Activation of c-Jun N-terminal kinase in A549 lung carcinoma cells by sodium dichromate: Role of dissociation of apoptosis signal regulating kinase-1 from its physiological inhibitor thioredoxin

Toxicology

Volumn 197, Issue 2, 2004, Pages 100-111

  Hodges, N J ^a   Smart, D ^a   Lee, A J ^a   Lewis, N A ^a   Chipman, J K ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

8 oxo 2 deoxyguanosine; 8 oxodG; Apoptosis signal regulating kinase 1; ASK 1; GSH; Inhibitory kappa B; I B; JNK; Jun N terminal kinase; MAP; Mitogen activated protein; NF B; Nuclear factor kappa B; Reactive oxygen species; Reduced glutathione; ROS; Trx

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1; DICHROMATE SODIUM; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOTAGMIN; THIOREDOXIN;

ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; CYTOSOL; DISSOCIATION; DOWNSTREAM PROCESSING; ENZYME ACTIVATION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LUNG CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STIMULATION; TIME; WESTERN BLOTTING;

EID: 1442348218     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2003.12.004     Document Type: Article

References (67)

1. Arrifo A.-P. Gene expression and the thiol redox state. Free Radic. Biol. Med. 27:1999;936-944.
2. Bagchi D., Bagchi M., Hassoun E.A., Stohs S.J. Chromium(VI) induced oxidative stress, apoptotic cell death and modulation of p53 tumour suppressor gene. Mol. Cell. Biochem. 222:2001;149-158.
3. Bagchi D., Stohs S.J., Downs B.W., Bagchi M., Preuss H.G. Cytotoxicity and oxidative mechanisms of different forms of chromium. Toxicology. 180:2002;5-22.
4. Berry A., Goodwin M., Moran C.L., Chambers T.C. AP-1 activation and altered AP-1 composition in association with increased phosphorylation and expression of specific Jun and Fos family proteins induced by vinblastine in KB-3 cells. Biochem. Pharmacol. 62:2001;581-591.
5. Blasiak J., Kowalik J. A comparison of the in vitro genotoxicity of tri- and hexavalent chromium. Mutat. Res. 469:2000;135-145.
6. Bloomfield K.L., Osborne S.A., Kennedy D.D., Clarke F.M., Tonissen K.F. Thioredoxin-mediated redox control of the transcription factor Sp1 and regulation of the thioredoxin gene promoter. Gene. 319:2003;107-116.
7. Bridgewater L.C., Manning F.C.R., Patierno S.R. Base-specific arrest of in vitro DNA replication by carcinogenic chromium: relationship to DNA interstrand cross linking. Carcinogenesis. 15:1994;2421-2427.
8. Cabantchik Z.I., Knauf P.A., Rothstein A. The anion transport system of the re blood cell. The role of membrane protein evaluated by the use of probes. Biochem. Biophys. Acta. 515:1978;239-302.
9. Chen Y.R., Wang X., Templeton D., Davis R.J., Tan T.H. The role of c-jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and γ irradiation. J. Biol. Chem. 271:1996;31929-31936.
10. Chen F., Ding M., Lu Y., Leonard S.S., Vallyathan V., Castranova V., Shi X. Participation of MAP kinase p38 and IkappaB kinase in chromium(VI)-induced NF-kappaB and AP-1 activation. Pathol. Toxicol. Oncol. 19:2000;231-238.
11. Chen F., Ding M., Castranova V., Shi X. Carcinogenic metals and NF-κB activation. Mol. Cell. Biochem. 222:2001;159-171.
12. Chen F., Bower J., Leonard S.S., Ding M., Lu Y., Rojanasakul Y., Kung H.-F., Vallyathan V., Castranova V., Shi X. Protective roles of NF-kB for chromium(VI)-induced cytotoxicity is revealed by expression of IkB kinase mutant. J. Biol. Chem. 277:2002;3342-3349.
13. Cho S.G., Lee Y.H., Park H.S., Ryoo K., Kang K.W., Park J., Eom S.J., Kim M.J., Chang T.S., Choi S.Y., Shim J., Kim Y., Lee M.J., Sesa D., Kim S.G., Ichijo H., Choi E.J. Glutathione S-transferase mu modulates the stress-activated signals by suppressing apoptosis signal regulating kinase-1. J. Biol. Chem. 276:2001;12749-12755.
