GSK3 as a sensor determining cell fate in the brain

Frontiers in Molecular Neuroscience

Volumn , Issue JANUARY 2012, 2012, Pages

  Cole, Adam R ^a  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

AD; Alzheimer's disease; Embryonic stem (cell); ES; Glycogen synthase kinase 3; GSK3; Neural progenitor cell; NPC

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; CYCLIN DEPENDENT KINASE 5; CYTOCHROME C; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; MYOCARDIN; TRANSCRIPTION FACTOR GLI3; WNT PROTEIN; TRANSCRIPTION FACTOR SNAIL;

ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; BRAIN FUNCTION; CELL FATE; CELL PROLIFERATION; CELL SURVIVAL; DNA BINDING; ENZYME DEFECT; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; HUMAN; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL DIFFERENTIATION; NEUROTRANSMISSION; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; CELL DIFFERENTIATION; CELL STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SPECIFICITY; NERVE CELL PLASTICITY; PROTEIN FUNCTION;

EID: 84856805691     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2012.00004     Document Type: Article

References (120)

1. Ackermann, T.F., Kempe, D.S., Lang, F., and Lang, U.E. (2010). Hyperactivity and enhanced curiosity of mice expressing PKB/SGK-resistant glycogen synthase kinase-3 (GSK-3). Cell Physiol Biochem 25, 775-786.
2. Al-Khouri, A.M., Ma, Y., Togo, S.H., Williams, S., and Mustelin, T. (2005). Cooperative phosphorylation of the tumor suppressor phosphatase and tensin homologue (PTEN) by casein kinases and glycogen synthase kinase 3beta. J Biol Chem 280, 35195-35202.
3. Aplin, A.E., Gibb, G.M., Jacobsen, J.S., Gallo, J.M., and Anderton, B.H. (1996). In vitro phosphorylation of the cytoplasmic domain of the amyloid precursor protein by glycogen synthase kinase-3beta. J Neurochem 67, 699-707.
4. Bachelder, R.E., Yoon, S.O., Franci, C., De Herreros, A.G., and Mercurio, A.M. (2005). Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription: implications for the epithelial-mesenchymal transition. J Cell Biol 168, 29-33.
5. Badorff, C., Seeger, F.H., Zeiher, A.M., and Dimmeler, S. (2005). Glycogen synthase kinase 3beta inhibits myocardin-dependent transcription and hypertrophy induction through site-specific phosphorylation. Circ Res 97, 645-654.
6. Bednarek, E., and Caroni, P. (2011). beta-Adducin is required for stable assembly of new synapses and improved memory upon environmental enrichment. Neuron 69, 1132-1146.
7. Bell, R.D., Deane, R., Chow, N., Long, X., Sagare, A., Singh, I., Streb, J.W., Guo, H., Rubio, A., Van Nostrand, W., Miano, J.M., and Zlokovic, B.V. (2009). SRF and myocardin regulate LRP-mediated amyloid-beta clearance in brain vascular cells. Nat Cell Biol 11, 143-153.
8. Bianchi, M., De Lucchini, S., Marin, O., Turner, D.L., Hanks, S.K., and Villa-Moruzzi, E. (2005). Regulation of FAK Ser-722 phosphorylation and kinase activity by GSK3 and PP1 during cell spreading and migration. Biochem J 391, 359-370.
9. Bijur, G.N., De Sarno, P., and Jope, R.S. (2000). Glycogen synthase kinase-3beta facilitates staurosporine- and heat shock-induced apoptosis. Protection by lithium. J Biol Chem 275, 7583-7590.
10. Bone, H.K., Damiano, T., Bartlett, S., Perry, A., Letchford, J., Ripoll, Y.S., Nelson, A.S., and Welham, M.J. (2009). Involvement of GSK-3 in regulation of murine embryonic stem cell self-renewal revealed by a series of bisindolylmaleimides. Chem Biol 16, 15-27.
