Lithium-induced activation of Akt and CaM kinase II contributes to its neuroprotective action in a rat microsphere embolism model

Brain Research

Volumn 1108, Issue 1, 2006, Pages 98-106

  Sasaki, Takuya ^a   Han, Feng ^a   Shioda, Norifumi ^a   Moriguchi, Shigeki ^a   Kasahara, Jiro ^a   Ishiguro, Koichi ^b   Fukunaga, Kohji ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b MITSUBISHI KAGAKU INSTITUTE OF LIFE SCIENCES   (Japan)

Author keywords

Akt; CaM kinase II; Glycogen synthase kinase 3 ; Lithium; Microsphere embolism

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM; MICROSPHERE; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE (CALCIUM,CALMODULIN) II; PROTEIN KINASE B BETA; TAU PROTEIN; TRANSCRIPTION FACTOR FKHR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHOSPHORYLATION; BRAIN EMBOLISM; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXPERIMENTAL MODEL; EXPERIMENTAL RAT; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; ANTIMANIC AGENTS; BRAIN INFARCTION; BRAIN ISCHEMIA; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASES; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FORKHEAD TRANSCRIPTION FACTORS; GLYCOGEN SYNTHASE KINASE 3; INTRACRANIAL EMBOLISM; LITHIUM CHLORIDE; MALE; NERVE TISSUE PROTEINS; NEUROPROTECTIVE AGENTS; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASES; PROTEIN PHOSPHATASE 2; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; SERINE; TAU PROTEINS; UP-REGULATION;

EID: 33747786681     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2006.06.009     Document Type: Article

References (49)

