Epithelial-mesenchymal transition during oncogenic transformation induced by hexavalent chromium involves reactive oxygen species-dependent mechanism in lung epithelial cells

Toxicology and Applied Pharmacology

Volumn 269, Issue 1, 2013, Pages 61-71

  Ding, Song Ze ^a,b   Yang, Yu Xiu ^a   Li, Xiu Ling ^a   Michelli Rivera, Audrey ^b   Han, Shuang Yin ^a   Wang, Lei ^b   Pratheeshkumar, Poyil ^b   Wang, Xin ^b   Lu, Jian ^b   Yin, Yuan Qin ^b   Budhraja, Amit ^b   Hitron, Andrew J ^b  

^a ZHENGZHOU UNIVERSITY   (China)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Cancer signaling; Epithelial cells; Epithelial mesenchymal transition; Hexavalent chromium; Histone; Oncogenic transformation

Indexed keywords

CARCINOGEN; CHROMIUM; MATRIGEL; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; UVOMORULIN; VIMENTIN;

ARTICLE; CANCER PREVENTION; CARCINOGENESIS; CELL STRUCTURE; CELL TRANSFORMATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; LUNG ALVEOLUS EPITHELIUM; METASTASIS; PROTEIN EXPRESSION; TUMOR INVASION;

CADHERINS; CARCINOGENS, ENVIRONMENTAL; CATALASE; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL SHAPE; CELL TRANSFORMATION, NEOPLASTIC; CHROMIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; REACTIVE OXYGEN SPECIES; RESPIRATORY MUCOSA; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; VIMENTIN;

EID: 84877804207     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.03.006     Document Type: Article

References (51)

