The role of GSK3beta in the development of the central nervous system
Received date: 24 Jan 2012
Accepted date: 02 Mar 2012
Published date: 01 Jun 2012
Copyright
Glycogen synthase kinase 3β (GSK3β) is a multifunctional serine/threonine kinase. It is particularly abundant in the developing central nervous system (CNS). Since GSK3β has diverse substrates ranging from metabolic/signaling proteins and structural proteins to transcription factors, it is involved in many developmental events in the immature brain, such as neurogenesis, neuronal migration, differentiation and survival. The activity of GSK3β is developmentally regulated and is affected by various environmental/cellular insults, such as deprivation of nutrients/trophic factors, oxidative stress and endoplasmic reticulum stress. Abnormalities in GSK3β activity may disrupt CNS development. Therefore, GSK3β is a critical signaling protein that regulates brain development. It may also determine neuronal susceptibility to damages caused by various environmental insults.
Key words： development; differentiation; neurogenesis; proliferation
Jia LUO . The role of GSK3beta in the development of the central nervous system[J]. Frontiers in Biology, 2012 , 7(3) : 212 -220 . DOI: 10.1007/s11515-012-1222-2
| 1 |
Arévalo J C, Chao M V (2005). Axonal growth: where neurotrophins meet Wnts. Curr Opin Cell Biol, 17(2): 112–115
|
| 2 |
Asada N, Sanada K (2010). LKB1-mediated spatial control of GSK3beta and adenomatous polyposis coli contributes to centrosomal forward movement and neuronal migration in the developing neocortex. J Neurosci, 30(26): 8852–8865
|
| 3 |
Baltzis D, Pluquet O, Papadakis A I, Kazemi S, Qu L K, Koromilas A E (2007). The eIF2alpha kinases PERK and PKR activate glycogen synthase kinase 3 to promote the proteasomal degradation of p53. J Biol Chem, 282(43): 31675–31687
|
| 4 |
Barth A I, Caro-Gonzalez H Y, Nelson W J (2008). Role of adenomatous polyposis coli (APC) and microtubules in directional cell migration and neuronal polarization. Semin Cell Dev Biol, 19(3): 245–251
|
| 5 |
Beurel E, Jope R S (2006). The paradoxical pro- and anti-apoptotic actions of GSK3 in the intrinsic and extrinsic apoptosis signaling pathways. Prog Neurobiol, 79(4): 173–189
|
| 6 |
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 tyrosine216 phosphorylation of glycogen synthase kinase-3beta in cellular and animal models of neuronal degeneration. Proc Natl Acad Sci USA, 97(20): 11074–11079
|
| 7 |
Bianchi M, De Lucchini S, Marin O, Turner D L, Hanks S K, 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(2): 359–370
|
| 8 |
Bijur G N, De Sarno P, Jope R S (2000). Glycogen synthase kinase-3beta facilitates staurosporine- and heat shock-induced apoptosis. Protection by lithium. J Biol Chem, 275(11): 7583–7590
|
| 9 |
Boku S, Nakagawa S, Masuda T, Nishikawa H, Kato A, Kitaichi Y, Inoue T, Koyama T (2009). Glucocorticoids and lithium reciprocally regulate the proliferation of adult dentate gyrus-derived neural precursor cells through GSK-3beta and beta-catenin/TCF pathway. Neuropsychopharmacology, 34(3): 805–815
|
| 10 |
Brewster J L, Linseman D A, Bouchard R J, Loucks F A, Precht T A, Esch E A, Heidenreich K A (2006). Endoplasmic reticulum stress and trophic factor withdrawal activate distinct signaling cascades that induce glycogen synthase kinase-3 beta and a caspase-9-dependent apoptosis in cerebellar granule neurons. Mol Cell Neurosci, 32(3): 242–253
|
| 11 |
