Endosulfan upregulates AP-1 binding and ARE-mediated transcription via ERK1/2 and p38 activation in HepG2 cells

Toxicology

Volumn 292, Issue 1, 2012, Pages 23-32

  Song, Min Ok ^a,b   Lee, Chang Ho ^c   Yang, Hyun Ok ^b   Freedman, Jonathan H ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b Korea Institute of Science and Technology   (South Korea)

^c Gangneung Wonju National University   (South Korea)

Author keywords

AP 1; ARE; Endosulfan; ERK; HepG2; P38

Indexed keywords

ENDOSULFAN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN C JUN; TRANSCRIPTION FACTOR AP 1;

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CELL STRAIN HEPG2; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; UPREGULATION;

ENDOSULFAN; ENZYME ACTIVATION; HEP G2 CELLS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; P38 MITOGEN-ACTIVATED PROTEIN KINASES; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 84855333939     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2011.11.013     Document Type: Article

References (68)

1. Agarwal D.K., Seth P.K., Gupta P.K. Effect of endosulfan on drug metabolizing enzymes and lipid peroxidation in rat. J. Environ. Sci. Health C 1978, 13:49-62.
2. Antherieu S., Ledirac N., Luzy A.P., Lenormand P., Caron J.C., Rahmani R. Endosulfan decreases cell growth and apoptosis in human HaCaT keratinocytes: partial ROS-dependent ERK1/2 mechanism. J. Cell. Physiol. 2007, 213:177-186.
3. Banerjee B.D., Hussain Q.Z. Effect of sub-chronic endosulfan exposure on humoral and cell-mediated immune responses in albino rats. Arch. Toxicol. 1986, 59:279-284.
4. Becker L., Scheringer M., Schenker U., Hungerbuhler K. Assessment of the environmental persistence and long-range transport of endosulfan. Environ. Pollut. 2011, 159:1737-1743.
5. Bergelson S., Pinkus R., Daniel V. Induction of AP-1 (Fos/Jun) by chemical agents mediates activation of glutathione S-transferase and quinone reductase gene expression. Oncogene 1994, 9:565-571.
6. Bulayeva N.N., Watson C.S. Xenoestrogen-induced ERK-1 and ERK-2 activation via multiple membrane-initiated signaling pathways. Environ. Health Perspect. 2004, 112:1481-1487.
7. Bursztyka J., Perdu E., Pettersson K., Pongratz I., Fernandez-Cabrera M., Olea N., Debrauwer L., Zalko D., Cravedi J.P. Biotransformation of genistein and bisphenol A in cell lines used for screening endocrine disruptors. Toxicol. In Vitro 2008, 22:1595-1604.
8. Ceron J.J., Panizo C.G., Montes A. Toxicological effects in rabbits induced by endosulfan, lindane, and methylparathion representing agricultural byproducts contamination. Bull. Environ. Contam. Toxicol. 1995, 54:258-265.
9. Choi E.Y., Park Z.Y., Choi E.J., Oh H.M., Lee S., Choi S.C., Lee K.M., Im S.H., Chun J.S., Jun C.D. Transcriptional regulation of IL-8 by iron chelator in human epithelial cells is independent from NF-kappa B but involves ERK1/2-and p38 kinase-dependent activation of AP-1. J. Cell. Biochem. 2007, 102:1442-1457.
10. Cobb M.H., Goldsmith E.J. How MAP kinases are regulated. J. Biol. Chem. 1995, 270:14843-14846.
11. Dalsenter P.R., Dallegrave E., Mello J.R., Langeloh A., Oliveira R.T., Faqi A.S. Reproductive effects of endosulfan on male offspring of rats exposed during pregnancy and lactation. Hum. Exp. Toxicol. 1999, 18:583-589.