11. Brittain, J.M., Duarte, D.B., Wilson, S.M., Zhu, W., Ballard, C., Johnson, P.L., Liu, N., Xiong, W., Ripsch, M.S., Wang, Y., Fehrenbacher, J.C., Fitz, S.D., Khanna, M., Park, C.K., Schmutzler, B.S., Cheon, B.M., Due, M.R., Brustovetsky, T., Ashpole, N.M., Hudmon, A., Meroueh, S.O., Hingtgen, C.M., Brustovetsky, N., Ji, R.R., Hurley, J.H., Jin, X., Shekhar, A., Xu, X.M., Oxford, G.S., Vasko, M.R., White, F.A., and Khanna, R. (2011). Suppression of inflammatory and neuropathic pain by uncoupling CRMP-2 from the presynaptic Ca(2) channel complex. Nat Med 17, 822-829.
12. Brown, M., Jacobs, T., Eickholt, B., Ferrari, G., Teo, M., Monfries, C., Qi, R.Z., Leung, T., Lim, L., and Hall, C. (2004). Alpha2-chimaerin, cyclin-dependent Kinase 5/p35, and its target collapsin response mediator protein-2 are essential components in semaphorin 3A-induced growth-cone collapse. J Neurosci 24, 8994-9004.
13. Cartwright, P., Mclean, C., Sheppard, A., Rivett, D., Jones, K., and Dalton, S. (2005). LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development 132, 885-896.
14. Chen, P., Gu, Z., Liu, W., and Yan, Z. (2007). Glycogen synthase kinase 3 regulates N-methyl-D- aspartate receptor channel trafficking and function in cortical neurons. Mol Pharmacol 72, 40-51.
15. Chen, Y., Yue, S., Xie, L., Pu, X.H., Jin, T., and Cheng, S.Y. (2011). Dual Phosphorylation of suppressor of fused (Sufu) by PKA and GSK3beta regulates its stability and localization in the primary cilium. J Biol Chem 286, 13502-13511.
16. Chiu, C.T., and Chuang, D.M. (2010). Molecular actions and therapeutic potential of lithium in preclinical and clinical studies of CNS disorders. Pharmacol Ther 128, 281-304.
17. Chu, B., Zhong, R., Soncin, F., Stevenson, M.A., and Calderwood, S.K. (1998). Transcriptional activity of heat shock factor 1 at 37 degrees C is repressed through phosphorylation on two distinct serine residues by glycogen synthase kinase 3 and protein kinases Calpha and Czeta. J Biol Chem 273, 18640-18646.
18. Clayton, E.L., Sue, N., Smillie, K.J., O'leary, T., Bache, N., Cheung, G., Cole, A.R., Wyllie, D.J., Sutherland, C., Robinson, P.J., and Cousin, M.A. (2010). Dynamin I phosphorylation by GSK3 controls activity-dependent bulk endocytosis of synaptic vesicles. Nat Neurosci 13, 845-851.
19. Cole, A., Frame, S., and Cohen, P. (2004a). Further evidence that the tyrosine phosphorylation of glycogen synthase kinase-3 (GSK3) in mammalian cells is an autophosphorylation event. Biochem J 377, 249-255.
20. Cole, A.R., Knebel, A., Morrice, N.A., Robertson, L.A., Irving, A.J., Connolly, C.N., and Sutherland, C. (2004b). GSK-3 phosphorylation of the Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J Biol Chem 279, 50176-50180.
21. Cole, A.R., Noble, W., Van Aalten, L., Plattner, F., Meimaridou, R., Hogan, D., Taylor, M., Lafrancois, J., Gunn-Moore, F., Verkhratsky, A., Oddo, S., Laferla, F., Giese, K.P., Dineley, K.T., Duff, K., Richardson, J.C., Yan, S.D., Hanger, D.P., Allan, S.M., and Sutherland, C. (2007). Collapsin response mediator protein-2 hyperphosphorylation is an early event in Alzheimer's disease progression. J Neurochem 103, 1132-1144.
22. Cole, A.R., Soutar, M.P., Rembutsu, M., Van Aalten, L., Hastie, C.J., Mclauchlan, H., Peggie, M., Balastik, M., Lu, K.P., and Sutherland, C. (2008). Relative resistance of Cdk5- phosphorylated CRMP2 to dephosphorylation. J Biol Chem 283, 18227-18237.
23. Ding, V.W., Chen, R.H., and Mccormick, F. (2000). Differential regulation of glycogen synthase kinase 3beta by insulin and Wnt signaling. J Biol Chem 275, 32475-32481.
