Reactive oxygen species mediate arsenic induced cell transformation and tumorigenesis through Wnt/β-catenin pathway in human colorectal adenocarcinoma DLD1 cells

Toxicology and Applied Pharmacology

Volumn 256, Issue 2, 2011, Pages 114-121

  Zhang, Zhuo ^a   Wang, Xin ^a   Cheng, Senping ^a   Sun, Lijuan ^a   Son, Young Ok ^a   Yao, Hua ^b   Li, Wenqi ^a   Budhraja, Amit ^a   Li, Li ^c   Shelton, Brent J ^d   Tucker, Thomas ^d   Arnold, Susanne M ^d   Shi, Xianglin ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b ZHEJIANG UNIVERSITY   (China)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

catenin; Arsenic; Cell transformation; NADPH oxidase; Reactive oxygen species; Tumorigenesis

Indexed keywords

ARSENIC; BETA CATENIN; CATALASE; PROTEIN; PROTEIN P47PHOX; PROTEIN P67PHOX; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CARCINOGENICITY; CARCINOMA CELL; CELL TRANSFORMATION; CHEMICAL CARCINOGENESIS; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; TUMOR VOLUME;

ADENOCARCINOMA; ANIMALS; ARSENICALS; BETA CATENIN; BLOTTING, WESTERN; CARCINOGENICITY TESTS; CATENINS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; COLORECTAL NEOPLASMS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYME ACTIVATION; HUMANS; MALE; MICE; MICE, NUDE; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 80053132303     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.07.016     Document Type: Article

References (58)