Carter J J, Tong M, Silbermann E, Lahousse S A, Ding F F, Longato L, Roper N, Wands J R, de la Monte S M (2008). Ethanol impaired neuronal migration is associated with reduced aspartyl-asparaginyl-beta-hydroxylase expression. Acta Neuropathol, 116(3): 303–315
|
| 12 |
Castelo-Branco G, Rawal N, Arenas E (2004). GSK-3beta inhibition/beta-catenin stabilization in ventral midbrain precursors increases differentiation into dopamine neurons. J Cell Sci, 117(24): 5731–5737
|
| 13 |
Chen G, Bower K A, Ma C, Fang S, Thiele C J, Luo J (2004). Glycogen synthase kinase 3beta (GSK3beta) mediates 6-hydroxydopamine-induced neuronal death. FASEB J, 18(10): 1162–1164
|
| 14 |
Chen G, Bower K A, Xu M, Ding M, Shi X, Ke Z J, Luo J (2009b). Cyanidin-3-glucoside reverses ethanol-induced inhibition of neurite outgrowth: role of glycogen synthase kinase 3 Beta. Neurotox Res, 15(4): 321–331
|
| 15 |
Chen Z L, Haegeli V, Yu H, Strickland S (2009a). Cortical deficiency of laminin gamma1 impairs the AKT/GSK-3beta signaling pathway and leads to defects in neurite outgrowth and neuronal migration. Dev Biol, 327(1): 158–168
|
| 16 |
Cheng T S, Hsiao Y L, Lin C C, Yu C T, Hsu C M, Chang M S, Lee C I, Huang C Y, Howng S L, Hong Y R (2007). Glycogen synthase kinase 3beta interacts with and phosphorylates the spindle-associated protein astrin. J Biol Chem, 283(4): 2454–2464
|
| 17 |
Ciani L, Salinas P C (2007). c-Jun N-terminal kinase (JNK) cooperates with Gsk3beta to regulate Dishevelled-mediated microtubule stability. BMC Cell Biol, 8(1): 27
|
| 18 |
Cole A, Frame S, Cohen P (2004). Further evidence that the tyrosine phosphorylation of glycogen synthase kinase-3 (GSK3) in mammalian cells is an autophosphorylation event. Biochem J, 377(1): 249–255
|
| 19 |
Coyle-Rink J, Del Valle L, Sweet T, Khalili K, Amini S (2002). Developmental expression of Wnt signaling factors in mouse brain. Cancer Biol Ther, 1(6): 640–645
|
| 20 |
Crowder R J, Freeman R S (2000). Glycogen synthase kinase-3 beta 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(44): 34266–34271
|
| 21 |
Cui H, Meng Y, Bulleit R F (1998). Inhibition of glycogen synthase kinase 3beta activity regulates proliferation of cultured cerebellar granule cells. Brain Res Dev Brain Res, 111(2): 177–188
|
| 22 |
D’Mello S R, Anelli R, Calissano P (1994). Lithium induces apoptosis in immature cerebellar granule cells but promotes survival of mature neurons. Exp Cell Res, 211(2): 332–338
|
| 23 |
Diehl J A, Cheng M, Roussel M F, Sherr C J (1998). Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev, 12(22): 3499–3511
|
| 24 |
Dill J, Wang H, Zhou F, Li S (2008). Inactivation of glycogen synthase kinase 3 promotes axonal growth and recovery in the CNS. J Neurosci, 28(36): 8914–8928
|
| 25 |
Doble B W, Woodgett J R (2003). GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci, 116(7): 1175–1186
|
| 26 |
Eom T Y, Roth K A, Jope R S (2007). Neural precursor cells are protected from apoptosis induced by trophic factor withdrawal or genotoxic stress by inhibitors of glycogen synthase kinase 3. J Biol Chem, 282(31): 22856–22864
|
| 27 |
Etienne-Manneville S, Hall A (2003). Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature, 421(6924): 753–756
|
| 28 |
Gärtner A, Huang X, Hall A (2006). Neuronal polarity is regulated by glycogen synthase kinase-3 (GSK-3beta) independently of Akt/PKB serine phosphorylation. J Cell Sci, 119(19): 3927–3934
|
| 29 |
Gonzalez-Billault C, Avila J, Cáceres A (2001). Evidence for the role of MAP1B in axon formation. Mol Biol Cell, 12(7): 2087–2098
|
| 30 |