12. Dalton T.P., Shertzer H.G., Puga A. Regulation of gene expression by reactive oxygen. Annu. Rev. Pharmacol. Toxicol. 1999, 39:67-101.
13. Davis R.J. Transcriptional regulation by MAP kinases. Mol. Reprod. Dev. 1995, 42:459-467.
14. Dehn P.F., Allen-Mocherie S., Karek J., Thenappan A. Organochlorine insecticides: impacts on human HepG2 cytochrome P4501A, 2B activities and glutathione levels. Toxicol. In Vitro 2005, 19:261-273.
15. Desalegn B., Takasuga T., Harada K.H., Hitomi T., Fujii Y., Yang H.R., Wang P., Senevirathna S., Koizumi A. Historical trends in human dietary intakes of endosulfan and toxaphene in China, Korea and Japan. Chemosphere 2011, 83:1398-1405.
16. Favreau L.V.a.C.B.P. Transcriptional regulation of the rat NAD(P)H:quinone reductase gene. Identification of regulatory elements controlling basal and inducible expression by planar aromatic compounds and phenolic antioxidants. J. Biol. Chem. 1991, 266:4556-4561.
17. Frigo D.E., Tang Y., Beckman B.S., Scandurro A.B., Alam J., Burow M.E., McLachlan J.A. Mechanism of AP-1-mediated gene expression by select organochlorines through the p38 MAPK pathway. Carcinogenesis 2003, 25(2):249-261.
18. Gupta P.K., Gupta R.C. Pharmacology, toxicology and degradation of endosulfan: a review. Toxicology 1979, 13:115-130.
19. Hack R., Ebert E., Leist K.H. Chronic toxicity and carcinogenicity studies with the insecticide endosulfan in rats and mice. Food Chem. Toxicol. 1995, 33:941-950.
20. Hincal F., Gurbay A., Giray B. Induction of lipid peroxidation and alteration of glutathione redox status by endosulfan. Biol. Trace Elem. Res. 1995, 47:321-326.
21. Huang H.P., Chang Y.C., Wu C.H., Hung C.N., Wang C.J. Anthocyanin-rich Mulberry extract inhibit the gastric cancer cell growth in vitro and xenograft mice by inducing signals of p38/p53 and c-jun. Food Chem. 2011, 129:1703-1709.
22. Jaiswal A.K. Jun and Fos regulation of NAD(P)H:quinone oxidoreductase gene expression. Pharmacogenetics 1994, 4:1-10.
23. Jeyapaul J., Jaiswal A.K. Nrf2 and c-Jun regulation of antioxidant response element (ARE)-mediated expression and induction of gamma-glutamylcysteine synthetase heavy subunit gene. Biochem. Pharmacol. 2000, 59:1433-1439.
24. Junttila M.R., Li S.P., Westermarck J. Phosphatase-mediated crosstalk between MAPK signalling pathways in the regulation of cell survival. FASEB J. 2008, 22:954-965.
25. Kamijima M., Casida J.E. Regional modification of [(3)H]ethynylbicycloorthobenzoate binding in mouse brain GABA(A) receptor by endosulfan, fipronil, and avermectin B(1a). Toxicol. Appl. Pharmacol. 2000, 163:188-194.
26. Kang K.S., Park J.E., Ryu D.Y., Lee Y.S. Effects and neuro-toxic mechanisms of 2,2',4,4',5,5'-hexachlorobiphenyl and endosulfan in neuronal stem cells. J. Vet. Med. Sci. 2001, 63:1183-1190.
27. Kannan K., Holcombe R.F., Jain S.K., Alvarez-Hernandez X., Chervenak R., Wolf R.E., Glass J. Evidence for the induction of apoptosis by endosulfan in a human T-cell leukemic line. Mol. Cell. Biochem. 2000, 205:53-66.
28. Kannan K., Jain S.K. Oxygen radical generation and endosulfan toxicity in Jurkat T-cells. Mol. Cell. Biochem. 2003, 247:1-7.
29. Karatas A.D., Aygun D., Baydin A. Characteristics of endosulfan poisoning: a study of 23 cases. Singapore Med. J. 2006, 47:1030-1032.
30. Karin M. The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 1995, 270:16483-16486.