1. Arnold R.S., Shi J., Murad E., Whalen A.M., Sun C.Q., Polavarapu R., et al. Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proc. Natl. Acad. Sci. U. S. A. 2001, 98(10):5550-5555.
2. Arnold L.L., Eldan M., van Gemert M., Capen C.C., Cohen S.M. Chronic studies evaluating the carcinogenicity of monomethylarsonic acid in rats and mice. Toxicology 2003, 190(3):197-219.
3. Barker N., Clevers H. Mining the Wnt pathway for cancer therapeutics. Nat. Rev. Drug Discov. 2006, 5(12):997-1014.
4. Barker N., Morin P.J., Clevers H. The Yin-Yang of TCF/beta-catenin signaling. Adv. Cancer Res. 2000, 77:1-24.
5. Benbrahim-Tallaa L., Waalkes M.P. Inorganic arsenic and human prostate cancer. Environ. Health Perspect. 2008, 116(2):158-164.
6. Bode A.M., Dong Z. The paradox of arsenic: molecular mechanisms of cell transformation and chemotherapeutic effects. Crit. Rev. Oncol. Hematol. 2002, 42(1):5-24.
7. Bokoch G.M., Knaus U.G. NADPH oxidases: not just for leukocytes anymore!. Trends Biochem. Sci. 2003, 28(9):502-508.
8. Bower J.J., Leonard S.S., Chen F., Shi X. As(III) transcriptionally activates the gadd45a gene via the formation of H2O2. Free Radic. Biol. Med. 2006, 41(2):285-294.
9. Brown D.I., Griendling K.K. Nox proteins in signal transduction. Free Radic. Biol. Med. 2009, 47(9):1239-1253.
10. Chen F., Shi X. Signaling from toxic metals to NF-kappaB and beyond: not just a matter of reactive oxygen species. Environ. Health Perspect. 2002, 110(Suppl 5):807-811.
11. Chen F., Shi X. Intracellular signal transduction of cells in response to carcinogenic metals. Crit. Rev. Oncol. Hematol. 2002, 42(1):105-121.
12. Chou W.C., Jie C., Kenedy A.A., Jones R.J., Trush M.A., Dang C.V. Role of NADPH oxidase in arsenic-induced reactive oxygen species formation and cytotoxicity in myeloid leukemia cells. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(13):4578-4583.
13. Coant N., Ben Mkaddem S., Pedruzzi E., Guichard C., Treton X., Ducroc R., et al. NADPH oxidase 1 modulates WNT and NOTCH1 signaling to control the fate of proliferative progenitor cells in the colon. Mol. Cell. Biol. 2010, 30(11):2636-2650.
14. Ding W., Hudson L.G., Liu K.J. Inorganic arsenic compounds cause oxidative damage to DNA and protein by inducing ROS and RNS generation in human keratinocytes. Mol. Cell. Biochem. 2005, 279(1-2):105-112.
15. Ding W., Hudson L.G., Sun X., Feng C., Liu K.J. As(III) inhibits ultraviolet radiation-induced cyclobutane pyrimidine dimer repair via generation of nitric oxide in human keratinocytes. Free Radic. Biol. Med. 2008, 45(8):1065-1072.
16. Dong Z. The molecular mechanisms of arsenic-induced cell transformation and apoptosis. Environ. Health Perspect. 2002, 110(Suppl 5):757-759.
17. Essers M.A., de Vries-Smits L.M., Barker N., Polderman P.E., Burgering B.M., Korswagen H.C. Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 2005, 308(5725):1181-1184.
18. Euhus D.M., Hudd C., LaRegina M.C., Johnson F.E. Tumor measurement in the nude mouse. J. Surg. Oncol. 1986, 31(4):229-234.
19. Fu W., Ma Q., Chen L., Li P., Zhang M., Ramamoorthy S., et al. MDM2 acts downstream of p53 as an E3 ligase to promote FOXO ubiquitination and degradation. J. Biol. Chem. 2009, 284(21):13987-14000.
20. Funato Y., Michiue T., Asashima M., Miki H. The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt-beta-catenin signalling through dishevelled. Nat. Cell Biol. 2006, 8(5):501-508.
21. Galanis A., Karapetsas A., Sandaltzopoulos R. Metal-induced carcinogenesis, oxidative stress and hypoxia signalling. Mutat. Res. 2009, 674(1-2):31-35.
22. Geiszt M., Leto T.L. The Nox family of NAD(P)H oxidases: host defense and beyond. J. Biol. Chem. 2004, 279(50):51715-51718.
23. Gianni D., Taulet N., DerMardirossian C., Bokoch G.M. c-Src-mediated phosphorylation of NoxA1 and Tks4 induces the reactive oxygen species (ROS)-dependent formation of functional invadopodia in human colon cancer cells. Mol. Biol. Cell 2010, 21(23):4287-4298.
24. Hammond E.M., Giaccia A.J. The role of p53 in hypoxia-induced apoptosis. Biochem. Biophys. Res. Commun. 2005, 331(3):718-725.
25. Harris G.K., Shi X. Signaling by carcinogenic metals and metal-induced reactive oxygen species. Mutat. Res. 2003, 533(1-2):183-200.
26. Huang C., Ke Q., Costa M., Shi X. Molecular mechanisms of arsenic carcinogenesis. Mol. Cell. Biochem. 2004, 255(1-2):57-66.
27. Huff J., Chan P., Nyska A. Is the human carcinogen arsenic carcinogenic to laboratory animals?. Toxicol. Sci. 2000, 55(1):17-23.
28. Jomova K., Valko M. Advances in metal-induced oxidative stress and human disease. Toxicology 2011, 283(2-3):65-87.
