Overcoming cell death and tau phosphorylation mediated by pi3kinhibition: A cell assay to measure neuroprotection

CNS and Neurological Disorders - Drug Targets

Volumn 10, Issue 2, 2011, Pages 208-214

  Simon, D ^a   Medina, M ^b   Avila, J ^a   Wandosell, F ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b Noscira   (Spain)

Author keywords

Cellular screening; Neurodegeneration; Neuroprotective drugs

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; AMYLOID BETA PROTEIN; ESTRADIOL; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; SOMATOMEDIN C; TAU PROTEIN; WNT PROTEIN;

ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; CELL DEATH; ENZYME INHIBITION; HUMAN; NERVE CELL NECROSIS; NEUROBLASTOMA CELL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PROTEIN PHOSPHORYLATION;

EID: 79551679637     PISSN: 18715273     EISSN: None     Source Type: Journal    
DOI: 10.2174/187152711794480401     Document Type: Article

References (60)

1. Pap, M.; Cooper, G.M. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway. J. Biol. Chem., 1998, 273(32); 19929-19932.
2. Sosa, L.; Dupraz, S.; Laurino, L.; Bollati, F.; Bisbal, M.; Caceres, A.; Pfenninger, K.H.; Santiago Quiroga, S. IGF-1 receptor is essential for the establishment of hippocampal neuronal polarity. Nat. Neurosci., 2006, 9(8), 993-995.
3. Shi, S.H.; Jan, L.Y.; Jan, Y.N. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell, 2003, 112(1), 63-75.
4. Sanchez, S.; Sayas, C.L.; Lim, F.; Diaz-Nido, J.; Avila, J.; Wandosell, F. The inhibition of phosphatidylinositol-3-kinase induces neurite retraction and activates GSK3. J. Neurochem., 2001, 78(3), 468-481.
5. Sutherland, C.; Leighton, I.A.; Cohen, P. Inactivation of glycogen synthase kinase-3 beta by phosphorylation: new kinase connections in insulin and growth-factor signalling. Biochem. J., 1993, 296(Pt 1), 15-19.
6. Zhou, F.Q.; Zhou, J.; Dedhar, S.; Wu, Y.H.; Snider, W.D. NGFinduced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron, 2004, 42(6), 897-912.
7. Ding, Q.; Xia, W.; Liu, J.C.; Yang, J.Y.; Lee, D.F.; Xia, J.; Bartholomeusz, G.; Li, Y.; Pan, Y.; Li, Z.; Bargou, R.F.; Qin, J.; Lai, C-C.; Tsai, F-J.; Tsai, C-H.; Hung, M-C. Erk associates with and primes GSK-3beta for its inactivation resulting in upregulation of beta-catenin. Mol. Cell, 2005, 19(2), 159-170.
8. Hashimoto, M.; Sagara, Y.; Langford, D.; Everall, I.P.; Mallory, M.; Everson, A.; Digicaylioglu, M.; Masliah, E. Fibroblast growth factor 1 regulates signaling via the glycogen synthase kinase-3beta pathway. Implications for neuroprotection. J. Biol. Chem., 2002, 277(36), 32985-32991.
9. Tsujio, I.; Tanaka, T.; Kudo, T.; Nishikawa, T.; Shinozaki, K.; Grundke-Iqbal, I.; Iqbal, K.; Takeda, M. Inactivation of glycogen synthase kinase-3 by protein kinase C delta: implications for regulation of tau phosphorylation. FEBS Lett., 2000, 469(1), 111-117.
10. Cross, D.A.; Watt, P.W.; Shaw, M.; van der Kaay, J.; Downes, C.P.; Holder, J.C.; Cohen, P. Insulin activates protein kinase B.; inhibits glycogen synthase kinase-3 and activates glycogen synthase by rapamycin-insensitive pathways in skeletal muscle and adipose tissue. FEBS Lett., 1997, 406(1-2), 211-215.
11. Shi, S.H.; Cheng, T.; Jan, L.Y.; Jan, Y.N. APC and GSK-3beta are involved in mPar3 targeting to the nascent axon and establishment of neuronal polarity. Curr. Biol., 2004, 14(22), 2025-2032.