31. Karin M., Liu Z., Zandi E. AP-1 function and regulation. Curr. Opin. Cell Biol. 1997, 9:240-246.
32. Kockel L., Zeitlinger J., Staszewski L.M., Mlodzik M., Bohmann D. Jun in Drosophila development: redundant and nonredundant functions and regulation by two MAPK signal transduction pathways. Genes Dev. 1997, 11:1748-1758.
33. Ledirac N., Antherieu S., d'Uby A.D., Caron J.C., Rahmani R. Effects of organochlorine insecticides on MAP kinase pathways in human HaCaT keratinocytes: key role of reactive oxygen species. Toxicol. Sci. 2005, 86:444-452.
34. Leppa S., Saffrich R., Ansorge W., Bohmann D. Differential regulation of c-Jun by ERK and JNK during PC12 cell differentiation. EMBO J. 1998, 17:4404-4413.
35. Li X., Zhang S., Safe S. Activation of kinase pathways in MCF-7 cells by 17beta-estradiol and structurally diverse estrogenic compounds. J. Steroid Biochem. Mol. Biol. 2006, 98:122-132.
36. Meister A. Glutathione deficiency produced by inhibition of its synthesis, and its reversal; applications in research and therapy. Pharmacol. Ther. 1991, 51:155-194.
37. Otto D.M., Sen C.K., Casley W.L., Moon T.W. Regulation of cytochrome P4501A metabolism by glutathione. Pharmacol. Toxicol. 1999, 84:201-210.
38. Peverali F.A., Isaksson A., Papavassiliou A.G., Plastina P., Staszewski L.M., Mlodzik M., Bohmann D. Phosphorylation of Drosophila Jun by the MAP kinase rolled regulates photoreceptor differentiation. EMBO J. 1996, 15:3943-3950.
39. Pulverer B.J., Kyriakis J.M., Avruch J., Nikolakaki E., Woodgett J.R. Phosphorylation of c-jun mediated by MAP kinases. Nature 1991, 353:670-674.
40. Ravingerova T., Barancik M., Strniskova M. Mitogen-activated protein kinases: a new therapeutic target in cardiac pathology. Mol. Cell. Biochem. 2003, 247:127-138.
41. Roe A.L., Snawder J.E., Benson R.W., Roberts D.W., Casciano D.A. HepG2 cells: an in vitro model for P450-dependent metabolism of acetaminophen. Biochem. Biophys. Res. Commun. 1993, 190:15-19.
42. Rushmore T.H., Morton M.R., Pickett C.B. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J. Biol. Chem. 1991, 266:11632-11639.
43. Schaeffer H.J., Weber M.J. Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol. Cell. Biol. 1999, 19:2435-2444.
44. Schnidar H., Eberl M., Klingler S., Mangelberger D., Kasper M., Hauser-Kronberger C., Regl G., Kroismayr R., Moriggl R., Sibilia M., Aberger F. Epidermal growth factor receptor signaling synergizes with Hedgehog/GLI in oncogenic transformation via activation of the MEK/ERK/JUN pathway. Cancer Res. 2009, 69:1284-1292.
45. Sen C.K., Packer L. Antioxidant and redox regulation of gene transcription. FASEB J. 1996, 10:709-720.
46. Sethunathan N., Megharaj M., Chen Z., Singh N., Kookana R.S., Naidu R. Persistence of endosulfan and endosulfan sulfate in soil as affected by moisture regime and organic matter addition. Bull. Environ. Contam. Toxicol. 2002, 68:725-731.
47. Shaulian E., Karin M. AP-1 as a regulator of cell life and death. Nat. Cell Biol. 2002, 4:E131-E136.
48. Shokri F., Heidari M., Gharagozloo S., Ghazi-Khansari M. In vitro inhibitory effects of antioxidants on cytotoxicity of T-2 toxin. Toxicology 2000, 146:171-176.
49. Singh N.D., Sharma A.K., Dwivedi P., Patil R.D., Kumar M. Citrinin and endosulfan induced teratogenic effects in Wistar rats. J. Appl. Toxicol. 2007, 27:143-151.