24. Doble, B.W., Patel, S., Wood, G.A., Kockeritz, L.K., and Woodgett, J.R. (2007). Functional redundancy of GSK-3alpha and GSK-3beta in Wnt/beta-catenin signaling shown by using an allelic series of embryonic stem cell lines. Dev Cell 12, 957-971.
25. Eldar-Finkelman, H., and Krebs, E.G. (1997). Phosphorylation of insulin receptor substrate 1 by glycogen synthase kinase 3 impairs insulin action. Proc Natl Acad Sci U S A 94, 9660-9664.
26. Eom, T.Y., and Jope, R.S. (2009). Blocked inhibitory serine-phosphorylation of glycogen synthase kinase-3alpha/beta impairs in vivo neural precursor cell proliferation. Biol Psychiatry 66, 494-502.
27. Farghaian, H., Turnley, A.M., Sutherland, C., and Cole, A.R. (2011). Bioinformatic prediction and confirmation of beta-adducin as a novel substrate of glycogen synthase kinase 3. J Biol Chem 286, 25274-25283.
28. Forlenza, O.V., Diniz, B.S., Radanovic, M., Santos, F.S., Talib, L.L., and Gattaz, W.F. (2011). Disease-modifying properties of long-term lithium treatment for amnestic mild cognitive impairment: randomised controlled trial. Br J Psychiatry 198, 351-356.
29. Frame, S., Cohen, P., and Biondi, R.M. (2001). A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol Cell 7, 1321-1327.
30. Franco, B., Bogdanik, L., Bobinnec, Y., Debec, A., Bockaert, J., Parmentier, M.L., and Grau, Y. (2004). Shaggy, the homolog of glycogen synthase kinase 3, controls neuromuscular junction growth in Drosophila. J Neurosci 24, 6573-6577.
31. Fuentealba, L.C., Eivers, E., Ikeda, A., Hurtado, C., Kuroda, H., Pera, E.M., and De Robertis, E.M. (2007). Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131, 980-993.
32. Garrido, J.J., Simon, D., Varea, O., and Wandosell, F. (2007). GSK3 alpha and GSK3 beta are necessary for axon formation. FEBS Lett 581, 1579-1586.
33. Gartner, A., Huang, X., and Hall, A. (2006). Neuronal polarity is regulated by glycogen synthase kinase-3 (GSK-3beta) independently of Akt/PKB serine phosphorylation. J Cell Sci 119, 3927-3934.
34. Goold, R.G., Owen, R., and Gordon-Weeks, P.R. (1999). Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J Cell Sci 112 (Pt 19), 3373-3384.
35. Green, M.F., Scott, J.W., Steel, R., Oakhill, J.S., Kemp, B.E., and Means, A.R. (2011). Ca2+/Calmodulin-dependent protein kinase kinase beta is regulated by multisite phosphorylation. J Biol Chem 286, 28066-28079.
36. Hall, A.C., Lucas, F.R., and Salinas, P.C. (2000). Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100, 525-535.
37. Hall, J., Guo, G., Wray, J., Eyres, I., Nichols, J., Grotewold, L., Morfopoulou, S., Humphreys, P., Mansfield, W., Walker, R., Tomlinson, S., and Smith, A. (2009). Oct4 and LIF/Stat3 additively induce Kruppel factors to sustain embryonic stem cell self-renewal. Cell Stem Cell 5, 597-609.
38. Han, S.P., Kim, J.H., Han, M.E., Sim, H.E., Kim, K.S., Yoon, S., Baek, S.Y., Kim, B.S., and Oh, S.O. (2011). SNAI1 is involved in the proliferation and migration of glioblastoma cells. Cell Mol Neurobiol 31, 489-496.
39. Hanger, D.P., Hughes, K., Woodgett, J.R., Brion, J.P., and Anderton, B.H. (1992). 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, 58-62.
40. Hergovich, A., Lisztwan, J., Thoma, C.R., Wirbelauer, C., Barry, R.E., and Krek, W. (2006). Priming-dependent phosphorylation and regulation of the tumor suppressor pVHL by glycogen synthase kinase 3. Mol Cell Biol 26, 5784-5796.
41. Hoeflich, K.P., Luo, J., Rubie, E.A., Tsao, M.S., Jin, O., and Woodgett, J.R. (2000). Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 406, 86-90.
