Apolipoprotein E and β-amyloid (1-42) regulation of glycogen synthase kinase-3β

Journal of Neurochemistry

Volumn 87, Issue 5, 2003, Pages 1152-1164

  Cedazo Mínguez, Angel ^a   Popescu, B O ^a   Blanco Millan J M ^a   Akterin, S ^a   Pei, J J ^a   Winblad, B ^a   Cowburn, R F ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Alzheimer's disease; Apolipoprotein E; Beta amyloid; Glycogen synthase kinase 3 ; Protein kinase B; Protein kinase C

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; AMYLOID BETA PROTEIN[1-42]; APOLIPOPROTEIN E; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; CALCIUM ION; CASPASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; ISOENZYME; PROTEIN KINASE B; PROTEIN KINASE C; REGULATOR PROTEIN;

ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INACTIVATION; ENZYME REGULATION; EXTRACELLULAR CALCIUM; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; NEUROPATHOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REDUCTION;

AMYLOID BETA-PROTEIN; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; APOLIPOPROTEINS E; BETA CATENIN; CALCIUM; CASPASE 3; CASPASES; CELL LINE, TUMOR; CELL SURVIVAL; CULTURE MEDIA, SERUM-FREE; CYTOSKELETAL PROTEINS; ENZYME ACTIVATION; GLYCOGEN SYNTHASE KINASE 3; HUMANS; NEUROBLASTOMA; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN KINASE C; PROTEIN KINASE C-ALPHA; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; TRANS-ACTIVATORS;

EID: 0345171818     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.02088.x     Document Type: Article

References (62)

