Glycogen Synthase Kinase 3: Role in Neurodegeneration and Neuroprotection

Glycogen Synthase Kinase 3 (GSK-3) and Its Inhibitors: Drug Discovery and Development

Volumn , Issue , 2006, Pages 173-187

  Facci, Laura ^a   Skaper, Stephen D ^a  

^a GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Amyotrophic lateral sclerosis (ALS); GSK 3 and neurodegeneration; GSK 3 inhibitors and neuroprotection

Indexed keywords

EID: 41749121323     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470052174.ch9     Document Type: Chapter

References (80)

1. Raff M.C., Barres B.A., Burne J., Coles H.S., Ishizaki Y., Jacobson M.D. (1993). Programmed cell death and the control of cell survival: lessons from the nervous system. Science, 262, 695-700.
2. Stefanis L., Burke R.E., Greene L.A. (1997). Apoptosis in neurodegenerative disorders. Curr. Opin. Neurobio., 10, 299-305.
3. Levi-Montalcini R. (1987). The nerve growth factor 35 years later. Science, 237, 1154-1162.
4. Datta S.R., Greenberg M.E. (1998). Molecular mechanisms of neuronal survival and apoptosis. In O'Malley B., ed., Hormones Signaling, San Diego: Academic Press, 257-306.
5. Yao R., Cooper G.M. (1995). Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science, 267, 2003-2006.
6. Miller T.M., Tansey M.G., Johnson E.M Jr., Creedon D.J. (1997). Inhibition of phosphatidylinositol 3-kinase activity blocks depolarization-and insulin-like growth factor I-mediated survival of cerebellar granule cells. J. Biol. Chem., 272, 9847-9853.
7. Crowder R.J., Freeman R.S. (1998). Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factordependent sympathetic neurons. J. Neurosci., 18, 2933-2943.
8. Dudek H., Datta S.R., Franke T.F., Birnbaum M.J., Yao R., Cooper G.M., Segal R.A., Kaplan D.R., Greenberg M.E. (1997). Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science, 275, 661-665.
9. Cross D.A., Alessi D.R., Cohen P., Andjelkovich M., Hemmings B.A. (1995). Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature, 378, 785-789.
10. Moule S.K., Welsh G.I., Edgell N.J., Foulstone E.J., Proud C.G., Denton R.M. (1997). Regulation of protein kinase B and glycogen synthase kinase-3 by insulin and beta-adrenergic agonists in rat epididymal fat cells: Activation of protein kinase B by wortmannin-sensitive and-insensitive mechanisms. J. Biol. Chem., 272, 7713-7719.
11. Pap M., Cooper G.M. (1998). Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J. Biol. Chem., 273, 19929-19932.
12. Hetman M., Cavanaugh J.E., Kimelman D., Xia Z. (2000). Role of glycogen synthase kinase-3ß in neuronal apoptosis induced by trophic withdrawal. J. Neurosci., 20, 2567-2574.
13. Bijur G.N., De Sarno P., Jope R.S. (2000). Glycogen synthease kinase-3ß facilitates staurosporine-and heat shock-induced apoptosis: Protection by lithium. J. Biol. Chem., 275, 7583-7590.
14. Woodgett J.R. (1990). Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J., 9, 2431-2438.
15. Delcommenne M., Tan C., Gray V., Rue L., Woodgett J., Dedhar S. (1998). Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proc. Nat. Acad. Sci. USA, 95, 11211-11216.
16. Kobayashi T., Cohen P. (1999). Activation of serum-and glucocorticoidregulated protein kinase by agonists that activate phosphatidylinositide 3-kinase is mediated by 3-phosphoinositide-dependent protein kinase-1 (PDK1) and PDK2. Biochem. J., 339, 319-328.
17. Crowder R.J., Freeman R.S. (2000). Glycogen synthase kinase-3ß activity is critical for neuronal death caused by inhibiting phosphatidylinositol 3-kinase or Akt but not for death caused by nerve growth factor withdrawal. J. Biol. Chem., 275, 34266-34271.
