Regulation of glycogen synthase kinase-3β by products of lipid peroxidation in human neuroblastoma cells

Journal of Neurochemistry

Volumn 89, Issue 5, 2004, Pages 1224-1232

  Dozza, Barbara ^a   Smith, Mark A ^b   Perry, George ^b   Tabaton, Massimo ^c   Strocchi, Paola ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c UNIVERSITY OF GENOA   (Italy)

Author keywords

AKT; Extracellular signal regulated kinase 1 2; Glycogen synthase kinase 3 ; Lipid peroxidation; Neuroblastoma cells; Signalling pathway

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 HYDROXYNONENAL; GLYCOGEN SYNTHASE KINASE 3BETA; MEMBRANE LIPID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B; RECOMBINANT PROTEIN; SERINE; TAU PROTEIN; TYROSINE;

ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ENZYME ASSAY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; LIPID PEROXIDATION; NEUROBLASTOMA CELL; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ALDEHYDES; CELL LINE, TUMOR; CELL SURVIVAL; ENZYME ACTIVATION; ENZYME INHIBITORS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; LIPID PEROXIDATION; MITOGEN-ACTIVATED PROTEIN KINASE 1; NEUROBLASTOMA; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 2642538349     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02413.x     Document Type: Article

References (55)

1. Ali A., Hoeflich K. P. and Woodgett J. R. (2001) Glycogen synthase kinase-3: properties, functions, and regulation. Chem. Rev. 101, 2527-2540.
2. Cohen P. and Frame S. (2001) The renaissance of GSK3. Nat. Rev. Mol. Cell Biol. 2, 769-776.
3. Cross D. A., Alessi D. R., Cohen P., Andjelkovich M. and Hemmings B. A. (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789.
4. Ding J., Takano T., Gao S., Han W., Noda C., Yanagi S. and Yamamura H. (2000) Syk is required for the activation of Akt survival pathway in B cells exposed to oxidative stress. J. Biol. Chem. 275, 30873-30877.
5. Droge W. (2002) Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95.
6. Dudek H., Datta S. R., Franke T. F., Birnbaum M. J., Yao R., Cooper G. M., Segal R. A., Kaplan D. R. and Greenberg M. E. (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275, 661-665.
7. English J., Pearson G., Wilsbacher J., Swantek J., Karandikar M., Xu S. and Cobb M. H. (1999) New insights into the control of MAP kinase pathways. Exp. Cell Res. 253, 255-270.
8. Ferrer I., Blanco R., Carmona M., Ribera R., Goutan E., Puig B., Rey M. J., Cardozo A., Vinals F. and Ribalta T. (2001) Phosphorylated Map kinase (ERK1, ERK2) expression is associated with early tau deposition in neurones and glial cells, but not with increased nuclear DNA vulnerability and cell death, in Alzheimer disease, Pick's disease, progressive supranuclear palsy and corticobasal degeneration. Brain Pathol. 11, 144-158.
9. Ferrer I., Barrachina M. and 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. (Berl.) 104, 583-591.
10. Frame S. and Cohen P. (2001) GSK3 takes centre stage more than 20 years after its discovery. Biochem. J. 359, 1-16.
11. Franke T. F., Yang S. I., Chan T. O., Datta K., Kazlauskas A., Morrison D. K., Kaplan D. R. and Tsichlis P. N. (1995) The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81, 727-736.
12. Grimes C. A. and Jope R. S. (2001) The multifaceted roles of glycogen synthase kinase 3β in cellular signaling. Prog. Neurobiol. 65, 391-426. Review.
13. 2. Role in cell survival following oxidant injury. J. Biol. Chem. 271, 4138-4142.
14. Hensley K., Floyd R. A., Zheng N. Y. et al. (1999) p38 kinase is activated in the Alzheimer's disease brain. J. Neurochem. 72, 2053-2058.
15. Huang C., Li J., Ding M., Leonard S. S., Wang L., Castranova V., Vallyathan V. and Shi X. (2001) UV induces phosphorylation of protein kinase B (Akt) at Ser-473 and Thr-308 in mouse epidermal Cl41 cells through hydrogen peroxide. J. Biol. Chem. 276, 40234-40240.