González-Billault C, Del Río J A, Ureña J M, Jiménez-Mateos E M, Barallobre M J, Pascual M, Pujadas L, Simó S, Torre A L, Gavin R, Wandosell F, Soriano E, Avila J (2004). A role of MAP1B in Reelin-dependent neuronal migration. Cereb Cortex, 15(8): 1134–1145
|
| 31 |
Goold R G, Gordon-Weeks P R (2001). Microtubule-associated protein 1B phosphorylation by glycogen synthase kinase 3beta is induced during PC12 cell differentiation. J Cell Sci, 114(Pt 23): 4273–4284
|
| 32 |
Goold R G, Gordon-Weeks P R (2005). The MAP kinase pathway is upstream of the activation of GSK3beta that enables it to phosphorylate MAP1B and contributes to the stimulation of axon growth. Mol Cell Neurosci, 28(3): 524–534
|
| 33 |
Grimes C A, Jope R S (2001). The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog Neurobiol, 65(4): 391–426
|
| 34 |
Guo W, Murthy A C, Zhang L, Johnson E B, Schaller E G, Allan A M, Zhao X (2011). Inhibition of GSK3 Improves Hippocampus-dependent Learning and Rescues Neurogenesis in a Mouse Model of Fragile X Syndrome. Hum Mol Genet
|
| 35 |
Hanks S K, Ryzhova L, Shin N Y, Brábek J (2003). Focal adhesion kinase signaling activities and their implications in the control of cell survival and motility. Front Biosci, 8(1-3): d982–d996
|
| 36 |
Hartigan J A, Johnson G V (1999). Transient increases in intracellular calcium result in prolonged site-selective increases in Tau phosphorylation through a glycogen synthase kinase 3beta-dependent pathway. J Biol Chem, 274(30): 21395–21401
|
| 37 |
Hartigan J A, Xiong W C, Johnson G V (2001). Glycogen synthase kinase 3beta is tyrosine phosphorylated by PYK2. Biochem Biophys Res Commun, 284(2): 485–489
|
| 38 |
Hetman M, Cavanaugh J E, Kimelman D, Xia Z (2000). Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J Neurosci, 20(7): 2567–2574
|
| 39 |
Hongisto V, Smeds N, Brecht S, Herdegen T, Courtney M J, Coffey E T (2003). Lithium blocks the c-Jun stress response and protects neurons via its action on glycogen synthase kinase 3. Mol Cell Biol, 23(17): 6027–6036
|
| 40 |
Hoshi M, Takashima A, Noguchi K, Murayama M, Sato M, Kondo S, Saitoh Y, Ishiguro K, Hoshino T, Imahori K (1996). Regulation of mitochondrial pyruvate dehydrogenase activity by tau protein kinase I/glycogen synthase kinase 3beta in brain. Proc Natl Acad Sci USA, 93(7): 2719–2723
|
| 41 |
Huang W, Chang H Y, Fei T, Wu H, Chen Y G (2007). GSK3 beta mediates suppression of cyclin D2 expression by tumor suppressor PTEN. Oncogene, 26(17): 2471–2482
|
| 42 |
Hur E M, Zhou F Q (2010). GSK3 signalling in neural development. Nat Rev Neurosci, 11(8): 539–551
|
| 43 |
Ille F, Sommer L (2005). Wnt signaling: multiple functions in neural development. Cell Mol Life Sci, 62(10): 1100–1108
|
| 44 |
Jiang H, Guo W, Liang X, 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(1): 123–135
|
| 45 |
Jin L, Hu X, Feng L (2005). NT3 inhibits FGF2-induced neural progenitor cell proliferation via the PI3K/GSK3 pathway. J Neurochem, 93(5): 1251–1261
|
| 46 |
Jope R S, Yuskaitis C J, Beurel E (2007). Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics. Neurochem Res, 32(4-5): 577–595
|
| 47 |
Kaytor M D, Orr H T (2002). The GSK3 beta signaling cascade and neurodegenerative disease. Curr Opin Neurobiol, 12(3): 275–278
|
| 48 |
Ke Z, Liu Y, Wang X, Fan Z, Chen G, Xu M, Bower K A, Frank J A, Ou X, Shi X, Luo J (2011). Cyanidin-3-glucoside ameliorates ethanol neurotoxicity in the developing brain. J Neurosci Res, 89(10): 1676–1684
|
| 49 |
Knoepfler P S, Kenney A M (2006). Neural precursor cycling at sonic speed: N-Myc pedals, GSK-3 brakes. Cell Cycle, 5(1): 47–52
|
| 50 |