18. Frame S., Cohen P. (2001). GSK3 takes centre stage more than 20 years after its discovery. Biochem. J., 359, 1-16.
19. Selkoe D.J. (1997). Alzheimer's disease: genotypes, phenotype and treatments. Science, 275, 630-631.
20. Selkoe D.J. (2001). Alzheimer's disease: Genes, proteins, and therapy. Physiol. Rev., 81, 741-766.
21. Lee V.M., Goedert M., Trojanowski J.Q. (2001). Neurodegenerative tauopathies. An. Rev. Neurosci., 24, 1121-1159.
22. Ferrer I., Barrachina M., Puig B. (2002). Glycogen synthase kinase-3 is associated with neuronal and glial hyperphosphorylated Tau deposits in Alzheimer's disease, Pick's disease, progressive supranuclear palsy and corticobasal degeneration. Acta Neuropathol., 104, 583-591.
23. Shiurba R.A., Ishiguro K., Takahashi M., Sato K., Spooner E.T., Mercken M., Yoshida R., Wheelock T.R., Yanagawa H., Imahori K., Nixon R.A. (1996). Immunocytochemistry of tau phosphoserine 413 and Tau protein kinase I in Alzheimer pathology. Brain Res., 737, 119-132.
24. Pei J.J., Braak E., Braak H., Grundke-Iqbal I., Iqbal K., Winblad B., Cowburn R.F. (1999). Distribution of active glycogen synthase kinase 3ß (GSK-3ß) in brains staged for Alzheimer disease neurofibrillary changes. J. Neuropathol. Exp. Neurol., 58, 1010-1019.
25. Mandelkow E.M., Drewes G., Biernat J., Gustke N., Van Lint J., Vandenheede J.R., Mandelkow E. (1992). Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS Lett., 314, 315-321.
26. Leroy K., Boutajangout A., Authelet M., Woodgett J.R., Anderton B.H., Brion J.-P. (2002). The active form of glycogen synthase kinase-3ß is associated with granulovacuolar degeneration in neurons in Alzheimer's disease. Acta Neuropathol., 103, 91-99.
27. Lovestone S., Reynolds C.H., Latimer D., Davis D.R., Anderton B.H., Gallo J.-M., Hanger D., Mulot S., Marquardt B., Stabel S., Woodgett J.R., Miller C.C.J. (1994). Alzheimer's disease-like phosphorylation of the microtubule-associated protein tau by glycogen synthase kinase-3 in transfected mammalian cells. Curr. Biol., 4, 1077-1086.
28. Lucas J.J., Hernández F., Gómez-Ramos P., Morán M.A., Hen R., Avila J. (2001). Decreased nuclear ß-catenin, Tau hyperphosphorylation and neurodegeneration in GSK-3ß conditional transgenic mice. EMBO J., 20, 27-39.
29. Hernández F., Borrell J., Guaza C., Avila J., Lucas J.J. (2002). Spatial learning deficit in transgenic mice that conditionally over-express GSK-3ß in the brain but do not form tau filaments. J. Neurochem., 83, 1529-1533.
30. Jackson G.R., Wiedau-Pazos M., Sang T.-K., Wagle N., Brown C.A., Massachi S., Geschwind D.H. (2002). Human wild-type Tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron, 34, 509-519.
31. Liu S.J., Zhang A.H., Li H.L., Wang Q., Deng H.M., Netzer W.J., Xu H., Wang J.Z. (2003). Overactivation of glycogen synthase kinase-3 by inhibition of phosphoinositol-3 kinase and protein kinase C leads to hyperphosphorylation of Tau and impairment of spatial memory. J. Neurochem., 87, 1333-1344.
32. Hernández F., Pérez M., Lucas J.J., Mata A.M., Bhat R., Avila J. (2004). Glycogen synthase kinase-3 plays a crucial role in tau exon 10 splicing and intranuclear distribution of SC35: Implications for Alzheimer's disease. J. Biol. Chem., 279, 3801-3806.
