattos S., Hassen Y.A., Soeiro I., Mufti G.J., Thomas N.S., Medema R.H., and Lam E.W. Direct transcriptional regulation of Bim by FoxO3a mediates STI571-induced apoptosis in Bcr-Abl-expressing cells. Oncogene 24 (2005) 2317-2329
12. Fukunaga K., Ishigami T., and Kawano T. Transcriptional regulation of neuronal genes and its effect on neural functions: expression and function of forkhead transcription factors in neurons. J Pharmacol Sci 98 (2005) 205-211
13. Fukunaga K., and Kawano T. Akt is a molecular target for signal transduction therapy in brain ischemic insult. J Pharmacol Sci 92 (2003) 317-327
14. Goldfine A.B., Simonson D.C., Folli F., Patti M.E., and Kahn C.R. In vivo and in vitro studies of vanadate in human and rodent diabetes mellitus. Mol Cell Biochem 153 (1995) 217-231
15. Han F., Shirasaki Y., and Fukunaga K. 3-[2-[4-(3-Chloro-2-methylphenylmethyl)-1-piperazinyl]ethyl]-5,6-dimethoxy-1-(4-imidazolylmethyl)-1H-indazole dihydro-chloride 3.5 hydrate (DY-9760e) is neuroprotective in rat microsphere embolism: role of the cross-talk between calpain and caspase-3 through calpastatin. J Pharmacol Exp Ther 317 (2006) 529-536
16. Hasegawa Y., Hamada J., Morioka M., Yano S., Kawano T., Kai Y., Fukunaga K., and Ushio Y. Neuroprotective effect of postischemic administration of sodium orthovanadate in rats with transient middle cerebral artery occlusion. J Cereb Blood Flow Metab 23 (2003) 1040-1051
17. Hasegawa Y., Morioka M., Hasegawa S., Matsumoto J., Kawano T., Kai Y., Yano S., Fukunaga K., and Kuratsu J.I. Therapeutic time window and dose dependence of neuroprotective effects of sodium orthovanadate following transient middle cerebral artery occlusion in rats. J Pharmacol Exp Ther 317 (2006) 875-881
18. Hashiguchi A., Yano S., Morioka M., Hamada J., Ushio Y., Takeuchi Y., and Fukunaga K. Up-regulation of endothelial nitric oxide synthase via phosphatidylinositol 3-kinase pathway contributes to ischemic tolerance in the CA1 subfield of gerbil hippocampus. J Cereb Blood Flow Metab 24 (2004) 271-279
19. Holtz-Heppelmann C.J., Algeciras A., Badley A.D., and Paya C.V. Transcriptional regulation of the human FasL promoter-enhancer region. J Biol Chem 273 (1998) 4416-4423
20. Jin K., Graham S.H., Mao X., Nagayama T., Simon R.P., and Greenberg D.A. Fas (CD95) may mediate delayed cell death in hippocampal CA1 sector after global cerebral ischemia. J Cereb Blood Flow Metab 21 (2001) 1411-1421
21. Kawano T., Fukunaga K., Takeuchi Y., Morioka M., Yano S., Hamada J., Ushio Y., and Miyamoto E. Neuroprotective effect of sodium orthovanadate on delayed neuronal death after transient forebrain ischemia in gerbil hippocampus. J Cereb Blood Flow Metab 21 (2001) 1268-1280
22. Kawano T., Morioka M., Yano S., Hamada J., Ushio Y., Miyamoto E., and Fukunaga K. Decreased Akt activity is associated with activation of Forkhead transcription factor after transient forebrain ischemia in gerbil hippocampus. J Cereb Blood Flow Metab 22 (2002) 926-934
23. Lin K., Dorman J.B., Rodan A., and Kenyon C. daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278 (1997) 1319-1322
24. Medema J.P., Scaffidi C., Kischkel F.C., Shevchenko A., Mann M., Krammer P.H., and Peter M.E. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO J 16 (1997) 2794-2804
25. Muzio M., Chinnaiyan A.M., Kischkel F.C., O'Rourke K., Shevchenko A., Ni J., Scaffidi C., Bretz J.D., Zhang J., Gentz R., Mann M., Krammer P.H., Peter M.E., and Dixit V.M. Flice, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (FAS/APO-1) death-inducing signaling complex. Cell 85 (1996) 817-827