1. Agarwal-Mawal A., Qureshi H.Y., Cafferty P.W., Yuan Z., Han D., Lin R., and Paudel H.K. 14-3-3 connects glycogen synthase kinase-3 beta to tau within a brain microtubule-associated tau phosphorylation complex. J. Biol. Chem. 278 (2003) 12722-12728
2. Bennecib M., Gong C.X., Grundke-Iqbal I., and Iqbal K. Role of protein phosphatase-2A and -1 in the regulation of GSK-3, cdk5 and cdc2 and the phosphorylation of tau in rat forebrain. FEBS. Lett. 485 (2000) 87-93
3. Bhat R.V., Shanley J., Correll M.P., Fieles W.E., Keith R.A., Scott C.W., and Lee C.W. Regulation and localization of tyrosine216 phosphorylation of glycogen synthase kinase-3β in cellular and animal models of neuronal degeneration. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 11074-11079
4. Bhat R.V., Budd Haeberlein S.L., and Avila J. Glycogen synthase kinase3: a drug target for CNS therapies. J. Neurochem. 89 (2004) 1313-1317
5. Billingsley M.L., and Kincaid R.L. Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneration. Biochem. J. 323 (1997) 577-591
6. Blomgren K., Kawashima S., Saido T.C., Karlsson J.O., Elmered A., and Hagberg H. Fodrin degradation and subcellular distribution of calpains after neonatal rat cerebral hypoxic-ischemia. Brain Res. 684 (1995) 143-149
7. Burgering B.M., and Kops G.J. Cell cycle and death control: long live forkheads. Trends Biochem. Sci. 27 (2002) 352-360
8. 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
9. Chalecka-Franaszek E., and Chuang D.M. Lithium activates the serine/threonine kinase Akt-1 and suppresses glutamate-induced inhibition of Akt-1 activity in neurons. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 8745-8750
10. Chuang D.M., Chen R.W., Chalecka-Franaszek E., Ren M., Hashimoto R., Senatorov V., Kanai H., Hough C., Hiroi T., and Leeds P. Neuroprotective effect of lithium in cultured cells and animal models of diseases. Bipolar Disord. 4 (2002) 129-136
11. 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
12. Fukunaga K. Signal transduction and development of drug for ischemic insult. Nippon Yakurigaku Zasshi 122 (2003) 22-24
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. Fukunaga K., and Miyamoto E. A working model of CaM kinase II activity in hippocampal long-term potentiation and memory. Neurosci. Res. 38 (2003) 3-17
15. 2+- and calmodulin-dependent protein kinase from rat brain. J. Neurochem. 391 (1982) 607-1617
16. Fukunaga K., Sato H., Takatsu K., Tominaga A., and Miyamoto E. Monoclonal antibody against a multifunctional calmodulin-dependent protein kinase from rat brain and the tissue distribution of the enzyme. Biomed. Res. 7 (1986) 405-413
17. Fukunaga K., Muller D., Ohmitsu M., Bako E., DePaoli-Roach AA., and Miyamoto E. Decreased protein phosphatase 2A activity in hippocampal long-term potentiation. J. Neurochem. 74 (2000) 807-817
18. 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
19. Haque N., Gong C.X., Sengupta A., Iqbal K., and Grundke-Iqbal I. Regulation of microtubule-associated proteins, protein kinases and protein phosphatases during differentiation of SY5Y cells. Mol. Brain Res. 129 (2004) 163-170
20. Hashiguchi A., Yano S., Morioka M., Hamada J., Shirasaki Y., Kochi M., and Fukunaga K. The post-ischemic administration of 3-[2-[4-(3-chloro-2-methylphenyl)-1-piperazinyl]ethyl]-5,6-dimethoxy-1-(4-imidazolylmethyl)-1H-indazole dihydrochloride 3.5 hydrate (DY-9760e), a novel calmodulin antagonist, prevents delayed neuronal death in gerbil hippocampus. J. Pharmacol. Sci. 96 (2004) 65-72
21. Hong M., Chen D.C., Klein P.S., and Lee V.M. Lithium reduces tau phosphorylation by inhibition of glycogen synthase kinase-3. J. Biol. Chem. 40 (1997) 25326-25332
22. Ishiguro K., Takamatsu M., Park J., Uchida T., and Imahori K. Analysis of phosphorylation of tau with antibodies specific for phosphorylation sites. Neurosci. Lett. 202 (1995) 81-84
23. Kang H.J., Noh J.S., Bae Y.S., and Gwag B.J. Calcium-dependent prevention of neuronal apoptosis by lithium ion: essential role of phosphoinositide 3-kinase and phospholipase C gamma. Mol. Pharmacol. 64 (2003) 228-234
24. 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
25. 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
26. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
27. Mailliot C., Podevin-Dimster V., Rosenthal R.E., Sergeant N., Delacourte A., Fiskum G., and Buee L. Rapid tau protein dephosphorylation and differential rephosphorylation during cardiac arrest-induced cerebral ischemia and reperfusion. J. Cereb. Blood Flow Metab. 20 (2000) 543-549
28. Miyake K., Takeo S., and Kaijihara H. Sustained decrease in brain regional blood flow after microsphere embolism in rats. Stroke 24 (1993) 415-420
29. + deprivation in cerebellar granule cells. J. Neurochem. 78 (2001) 199-206
30. Mora A., Sabio G., Risco A.M., Cuenda A., Alonso J.C., Soler G., and Centeno F. Lithium blocks the PKB and GSK3 dephosphorylation induced by ceramide through protein phosphatase-2A. Cell Signalling 14 (2002) 557-562
31. 2+/calmodulin-dependent protein kinase II and calcineurin in the hippocampus of rat brain after transient forebrain ischemia. J. Neurochem. 58 (1992) 1798-1809
32. Nonaka S., and Chuang D.M. Neuroprotective effects of chronic lithium on focal cerebral ischemia in rats. NeuroReport 9 (1998) 2081-2084
33. Nonaka S., Katsube N., and Chuang D.M. Lithium protects rat cerebellar granule cells against apoptosis induced by anticonvulsants, phenytoin and carbamazepine. J. Pharmacol. Exp. Ther. 286 (1998) 539-547
34. 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
35. Ren M., Senatorov V.V., Chen R.W., and Chuang D.M. Postinsult treatment with lithium reduces brain damage and facilitates neurological recovery in a rat ischemia/reperfusion model. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 6210-6215
36. 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
37. Shackelford D.A., and Nelson K.E. Changes in phosphorylation of tau during ischemia and reperfusion in the rabbit spinal cord. J. Neurochem. 66 (1996) 286-295
38. Shackelford D.A., and Yeh R.Y. Dephosphorylation of tau during transient forebrain ischemia in the rat. Mol. Chem. Teuropathol. 34 (1998) 103-120
39. Shirakura T., Han F., Shiota N., Moriguchi S., Kasahara J., Sato T., Shirasaki Y., and Fukunaga K. Inhibition of nitric oxide production and protein tyrosine nitration contribute to neuroprotection by a novel calmodulin antagonist, DY-9760e, in the rat microsphere embolism. Biol. Pharm. Bull. 28 (2005) 1658-1661
40. Song J.S., and Yang S.D. Tau protein kinase l/GSK-3beta/kinase FA in heparin phosphorylates tau on Ser199, Thr231, Ser235, Ser262, Ser369, and Ser400 sites phosphorylated in Alzheimer disease brain. J. Protein. Chem. 14 (1995) 95-105
41. 2+-calmodulin dependent kinase and relationship with tau phosphorylation in Alzheimer tangles. EMBO J. 9 (1990) 3539-3544
42. 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
43. Takagaki Y., Itoh Y., Aoki Y., Ukai Y., Yoshikuni Y., and Kimura K. Inhibition of ischemia-induced fodrin breakdown by a novel phenylpyrimidine derivative NS-7: an implication for its neuroprotective action in rats with middle cerebral artery occlusion. J. Neurochem. 68 (1997) 2507-2513
44. Wang Y.J., Chen G.H., Hu X.Y., Lu Y.P., Zhou J.N., and Liu R.Y. The expression of calcium/calmodulin-dependent protein kinase II-alpha in the hippocampus of patients with Alzheimer's disease and its links with AD-related pathology. Brain Res. 1031 (2005) 101-108
45. Williams R.S., and Harwood A.J. Lithium therapy and signal transduction. Trends Pharmacol. Sci. 21 (2000) 61-64
46. Xing G., Russell S., Hough C., O'Grady J., Zhang L., Yang S., Zhang L.X., and Post R. Decreased prefrontal CaMKII alpha mRNA in bipolar illness. NeuroReport. 13 (2002) 501-505
47. Xu J., Culman J., Blume A., Brecht S., and Gohlke P. Chronic treatment with a low dose of lithium protects the brain against ischemic injury by reducing apoptotic death. Stroke 34 (2003) 1287-1292
48. Zhang J., and Johnson G.V. Tau protein hyperphosphorylated in a site-specific manner in apoptotic neuronal PC12 cells. J. Neurochem. 75 (2000) 2346-2357
49. Zhang F., Phiel C.J., Spece L., Gurvich N., and Klein P.S. Inhibitory phosphorylation of glycogen synthase kinase-3 (GSK-3) in response to lithium. J. Biol. Chem. 278 (2003) 33067-33077