1. Aberle H., Bauer A., Stappert J., Kispert A. and Kemler R. (1997) betacatenin is a target for the ubiquitin-proteasome pathway. EMBO J 16, 3797-3804.
2. Behrens J., von Kries J. P., Kuhl M., Bruhn L., Wedlich D., Grosschedl R. and Birchmeier W. (1996) Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382, 638-642.
3. Bhat R. V., Shanley J., Correll M. P., Fieles W. E., Keith R. A., Scott C. W. and 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, 11074-11079.
4. Bijur G. N., De Samo 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.
5. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
6. Brazil D. P. and Hemmings B. A. (2001) Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem. Sci. 26, 657-664.
7. Cedazo-Minguez A. and Cowburn R. F. (2001) Apolipoprotein E: a major piece in the Alzheimer's disease puzzle. J. Cell. Mol. Med. 5, 254-266.
8. Cedazo-Minguez A., Huttinger M. and Cowburn R. F. (2001a) Beta-VLDL protects against A beta (1-42) and apoE toxicity in human SH-SY5Y neuroblastoma cells. Neuroreport 12, 201-206.
9. Cedazo-Minguez A., Wiehager B., Winblad B., Huttinger M. and Cowburn R. F. (2001b) Effects of apolipoprotein E (apoE) isoforms, beta-amyloid (Abeta) and apoE/Abeta complexes on protein kinase C-alpha (PKC-alpha) translocation and amyloid precursor protein (APP) processing in human SH-SY5Y neuroblastoma cells and fibroblasts. Neurochem. Int. 38, 615-625.
10. Cedazo-Minguez A., Hamker U., Meske V., Veh R. W., Hellweg R., Jacobi C., Albert F., Cowburn R. F. and Ohm T. G. (2001c) Regulation of apolipoprotein E secretion in rat primary hippocampal astrocyte cultures. Neuroscience 105, 651-661.
11. Cedazo-Minguez A., Popescu B. O., Ankarcrona M., Nishimura T. and Cowburn R. F. (2002) The presenilin 1 deltaE9 mutation gives enhanced basal phospholipase C activity and a resultant increase in intracellular calcium concentrations. J. Biol. Chem. 277, 36646-36655.
12. Cobb M. H. and Goldsmith E. J. (1995) How MAP kinases are regulated, J. Biol. Chem. 270, 14843-14846.
13. Corder E. H., Lannfelt L., Bogdanovic N., Fratiglioni L. and Mori H. (1998) The role of APOE polymorphisms in late-onset dementias. Cell. Mol. Life Sci. 54, 928-934.
14. Dekroon R. M. and Armati P. J. (2001) Synthesis and processing of apolipoprotein E in human brain cultures. Glia 33, 298-305.
15. DeMattos R. B., Curtiss L. K. and Williams D. L. (1998) A minimally lipidated form of cell-derived apolipoprotein E exhibits isoform-specific stimulation of neurite outgrowth in the absence of exogenous lipids or lipoproteins. J. Biol. Chem. 273, 4206-4212.
16. Elyaman W., Terro F., Wong N. S. and Hugon J. (2002) In vivo activation and nuclear translocation of phosphorylated glycogen synthase kinase-3beta in neuronal apoptosis: links to tau phosphorylation. Eur. J. Neurosci 15, 651-660.
17. Fang X. YuS., Tanyi J. L., Lu Y., Woodgett J. R. and Mills G. B. (2002) Convergence of multiple signaling cascades at glycogen synthase kinase 3: Edg receptor-mediated phosphorylation and inactivation by lysophosphatidic acid through a protein kinase C-dependent intracellular pathway. Mol. Cell Biol. 22, 2099-2110.
18. Favit A., Grimaldi M., Nelson T. J. and Alkon D. L. (1998) Alzheimer's-specific effects of soluble beta-amyloid on protein kinase C-alpha and -gamma degradation in human fibroblasts. Proc. Natl Acad. Sci. USA 95, 5562-5567.
19. Ferrari A., Hoemdli F., Baechi T., Nitsch R. M. and Gotz J. (2003) beta-amyloid induces PHF-like tau filaments in tissue culture. J. Biol. Chem. 278, 40162-40168.
20. Genis L., Chen Y., Shohami E. and Michaelson D. M. (2000) Tau hyperphosphorylation in apolipoprotein E-deficient and control mice after closed head injury. J. Neurosci. Res. 60, 559-564.
21. Grimes C. A. and Jope R. S. (2001) The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog. Neutrobiol. 65, 391-426.
22. Hartigan J. A. and 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, 21395-21401.