26. O'Reilly L.A., Cullen L., Visvader J., Lindeman G.J., Print C., Bath M.L., Huang D.C., and Strasser A. The proapoptotic BH3-only protein bim is expressed in hematopoietic, epithelial, neuronal, and germ cells. Am J Pathol 157 (2000) 449-461
27. Pap M., and 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
28. Reul B.A., Amin S.S., Buchet J.P., Ongemba L.N., Crans D.C., and Brichard S.M. Effects of vanadium complexes with organic ligands on glucose metabolism: a comparison study in diabetic rats. Br J Pharmacol 126 (1999) 467-477
29. Rodriguez J., and Lazebnik Y. Caspase-9 and APAF-1 form an active holoenzyme. Genes Dev 13 (1999) 3179-3184
30. Saido T.C., Yokota M., Nagao S., Yamaura I., Tani E., Tsuchiya T., Suzuki K., and Kawashima S. Spatial resolution of fodrin proteolysis in postischemic brain. J Biol Chem 268 (1993) 25239-25243
31. Sakurai H., Sano H., Takino T., and Yasui H. An orally active antidiabetic vanadyl complex, bis(1-oxy-2-pyridinethiolato)oxovanadium(IV), with VO(S2O2) coordination mode; in vitro and in vivo evaluations in rats. J Inorg Biochem 80 (2000) 99-105
32. Sato T., Morishima Y., Sugimura M., Uchida T., and Shirasaki Y. DY-9760e, a novel calmodulin antagonist, reduces brain damage induced by transient focal cerebral ischemia. Eur J Pharmacol 370 (1999) 117-123
33. Scaffidi C., Fulda S., Srinivasan A., Friesen C., Li F., Tomaselli K.J., Debatin K.M., Krammer P.H., and Peter M.E. Two CD95 (APO-1/Fas) signaling pathways. EMBO J 17 (1998) 1675-1687
34. Schabitz W.R., and Fisher M. Perspectives on neuroprotective stroke therapy. [review]. Biochem Soc Trans 34 (2006) 1271-1276
35. Schreiber E., Matthias P., Muller M.M., and Schaffner W. Rapid detection of octamer binding proteins with "mini-extracts," prepared from a small number of cells. Nucleic Acids Res 17 (1989) 6419
36. Shibata M., Hattori H., Sasaki T., Gotoh J., Hamada J., and Fukuuchi Y. Temporal profiles of the subcellular localization of Bim, a BH3-only protein, during middle cerebral artery occlusion in mice. J Cereb Blood Flow Metab 22 (2002) 810-820
37. Siman R., Card J.P., and Davis L.G. Proteolytic processing of beta-amyloid precursor by calpain I. J Neurosci 10 (1990) 2400-2411
38. Swarup G., Cohen S., and Garbers D.L. Inhibition of membrane phosphotyrosyl-protein phosphatase activity by vanadate. Biochem Biophys Res Commun 107 (1982) 1104
39. Takada Y., Hashimoto M., Kasahara J., Aihara K., and Fukunaga K. Cytoprotective effect of sodium orthovanadate on ischemia/reperfusion-induced injury in the rat heart involves Akt activation and inhibition of fodrin breakdown and apoptosis. J Pharmacol Exp Ther 311 (2004) 1249-1255
40. Towbin H., Staehelin T., and Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76 (1979) 4350-4354
41. Vijaya S., Crane F.L., and Ramasarma T. A vanadate-stimulated NADH oxidase in erythrocyte membrane generates hydrogen peroxide. Mol Cell Biochem 62 (1984) 175-185
42. White B.C., Sullivan J.M., DeGracia D.J., O'Neil B.J., Neumar R.W., Grossman L.I., Rafols J.A., and Krause G.S. Brain ischemia and reperfusion: molecular mechanisms of neuronal injury. J Neurol Sci 179 (2000) 1-33
43. Yano S., Morioka M., Fukunaga K., Kawano T., Hara T., Kai Y., Hamada J., Miyamoto E., and Ushio Y. Activation of Akt/protein kinase B contributes to induction of ischemic tolerance in the CA1 subfield of gerbil hippocampus. J Cereb Blood Flow Metab 21 (2001) 351-360
44. Zou H., Henzel W.J., Liu X., Lutschg A., and Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90 (1997) 405-413