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-3beta activity in motor neuronal cell death induced by G93A or A4V mutant hSOD1 gene. Eur J Neurosci, 22(2): 301–309
|
| 51 |
Lee K Y, Koh S H, Noh M Y, Park K W, Lee Y J, Kim S H (2007). Glycogen synthase kinase-3beta activity plays very important roles in determining the fate of oxidative stress-inflicted neuronal cells. Brain Res, 1129(1): 89–99
|
| 52 |
Leroy K, Brion J P (1999). Developmental expression and localization of glycogen synthase kinase-3beta in rat brain. J Chem Neuroanat, 16(4): 279–293
|
| 53 |
Lesort M, Jope R S, Johnson G V (1999). Insulin transiently increases tau phosphorylation: involvement of glycogen synthase kinase-3beta and Fyn tyrosine kinase. J Neurochem, 72(2): 576–584
|
| 54 |
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, Heidenreich K A (2004). Glycogen synthase kinase-3beta phosphorylates Bax and promotes its mitochondrial localization during neuronal apoptosis. J Neurosci, 24(44): 9993–10002
|
| 55 |
Liu Y, Chen G, Ma C, Bower K A, Xu M, Fan Z, Shi X, Ke Z J, Luo J (2009). Over-expression of GSK3 beta sensitizes neuronal cells to ethanol toxicity. J Neurosci Res, 87(12): 2793–2802
|
| 56 |
Lossi L, Merighi A (2003). In vivo cellular and molecular mechanisms of neuronal apoptosis in the mammalian CNS. Prog Neurobiol, 69(5): 287–312
|
| 57 |
Lucas J J, Hernández F, Gómez-Ramos P, Morán M A, Hen R, Avila J (2001). Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J, 20(1): 27–39
|
| 58 |
Luo J (2009a). Glycogen synthase kinase 3beta (GSK3beta) in tumorigenesis and cancer chemotherapy. Cancer Lett, 273(2): 194–200
|
| 59 |
Luo J (2009b). GSK3beta in ethanol neurotoxicity. Mol Neurobiol, 40(2): 108–121
|
| 60 |
Ma C, Wang J, Gao Y, Gao T W, Chen G, Bower K A, Odetallah M, Ding M, Ke Z, Luo J (2007). The role of glycogen synthase kinase 3beta in the transformation of epidermal cells. Cancer Res, 67(16): 7756–7764
|
| 61 |
Madalosso S H, Pérez-Villegas E M, Armengol J A (2005). Naturally occurring neuronal death during the postnatal development of Purkinje cells and their precerebellar afferent projections. Brain Res Brain Res Rev, 49(2): 267–279
|
| 62 |
Malaterre J, Ramsay R G, Mantamadiotis T (2007). Wnt-Frizzled signalling and the many paths to neural development and adult brain homeostasis. Front Biosci, 12(1): 492–506
|
| 63 |
Manoukian A S, Woodgett J R (2002). Role of glycogen synthase kinase-3 in cancer: regulation by Wnts and other signaling pathways. Adv Cancer Res, 84: 203–229
|
| 64 |
Maurer M H, Brömme J O, Feldmann R E Jr, Järve A, Sabouri F, Bürgers H F, Schelshorn D W, Krüger C, Schneider A, Kuschinsky W (2007). Glycogen synthase kinase 3beta (GSK3beta) regulates differentiation and proliferation in neural stem cells from the rat subventricular zone. J Proteome Res, 6(3): 1198–1208
|
| 65 |
Meares G P, Jope R S (2007). Resolution of the nuclear localization mechanism of glycogen synthase kinase-3: functional effects in apoptosis. J Biol Chem, 282(23): 16989–17001
|
| 66 |
Mishra R, Barthwal M K, Sondarva G, Rana B, Wong L, Chatterjee M, Woodgett J R, Rana A (2007). Glycogen synthase kinase-3beta induces neuronal cell death via direct phosphorylation of mixed lineage kinase 3. J Biol Chem, 282(42): 30393–30405
|
| 67 |
Muñoz-Montaño J R, Lim F, Moreno F J, Avila J, Díaz-Nido J (1999). Glycogen synthase kinase-3 modulates neurite outgrowth in cultured neurons: possible implications for neurite pathology in Alzheimer’s disease. J Alzheimers Dis, 1(6): 361–378
|
| 68 |