50. Singh S.K., Pandey R.S. Toxicity of endosulfan on kidney of male rats in relation to drug metabolizing enzymes and microsomal lipid peroxidation. Indian J. Exp. Biol. 1989, 27:725-728.
51. Sinha N., Narayan R., Shanker R., Saxena D.K. Endosulfan-induced biochemical changes in the testis of rats. Vet. Hum. Toxicol. 1995, 37:547-549.
52. Smeal T., Binetruy B., Mercola D.A., Birrer M., Karin M. Oncogenic and transcriptional cooperation with Ha-Ras requires phosphorylation of c-Jun on serines 63 and 73. Nature 1991, 354:494-496.
53. Smeal T., Binetruy B., Mercola D., Grover-Bardwick A., Heidecker G., Rapp U.R., Karin M. Oncoprotein-mediated signalling cascade stimulates c-Jun activity by phosphorylation of serines 63 and 73. Mol. Cell. Biol. 1992, 12:3507-3513.
54. Sohn H.Y., Kwon C.S., Kwon G.S., Lee J.B., Kim E. Induction of oxidative stress by endosulfan and protective effect of lipid-soluble antioxidants against endosulfan-induced oxidative damage. Toxicol. Lett. 2004, 151:357-365.
55. 2(-)-ATPase by endosulfan in rat brain. J. Toxicol. Environ. Health 1989, 28:473-481.
56. Su B., Karin M. Mitogen-activated protein kinase cascades and regulation of gene expression. Curr. Opin. Immunol. 1996, 8:402-411.
57. Suolinna E.M. Isolation and culture of liver cells and their use in the biochemical research of xenobiotics. Med. Biol. 1982, 60:237-254.
58. Sutherland T.D., Home I., Weir K.M., Russell R.J., Oakeshott J.G. Toxicity and residues of endosulfan isomers. Rev. Environ. Contam. Toxicol. 2004, 183:99-113.
59. Taylor L.M., Khachigian L.M. Induction of platelet-derived growth factor B-chain expression by transforming growth factor-beta involves transactivation by Smads. J. Biol. Chem. 2000, 275:16709-16716.
60. Tharappel J.C., Lee E.Y., Robertson L.W., Spear B.T., Glauert H.P. Regulation of cell proliferation, apoptosis, and transcription factor activities during the promotion of liver carcinogenesis by polychlorinated biphenyls. Toxicol. Appl. Pharmacol. 2002, 179:172-184.
61. Torres M., Forman H.J. Redox signaling and the MAP kinase pathways. Biofactors 2003, 17:287-296.
62. Turner K.O., Syvanen M., Meizel S. The human acrosome reaction is highly sensitive to inhibition by cyclodiene insecticides. J. Androl. 1997, 18:571-575.
63. Turpaev K.T. Reactive oxygen species and regulation of gene expression. Biochemistry (Mosc.) 2002, 67:281-292.
64. Waskiewicz A.J., Cooper J.A. Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast. Curr. Opin. Cell Biol. 1995, 7:798-805.
65. Wilkening S., Bader A. Influence of culture time on the expression of drug-metabolizing enzymes in primary human hepatocytes and hepatoma cell line HepG2. J. Biochem. Mol. Toxicol. 2003, 17:207-213.
66. Yavuz Y., Yurumez Y., Kucuker H., Ela Y., Yuksel S. Two cases of acute endosulfan toxicity. Clin. Toxicol. (Phila.) 2007, 45:530-532.
67. Yu R., Lei W., Mandlekar S., Weber M.J., Der C.J., Wu J., Kong A.T. Role of a mitogen-activated protein kinase pathway in the induction of phase II detoxifying enzymes by chemicals. J. Biol. Chem. 1999, 274:27545-27552.
68. Zeiger M., Haag R., Hockel J., Schrenk D., Schmitz H.J. Inducing effects of dioxin-like polychlorinated biphenyls on CYP1A in the human hepatoblastoma cell line HepG2, the rat hepatoma cell line H4IIE, and rat primary hepatocytes: comparison of relative potencies. Toxicol. Sci. 2001, 63:65-73.