16. 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.
17. Jope R. S., Zhang L. and Song L. (2000) Peroxynitrite modulates the activation of p38 and extracellular regulated kinases in PC12 cells. Arch. Biochem. Biophys. 376, 365-370.
18. Kerkhoff E. and Rapp U. R. (2001) The Ras-Raf relationship: an unfinished puzzle. Adv. Enzyme Regul. 41, 261-267.
19. Klotz L. O., Schieke S. M., Sies H. and Holbrook N. J. (2000) Peroxynitrite activates the phosphoinositide 3-kinase/Akt pathway in human skin primary fibroblasts. Biochem. J. 352, 219-225.
20. Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
21. Leroy K. and Brion J. P. (1999) Developmental expression and localization of glycogen synthase kinase-3β in rat brain. J. Chem. Neuroanat 16, 279-293.
22. Leroy K., Boutajangout A., Authelet M., Woodgett J. R., Anderton B. H. and Brion J. P. (2002) The active form of glycogen synthase kinase-3β is associated with granulovacuolar degeneration in neurons in Alzheimer's disease. Acta Neuropathol. (Berl.) 103, 91-99.
23. Liu W., Akhand A. A., Kato M., Yokoyama I., Miyata T., Kurokawa K., Uchida K. and Nakashima I. (1999) 4-hydroxynonenal triggers an epidermal growth factor receptor-linked signal pathway for growth inhibition. J. Cell Sci. 112, 2409-2417.
24. Markesbery W. R. and Lovell M. A. (1998) Four-hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease. Neurobiol. Aging 19, 33-36.
25. Martindale J. L. and Holbrook N. J. (2002) Cellular response to oxidative stress: signaling for suicide and survival. J. Cell Physiol. 192, 1-15.
26. Montine K. S., Kim P. J., Olson S. J., Markesbery W. R. and Montine T. J. (1997) 4-hydroxy-2-nonenal pyrrole adducts in human neurodegenerative disease. J. Neuropathol. Exp. Neurol. 56, 866-871.
27. Montine K. S., Reich E., Neely M. D., Sidell K. R., Olson S. J., Markesbery W. R. and Montine T. J. (1998) Distribution of reducible 4-hydroxynonenal adduct immunoreactivity in Alzheimer disease is associated with APOE genotype. J. Neuropathol. Exp. Neurol. 57, 415-425.
28. Murai H. and 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.
29. 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.
30. Pei J. J., Braak E., Braak H., Grundke-Iqbal I., Iqbal K., Winblad B. and Cowburn R. F. (1999) Distribution of active glycogen synthase kinase 3β (GSK-3β) in brains staged for Alzheimer disease neurofibrillary changes. J. Neuropathol. Exp. Neurol. 58, 1010-1019.
31. Pei J. J., Braak H., An W. L., Winblad B., Cowburn R. F., Iqbal K. and Grundke-Iqbal I. (2002) Up-regulation of mitogen-activated protein kinases ERK1/2 and MEK1/2 is associated with the progression of neurofibrillary degeneration in Alzheimer's disease. Brain Res. Mol. Brain Res. 109, 45-55.
32. Pei J. J., Khatoon S., An W. L. et al. (2003) Role of protein kinase B in Alzheimer's neurofibrillary pathology. Acta Neuropathol. (Berl.) 105, 381-392.
33. Perry G. and Smith M. A. (1998) Is oxidative damage central to the pathogenesis of Alzheimer disease? Acta Neurol. Belg. 98, 175-179.
34. Perry G., Roder H., Nunomura A. et al. (1999) Activation of neuronal extracellular receptor kinase (ERK) in Alzheimer disease links oxidative stress to abnormal phosphorylation. Neuroreport 10, 2411-2415.
35. Plyte S. E., Hughes K., Nikolakaki E., Pulverer B. J. and Woodgett J. R. (1992) Glycogen synthase kinase-3: functions in oncogenesis and development. Biochim. Biophys. Acta 1114, 147-62.
36. Rao G. N. (1996) Hydrogen peroxide induces complex formation of SHC-Grb2-SOS with receptor tyrosine kinase and activates Ras and extracellular signal-regulated protein kinases group of mitogen-activated protein kinases. Oncogene 13, 713-719.