42. Hooper, C., Markevich, V., Plattner, F., Killick, R., Schofield, E., Engel, T., Hernandez, F., Anderton, B., Rosenblum, K., Bliss, T., Cooke, S.F., Avila, J., Lucas, J.J., Giese, K.P., Stephenson, J., and Lovestone, S. (2007). Glycogen synthase kinase-3 inhibition is integral to long-term potentiation. Eur J Neurosci 25, 81-86.
43. Hu, G., Wang, X., Saunders, D.N., Henderson, M., Russell, A.J., Herring, B.P., and Zhou, J. (2010). Modulation of myocardin function by the ubiquitin E3 ligase UBR5. J Biol Chem 285, 11800-11809.
44. Ikeda, S., Kishida, S., Yamamoto, H., Murai, H., Koyama, S., and Kikuchi, A. (1998). Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin. EMBO J 17, 1371-1384.
45. Jia, J., Amanai, K., Wang, G., Tang, J., Wang, B., and Jiang, J. (2002). Shaggy/GSK3 antagonizes Hedgehog signalling by regulating Cubitus interruptus. Nature 416, 548-552.
46. Jiang, H., Guo, W., Liang, X., and Rao, Y. (2005). Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 120, 123-135.
47. Jiang, J., Chan, Y.S., Loh, Y.H., Cai, J., Tong, G.Q., Lim, C.A., Robson, P., Zhong, S., and Ng, H.H. (2008). A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat Cell Biol 10, 353-360.
48. Kelly, K.F., Ng, D.Y., Jayakumaran, G., Wood, G.A., Koide, H., and Doble, B.W. (2011). beta- catenin enhances Oct-4 activity and reinforces pluripotency through a TCF-independent mechanism. Cell Stem Cell 8, 214-227.
49. Kessing, L.V., Forman, J.L., and Andersen, P.K. (2010). Does lithium protect against dementia? Bipolar Disord 12, 87-94.
50. Kim, W.Y., Wang, X., Wu, Y., Doble, B.W., Patel, S., Woodgett, J.R., and Snider, W.D. (2009). GSK-3 is a master regulator of neural progenitor homeostasis. Nat Neurosci 12, 1390-1397.
51. Leroy, K., Ando, K., Heraud, C., Yilmaz, Z., Authelet, M., Boeynaems, J.M., Buee, L., De Decker, R., and Brion, J.P. (2010). Lithium treatment arrests the development of neurofibrillary tangles in mutant tau transgenic mice with advanced neurofibrillary pathology. J Alzheimers Dis 19, 705-719.
52. Li, B., Ryder, J., Su, Y., Zhou, Y., Liu, F., and Ni, B. (2003). FRAT1 peptide decreases Abeta production in swAPP(751) cells. FEBS Lett 553, 347-350.
53. Li, Y.C., Xi, D., Roman, J., Huang, Y.Q., and Gao, W.J. (2009). Activation of glycogen synthase kinase-3 beta is required for hyperdopamine and D2 receptor-mediated inhibition of synaptic NMDA receptor function in the rat prefrontal cortex. J Neurosci 29, 15551-15563.
54. Liberman, Z., and Eldar-Finkelman, H. (2005). Serine 332 phosphorylation of insulin receptor substrate-1 by glycogen synthase kinase-3 attenuates insulin signaling. J Biol Chem 280, 4422-4428.
55. Linseman, D.A., Butts, B.D., Precht, T.A., Phelps, R.A., Le, S.S., Laessig, T.A., Bouchard, R.J., Florez-Mcclure, M.L., and Heidenreich, K.A. (2004). Glycogen synthase kinase-3beta phosphorylates Bax and promotes its mitochondrial localization during neuronal apoptosis. J Neurosci 24, 9993-10002.
56. Litovchick, L., Chestukhin, A., and Decaprio, J.A. (2004). Glycogen synthase kinase 3 phosphorylates RBL2/p130 during quiescence. Mol Cell Biol 24, 8970-8980.
57. Liu, N., Li, H., Li, S., Shen, M., Xiao, N., Chen, Y., Wang, Y., Wang, W., Wang, R., Wang, Q., Sun, J., and Wang, P. (2010). The Fbw7/human CDC4 tumor suppressor targets proproliferative factor KLF5 for ubiquitination and degradation through multiple phosphodegron motifs. J Biol Chem 285, 18858-18867.