33. Takashima A., Noguchi K., Michel G., Mercken M., Hoshi M., Ishiguro K., Imahori K. (1996). Exposure of rat hippocampal neurons to amyloid ß peptide (25-35) induces the inactivation of phosphatidyl inositol-3 kinase and the activation of Tau protein kinase I/glycogen synthase kinase-3ß. Neurosci. Lett., 203, 33-36.
34. Kim H.-S., Kim E.-M., Lee J.-P., Park C.H., Kim S., Seo J.-H., Chang K.-A., Yu E., Jeong S.-J., Chong Y.H., Suh Y.-H. (2003). C-terminal fragments of amyloid precursor protein exert neurotoxicity by inducing glycogen synthase kinase-3ß expression. FASEB J., Express Article doi: 10.1096/fj.03-010fje.
35. Hoshi M., Sato M., Matsumoto S., Noguchi A., Yasutake K., Yoshida N., Sato K. (2003). Spherical aggregates of ß-amyloid (amylospheroid) show high neurotoxicity and activate Tau protein kinase I/glycogen synthase kinase-3ß. Proc. Nat. Acad. Sci. USA, 100, 6370-6375.
36. Takashima A., Noguchi K., Sato K., Hoshino T., Imahori K. (1993). Tau protein kinase I is essential for amyloid ß-protein-induced neurotoxicity. Proc. Nat. Acad. Sci. USA, 90, 7789-7793.
37. Busciglio J., Lorenzo A., Yeh J., Yankner B.A. (1995). ß-Amyloid fibrils induce Tau phosphorylation and loss of microtubule binding. Neuron, 14, 879-888.
38. Alvarez G., Muñoz-Montaño J.R., Satrústegui J., Avila J., Bogónez E., Díaz-Nido J. (1999). Lithium protects cultured neurons against ß-amyloid-induced neurodegeneration. FEBS Lett., 453, 260-264.
39. Takashima A., Honda T., Yasutake K., Michel G., Murayama O., Murayama M., Ishiguro K., Yamaguchi H. (1998). Activation of Tau protein kinase I/glycogen synthase kinase-3ß by amyloid ß peptide (25-35) enhances phosphorylation of Tau in hippocampal neurons. Neurosci. Res., 31, 317-323.
40. Bhat R.V., Shanley J., Correll M.P., Fieles W.E., Keith R.A., Scott C.W., Lee C.-M. (2000). Regulation and localization of tyrosine 216 phosphorylation of glycogen synthase kinase-3ß in cellular and animal models of neuronal degeneration. Proc. Nat. Acad. Sci. USA, 97, 11074-11079.
41. Salinas P.C., Hall A.C. (1999). Lithium and synaptic plasticity. Bipolar Disord., 1, 87-90.
42. Grimes C.A., Jope R.S. (2001). The multifaceted roles of glycogen synthase kinase 3ß in cellular signalling. Progr. Neurobiol., 65, 391-426.
43. Prusiner S.B. (1998). Prions. Proc. Nat. Acad. Sci. USA, 95, 13363-13383.
44. Forloni F., Angeretti N., Chiesa R., Monzani E., Salmona M., Bugiani O., Tagliavini F. (1993). Neurotoxicity of a prion protein fragment. Nature, 362, 543-546.
45. Pérez M., Rojo A.I., Wandosell F., Díaz-Nido J., Avila J. (2003). Prion peptide induces neuronal cell death through a pathway involving glycogen synthase kinase 3. Biochem. J., 372, 129-136.
46. Sabatier J.M., Vives E., Mabrouk K., Benjouad A., Rochat H., Duval A., Hue B., Bahraoui E. (1991). Evidence for neurotoxic activity of tat from human immunodeficiency virus type 1. J. Viro., 65, 961-967.
