Akt/GSK3β signaling is involved in fipronil-induced apoptotic cell death of human neuroblastoma SH-SY5Y cells

Toxicology Letters

Volumn 202, Issue 2, 2011, Pages 133-141

  Lee, Jeong Eun ^a   Kang, Jin Sun ^a   Ki, Yeo Woon ^a   Lee, Sang Hun ^a   Lee, Soo Jin ^a   Lee, Kyung Suk ^b   Koh, Hyun Chul ^a  

^a Hanyang University   (South Korea)

^b National Institute of Animal Science   (South Korea)

Author keywords

Akt GSK3 ; Apoptosis; Fipronil; Human dopaminergic neuroblastoma SH SY5Y cells; Reactive oxygen species

Indexed keywords

CASPASE 3; CYTOCHROME C; DOPAMINE; FIPRONIL; GLUTAMATE DECARBOXYLASE 65; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN P53; REACTIVE OXYGEN METABOLITE; TYROSINE 3 MONOOXYGENASE;

APOPTOSIS; ARTICLE; CELL SURVIVAL; CELL VIABILITY; CYTOSOL; CYTOTOXICITY; DOPAMINERGIC NERVE CELL; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME RELEASE; GABAERGIC SYSTEM; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; CELL LINE, TUMOR; CELL SURVIVAL; CYTOCHROMES C; GLYCOGEN SYNTHASE KINASE 3; HUMANS; INSECTICIDES; MICROSCOPY, FLUORESCENCE; NEURONS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRAZOLES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

HEXAPODA;

EID: 79952627440     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2011.01.030     Document Type: Article

References (56)