37. Sayre L. M., Zelasko D. A., Harris P. L., Perry G., Salomon R. G. and Smith M. A. (1997) 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease. J. Neurochem. 68, 2092-2097.
38. Shaw M. and Cohen P. (1999) Role of protein kinase B and the MAP kinase cascade in mediating the EGF-dependent inhibition of glycogen synthase kinase 3 in Swiss 3T3 cells. FEBS Lett. 461, 120-124.
39. Sonoda Y., Watanabe S., Matsumoto Y., Aizu-Yokota E. and Kasahara T. (1999) FAK is the upstream signal protein of the phosphatidy-linositol 3-kinase-Akt survival pathway in hydrogen peroxide-induced apoptosis of a human glioblastoma cell line. J. Biol. Chem. 274, 10566-10570.
40. Stambolic V. and Woodgett J. R. (1994) Mitogen inactivation of glycogen synthase kinase-3β in intact cells via serine 9 phosphorylation. Biochem. J. 303, 701-704.
41. Sturgill T. W., Ray L. B., Erikson E. and Maller J. L. (1988) Insulin-stimulated MAP-2 kinase phosphorylates and activates ribosomal protein S6 kinase II. Nature 334, 715-718.
42. Sutherland C., Leighton I. A. and Cohen P. (1993) Inactivation of glycogen synthase kinase-3β by phosphorylation: new kinase connections in insulin and growth-factor signalling. Biochem. J. 296, 15-19.
43. Takeda A., Smith M. A., Avilá J., Nunomura A., Siedlak S. L., Zhu X., Perry G. and Sayre L. M. (2000) In Alzheimer's disease, heme oxygenase is coincident with Alz50, an epitope of τ induced by 4-hydroxy-2-nonenal modification. J. Neurochem. 75, 1234-1241.
44. Tanoue T., Adachi M., Moriguchi T. and Nishida E. (2000) A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat. Cell Biol. 2, 110-116.
45. Tanoue T., Maeda R., Adachi M. and Nishida E. (2001) Identification of a docking groove on ERK and p38 MAP kinases that regulates the specificity of docking interactions. EMBO J. 20, 466-479.
46. Tsukagoshi H., Kawata T., Shimizu Y., Ishizuka T., Dobashi K. and Mori M. (2002) 4-Hydroxy-2-nonenal enhances fibronectin production by IMR-90 human lung fibroblasts partly via activation of epidermal growth factor receptor-linked extracellular signal-regulated kinase p44/42 pathway. Toxicol. Appl. Pharmacol. 184, 127-135.
47. Tumilowicz J. J., Nichols W. W., Cholon J. J. and Greene A. E. (1970) Definition of a continuous human cell line derived from neuroblastoma. Cancer Res. 30, 2110-2118.
48. Wang Q. M., Fiol C. J., DePaoli-Roach A. A. and Roach P. J. (1994) Glycogen synthase kinase-3β is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation. J. Biol. Chem. 269, 14566-14574.
49. Wang X., Martindale J. L., Liu Y. and Holbrook N. J. (1998) The cellular response to oxidative stress: influences of mitogen-activated protein kinase signalling pathways on cell survival. Biochem. J. 333, 291-300.
50. Wang X., McCullough K. D., Franke T. F. and Holbrook N. J. (2000) Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J. Biol. Chem. 275, 14624-14631.
51. Wataya T., Nunomura A., Smith M. A. et al. (2002) High molecular weight neurofilament proteins are physiological substrates of adduction by the lipid peroxidation product hydroxynonenal. J. Biol. Chem. 277, 4644-4648.
52. Whitmarsh A. J. and Davis R. J. (1998) Structural organization of MAP-kinase signaling modules by scaffold proteins in yeast and mammals. Trends Biochem. Sci. 23, 481-485.
53. Zhang P., Wang Y. Z., Kagan E. and Bonner J. C. (2000) Peroxynitrite targets the epidermal growth factor receptor, Raf-1, and MEK independently to activate MAPK. J. Biol. Chem. 275, 22479-22486.
54. Zhu X., Castellani R. J., Takeda A., Nunomura A., Atwood C. S., Perry G. and Smith M. A. (2001) Differential activation of neuronal ERK, JNK/SAPK and p38 in Alzheimer disease: the 'two hit' hypothesis. Mech. Ageing Dev. 123, 39-46.
55. Zhu X., Sun Z., Lee H. G., Siedlak S. L., Perry G. and Smith M. A. (2003) Distribution, levels, and activation of MEK1 in Alzheimer's disease. J. Neurochem. 86, 136-142.