1. Batlle E., Sancho E., Franci C., Dominguez D., Monfar M., Baulida J., Garcia De Herreros A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2000, 2:84-89.
2. Beaver L.M., Stemmy E.J., Constant S.L., Schwartz A., Little L.G., Gigley J.P., Chun G., Sugden K.D., Ceryak S.M., Patierno S.R. Lung injury, inflammation and Akt signaling following inhalation of particulate hexavalent chromium. Toxicol. Appl. Pharmacol. 2009, 235:47-56.
3. Berx G., Cleton-Jansen A.M., Nollet F., de Leeuw W.J., van de Vijver M., Cornelisse C., van Roy F. E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. EMBO J. 1995, 14:6107-6115.
4. Bolos V., Peinado H., Perez-Moreno M.A., Fraga M.F., Esteller M., Cano A. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J. Cell Sci. 2003, 116:499-511.
5. Borges K.M., Wetterhahn K.E. Chromium cross-links glutathione and cysteine to DNA. Carcinogenesis 1989, 10:2165-2168.
6. Ceryak S., Zingariello C., O'Brien T., Patierno S.R. Induction of pro-apoptotic and cell cycle-inhibiting genes in chromium (VI)-treated human lung fibroblasts: lack of effect of ERK. Mol. Cell. Biochem. 2004, 255:139-149.
7. Comijn J., Berx G., Vermassen P., Verschueren K., van Grunsven L., Bruyneel E., Mareel M., Huylebroeck D., van Roy F. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol. Cell 2001, 7:1267-1278.
8. Costa A.N., Moreno V., Prieto M.J., Urbano A.M., Alpoim M.C. Induction of morphological changes in BEAS-2B human bronchial epithelial cells following chronic sub-cytotoxic and mildly cytotoxic hexavalent chromium exposures. Mol. Carcinog. 2010, 49:582-591.
9. Ding S.Z., O'Hara A.M., Denning T.L., Dirden-Kramer B., Mifflin R.C., Reyes V.E., Ryan K.A., Elliott S.N., Izumi T., Boldogh I., Mitra S., Ernst P.B., Crowe S.E. Helicobacter pylori and H2O2 increase AP endonuclease-1/redox factor-1 expression in human gastric epithelial cells. Gastroenterology 2004, 127:845-858.
10. Ding S.Z., Fischer W., Kaparakis-Liaskos M., Liechti G., Merrell D.S., Grant P.A., Ferrero R.L., Crowe S.E., Haas R., Hatakeyama M., Goldberg J.B. Helicobacter pylori-induced histone modification, associated gene expression in gastric epithelial cells, and its implication in pathogenesis. PLoS One 2010, 5:e9875.
11. Gibb H.J., Lees P.S., Pinsky P.F., Rooney B.C. Lung cancer among workers in chromium chemical production. Am. J. Ind. Med. 2000, 38:115-126.
12. Gray J.W. Evidence emerges for early metastasis and parallel evolution of primary and metastatic tumors. Cancer Cell 2003, 4:4-6.
13. Hunter K.W. Host genetics and tumour metastasis. Br. J. Cancer 2004, 90:752-755.
14. Johnen N., Francart M.E., Thelen N., Cloes M., Thiry M. Evidence for a partial epithelial-mesenchymal transition in postnatal stages of rat auditory organ morphogenesis. Histochem. Cell Biol. 2012, 138:477-488.
15. Lee S.K., Kim J.H., Lee Y.C., Cheong J., Lee J.W. Silencing mediator of retinoic acid and thyroid hormone receptors, as a novel transcriptional corepressor molecule of activating protein-1, nuclear factor-kappaB, and serum response factor. J. Biol. Chem. 2000, 275:12470-12474.
16. Leroy P., Mostov K.E. Slug is required for cell survival during partial epithelial-mesenchymal transition of HGF-induced tubulogenesis. Mol. Biol. Cell 2007, 18:1943-1952.
17. Liou G.Y., Storz P. Reactive oxygen species in cancer. Free Radic. Res. 2010, 44:479-496.
18. Liu K.J., Jiang J., Swartz H.M., Shi X. Low-frequency EPR detection of chromium(V) formation by chromium(VI) reduction in whole live mice. Arch. Biochem. Biophys. 1994, 313:248-252.
19. Ma L., Young J., Prabhala H., Pan E., Mestdagh P., Muth D., Teruya-Feldstein J., Reinhardt F., Onder T.T., Valastyan S., Westermann F., Speleman F., Vandesompele J., Weinberg R.A. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat. Cell Biol. 2010, 12:247-256.
20. Majumder S., Ghoshal K., Summers D., Bai S., Datta J., Jacob S.T. Chromium(VI) down-regulates heavy metal-induced metallothionein gene transcription by modifying transactivation potential of the key transcription factor, metal-responsive transcription factor 1. J. Biol. Chem. 2003, 278:26216-26226.
21. Matsuyama R., Takada I., Yokoyama A., Fujiyma-Nakamura S., Tsuji N., Kitagawa H., Fujiki R., Kim M., Kouzu-Fujita M., Yano T., Kato S. Double PHD fingers protein DPF2 recognizes acetylated histones and suppresses the function of estrogen-related receptor alpha through histone deacetylase 1. J. Biol. Chem. 2010, 285:18166-18176.
22. McCaffrey J., Wolf C.M., Hamilton J.W. Effects of the genotoxic carcinogen chromium(VI) on basal and hormone-inducible phosphoenolpyruvate carboxykinase gene expression in vivo: correlation with glucocorticoid- and developmentally regulated expression. Mol. Carcinog. 1994, 10:189-198.
23. Nawrocki-Raby B., Gilles C., Polette M., Martinella-Catusse C., Bonnet N., Puchelle E., Foidart J.M., Van Roy F., Birembaut P. E-Cadherin mediates MMP down-regulation in highly invasive bronchial tumor cells. Am. J. Pathol. 2003, 163:653-661.
24. Nickens K.P., Patierno S.R., Ceryak S. Chromium genotoxicity: a double-edged sword. Chem. Biol. Interact. 2010, 188:276-288.