Nedachi T, Kawai T, Matsuwaki T, Yamanouchi K, Nishihara M (2011). Progranulin enhances neural progenitor cell proliferation through glycogen synthase kinase 3β phosphorylation. Neuroscience, 185: 106–115
|
| 69 |
Orme M H, Giannini A L, Vivanco M D, Kypta R M (2003). Glycogen synthase kinase-3 and Axin function in a beta-catenin-independent pathway that regulates neurite outgrowth in neuroblastoma cells. Mol Cell Neurosci, 24(3): 673–686
|
| 70 |
Owen R, 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(4): 626–637
|
| 71 |
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(32): 19929–19932
|
| 72 |
Pap M, Cooper G M (2002). Role of translation initiation factor 2B in control of cell survival by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3beta signaling pathway. Mol Cell Biol, 22(2): 578–586
|
| 73 |
Patapoutian A, Reichardt L F (2000). Roles of Wnt proteins in neural development and maintenance. Curr Opin Neurobiol, 10(3): 392–399
|
| 74 |
Saito M, Chakraborty G, Mao R F, Paik S M, Vadasz C, Saito M (2010). Tau phosphorylation and cleavage in ethanol-induced neurodegeneration in the developing mouse brain. Neurochem Res, 35(4): 651–659
|
| 75 |
Sayas C L, Ariaens A, Ponsioen B, Moolenaar W H (2006). GSK-3 is activated by the tyrosine kinase Pyk2 during LPA1-mediated neurite retraction. Mol Biol Cell, 17(4): 1834–1844
|
| 76 |
Seng S, Avraham H K, Jiang S, Venkatesh S, Avraham S (2006). KLHL1/MRP2 mediates neurite outgrowth in a glycogen synthase kinase 3beta-dependent manner. Mol Cell Biol, 26(22): 8371–8384
|
| 77 |
Shimizu T, Kagawa T, Inoue T, Nonaka A, Takada S, Aburatani H, Taga T (2008). Stabilized beta-catenin functions through TCF/LEF proteins and the Notch/RBP-Jkappa complex to promote proliferation and suppress differentiation of neural precursor cells. Mol Cell Biol, 28(24): 7427–7441
|
| 78 |
Song L, De Sarno P, Jope R S (2002). Central role of glycogen synthase kinase-3beta in endoplasmic reticulum stress-induced caspase-3 activation. J Biol Chem, 277(47): 44701–44708
|
| 79 |
Spittaels K, Van den Haute C, Van Dorpe J, Geerts H, Mercken M, Bruynseels K, Lasrado R, Vandezande K, Laenen I, Boon T, Van Lint J, Vandenheede J, Moechars D, Loos R, Van Leuven F (2000). Glycogen synthase kinase-3beta phosphorylates protein tau and rescues the axonopathy in the central nervous system of human four-repeat tau transgenic mice. J Biol Chem, 275(52): 41340–41349
|
| 80 |
Spittaels K, Van den Haute C, Van Dorpe J, Terwel D, Vandezande K, Lasrado R, Bruynseels K, Irizarry M, Verhoye M, Van Lint J, Vandenheede J R, Ashton D, Mercken M, Loos R, Hyman B, Van der Linden A, Geerts H, Van Leuven F (2002). Neonatal neuronal overexpression of glycogen synthase kinase-3 beta reduces brain size in transgenic mice. Neuroscience, 113(4): 797–808
|
| 81 |
Sui Z, Sniderhan L F, Fan S, Kazmierczak K, Reisinger E, Kovács A D, Potash M J, Dewhurst S, Gelbard H A, Maggirwar S B (2006). Human immunodeficiency virus-encoded Tat activates glycogen synthase kinase-3beta to antagonize nuclear factor-kappaB survival pathway in neurons. Eur J Neurosci, 23(10): 2623–2634
|
| 82 |
Sun Y, Kim N H, Yang H, Kim S H, Huh S O (2011). Lysophosphatidic acid induces neurite retraction in differentiated neuroblastoma cells via GSK-3β activation. Mol Cells, 31(5): 483–489
|
| 83 |
Takadera T, Fujibayashi M, Kaniyu H, Sakota N, Ohyashiki T (2007). Caspase-dependent apoptosis induced by thapsigargin was prevented by glycogen synthase kinase-3 inhibitors in cultured rat cortical neurons. Neurochem Res, 32(8): 1336–1342
|
| 84 |