12. Garrido, J.J.; Simon, D.; Varea, O.; Wandosell, F. GSK3 alpha and GSK3 beta are necessary for axon formation. FEBS Lett., 2007, 581(8), 1579-1586.
13. Mendez, P.; Azcoitia, I.; Garcia-Segura, L.M. Interdependence of oestrogen and insulin-like growth factor-I in the brain: potential for analysing neuroprotective mechanisms. J. Endocrinol., 2005, 185(1), 11-17.
14. Mendez, P.; Azcoitia, I.; Garcia-Segura, L.M. Estrogen receptor alpha forms estrogen-dependent multimolecular complexes with insulin-like growth factor receptor and phosphatidylinositol 3-kinase in the adult rat brain. Brain Res., 2003, 112(1-2), 170-176.
15. Varea, O.; Garrido, J.J.; Dopazo, A.; Mendez, P.; Garcia-Segura, L.M.; Wandosell, F. Estradiol activates beta-catenin dependent transcription in neurons. PLoS One, 2009, 4(4), e5153.
16. Cardona-Gomez, P.; Perez, M.; Avila, J.; Garcia-Segura, L.M.; Wandosell, F. Estradiol inhibits GSK3 and regulates interaction of estrogen receptors.; GSK3.; and beta-catenin in the hippocampus. Molec. Cell. Neurosci., 2004, 25(3), 363-373.
17. Salinas, P.C.; Zou, Y. Wnt signaling in neural circuit assembly. Annu. Rev. Neurosci., 2008, 31, 339-358.
18. Schlessinger, K.; Hall, A.; Tolwinski, N. Wnt signaling pathways meet Rho GTPases. Genes Dev., 2009, 23(3), 265-277.
19. Speese, S.D.; Budnik, V. Wnts: up-and-coming at the synapse. Trends Neurosci., 2007, 30(6), 268-275.
20. Salinas, P.C. Signaling at the vertebrate synapse: new roles for embryonic morphogens? J. Neurobiol., 2005, 64(4), 435-445.
21. Rosso, S.B.; Sussman, D.; Wynshaw-Boris, A.; Salinas, P.C. Wnt signaling through Dishevelled.; Rac and JNK regulates dendritic development. Nat. Neurosci., 2005, 8(1), 34-42.
22. Del Rio, J.A.; Gonzalez-Billault, C.; Urena, J.M.; Jimenez, E.M.; Barallobre, M.J.; Pascual, M.; Pujadas, L.; Simó, S.; La Torre, A.; Wandosell, F.; Avila, J.; Soriano, E. MAP1B is required for Netrin 1 signaling in neuronal migration and axonal guidance. Curr. Biol., 2004, 14(10), 840-850.
23. Gonzalez-Billault, C.; Del Rio, J.A.; Urena, J.M.; Jimenez-Mateos, E.M.; Barallobre, M.J.; Pascual, M.; Pujadas, L.; Simó, S.; Torre, A.L.; Gavin, R.; Wandosell, F.; Soriano, E.; Avila, J. A role of MAP1B in Reelin-dependent neuronal migration. Cereb. Cortex, 2005, 15(8), 1134-1145.
24. Lucas, F.R.; Salinas, P.C. WNT-7a induces axonal remodeling and increases synapsin I levels in cerebellar neurons. Dev. Biol., 1997, 192(1), 31-44.
25. Alessi, D.R.; Caudwell, F.B.; Andjelkovic, M.; Hemmings, B.A.; Cohen, P. Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett., 1996, 399(3), 333-338.
26. Hart, M.J.; de los Santos, R.; Albert, I.N.; Rubinfeld, B.; Polakis, P. Downregulation of beta-catenin by human Axin and its association with the APC tumor suppressor.; beta-catenin and GSK3 beta. Curr. Biol., 1998, 8(10), 573-581.
27. Frame, S.; Cohen, P. GSK3 takes centre stage more than 20 years after its discovery. Biochem. J., 2001, 359(Pt 1), 1-16.
28. Grimes, C.A.; Jope, R.S. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog. Neurobiol., 2001, 65(4), 391-426.
29. Takahashi, M.; Tomizawa, K.; Kato, R.; Sato, K.; Uchida, T.; Fujita, S.C.; Imahori K. Localization and developmental changes of tau protein kinase I/glycogen synthase kinase-3 beta in rat brain. J. Neurochem., 1994, 63(1), 245-255.