47. Maggirwar S.B., Tong N., Ramirez S., Gelbard H.A., Dewhurst S. (1999). HIV-1 Tat-mediated activation of glycogen synthase kinase-3ß contributes to Tatmediated neurotoxicity. J. Neurochem., 73, 578-586.
48. Costall B., Naylor R.J. (1975). Neuropharmacological studies on D145 (1,3-dimethyl-5-aminoadamantan). Psychpharmacologia, 43, 53-56.
49. Chen G., Bower K.A., Ma C., Fang S., Thiele C.J., Luo J. (2004). Glycogen synthase kinase 3ß (GSK3ß) mediates 6-hydroxydopamine-induced neuronal death. FASEB J., 18, 1162-1164.
50. Kikuchi A. (1999). Roles of axin in the Wnt signalling pathway. Cell. Signal., 11, 777-788.
51. Ding V.W., Chen R.-H., McCormick F. (2000). Differential regulation of glycogen synthase kinase 3b by insulin and Wnt signalling. J. Biol. Chem., 275, 32475-32481.
52. Stambolic V., Ruel L., Woodgett J.R. (1996). Lithium inhibits glycogen synthase kinase-3 activity and mimics Wingless signalling in intact cells. Curr. Biol., 6, 1664-1668.
53. Pérez M., Hernández F., Lim F., Díaz-Nido J., Avila J. (2003). Chronic lithium treatment decreases mutant Tau protein aggregation in a transgenic mouse model. J. Alzheimer Dis., 5, 301-308.
54. Mudher A., Shepherd D., Newman T.A., Mildren P., Jukes J.P., Squire A., Mears A., Berg S., MacKay D., Asuni A.A., Bhat R., Lovestone S. (2004). GSK-3ß inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila. Mol. Psychiat., 9, 522-530.
55. Noble W., Planel E., Zehr C., Olm V., Meyerson J., Suleman F., Gaynor K., Wang D., LaFrancois J., Feinstein B., Burns M., Krishnamurthy P., Wen Y., Bhat R., Lewis J., Dickson D., Duff K. (2005). Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc. Nat. Acad. Sci. USA, 102, 6990-6995.
56. Phiel C.J., Wilson C.A., Lee V. M.-Y., Klein P.S. (2003). GSK-3a regulates production of Alzheimer's disease amyloid-ß peptides. Nature, 423, 435-439.
57. Everall I.P., Bell C., Mallory M., Langford D., Adame A., Rockestein E., Masliah E. (2002). Lithium ameliorates HIV-gp120-mediated neurotoxicity. Mol. Cell. Neurosci., 21, 493-501.
58. Chuang D.-M., Chen R.-W., Chalecka-Franaszek E., Ren M., Hashimoto R., Senatorov V., Kanai H., Hough C., Hiroi T., Leeds P. (2002). Neuroprotective effects of lithium in cultured cells and animal models of diseases. Bipolar Disord., 4, 129-136.
59. Goodenough S., Conrad S., Skutella T., Behl C. (2004). Inactivation of glycogen synthase kinase-3ß protects against kainic acid-induced neurotoxicity in vivo. Brain Res., 1026, 116-125.
60. Berridge M.J., Downes C.P., Hanley M.R. (1989). Neural and developmental actions of lithium: A unifying hypothesis. Cell, 59, 411-419.
61. Davies S.P., Reddy H., Caivano M., Cohen P. (2000). Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J., 351, 95-105.
62. Chalecka-Franaszek E., Chuang D.-M. (1999). Lithium activates the serine/threonine kinase Akt-1 and suppresses glutamate-induced inhibition of Akt-1 activity in neurons. Proc. Nat. Acad. Sci. USA, 96, 8745-8750.
63. Yuan P., Chen G., Manjii H.K. (1999). Lithium activates the c-Jun NH2-terminal kinases in vitro and in the CNS in vivo. J. Neurochem., 73, 2299-2309.
64. Meijer L., Flajolet M., Greengard P. (2004). Pharmacological inhibitors of glycogen synthase kinase 3. Trends Pharmacol. Sci., 25, 471-480.