1. Avila J., Hernandez F. GSK-3 inhibitions for Alzheimer's disease. Expert. Rev. Neurother. 2007, 7:1527-1533.
2. Avraham E., Szargel R., Eyal A., Rott R., Engelender S. Glycogen synthase kinase 3beta modulates synphilin-1 ubiquitylation and cellular inclusion formation by SIAH: implications for proteasomal function and Lewy body formation. J. Biol. Chem. 2005, 280:42877-42886.
3. Beaulieu J.M., Sotnikova T.D., Yao W.D., Kockeritz L., Woodgett J.R., Gainetdinov R.R., Caron M.G. Lithium antagonizes dopamine-dependent behaviors mediated by an AKT/glycogen synthase kinase 3 signaling cascade. Proc. Natl. Acad. Sci. USA 2004, 101:5099-5104.
4. Bonneh-Barkay D., Langston W.J., Di Monte D.A. Toxicity of redox cycling pesticides in primary mesencephalic cultures. Antioxid. Redox. Signal. 2005, 7:649-653.
5. Chen G., Bower K.A., Ma C., Fang S., Thiele C.J. Glycogen synthase kinase 3beta(GSK3beta) mediates 6-hydroxydopamine-induced neuronal death. FASEB J. 2004, 18:1162-1164.
6. Das P.C., Cao Y., Cherrington N., Hodgson E., Rose R.L. Fipronil induces CYP isoforms and cytotoxicity in human hepatocytes. Chem. Biol. Interact. 2006, 164:200-214.
7. Datta S.R., Dudek H., Tao S., Masters S., Fu H., Gotoh Y., Greenberg M.E. Akt phosphorylation of BAD couples survival signals to the cell intrinsic death machinery. Cell 1997, 91:231-241.
8. De Sarno P., Li X., Jope R.S. Regulation of Akt and glycogen synthase kinase-3 beta phosphorylation by sodium valproate and lithium. Neuropharmacology 2002, 43:1158-1164.
9. DiCiero Miranda M., de Bruin V.M., Vale M.R., Viana G.S. Lipid peroxidation and nitrite plus nitrate levels in brain tissue from patients with Alzheimer's disease. Gerontology 2000, 46:179-184.
10. Dinis-Oliveira R.J., Remião F., Carmo H., Duarte J.A., Navarro A.S., Bastos M.L., Chavalho F. Paraquat exposure as an etiological factor of Parkinson's disease. Neurotoxicology 2006, 27:1110-1122.
11. Dominik H., Loretta M.C., Casida J.E. Mechanisms for selective toxicity of fipronil insecticide and its sulfone metabolite and desulfinyl photoproduct. Chem. Res. Toxicol. 1998, 11:1529-1535.
12. Embi N., Rylatt D.B., Cohen P. Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclin-AMP-dependent protein kinase and phosphorylase kinase. Eur. J. Biochem. 1980, 107:519-527.
13. Frame S., Cohen P. GSK3 takes centre stage more than 20 years after its discovery. Biochem. J. 2001, 359:11-16.
14. Grimes C.A., Jope R.S. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog. Neurobiol. 2001, 65:391-426.
15. Hetman M., Cavanaugh J.E., Kimelman D., Xia Z. Role of glycogen synthase kinase-3β in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 2000, 20:2567-2574.
16. Hockenbery D.M., Oltvai Z.N., Yin X.M., Milliman C.L., Korsmeyer S.J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 1993, 75:241-251.
17. Hu J.M., Zhu X.Z. Rotenone-induced neurotoxicity of THP-1 cells requires production of reactive oxygen species and activation of phosphatidylinositol-3-kinase. Brain Res. 2007, 1153:12-19.
18. Ikeda T., Zhao X., Nagata K., Kono Y., Yeh J.Z., Narahashi T. Fipronil modulation of gamma-aminobutyric acid(A) receptors in rat dorsal root ganglion neurons. J. Pharmacol. Exp. Ther. 2001, 296:914-921.
19. Jenner P. Oxidative stress in Parkinson's disease. Ann. Neurol. 2003, 3:26-36.
20. Jope R.S. Lithium and GSK-3: one inhibitor, two inhibitory actions, multiple outcomes. Trends Pharmacol. Sci. 2003, 24:441-443.
21. Julien L., Véronique G., Nicole P.H., Marion C. Fipronil-induced disruption of thyroid function in rats is mediated by increased total and free thyroxine clearances concomitantly to increased activity of hepatic enzymes. Toxicology 2009, 255:38-44.
22. Kane D.J., Sarafian T.A., Anton R., Hahn H., Gralla E.B., Valentine J.S., Ord T., Bredesen D.E. Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science 1993, 262:1274-1277.
23. Kang M.J., Gil S.J., Koh H.C. Paraquat induces alternation of the dopamine catabolic pathways and glutathione levels in the substantia nigra of mice. Toxicol. Lett. 2009, 188:148-152.
24. King T.D., Bijur G.N., Jope R.S. Caspase-3 activation induced by mitochondrial complex I is facilitated by glycogen synthase kinase-2beta and attenuated by lithium. Brain Res. 2001, 919:106-114.
25. King T.D., Jope R.S. Inhibition of glycogen synthase kinase-3 protects cells from intrinsic but not extrinsic oxidative stress. Neuroreport 2005, 16:597-601.
26. Kitazawa M., Anantharam V., Kanthasamy A.G. Dieldrin induces apoptosis by promoting caspase-3-dependent proteolytic cleavage of protein kinase Cdelta in dopaminergic cells: relevance to oxidative stress and dopaminergic degeneration. Neuroscience 2003, 119:945-964.
27. Klintworth H., Newhouse K., Li T., Choi W.S., Faigle R., Xia Z. Activation of c-Jun N-terminal protein kinase is a common mechanism underlying paraquat- and rotenone-induced dopaminergic cell apoptosis. Toxicol. Sci. 2007, 97:149-162.
28. Koh S.H., Noh M.Y., Kim S.H. Amyloid-beta-induced neurotoxicity is reduced by inhibition of glycogen synthase kinase-3. Brain Res. 2008, 1188:254-262.