29. Kimelman D., Xu W. beta-Catenin destruction complex: insights and questions from a structural perspective. Oncogene 2006, 25(57):7482-7491.
30. Kitchin K.T., Wallace K. The role of protein binding of trivalent arsenicals in arsenic carcinogenesis and toxicity. J. Inorg. Biochem. 2008, 102(3):532-539.
31. Klaus A., Birchmeier W. Wnt signalling and its impact on development and cancer. Nat. Rev. Cancer 2008, 8(5):387-398.
32. Kligerman A.D., Doerr C.L., Tennant A.H., Harrington-Brock K., Allen J.W., Winkfield E., et al. Methylated trivalent arsenicals as candidate ultimate genotoxic forms of arsenic: induction of chromosomal mutations but not gene mutations. Environ. Mol. Mutagen. 2003, 42(3):192-205.
33. Korinek V., Barker N., Morin P.J., van Wichen D., de Weger R., Kinzler K.W., et al. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 1997, 275(5307):1784-1787.
34. Korswagen H.C. Regulation of the Wnt/beta-catenin pathway by redox signaling. Dev. Cell 2006, 10(6):687-688.
35. Ladelfa M.F., Toledo M.F., Laiseca J.E., Monte M. Interaction of p53 with tumor suppressive and oncogenic signaling pathways to control cellular reactive oxygen species production. Antioxid. Redox Signal. 2011.
36. Lambeth J.D. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 2004, 4(3):181-189.
37. Lambeth J.D. Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radic. Biol. Med. 2007, 43(3):332-347.
38. Lander H.M. An essential role for free radicals and derived species in signal transduction. FASEB J. 1997, 11(2):118-124.
39. Leonard S.S., Harris G.K., Shi X. Metal-induced oxidative stress and signal transduction. Free Radic. Biol. Med. 2004, 37(12):1921-1942.
40. Li J.J., Oberley L.W., Fan M., Colburn N.H. Inhibition of AP-1 and NF-kappaB by manganese-containing superoxide dismutase in human breast cancer cells. FASEB J. 1998, 12(15):1713-1723.
41. Li Y., Bavarva J.H., Wang Z., Guo J., Qian C., Thibodeau S.N., et al. HEF1, a novel target of Wnt signaling, promotes colonic cell migration and cancer progression. Oncogene 2011.
42. Liu S.X., Athar M., Lippai I., Waldren C., Hei T.K. Induction of oxyradicals by arsenic: implication for mechanism if genotoxicity. Proc. Natl. Acad. Sci. U.S.A. 2001, 98(4):1643-1648.
43. MacDonald B.T., Tamai K., He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 2009, 17(1):9-26.
44. Morin P.J., Sparks A.B., Korinek V., Barker N., Clevers H., Vogelstein B., et al. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 1997, 275(5307):1787-1790.
45. Perkins C., Kim C.N., Fang G., Bhalla K.N. Arsenic induces apoptosis of multidrug-resistant human myeloid leukemia cells that express Bcr-Abl or overexpress MDR, MRP, Bcl-2, or Bcl-x(L). Blood 2000, 95(3):1014-1022.
46. Polakis P. Wnt signaling and cancer. Genes Dev. 2000, 14(15):1837-1851.
47. Qian Y., Liu K.J., Chen Y., Flynn D.C., Castranova V., Shi X. Cdc42 regulates arsenic-induced NADPH oxidase activation and cell migration through actin filament reorganization. J. Biol. Chem. 2005, 280(5):3875-3884.
48. Reya T., Clevers H. Wnt signalling in stem cells and cancer. Nature 2005, 434(7035):843-850.
49. Segditsas S., Tomlinson I. Colorectal cancer and genetic alterations in the Wnt pathway. Oncogene 2006, 25(57):7531-7537.
50. Sen C.K., Packer L. Antioxidant and redox regulation of gene transcription. FASEB J. 1996, 10(7):709-720.
51. Shi H., Hudson L.G., Liu K.J. Oxidative stress and apoptosis in metal ion-induced carcinogenesis. Free Radic. Biol. Med. 2004, 37(5):582-593.
52. Shi H., Hudson L.G., Ding W., Wang S., Cooper K.L., Liu S., et al. Arsenite causes DNA damage in keratinocytes via generation of hydroxyl radicals. Chem. Res. Toxicol. 2004, 17(7):871-878.
53. Stevens J.J., Graham B., Walker A.M., Tchounwou P.B., Rogers C. The effects of arsenic trioxide on DNA synthesis and genotoxicity in human colon cancer cells. Int. J. Environ. Res. Public Health 2010, 7(5):2018-2032.
54. Tchounwou P.B., Patlolla A.K., Centeno J.A. Carcinogenic and systemic health effects associated with arsenic exposure-a critical review. Toxicol. Pathol. 2003, 31(6):575-588.
55. Tomayko M.M., Reynolds C.P. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother. Pharmacol. 1989, 24(3):148-154.
56. van der Flier L.G., Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu. Rev. Physiol. 2009, 71:241-260.
57. Waalkes M.P., Liu J., Ward J.M., Diwan B.A. Mechanisms underlying arsenic carcinogenesis: hypersensitivity of mice exposed to inorganic arsenic during gestation. Toxicology 2004, 198(1-3):31-38.
58. Yang C.Y., Chang C.C., Ho S.C., Chiu H.F. Is colon cancer mortality related to arsenic exposure?. J. Toxicol. Environ. Health A 2008, 71(8):533-538.