58. Lucas, J.J., Hernandez, F., Gomez-Ramos, P., Moran, M.A., Hen, R., and Avila, J. (2001). Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK3beta conditional transgenic mice. EMBO J 20, 27-39.
59. Maccario, H., Perera, N.M., Davidson, L., Downes, C.P., and Leslie, N.R. (2007). PTEN is destabilized by phosphorylation on Thr366. Biochem J 405, 439-444.
60. Mao, Y., Ge, X., Frank, C.L., Madison, J.M., Koehler, A.N., Doud, M.K., Tassa, C., Berry, E.M., Soda, T., Singh, K.K., Biechele, T., Petryshen, T.L., Moon, R.T., Haggarty, S.J., and Tsai, L.H. (2009). Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3beta/beta-catenin signaling. Cell 136, 1017-1031.
61. Maurer, U., Charvet, C., Wagman, A.S., Dejardin, E., and Green, D.R. (2006). Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell 21, 749-760.
62. Mines, M.A., Beurel, E., and Jope, R.S. (2011). Regulation of cell survival mechanisms in Alzheimer's disease by glycogen synthase kinase-3. Int J Alzheimers Dis 2011, 861072.
63. Moberg, K.H., Mukherjee, A., Veraksa, A., Artavanis-Tsakonas, S., and Hariharan, I.K. (2004). The Drosophila F box protein archipelago regulates dMyc protein levels in vivo. Curr Biol 14, 965-974.
64. Mottet, D., Dumont, V., Deccache, Y., Demazy, C., Ninane, N., Raes, M., and Michiels, C. (2003). Regulation of hypoxia-inducible factor-1alpha protein level during hypoxic conditions by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3beta pathway in HepG2 cells. J Biol Chem 278, 31277-31285.
65. Murray, J.T., Campbell, D.G., Morrice, N., Auld, G.C., Shpiro, N., Marquez, R., Peggie, M., Bain, J., Bloomberg, G.B., Grahammer, F., Lang, F., Wulff, P., Kuhl, D., and Cohen, P. (2004). Exploitation of KESTREL to identify NDRG family members as physiological substrates for SGK1 and GSK3. Biochem J 384, 477-488.
66. Murray, S.A., and Gridley, T. (2006). Snail family genes are required for left-right asymmetry determination, but not neural crest formation, in mice. Proc Natl Acad Sci U S A 103, 10300-10304.
67. Nakashima, H., Ishihara, T., Suguimoto, P., Yokota, O., Oshima, E., Kugo, A., Terada, S., Hamamura, T., Trojanowski, J.Q., Lee, V.M., and Kuroda, S. (2005). Chronic lithium treatment decreases tau lesions by promoting ubiquitination in a mouse model of tauopathies. Acta Neuropathol 110, 547-556.
68. Nishimura, T., Fukata, Y., Kato, K., Yamaguchi, T., Matsuura, Y., Kamiguchi, H., and Kaibuchi, K. (2003). CRMP-2 regulates polarized Numb-mediated endocytosis for axon growth. Nat Cell Biol 5, 819-826.
69. Noble, W., Planel, E., Zehr, C., Olm, V., Meyerson, J., Suleman, F., Gaynor, K., Wang, L., Lafrancois, J., Feinstein, B., Burns, M., Krishnamurthy, P., Wen, Y., Bhat, R., Lewis, J., Dickson, D., and Duff, K. (2005). Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc Natl Acad Sci U S A 102, 6990-6995.
70. Nunes, P.V., Forlenza, O.V., and Gattaz, W.F. (2007). Lithium and risk for Alzheimer's disease in elderly patients with bipolar disorder. Br J Psychiatry 190, 359-360.
71. Owen, R., and Gordon-Weeks, P.R. (2003). Inhibition of glycogen synthase kinase 3beta in sensory neurons in culture alters filopodia dynamics and microtubule distribution in growth cones. Mol Cell Neurosci 23, 626-637.
72. Pan, Y., Bai, C.B., Joyner, A.L., and Wang, B. (2006). Sonic hedgehog signaling regulates Gli2 transcriptional activity by suppressing its processing and degradation. Mol Cell Biol 26, 3365-3377.
73. Pap, M., and 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.
74. Pastorino, J.G., Hoek, J.B., and Shulga, N. (2005). Activation of glycogen synthase kinase 3beta disrupts the binding of hexokinase II to mitochondria by phosphorylating voltage-dependent anion channel and potentiates chemotherapy-induced cytotoxicity. Cancer Res 65, 10545-10554.