30. Hoeflich, K.P.; Luo, J.; Rubie, E.A.; Tsao, M.S.; Jin, O.; Woodgett, J.R. Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature, 2000, 406(6791), 86-90.
31. Takashima, A.; Noguchi, K.; Michel, G.; Mercken, M.; Hoshi, M.; Ishiguro, K.; Imahori K. Exposure of rat hippocampal neurons to amyloid beta peptide (25-35) induces the inactivation of phosphatidyl inositol-3 kinase and the activation of tau protein kinase I/glycogen synthase kinase-3 beta. Neurosci. Lett., 1996, 203(1), 33-36.
32. Takashima, A.; Honda, T.; Yasutake, K.; Michel, G.; Murayama, O.; Murayama, M.; Ishiguro K, Yamaguchi H. Activation of tau protein kinase I/glycogen synthase kinase-3beta by amyloid beta peptide (25-35) enhances phosphorylation of tau in hippocampal neurons. Neurosci. Res., 1998, 31(4), 317-323.
33. Munoz-Montano, J.R.; Moreno, F.J.; Avila, J.; Diaz-Nido, J. Lithium inhibits Alzheimer's disease-like tau protein phosphorylation in neurons. FEBS Lett., 1997, 411(2-3), 183-188.
34. Sayas, C.L.; Avila, J.; Wandosell, F. Glycogen synthase kinase-3 is activated in neuronal cells by Galpha12 and Galpha13 by Rhoindependent and Rho-dependent mechanisms. J. Neurosci., 2002, 22(16), 6863-6875.
35. Lesort, M.; Jope, R.S.; Johnson, G.V. Insulin transiently increases tau phosphorylation: involvement of glycogen synthase kinase- 3beta and Fyn tyrosine kinase. J. Neurochem., 1999, 72(2), 576-584.
36. Kim, L.; Liu, J.; Kimmel, A.R. The novel tyrosine kinase ZAK1 activates GSK3 to direct cell fate specification. Cell, 1999, 99(4), 399-408.
37. Kim, L.; Harwood, A.; Kimmel, A.R. Receptor-dependent and tyrosine phosphatase-mediated inhibition of GSK3 regulates cell fate choice. Dev. Cell, 2002, 3(4), 523-532.
38. Goni-Oliver, P.; Lucas, J.J.; Avila, J.; Hernandez, F. N-terminal cleavage of GSK-3 by calpain: a new form of GSK-3 regulation. J. Biol. Chem., 2007, 282(31), 22406-22413.
39. Goni-Oliver, P.; Avila, J.; Hernandez, F. Calpain-mediated truncation of GSK-3 in post-mortem brain samples. J. Neurosci. Res., 2009, 87(5), 1156-1161.
40. Busciglio, J.; Lorenzo, A.; Yeh, J.; Yankner, B.A. beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron, 1995, 14(4), 879-888.
41. 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. Alzheimer's disease-like phosphorylation of the microtubule-associated protein tau byglycogen synthase kinase-3 in transfected mammalian cells. Curr. Biol., 1994, 4(12), 1077-1086.
42. Alvarez, A.R.; Godoy, J.A.; Mullendorff, K.; Olivares, G.H.; Bronfman, M.; Inestrosa, N.C. Wnt-3a overcomes beta-amyloid toxicity in rat hippocampal neurons. Exp. Cell Res., 2004, 297(1), 186-196.
43. De Ferrari, G.V.; Chacon, M.A.; Barria, M.I.; Garrido, J.L.; Godoy, J.A.; Olivares, G.; Reyes, A.E.; Alvarez, A.; Bronfman, M.; Inestrosa, N.C. Activation of Wnt signaling rescues neurodegeneration and behavioral impairments induced by betaamyloid fibrils. Mol. Psychiatry, 2003, 8(2), 195-208.
44. Bijur, G.N.; Jope, R.S. Proapoptotic stimuli induce nuclear accumulation of glycogen synthase kinase-3 beta. J. Biol. Chem., 2001, 276(40), 37436-37442.
45. Bijur, G.N.; Jope, R.S. Glycogen synthase kinase-3 beta is highly activated in nuclei and mitochondria. Neuroreport, 2003, 19, 14(18), 2415-2419.
46. Pei, J.J.; Braak, E.; Braak, H.; Grundke-Iqbal, I.; Iqbal, K.; Winblad, B.; Cowburn, R.F. Distribution of active glycogen synthase kinase 3beta (GSK-3beta) in brains staged for Alzheimer disease neurofibrillary changes. J. Neuropathol. Exp. Neurol., 1999, 58(9), 1010-1019.