23. Hartley D. M., Walsh D. M. Diehl T., Vasquez S., Vassilev P. M., Teplow D. B. and Selkoe D. J. (1999) Protofibrillar intermediates of amyloid beta-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J. Neurosci. 19, 8876-8884.
24. Hartmann H., Eckert A. and Muller W. E. (1994) Apolipoprotein E and cholesterol affect neuronal calcium signalling: the possible relationship to beta-amyloid neurotoxicity. Biochem. Biophys. Res. Commun. 200, 1185-1192.
25. Hashimoto Y., Jiang H., Niikura T., Ito Y., Hagiwara A., Umezawa K., Abe Y., Murayama Y. and Nishimoto I. (2000) Neuronal apoptosis by apolipoprotein E4 through low-density lipoprotein receptor-related protein and heterotrimeric GTPases. J. Neurosci. 20, 8401-8409.
26. van der Heide L. P., Hoeknian M. F., Biessels G. J. and Gispen W. H. (2003) Insulin inhibits extracellular regulated kinase 1/2 phosphorylation in a phosphatidylinositol 3-kinase (PI3) kinase-dependent manner in Neuro2a cells. J. Neurochem. 86, 86-91.
27. Hetman M., Cavanaugh J. E., Kimelman D. and Xia Z. (2000) Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 20, 2567-2574.
28. Hughes K., Nikolakaki E., Plyte S. E., Totty N. F. and Woodgett J. R. (1993) Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. EMBO J. 12, 803-808.
29. Kuperstein F. and Yavin E. (2003) Pro-apoptotic signaling in neuronal cells following iron and amyloid beta peptide neurotoxicity. J. Neurochem. 86, 114-125.
30. Kuperstein F., Reiss N., Koudinova N. and Yavin E. (2001) Biphasic modulation of protein kinase C and enhanced cell toxicity by amyloid beta peptide and anoxia in neuronal cultures. Neurochem. 76, 758-767.
31. LaFerla F. M. (2002) Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease. Nat. Rev. Neurosci. 3, 862-872.
32. Lesort M., Jope R. S. and Johnson G. V. (1999) Insulin transiently increases tau phosphorylation: involvement of glycogen synthase kinase-3beta and Fyn tyrosine kinase. J. Neurochem. 72, 576-584.
33. Li M., Wang X., Meintzer M. K., Laessig T., Bimbaum M. J. and Heidenreich K. A. (2000) Cyclic AMP promotes neuronal survival by phosphorylation of glycogen synthase kinase 3beta. Mol. Cell Biol. 20, 9356-9363.
34. Lovestone S., Anderton B. H., Hartley C., Jensen T. G. and Jorgensen A. L. (1996) The intracellular fate of apolipoprotein E is tau dependent and apoe allele-specific. Neuroreport 7, 1005-1008.
35. Luo Y., Hawver D. B., Iwasaki K., Sunderland T., Roth G. S. and Wolozin B. (1997) Physiological levels of beta-amyloid peptide stimulate protein kinase C in PC12 cells. Brain Res. 769, 287-295.
36. Mattson M. P. and Chan S. L. (2001) Dysregulation of cellular calcium homeostasis in Alzheimer's disease: bad genes and bad habits. J. Mol. Neurosci. 17, 205-224.
37. Molenaar M., van de Wetering M., Oosterwegel M., Peterson-Maduro J., Godsave S., Korinek V., Roose J., Destree O. and Clevers H. (1996) XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86, 391-399.
38. Mosmann T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63.
39. Murai H., Okazaki M. and Kikuchi A. (1996) Tyrosine dephosphorylation of glycogen synthase kinase-3 is involved in its extracellular signal-dependent inactivation. FEBS Lett. 392, 153-160.
40. Murayama M., Tanaka S., Palacino J., Murayama O., Honda T., Sun X., Yasutake K., Nihonmatsu N., Wolozin B. and Takashima A. (1998) Direct association of presenilin-1 with beta-catenin. FEBS Lett. 433, 73-77.
41. Novak A. and Dedhar S. (1999) Signaling through beta-catenin and Lef/Tcf. Cell. Mol. Life Sci. 56, 523-537.
42. Ohkubo N., Mitsuda N., Tamatani M., Yamaguchi A., Lee Y. D., Ogihara T., Vitek M. P. and Tohyama M. (2001) Apolipoprotein E4 stimutates cAMP response element-binding protein transcriptional activity through the extracellular signal-regulated kinase pathway. J. Biol. Chem. 276, 3046-3053.
43. 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.
44. Pei J. J., Tanaka T., Tung Y. C., Braak E., Iqbal K. and Grundke-Iqbal I. (1997) Distribution, levels, and activity of glycogen synthase kinase-3 in the Alzheimer disease brain. J. Neuropathol. Exp. Neurol. 56, 70-78.