14. Chuang S.-M., Liou G.Y., Yang J.L. Activation of JNK, p38 and ERK mitogen-activated protein kinases by chromium(VI) is mediated through oxidative stress but does not affect cytotoxicity. Carcinogenesis. 21:2000;1491-1500.
15. Chuang S.-M., Yang J.L. Comparison of roles of three mitogen-activated protein kinases induced by chromium(VI) and cadmium in non small cell lung carcinoma cells. Mol. Cell. Biochem. 222:2001;85-95.
16. Cohen M.D., Kargacin B., Klein C.B., Costa M. Mechanism of chromium carcinogenicity and toxicity. Crit. Rev. Toxicol. 23:1993;255-281.
17. Cupo D.Y., Wetterhahn K.E. Binding of chromium to chromatin and DNA from liver and kidney of rats. Cancer Res. 45:1985;1146-1151.
18. D'Agostini F., Izzotti A., Bennicelli C., Camoirano A., Tampa E., De Flora S. Induction of apoptosis in the lung but not in the liver of rats receiving intra-tracheal instillations of chromium(VI). Carcinogenesis. 23:2002;587-593.
19. Das K.C., Das C.K. Thioredoxin a singlet oxygen quencher and hydroxyl radical scavenger: redox independent functions. Biochem. Biophys. Res. Commun. 277:2000;443-447.
20. Didier C., kerblat I., Drouet C., Favier A., Beani J.-C., Richard M.-J. Induction of thioredoxin by ultraviolet-A radiation prevents oxidative-mediated cell death in human skin fibroblasts. Free Radic. Biol. Med. 31:2001a;585-598.
21. Didier C., Pouget J.-P., Cadet J., Favier A., Beani J.-C., Richard M.-J. Modulation of exogenous and endogenous levels of thioredoxin in human skin fibroblasts prevents DNA damaging effects of ultraviolet A radiation. Free Radic. Biol. Med. 30:2001b;537-546.
22. Dubbrovskya V.A., Wetterhahn K.E. Effects of Cr(VI) on the expression of the oxidative stress genes in human lung cells. Carcinogenesis. 19:1998;1401-1407.
23. Dunn C., Wiltshire C., MacLaren A., Gillespie D.A.F. Molecular mechanism and biological functions of c-Jun N-terminal kinase signalling via the c-Jun transcription factor. Cell. Signal. 14:2002;585-593.
24. Faux S.P., Gao M., Chipman J.K., Levy L.S. Production of 8-hydroxydeoxyguanosine in isolated DNA by chromium(VI) and chromium(V). Carcinogenesis. 13:1992;1667-1669.
25. Fernandes M.A., Geraldes C.F., Oliveira C.R., Alpoim M.C. Chromate-induced human erythrocytes haemoglobin oxidation and peroxidation: influence of vitamin E, vitamin C, salicylate, deferoxamine, and N-ethylmaleimide. Toxicol. Lett. 114:2000;237-243.
26. Gaiddon C., Moorthy N.C., Prives C. Ref-1 regulates transactivation and proapoptotic functions of p53 in vivo. EMBO J. 18:1999;5609-5621.
27. Gao M., Binks S.P., Chipman J.K., Levy L.S., Braithwaite R.A., Brown S.S. Induction of DNA strand breaks in peripheral lymphocytes by soluble chromium compounds. Hum. Exp. Toxicol. 11:1992;77-82.
28. Gon Y., Sasada T., Matsui M., Hashimoto S., Takagi Y., Iwata S., Wada H., Horie T., Yodoi J. Expression of thioredoxin in bleomycin-injured airway epithelium: possible role of protection against bleomycin induced epithelial injury. Life Sci. 68:2000;1877-1888.
29. Gotoh Y., Cooper J.A. Reactive oxygen species- and dimerisation-induced activation of apoptosis signal regulating kinase 1 in tumour necrosis factor-α signal transduction. J. Biol. Chem. 272:1998;17477-17482.
30. Haddad J.J. Antioxidant and prooxidant mechanisms in the regulation of redox(y)-sensitive transcription factors. Cell. Signal. 14:2002;879-897.
31. Hodges N.J., Ádám B., Lee A.J., Cross H.J., Chipman J.K. Induction of DNA-strand breaks in human peripheral blood lymphocytes and A549 lung cells by sodium dichromate: association with 8-oxo-2-deoxyguanosine formation and inter-individual variation. Mutagenesis. 16:2001;467-474.