Takahashi M, Tomizawa K, Ishiguro K (2000). Distribution of tau protein kinase I/glycogen synthase kinase-3beta, phosphatases 2A and 2B, and phosphorylated tau in the developing rat brain. Brain Res, 857(1-2): 193–206
|
| 85 |
Takahashi M, Yasutake K, Tomizawa K (1999). Lithium inhibits neurite growth and tau protein kinase I/glycogen synthase kinase-3beta-dependent phosphorylation of juvenile tau in cultured hippocampal neurons. J Neurochem, 73(5): 2073–2083
|
| 86 |
Takahashi-Yanaga F, Shiraishi F, Hirata M, Miwa Y, Morimoto S, Sasaguri T (2004). Glycogen synthase kinase-3beta is tyrosine-phosphorylated by MEK1 in human skin fibroblasts. Biochem Biophys Res Commun, 316(2): 411–415
|
| 87 |
Tong N, Sanchez J F, Maggirwar S B, Ramirez S H, Guo H, Dewhurst S, Gelbard H A (2001). Activation of glycogen synthase kinase 3 beta (GSK-3beta) by platelet activating factor mediates migration and cell death in cerebellar granule neurons. Eur J Neurosci, 13(10): 1913–1922
|
| 88 |
Trivedi N, Marsh P, Goold R G, Wood-Kaczmar A, 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(5): 993–1005
|
| 89 |
Tsukane M, Yoshizaki C, Yamauchi T (2007). Development and specific induction of apoptosis of cultured cell models overexpressing human tau during neural differentiation: Implication in Alzheimer’s disease. Anal Biochem, 360(1): 114–122
|
| 90 |
Valerio A, Ghisi V, Dossena M, Tonello C, Giordano A, Frontini A, Ferrario M, Pizzi M, Spano P, Carruba M O, Nisoli E (2006). Leptin increases axonal growth cone size in developing mouse cortical neurons by convergent signals inactivating glycogen synthase kinase-3beta. J Biol Chem, 281(18): 12950–12958
|
| 91 |
Vohra B P, Fu M, Heuckeroth R O (2007). Protein kinase Czeta and glycogen synthase kinase-3beta control neuronal polarity in developing rodent enteric neurons, whereas SMAD specific E3 ubiquitin protein ligase 1 promotes neurite growth but does not influence polarity. J Neurosci, 27(35): 9458–9468
|
| 92 |
Wang H Y, Juo L I, Lin Y T, Hsiao M, Lin J T, Tsai C H, Tzeng Y H, Chuang Y C, Chang N S, Yang C N, Lu P J (2011). WW domain-containing oxidoreductase promotes neuronal differentiation via negative regulation of glycogen synthase kinase 3β. Cell Death Differ, Online Available December 23, 2011
|
| 93 |
Watcharasit P, Bijur G N, Song L, Zhu J, Chen X, Jope R S (2003). Glycogen synthase kinase-3beta (GSK3beta) binds to and promotes the actions of p53. J Biol Chem, 278(49): 48872–48879
|
| 94 |
Woodgett J R (1990). Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J, 9(8): 2431–2438
|
| 95 |
Yeste-Velasco M, Folch J, Trullàs R, Abad M A, Enguita M, Pallàs M, Camins A (2007). Glycogen synthase kinase-3 is involved in the regulation of the cell cycle in cerebellar granule cells. Neuropharmacology, 53(2): 295–307
|
| 96 |
Yoshimura T, Kawano Y, Arimura N, Kawabata S, Kikuchi A, Kaibuchi K (2005). GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell, 120(1): 137–149
|
| 97 |
Yuskaitis C J, Jope R S (2009). Glycogen synthase kinase-3 regulates microglial migration, inflammation, and inflammation-induced neurotoxicity. Cell Signal, 21(2): 264–273
|
| 98 |
Zhang W, Smith A, Liu J P, Cheung N S, Zhou S, Liu K, Li Q T, Duan W (2009). GSK3beta modulates PACAP-induced neuritogenesis in PC12 cells by acting downstream of Rap1 in a caveolae-dependent manner. Cell Signal, 21(2): 237–245
|
| 99 |
Zhou F, Zhang L, Wang A, Song B, Gong K, Zhang L, Hu M, Zhang X, Zhao N, Gong Y (2008). The association of GSK3 beta with E2F1 facilitates nerve growth factor-induced neural cell differentiation. J Biol Chem, 283(21): 14506–14515
|
/
| 〈 |
|
〉 |