45. Popescu B. O., Cedazo-Minguez A., Popescu L. M., Winblad B., Cowburn R. F. and Ankarcrona M. (2001) Caspase cleavage of exon 9 deleted presenilin-1 is an early event in apoptosis induced by calcium ionophore A 23187 in SH-SY5Y neuroblastoma cells. J. Neurosci. Res. 66, 122-134.
46. Rubinfeld B., Albert I., Porfiri E., Fiol C., Munemitsu S. and Polakis P. (1996) Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272, 1023-1026.
47. Selkoe D. J. (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81, 741-766.
48. Stambolic 'V. and Woodgett J. R. (1994) Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation. Biochem. J. 303, 701-704.
49. Strittmatter W. J., Weisgraber K. H., Goedert M., Saunders A. M., Huang D., Corder E. H., Dong L. M., Jakes R., Alberts M. J., Gilbert J. R. et al. (1994) Hypothesis: microtubule instability and paired helical filament formation in the Alzheimer disease brain are related to apolipoprotein E genotype. Exp. Neurol. 125, 163-171; discussion 172-164.
50. Suhara T., Magrane J., Rosen K., Christensen R., Kim H. S., Zheng B., McPhie D. L., Walsh K. and Querfurth H. (2003) Abeta42 generation is toxic to endothelial cells and inhibits eNOS function through an Akt/GSK-3beta signaling-dependent mechanism. Neurobiol. Aging 24, 437-451.
51. Sutherland C., Leighton I. A. and Cohen P. (1993) Inactivation of glycogen synthase kinase-3 beta by phosphorylation: new kinase connections in insulin and growth-factor signalling. Biochem. J. 296, 15-19.
52. Takashima A., Noguchi K., Michel G., Mercken M., Hoshi M., Ishiguro K. and Imahori K. (1996) Exposure of rat hippocampal neurons to amyloid beta peptide (25-35) induces the inactivation of phosphatidylinositol-3 kinase and the activation of tau protein kinase I/glycogen synthase kinase-3 beta. Neurosci. Lett. 203, 33-36.
53. Takashima A., Murayama M., Murayama O., Kohno T., Honda T., Yasutake K., Nihonmatsu N., Mercken M., Yamaguchi H., Sugihara S. et al. (1998) Presenilin 1 associates with glycogen synthase kinase-3beta and its substrate tau. Proc. Natl Acad. Sci. USA 95, 9637-9641.
54. Tesseur I., Van Dorpe J., Spittaels K., Van den Haute C., Moechars D. and Van Leuven F. (2000) Expression of human apolipoprotein E4 in neurons causes hyperphosphorylation of protein tau in the brains of transgenic mice. Am. J. Pathol. 156, 951-964.
55. Tsujio I., Tanaka T., Kudo T., Nishikawa T., Shinozaki K., Grundke-Iqbal I., Iqbal K. and Takeda M. (2000) Inactivation of glycogen synthase kinase-3 by protein kinase C delta: implications for regulation of tau phosphorylation. FEBS Lett. 469, 111-117.
56. Veinbergs I., Everson A., Sagara Y. and Masliah E. (2002) Neurotoxic effects of apolipoprotein E4 are mediated via dysregulation of calcium homeostasis. J. Neurosci. Res. 67, 379-387.
57. Wang Q. M., Fiol C. J., DePaoli-Roach A. A. and Roach P. J. (1994) Glycogen synthase kinase-3 beta is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation. J. Biol. Chem. 269, 14566-14574.
58. Wang X., Luebbe P., Gruenstein E. and Zemlan F. (1998) Apolipoprotein E (ApoE) peptide regulates tau phosphorylation via two different signaling pathways. J. Neurosci. Res. 51, 658-665.
59. Weisgraber K. H., Roses A. D. and Strittmatter W. J. (1994) The role of apolipoprotein E in the nervous system. Curr. Opin. Lipidol, 5, 110-116.
60. Yost C., Torres M., Miller J. R., Huang E., Kimelman D. and Moon R. T. (1996) The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev. 10, 1443-1454.
61. Zeidman R., Troller U., Raghunath A., Pahlman S. and Larsson C. (2002) Protein kinase Cepsilon actin-binding site is important for neurite outgrowth during neuronal differentiation. Mol. Biol. Cell 13, 12-24.
62. Zhang Z., Hartmann H., Do V. M., Abramowski D., Sturchler-Pierrat C., Staufenbiel M., Sommer B., van de Wetering M., Clevers H., Saftig P. et al. (1998) Destabilization of beta-catenin by mutations in presenilin-1 potentiates neuronal apoptosis. Nature 395, 698-702.