75. Peineau, S., Nicolas, C.S., Bortolotto, Z.A., Bhat, R.V., Ryves, W.J., Harwood, A.J., Dournaud, P., Fitzjohn, S.M., and Collingridge, G.L. (2009). A systematic investigation of the protein kinases involved in NMDA receptor-dependent LTD: evidence for a role of GSK-3 but not other serine/threonine kinases. Mol Brain 2, 22.
76. Peineau, S., Taghibiglou, C., Bradley, C., Wong, T.P., Liu, L., Lu, J., Lo, E., Wu, D., Saule, E., Bouschet, T., Matthews, P., Isaac, J.T., Bortolotto, Z.A., Wang, Y.T., and Collingridge, G.L. (2007). LTP inhibits LTD in the hippocampus via regulation of GSK3beta. Neuron 53, 703-717.
77. Perez, M., Hernandez, F., Lim, F., Diaz-Nido, J., and Avila, J. (2003). Chronic lithium treatment decreases mutant tau protein aggregation in a transgenic mouse model. J Alzheimers Dis 5, 301-308.
78. Phiel, C.J., Wilson, C.A., Lee, V.M., and Klein, P.S. (2003). GSK-3alpha regulates production of Alzheimer's disease amyloid-beta peptides. Nature 423, 435-439.
79. Pielage, J., Bulat, V., Zuchero, J.B., Fetter, R.D., and Davis, G.W. (2011). Hts/Adducin controls synaptic elaboration and elimination. Neuron 69, 1114-1131.
80. Price, M.A., and Kalderon, D. (2002). Proteolysis of the Hedgehog signaling effector Cubitus interruptus requires phosphorylation by Glycogen Synthase Kinase 3 and Casein Kinase 1. Cell 108, 823-835.
81. Pulverer, B.J., Fisher, C., Vousden, K., Littlewood, T., Evan, G., and Woodgett, J.R. (1994). Site- specific modulation of c-Myc cotransformation by residues phosphorylated in vivo. Oncogene 9, 59-70.
82. Ruediger, S., Vittori, C., Bednarek, E., Genoud, C., Strata, P., Sacchetti, B., and Caroni, P. (2011). Learning-related feedforward inhibitory connectivity growth required for memory precision. Nature 473, 514-518.
83. Ryder, J., Su, Y., Liu, F., Li, B., Zhou, Y., and Ni, B. (2003). Divergent roles of GSK3 and CDK5 in APP processing. Biochem Biophys Res Commun 312, 922-929.
84. Rylatt, D.B., Aitken, A., Bilham, T., Condon, G.D., Embi, N., and Cohen, P. (1980). 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, 529-537.
85. Sanchez, C., Perez, M., and Avila, J. (2000). GSK3beta-mediated phosphorylation of the microtubule-associated protein 2C (MAP2C) prevents microtubule bundling. Eur J Cell Biol 79, 252-260.
86. Sapkota, G., Alarcon, C., Spagnoli, F.M., Brivanlou, A.H., and Massague, J. (2007). Balancing BMP signaling through integrated inputs into the Smad1 linker. Mol Cell 25, 441-454.
87. Sato, N., Meijer, L., Skaltsounis, L., Greengard, P., and Brivanlou, A.H. (2004). Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 10, 55-63.
88. Sereno, L., Coma, M., Rodriguez, M., Sanchez-Ferrer, P., Sanchez, M.B., Gich, I., Agullo, J.M., Perez, M., Avila, J., Guardia-Laguarta, C., Clarimon, J., Lleo, A., and Gomez-Isla, T. (2009). A novel GSK-3beta inhibitor reduces Alzheimer's pathology and rescues neuronal loss in vivo. Neurobiol Dis 35, 359-367.
89. Somervaille, T.C., Linch, D.C., and Khwaja, A. (2001). Growth factor withdrawal from primary human erythroid progenitors induces apoptosis through a pathway involving glycogen synthase kinase-3 and Bax. Blood 98, 1374-1381.