32. Hodges N.J., Chipman J.K. Down-regulation of the DNA-repair endonuclease 8-oxo-guanine DNA glycosylase 1 (hOGG1) by sodium dichromate in cultured human A549 lung carcinoma cells. Carcinogenesis. 23:2002;55-60.
33. Hirota K., Murata M., Sachi Y., Nakamura H., Takeuchi J., Mori K., Yodoi J. Distinct roles of thioredoxin in the cytoplasm and in the nucleus. A two-step mechanism of redox regulation of transcription factor NF-kappaB. J. Biol. Chem. 274:1999;27891-27897.
34. Ichijo H., Nishida E., Irie K., ten Dijke P., Saitoh M., Moriguchi T., Takagi M., Matsumoto K., Miyazono K., Gotoh Y. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAP/JNK and p38 signaling pathways. Science. 275:1997;90-94.
35. Ip Y.T., Davis R.J. Signal transduction by the c-Jun N-terminal kinase (JNK) - from inflammation to development. Curr. Opin. Cell Biol. 10:1998;205-219.
36. Ishikawa Y., Yokoo T., Kitamura M. c-Jun/AP-1, but not NF-B, is a mediator for oxidant-initiated apoptosis in glomerular mesangial cells. Biochem. Biophys. Res. Commun. 240:1997;496-501.
37. Izzoti A., Cartiglia C., Balansky R., D'Agostini F., Longobardi M., De Flora S. Selective induction of gene expression in rat lung by hexavalent chromium. Mol. Carcinog. 35:2002;75-84.
38. Jeyapaul J., Jaiswal A.K. Nrf2 and c-Jun regulation of antioxidant response element (ARE)-mediated expression and induction of glutamylcysteine synthetase heavy subunit gene. Biochem. Pharmacol. 59:2000;1433-1439.
39. Kaltreieder R.C., Pesce C.A., Ihnat M.A., Lariviere J.P., Hamiltion J.W. Differential effects of arsenic(III) and chromium(VI) on nuclear transcription factor binding. Mol. Carcinog. 25:1999;219-229.
40. Kim Y.C., Yamaguchi Y., Kondo N., Masutani H., Yodoi J. Thioredoxin-dependent redox regulation of the antioxidant responsive element (ARE) in electrophile response. Oncogene. 12:2003;1860-1865.
41. Liu Y., Min W. Thioredoxin promotes ASK-1 ubiquitination and degradation to inhibit ASK-1 mediated apoptosis in a redox activity-independent manner. Circ. Res. 90:2002;1259-1266.
42. Martin B.D., Schoenhard J.A., Sugden K.D. Hypervalent chromium mimics reactive oxygen species as measured by the oxidant-sensitive dyes 2′,7′-dichlorofluorescin and dihydrorhodamine. Chem. Res. Toxicol. 11:1998;1402-1410.
43. Matsuzawa A., Ichijo H. Molecular mechanisms of the decision between life and death: regulation of apoptosis signal regulating kinase 1. J. Biochem. 130:2001;1-8.
44. Mitsui A., Hirakawa T., Yodoi Y. Reactive oxygen reducing and protein refolding activities of adult T cell leukemia-derived factor/human thioredoxin. Biochem. Biophys. Res. Commun. 186:1992;1220-1226.
45. Nishitoh N., Saitoh M., Mochida Y., Takeda K., Nakano H., Rothe M., Miyazono K., Ichijo H. ASK1 is essential for JNK/SAPK activation by TRAF2. Mol. Cell. 2:1998;389-395.
46. Nishiyama A., Ohno T., Iwata S., Matsui M., Hirota K., Masutani H., Nakamura H., Yodoi J. Demonstration of the interaction of thioredoxin with p40phox, a phagocyte oxidase component, using a yeast two-hybrid system. Immunol. Lett. 68:1999;155-159.
47. Qian Y., Jiang B.-H., Flynn D.C., Leonard S.S., Wang S., Zhang Z., Ye J., Chen F., Wang L., Shi X. Cr(VI) increases tyrosine phosphorylation through reactive oxygen species mediated reactions. Mol. Cell. Biochem. 222:2001;199-204.
48. Ruppitsch W., Meisslitzer C., Hirsch-Kaufmann M., Schweiger M. Overexpression of thioredoxin in Fanconi anemia fibroblasts prevents the cytotoxic and DNA damaging effects of mitomycin C and diepoxybutane. FEBS Lett. 422:1998;99-102.
49. Saitoh M., Nishitoh H., Fujii M., Takeda K., Tobuime K., Sawada Y., Kawabata M., Miyazono K., Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase 1 (ASK-1). EMBO J. 17:1998;2596-2606.