25. O'Brien T., Xu J., Patierno S.R. Effects of glutathione on chromium-induced DNA crosslinking and DNA polymerase arrest. Mol. Cell. Biochem. 2001, 222:173-182.
26. O'Brien T.J., Ceryak S., Patierno S.R. Complexities of chromium carcinogenesis: role of cellular response, repair and recovery mechanisms. Mutat. Res. 2003, 533:3-36.
27. O'Hara K.A., Vaghjiani R.J., Nemec A.A., Klei L.R., Barchowsky A. Cr(VI)-stimulated STAT3 tyrosine phosphorylation and nuclear translocation in human airway epithelial cells requires Lck. Biochem. J. 2007, 402:261-269.
28. Onder T.T., Gupta P.B., Mani S.A., Yang J., Lander E.S., Weinberg R.A. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res. 2008, 68:3645-3654.
29. Pena C., Garcia J.M., Silva J., Garcia V., Rodriguez R., Alonso I., Millan I., Salas C., de Herreros A.G., Munoz A., Bonilla F. E-cadherin and vitamin D receptor regulation by SNAIL and ZEB1 in colon cancer: clinicopathological correlations. Hum. Mol. Genet. 2005, 14:3361-3370.
30. Perl A.K., Wilgenbus P., Dahl U., Semb H., Christofori G. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 1998, 392:190-193.
31. Schnekenburger M., Peng L., Puga A. HDAC1 bound to the Cyp1a1 promoter blocks histone acetylation associated with Ah receptor-mediated trans-activation. Biochim. Biophys. Acta 2007, 1769:569-578.
32. Schnekenburger M., Talaska G., Puga A. Chromium cross-links histone deacetylase 1-DNA methyltransferase 1 complexes to chromatin, inhibiting histone-remodeling marks critical for transcriptional activation. Mol. Cell. Biol. 2007, 27:7089-7101.
33. Shi X., Dalal N.S. Generation of hydroxyl radical by chromate in biologically relevant systems: role of Cr(V) complexes versus tetraperoxochromate(V). Environ. Health Perspect. 1994, 102(Suppl. 3):231-236.
34. Shi X., Dong Z., Dalal N.S., Gannett P.M. Chromate-mediated free radical generation from cysteine, penicillamine, hydrogen peroxide, and lipid hydroperoxides. Biochim. Biophys. Acta 1994, 1226:65-72.
35. Snow E.T. Effects of chromium on DNA replication in vitro. Environ. Health Perspect. 1994, 102(Suppl. 3):41-44.
36. Stearns D.M., Kennedy L.J., Courtney K.D., Giangrande P.H., Phieffer L.S., Wetterhahn K.E. Reduction of chromium(VI) by ascorbate leads to chromium-DNA binding and DNA strand breaks in vitro. Biochemistry 1995, 34:910-919.
37. Strathdee G. Epigenetic versus genetic alterations in the inactivation of E-cadherin. Semin. Cancer Biol. 2002, 12:373-379.
38. Takahashi Y., Kondo K., Hirose T., Nakagawa H., Tsuyuguchi M., Hashimoto M., Sano T., Ochiai A., Monden Y. Microsatellite instability and protein expression of the DNA mismatch repair gene, hMLH1, of lung cancer in chromate-exposed workers. Mol. Carcinog. 2005, 42:150-158.
39. Takahashi Y., Kondo K., Ishikawa S., Uchihara H., Fujino H., Sawada N., Miyoshi T., Sakiyama S., Izumi K., Monden Y. Microscopic analysis of the chromium content in the chromium-induced malignant and premalignant bronchial lesions of the rat. Environ. Res. 2005, 99:267-272.
40. Thiery J.P., Sleeman J.P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 2006, 7:131-142.
41. Thiery J.P., Lim C.T. Tumor Dissemination: An EMT Affair. Cancer Cell 2013, 23:272-273.
42. Turgeon N., Valiquette C., Blais M., Routhier S., Seidman E.G., Asselin C. Regulation of C/EBPdelta-dependent transactivation by histone deacetylases in intestinal epithelial cells. J. Cell. Biochem. 2008, 103:1573-1583.
43. Umbas R., Isaacs W.B., Bringuier P.P., Schaafsma H.E., Karthaus H.F., Oosterhof G.O., Debruyne F.M., Schalken J.A. Decreased E-cadherin expression is associated with poor prognosis in patients with prostate cancer. Cancer Res. 1994, 54:3929-3933.
44. van Roy F., Berx G. The cell-cell adhesion molecule E-cadherin. Cell Mol. Life Sci. 2008, 65:3756-3788.
45. Wang X., Zheng M., Liu G., Xia W., McKeown-Longo P.J., Hung M.C., Zhao J. Kruppel-like factor 8 induces epithelial to mesenchymal transition and epithelial cell invasion. Cancer Res. 2007, 67:7184-7193.
46. Wang X., Son Y.O., Chang Q., Sun L., Hitron J.A., Budhraja A., Zhang Z., Ke Z., Chen F., Luo J., Shi X. NADPH oxidase activation is required in reactive oxygen species generation and cell transformation induced by hexavalent chromium. Toxicol. Sci. 2011, 123:399-410.
47. Wei Y.D., Tepperman K., Huang M.Y., Sartor M.A., Puga A. Chromium inhibits transcription from polycyclic aromatic hydrocarbon-inducible promoters by blocking the release of histone deacetylase and preventing the binding of p300 to chromatin. J. Biol. Chem. 2004, 279:4110-4119.
48. Wise S.S., Holmes A.L., Wise J.P. Particulate and soluble hexavalent chromium are cytotoxic and genotoxic to human lung epithelial cells. Mutat. Res. 2006, 610:2-7.
49. Wise S.S., Holmes A.L., Wise J.P. Hexavalent chromium-induced DNA damage and repair mechanisms. Rev. Environ. Health 2008, 23:39-57.
50. Xie H., Holmes A.L., Wise S.S., Huang S., Peng C., Wise J.P. Neoplastic transformation of human bronchial cells by lead chromate particles. Am. J. Respir. Cell Mol. Biol. 2007, 37:544-552.
51. Yang J., Mani S.A., Donaher J.L., Ramaswamy S., Itzykson R.A., Come C., Savagner P., Gitelman I., Richardson A., Weinberg R.A. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117:927-939.