47. Takashima, A.; Murayama, M.; Murayama, O.; Kohno, T.; Honda, T.; Yasutake, K.; Nihonmatsu, N.; Mercken, M.; Yamaguchi, H.; Sugihara, S.; Wolozin, B. Presenilin 1 associates with glycogen synthase kinase-3beta and its substrate tau. Proc. Natl. Acad. Sci. USA, 1998, 95(16), 9637-9641.
48. Lucas, J.J.; Hernandez, F.; Gomez-Ramos, P.; Moran, M.A.; Hen, R.; Avila, J. Decreased nuclear beta-catenin.; tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J., 2001, 20(1-2), 27-39.
49. Hernandez, F.; Borrell, J.; Guaza, C.; Avila, J.; Lucas, J.J. Spatial learning deficit in transgenic mice that conditionally over-express GSK-3beta in the brain but do not form tau filaments. J. Neurochem., 2002, 83(6), 1529-1533.
50. Martinez, A.; Alonso, M.; Castro, A.; Perez, C.; Moreno, F.J. First non-ATP competitive glycogen synthase kinase 3 beta (GSK-3beta) inhibitors: thiadiazolidinones (TDZD) as potential drugs for the treatment of Alzheimer's disease. J. Med. Chem., 2002, 45(6), 1292-1299.
51. Bhat, R.; Xue, Y.; Berg, S.; Hellberg, S.; Ormo, 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. Structural insights and biological effects of glycogen synthase kinase 3-specific inhibitor AR-A014418. J. Biol. Chem., 2003, 278(46), 45937-45945.
52. Mattson, M.P. Pathways towards and away from Alzheimer's disease. Nature, 2004, 430(7000), 631-639.
53. Engel, T.; Hernandez, F.; Avila, J.; Lucas, J.J. Full reversal of Alzheimer's disease-like phenotype in a mouse model with conditional overexpression of glycogen synthase kinase-3. J. Neurosci., 2006, 26(19), 5083-5090.
54. Conde, S.; Perez, D.I.; Martinez, A.; Perez, C.; Moreno, F.J. Thienyl and phenyl alpha-halomethyl ketones: new inhibitors of glycogen synthase kinase (GSK-3beta) from a library of compound searching. J. Med. Chem., 2003, 46(22), 4631-4633.
55. Martinez, A.; Alonso, M.; Castro, A.; Dorronsoro, I.; Gelpi, J.L.; Luque, FJ.; Pérez, C.; Moreno, F.J. SAR and 3D-QSAR studies on thiadiazolidinone derivatives: exploration of structural requirements for glycogen synthase kinase 3 inhibitors. J. Med. Chem., 2005, 48(23), 7103-7112.
56. Castro, A.; Encinas, A.; Gil, C.; Brase, S.; Porcal, W.; Perez, C.; Moreno, F.J.; Martínez, A. Non-ATP competitive glycogen synthase kinase 3beta (GSK-3beta) inhibitors: study of structural requirements for thiadiazolidinone derivatives. Bioorg. Med. Chem., 2008, 16(1), 495-510.
57. Lovestone, S.; Hartley, C.L.; Pearce, J.; Anderton, B.H. Phosphorylation of tau by glycogen synthase kinase-3 beta in intact mammalian cells: the effects on the organization and stability of microtubules. Neuroscience, 1996, 73(4), 1145-1157.
58. Singh, T.J.; Zaidi, T.; Grundke-Iqbal, I.; Iqbal, K. Non-prolinedependent protein kinases phosphorylate several sites found in tau from Alzheimer disease brain. Mol. Cell. Biochem., 1996, 154(2), 143-151.
59. Szendrei, G.I.; Lee, V.M.; Otvos, L., Jr. Recognition of the minimal epitope of monoclonal antibody Tau-1 depends upon the presence of a phosphate group but not its location. J. Neurosci. Res., 1993, 34(2), 243-249.
60. Sayas, C.L.; Moreno-Flores, M.T.; Avila, J.; Wandosell, F. The neurite retraction induced by lysophosphatidic acid increases Alzheimer's disease-like Tau phosphorylation. J. Biol. Chem., 1999, 274(52), 37046-37052.