29. Kunick C., Lauenroth K., Leost M., Meijer L., Lemcke T. 1-Azakenpaullone is a selective inhibitor of glycogen synthase kinase-3 beta. Bioorg. Med. Chem. Lett. 2004, 14:413-416.
30. Lassiter T., Mackillop E.A., Ryde I.T., Seidler F.J., Slotkin T.A. Is fipronil safer than chlorpyrifos? Comparative developmental neurotoxicity modeled in PC12 cells. Brain Res. Bull. 2009, 78:313-322.
31. Lee C.S., Park W.J., Ko H.H., Han E.S. Differential involvement of mitochondrial permeability transition in cytotoxicity of 1-methyl-4-phenylpyridinium and 6-hydroxydopamine. Mol. Cell. Biochem. 2006, 289:193-200.
32. Li X., Friedman A.B., Zhu W., Wang L., Boswell S., May R.S., Davis L.L., Jope R.S. Lithium regulates glycogen synthase kinase-3beta in human peripheral blood mononuclear cells: implication in the treatment of bipolar disorder. Biol. Psychiatry 2007, 61:216-222.
33. Lizcano J.M., Alessi D.R. The insulin signalling pathway. Curr. Biol. 2002, 12:236-238.
34. Lotharius J., Dugan L.L., O'Malley K.L. Distinct mechanisms underlie neurotoxin-mediated cell death in cultured dopaminergic neurons. J. Neurosci. 1999, 19:1284-1293.
35. Lotharius J., O'Malley K.L. The parkinsonism-inducing drug 1-methyl-4-phenylpyridinium triggers intracellular dopamine oxidation. A novel mechanism of toxicity. J. Biol. Chem. 2000, 275:38581-38588.
36. Martinez A., Alonso M., Castro A., Pérez 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, 45:1292-1299.
37. Mori A., Ohashi S., Nakai M., Moriizumi T., Mitsumoto Y. Neural mechanisms underlying motor dysfunction as detected by the tail suspension test in MPTP-treated C57BL/6 mice. Neurosci. Res. 2005, 51:265-274.
38. Muyllaert D., Kremer A., Jaworski T., Borghgraef P., Devijver H. Glycogen synthase kinase-3beta, or a link between amyloid and tau pathology?. Genes Brain Behav. 2008, 7(Suppl. 1):57-66.
39. Pap M., Cooper G.M. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J. Biol. Chem. 1998, 273:19929-19932.
40. Perier C., Tieu K., Guégan C., Caspersen C., Jackson-Lewis V., Carelli V., Martinuzzi A., Hirano M., Przedborski S., Vila M. Complex I deficiency primes Bax-dependent neuronal apoptosis through mitochondrial oxidative damage. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:19126-19131.
41. Petit-Paitel A., Brau F., Cazareth J., Chabry J. Involvement of cytosolic and mitochondrial GSK-3beta in mitochondrial dysfunction and neuronal cell death of MPTP/MPP-treated neurons. PLoS One 2009, 4:e5491.
42. Przedborski S., Vila M. The 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model: a tool to explore the pathogenesis of Parkinson's disease. Ann. N. Y. Acad. Sci. 2003, 991:189-198.
43. Ratra G.S., Erkkila B.E., Weiss D.S., Casida J.E. Unique insecticide specificity of human homomeric rho 1 GABA(C) receptor. Toxicol. Lett. 2002, 129:47-53.
44. Richardson J.R., Quan Y., Sherer T.B., Greenamyre J.T., Miller G.W. Paraquat neurotoxicity is distinct from that of MPTP and rotenone. Toxicol. Sci. 2005, 88:193-201.
45. Saulsbury M.D., Heyliger S.O., Wang K., Johnson D.J. Chlorpyrifos induces oxidative stress in oligodendrocyte progenitor cells. Toxicology 2009, 259:1-9.
46. Shen J.H., Zhan Y., Wu N.H., Shen Y.F. Resistance to geldanamycin-induced apoptosis in differentiated neuroblastoma SH-SY5Y cells. Neurosci. Lett. 2007, 414:110-114.
47. Stehr C.M., Linbo T.L., Incardona J.P., Scholz N.L. The developmental neurotoxicity of fipronil: notochord degeneration and locomotor defects in zebrafish embryos and larvae. Toxicol. Sci. 2006, 92:270-278.
48. Steinman H.M. The Bcl-2 oncoprotein functions as a pro-oxidant. J. Biol. Chem. 1995, 270:3487-3490.
49. Tingle C.C., Rother C.F., Lauer D.S., King W.J. Fipronil: environmental fate, ecotoxicology, and human health concerns. Rev. Environ. Contam. Toxicol. 2003, 176:1-66.
50. Varró P., Gyori J., Világi I. In vitro effects of fipronil on neuronal excitability in mammalian and molluscan nervous systems. Ann. Agric. Environ. Med. 2009, 16:71-77.
51. Vogelstein B., Lane D., Levine A.J. Surfing the p53 network. Nature 2000, 408:307-310.
52. Wang W., Yang Y., Ying C., Li W., Ruan H., Zhu X., You Y., Han Y., Chen R., Wang Y., Li M. Inhibition of glycogen synthase kinase-3beta protects dopaminergic neurons from MPTP toxicity. Neuropharmacology 2007, 52:678-684.
53. Watabe M., Nakaki T. Mitochondrial complex 1 inhibitor rotenone-elicited dopamine redistribution from vesicles to cytosol in human dopaminergic SH-SY5Y cells. J. Pharmacol. Exp. Ther. 2007, 323:499-507.
54. Woodgett J.R., Cohen P. Multisite phosphorylation of glycogen synthase Molecular basis for the substrate specificity of glycogen synthase kinase-3 and casein kinase-II(glycogen synthase kinase-5). Biochem. Biophys. Acta 1984, 788:339-347.
55. Yoshimoto T., Uchino H., He Q.P., Li P.A., Siesjo B.K. Cyclosporin A, but not FK506, prevents the downregulation of phosphorylated Akt after transient focal ischemia in the rat. Brain Res. 2001, 899:148-158.
56. Youdim M.B., Arraf Z. Prevention of MPTP (N-methyl-4-phenyl-1,2,3,6-tetra-hydropyridine) dopaminergic neurotoxicity in mice by chronic lithium: involvements of Bcl-2 and Bax. Neuropharmacology 2004, 46:1130-1140.