90. Streets, A.J., Moon, D.J., Kane, M.E., Obara, T., and Ong, A.C. (2006). Identification of an N- terminal glycogen synthase kinase 3 phosphorylation site which regulates the functional localization of polycystin-2 in vivo and in vitro. Hum Mol Genet 15, 1465-1473.
91. Su, Y., Ryder, J., Li, B., Wu, X., Fox, N., Solenberg, P., Brune, K., Paul, S., Zhou, Y., Liu, F., and Ni, B. (2004). Lithium, a common drug for bipolar disorder treatment, regulates amyloid- beta precursor protein processing. Biochemistry 43, 6899-6908.
92. Sun, X., Sato, S., Murayama, O., Murayama, M., Park, J.M., Yamaguchi, H., and Takashima, A. (2002). Lithium inhibits amyloid secretion in COS7 cells transfected with amyloid precursor protein C100. Neurosci Lett 321, 61-64.
93. Sutherland, C. (2011). What Are the bona fide GSK3 Substrates? Int J Alzheimers Dis 2011, 505607.
94. Tempe, D., Casas, M., Karaz, S., Blanchet-Tournier, M.F., and Concordet, J.P. (2006). Multisite protein kinase A and glycogen synthase kinase 3beta phosphorylation leads to Gli3 ubiquitination by SCFbetaTrCP. Mol Cell Biol 26, 4316-4326.
95. Thomas, G.M., Frame, S., Goedert, M., Nathke, I., Polakis, P., and Cohen, P. (1999). A GSK3- binding peptide from FRAT1 selectively inhibits the GSK3-catalysed phosphorylation of axin and beta-catenin. FEBS Lett 458, 247-251.
96. Trivedi, N., Marsh, P., Goold, R.G., Wood-Kaczmar, A., and Gordon-Weeks, P.R. (2005). Glycogen synthase kinase-3beta phosphorylation of MAP1B at Ser1260 and Thr1265 is spatially restricted to growing axons. J Cell Sci 118, 993-1005.
97. Tsai, L.K., Wang, Z., Munasinghe, J., Leng, Y., Leeds, P., and Chuang, D.M. (2011). Mesenchymal stem cells primed with valproate and lithium robustly migrate to infarcted regions and facilitate recovery in a stroke model. Stroke 42, 2932-2939.
98. Uchida, Y., Ohshima, T., Sasaki, Y., Suzuki, H., Yanai, S., Yamashita, N., Nakamura, F., Takei, K., Ihara, Y., Mikoshiba, K., Kolattukudy, P., Honnorat, J., and Goshima, Y. (2005). Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3beta phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer's disease. Genes Cells 10, 165-179.
99. Viatour, P., Dejardin, E., Warnier, M., Lair, F., Claudio, E., Bureau, F., Marine, J.C., Merville, M.P., Maurer, U., Green, D., Piette, J., Siebenlist, U., Bours, V., and Chariot, A. (2004). GSK3-mediated BCL-3 phosphorylation modulates its degradation and its oncogenicity. Mol Cell 16, 35-45.
100. Wang, B., and Li, Y. (2006). Evidence for the direct involvement of {beta}TrCP in Gli3 protein processing. Proc Natl Acad Sci U S A 103, 33-38.
101. Wang, H., Ge, G., Uchida, Y., Luu, B., and Ahn, S. (2011). Gli3 is required for maintenance and fate specification of cortical progenitors. J Neurosci 31, 6440-6448.
102. Wang, X., She, H., and Mao, Z. (2009). Phosphorylation of neuronal survival factor MEF2D by glycogen synthase kinase 3beta in neuronal apoptosis. J Biol Chem 284, 32619-32626.
103. Watanabe, T., Noritake, J., Kakeno, M., Matsui, T., Harada, T., Wang, S., Itoh, N., Sato, K., Matsuzawa, K., Iwamatsu, A., Galjart, N., and Kaibuchi, K. (2009). Phosphorylation of CLASP2 by GSK-3beta regulates its interaction with IQGAP1, EB1 and microtubules. J Cell Sci 122, 2969-2979.
104. Wei, J., Liu, W., and Yan, Z. (2010). Regulation of AMPA receptor trafficking and function by glycogen synthase kinase 3. J Biol Chem 285, 26369-26376.
105. Wei, W., Jin, J., Schlisio, S., Harper, J.W., and Kaelin, W.G., Jr. (2005). The v-Jun point mutation allows c-Jun to escape GSK3-dependent recognition and destruction by the Fbw7 ubiquitin ligase. Cancer Cell 8, 25-33.