50. Samet J.M., Graves L.M., Quay J., Dailey L.A., Devlin R.B., Ghio A.J., Wu W., Bromberg P.A., Reed W. Activation of MAPKs in human bronchial epithelial cells exposed to metals. Am. J. Physiol. 275:1998;L551-L558.
51. Shi X., Mao Y., Knapton A.D., Ding M., Rojanasakui Y., Gannet P.M., Dalal N., Liu K. Reaction of Cr(VI) with ascorbate and hydrogen peroxide generates hydroxyl radicals and causes DNA damage: role of a Cr(IV)-mediated Fenton-like reaction. Carcinogenesis. 15:1994;2475-2478.
52. Shi X., Ding M., Ye Y., Wang S., Leonard S.S., Zang L., Castranova V., Vallyathan V., Chiu A., Dalal N., Liu K. Cr(IV) causes activation of nuclear transcription factor-κB, DNA strand breaks and dG hydroxylation via free radical reactions. J. Inorg. Biochem. 75:1999;37-44.
53. Shumilla J.A., Broderick R.J., Wang Y., Barchowsky A. Chromium(VI) inhibits the transcriptional activity of nuclear factor-B by decreasing the interaction of p65 with cAMP-responsive element-binding protein-binding protein. J. Biol. Chem. 274:1999;36207-36212.
54. Tobiume K., Matsuzawa A., Takahashi T., Nishitoh H., Morita K.I., Takeda K., Minowa O., Miyazono K., Noda T., Ichijo H. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep. 2:2001;222-228.
55. Tobiume K., Saitoh M., Ichijo H. Activation of apoptosis signal regulating kinase-1 by the stress-induced activation phosphorylation of pre-formed oligomer. J. Cell. Physiol. 191:2002;95-104.
56. Travacio M., Polo J.M., Llesuy S. Chromium(VI) induces oxidative stress in the mouse brain. Toxicology. 150:2000;137-146.
57. Wang S., Leonard S.S., Ye J., Ding M., Shi X. The role of hydroxyl radical as a messenger in Cr(VI)-induced p53 activation. Am. J. Physiol. Cell Physiol. 273:2000;C868-883.
58. Wei S.J., Botero A., Hirota K., Bradbury C.M., Markovina S., Laszlo A., Spitz D.R., Goswami P.C., Yodoi J., Gius D. Thioredoxin nuclear translocation and interaction with redox factor-1 activates the activator protein-1 transcription factor in response to ionizing radiation. Cancer Res. 60:2000;6688-6695.
59. Wenbo Q., Reiter R.J., Dun-Xian T., Garcia J.J., Manchester L.C., Karbownik K., Calvo J.R. Chromium(III)-induced 8-hydroxydeoxyguanosine in DNA and its reduction by antioxidants: comparative effects of melatonin, ascorbate and vitamin E. Environ. Health Perspect. 108:2000;399-402.
60. Wisdom R. AP-1: one switch for many signals. Exp. Cell Res. 253:1999;180-185.
61. Wise J.P., Stearns D.M., Wetterhahn K.E., Patierno S.R. Inhibition of lead chromate clastogenesis by ascorbate: relationship to particle dissolution and uptake. Carcinogenesis. 14:1993;429-434.
62. World Health Organisation (WHO), 1990. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Chromium, Nickel and Welding, vol. 49. International Agency for Research on Cancer (IARC), Lyon.
63. Xu J., Manning F.C., Patierno S. Preferential formation and repair of chromium-induced DNA adducts and DNA-protein cross links in nuclear matrix DNA. Carcinogenesis. 15:1994;1443-1450.
64. Ye J., Zhang X., Young H.A., Mao Y., Shi X. Chromium(VI)-induced nuclear factor-kappa B activation in intact cells via free radical reactions. Carcinogenesis. 16:1995;2401-2405.
65. Ye J., Wang S., Leonard S.S., Sun Y., Butterworth L., Antonini J., Ding M., Rojansakul Y., Vallyathan V., Castranova V., Shi X. Role of reactive oxygen species and p53 in chromium(VI)-induced apoptosis. J. Biol. Chem. 274:1999;34974-34980.
66. Ye J., Shi X. Gene expression profile in response to chromium-induced cell stress in A549 cells. Mol. Cell. Biochem. 222:2001;189-197.
67. Zhang Z., Leonard S.S., Wang S., Vallyathan V., Castranova V., Shi X. Cr(VI) induces cell growth arrest through hydrogen peroxide mediated reactions. Mol. Cell. Biochem. 222:2001;77-83.