65. Coghlan M.P., Culbert A.A., Cross D.A.E., Corcoran S.L., Yates J.W., Pearce N.J., Rausch O.L., Murphy G.J., Carter P.S., Cox L.R., Mills D., Brown M.J., Haigh D., Ward R.W., Smith D.G., Murray K.J., Reith A.D., Holder J.C. (2000). Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription. Chem. Biol., 7, 793-803.
66. Cross D.A.E., Culbert A.A., Chalmers K.A., Facci L., Skaper S.D., Reith A.D. (2001). Selective small-molecule inhibitors of glycogen synthase kinase-3 activity protect primary neurons from death. J. Neurochem., 77, 94-102.
67. Facci L., Stevens A., Pangallo M., Franceschini D., Skaper S.D., Strijbos P.J.L.M. (2003). Corticotropin-releasing factor (CRF) and related peptides confer neuroprotection via type 1 CRF receptors. Neuropharmacology, 45, 623-636.
68. Chin P.C., Majdzadeh N., D'Mello S.R. (2005). Inhibition of GSK3ß is a common event in neuroprotection by different survival factors. Mol. Brain Res., 137, 193-201.
69. Choi D.W. (1992). Excitotoxic cell death. J. Neurobiol., 23, 1261-1276.
70. Meldrum B., Garthwaite J. (1990). Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Pharmacol. Sci., 11, 379-387.
71. Blandini F., Porter R.H., Greenamyre J.T. (1996). Glutamate and Parkinson's disease. Mol. Neurobiol., 12, 73-94.
72. Facci L., Stevens D.A., Skaper S.D. (2003). Glycogen synthase kinase-3 inhibitors protect central neurons against excitotoxicity. NeuroReport, 14, 1467-1470.
73. Woodgett J.R. (1991). A common denominator linking glycogen metabolism, nuclear oncogenes and development. Trends Pharmacol. Sci., 16, 177-181.
74. Kelly S., Zhao H., Sun G.H., Cheng D., Qiao Y., Luo J., Martin K., Steinberg G.K., Harrison S.D., Yenari M.A. (2004). Glycogen synthase kinase 3ß inhibitor Chir025 reduces neuronal death resulting from oxygen-glucose deprivation, glutamate excitotoxicity, and cerebral ischemia. Exp. Neurol., 188, 378-386.
75. 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.W., Harrison S.D. (2003). Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes, 52, 588-595.
76. Ho L.H., Carmichael J., Swartz J., Wyttenbach A., Rankin J., Rubinsztein D.C. (2001). The molecular biology of Huntington's disease. Psychol. Med., 31, 3-14.
77. Carmichael J., Sugars K.L., Bao Y.P., Rubinsztein D.C. (2002). Glycogen synthase kinase-3ß inhibitors prevent cellular polyglutamine toxicity caused by the Huntington's disease mutation. J. Biol. Chem., 277, 33791-33798.
78. Koh S.H., Lee Y.-B., Kim K.S., Kim H.-J., Kim M., Lee Y.J., Kim J., Lee K.W., Kim S.H. (2005). Role of GSK-3ß activity in motor neuronal cell death induced by G93A or A4V mutant hSOD1 gene. Eur. J. Neurosci., 22, 301-309.
79. Naerum L., Norskov-Lauritsen L., Olesen P.H. (2002). Scaffold hopping and optimization towards libraries of glycogen synthase kinase-3 inhibitors. Bioorg. Med. Chem. Lett., 12, 1525-1528.
80. Bhat R., Xue Y., Berg S., Hellberg S., Ormö M., Nilsson Y., Radesäter A.-C., Jerning E., Markgren P.O., Borgegård T., Nylöf M., Giménez-Cassina A., Hernández F., Lucas J.J., Díaz-Nido J., Avila J. (2003). Structural insights and biological effects of glycogen synthase kinase 3-specific inhibitor AR-A014418. J. Biol. Chem., 278, 45937-45945.