106. Welcker, M., Orian, A., Jin, J., Grim, J.E., Harper, J.W., Eisenman, R.N., and Clurman, B.E. (2004). The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation- dependent c-Myc protein degradation. Proc Natl Acad Sci U S A 101, 9085-9090.
107. Welcker, M., Singer, J., Loeb, K.R., Grim, J., Bloecher, A., Gurien-West, M., Clurman, B.E., and Roberts, J.M. (2003). Multisite phosphorylation by Cdk2 and GSK3 controls cyclin E degradation. Mol Cell 12, 381-392.
108. Welsh, G.I., and Proud, C.G. (1993). Glycogen synthase kinase-3 is rapidly inactivated in response to insulin and phosphorylates eukaryotic initiation factor eIF-2B. Biochem J 294 (Pt 3), 625-629.
109. Williamson, R., Van Aalten, L., Mann, D.M., Platt, B., Plattner, F., Bedford, L., Mayer, J., Howlett, D., Usardi, A., Sutherland, C., and Cole, A.R. (2011). CRMP2 Hyperphosphorylation is Characteristic of Alzheimer's Disease and Not a Feature Common to Other Neurodegenerative Diseases. J Alzheimers Dis.
110. Wittmann, T., and Waterman-Storer, C.M. (2005). Spatial regulation of CLASP affinity for microtubules by Rac1 and GSK3beta in migrating epithelial cells. J Cell Biol 169, 929-939.
111. Wray, J., Kalkan, T., Gomez-Lopez, S., Eckardt, D., Cook, A., Kemler, R., and Smith, A. (2011). Inhibition of glycogen synthase kinase-3 alleviates Tcf3 repression of the pluripotency network and increases embryonic stem cell resistance to differentiation. Nat Cell Biol 13, 838-845.
112. Xie, P., Fan, Y., Zhang, H., Zhang, Y., She, M., Gu, D., Patterson, C., and Li, H. (2009). CHIP represses myocardin-induced smooth muscle cell differentiation via ubiquitin-mediated proteasomal degradation. Mol Cell Biol 29, 2398-2408.
113. Yada, M., Hatakeyama, S., Kamura, T., Nishiyama, M., Tsunematsu, R., Imaki, H., Ishida, N., Okumura, F., Nakayama, K., and Nakayama, K.I. (2004). Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. EMBO J 23, 2116-2125.
114. Ying, Q.L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P., and Smith, A. (2008). The ground state of embryonic stem cell self-renewal. Nature 453, 519-523.
115. Yook, J.I., Li, X.Y., Ota, I., Hu, C., Kim, H.S., Kim, N.H., Cha, S.Y., Ryu, J.K., Choi, Y.J., Kim, J., Fearon, E.R., and Weiss, S.J. (2006). A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells. Nat Cell Biol 8, 1398-1406.
116. Yoshimura, T., Kawano, Y., Arimura, N., Kawabata, S., Kikuchi, A., and Kaibuchi, K. (2005). GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120, 137-149.
117. Zhao, D., Zheng, H.Q., Zhou, Z., and Chen, C. (2010). The Fbw7 tumor suppressor targets KLF5 for ubiquitin-mediated degradation and suppresses breast cell proliferation. Cancer Res 70, 4728-4738.
118. Zhou, B.P., Deng, J., Xia, W., Xu, J., Li, Y.M., Gunduz, M., and Hung, M.C. (2004). Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial- mesenchymal transition. Nat Cell Biol 6, 931-940.
119. Zhu, L.Q., Liu, D., Hu, J., Cheng, J., Wang, S.H., Wang, Q., Wang, F., Chen, J.G., and Wang, J.Z. (2010). GSK-3 beta inhibits presynaptic vesicle exocytosis by phosphorylating P/Q-type calcium channel and interrupting SNARE complex formation. J Neurosci 30, 3624-3633.
120. Zhu, L.Q., Wang, S.H., Liu, D., Yin, Y.Y., Tian, Q., Wang, X.C., Wang, Q., Chen, J.G., and Wang, J.Z. (2007). Activation of glycogen synthase kinase-3 inhibits long-term potentiation with synapse-associated impairments. J Neurosci 27, 12211-12220.