Cadmium induces carcinogenesis in BEAS-2B cells through ROS-dependent activation of PI3K/AKT/GSK-3β/β-catenin signaling

Toxicology and Applied Pharmacology

Volumn 264, Issue 2, 2012, Pages 153-160

  Son, Young Ok ^a   Wang, Lei ^a   Poyil, Pratheeshkumar ^a   Budhraja, Amit ^a   Hitron, J Andrew ^a   Zhang, Zhuo ^a   Lee, Jeong Chae ^a,b   Shi, Xianglin ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b Chonbuk National University   (South Korea)

Author keywords

catenin; Cadmium; Carcinogenesis; GSK 3 ; ROS

Indexed keywords

BETA CATENIN; CADMIUM; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; GLYCOGEN SYNTHASE KINASE 3BETA; MANGANESE SUPEROXIDE DISMUTASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHUS MUCOSA; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL TRANSFORMATION; CLONOGENIC ASSAY; COLONY FORMATION; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ANIMALS; BETA CATENIN; BLOTTING, WESTERN; BRONCHI; CADMIUM; CARCINOGENS; CELL LINE; CELL MOVEMENT; CELL TRANSFORMATION, NEOPLASTIC; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; ONCOGENE PROTEIN V-AKT; PHOSPHATIDYLINOSITOL 3-KINASES; PLASMIDS; REACTIVE OXYGEN SPECIES; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION; TRANSFECTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MUS; MUS MUSCULUS;

EID: 84866883489     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.07.028     Document Type: Article

References (48)

1. Arita A., Costa M. Epigenetics in metal carcinogenesis: nickel, arsenic, chromium and cadmium. Metallomics 2009, 1:222-228.
2. Bagchi D., Joshi S.S., Bagchi M., Balmoori J., Benner E.J., Kuszynski C.A., Stohs S.J. Cadmium- and chromium-induced oxidative stress, DNA damage, and apoptotic cell death in cultured human chronic myelogenous leukemic K562 cells, promyelocytic leukemic HL-60 cells, and normal human peripheral blood mononuclear cells. J. Biochem. Mol. Toxicol. 2000, 14:33-41.
3. Barrett J.C., Hesterberg T.W., Thomassen D.G. Use of cell transformation systems for carcinogenicity testing and mechanistic studies of carcinogenesis. Pharmacol. Rev. 1984, 36:53S-70S.
4. Behrens J. The role of the Wnt signalling pathway in colorectal tumorigenesis. Biochem. Soc. Trans. 2005, 33:672-675.
5. Chakraborty P.K., Lee W.K., Molitor M., Wolff N.A., Thevenod F. Cadmium induces Wnt signaling to upregulate proliferation and survival genes in sub-confluent kidney proximal tubule cells. Mol. Cancer 2010, 9:102.
6. Chang Q., Pan J., Wang X., Zhang Z., Chen F., Shi X. Reduced reactive oxygen species-generating capacity contributes to the enhanced cell growth of arsenic-transformed epithelial cells. Cancer Res. 2010, 70:5127-5135.
7. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006, 127:469-480.
8. Cohen P., Frame S. The renaissance of GSK3. Nat. Rev. Mol. Cell Biol. 2001, 2:769-776.
9. Cross D.A., Alessi D.R., Cohen P., Andjelkovich M., Hemmings B.A. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995, 378:785-789.
10. Diehn M., Cho R.W., Lobo N.A., Kalisky T., Dorie M.J., Kulp A.N., Qian D., Lam J.S., Ailles L.E., Wong M., Joshua B., Kaplan M.J., Wapnir I., Dirbas F.M., Somlo G., Garberoglio C., Paz B., Shen J., Lau S.K., Quake S.R., Brown J.M., Weissman I.L., Clarke M.F. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458:780-783.
11. Ercal N., Gurer-Orhan H., Aykin-Burns N. Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr. Top. Med. Chem. 2001, 1:529-539.
12. Fang M.Z., Mar W., Cho M.H. Cadmium affects genes involved in growth regulation during two-stage transformation of Balb/3T3 cells. Toxicology 2002, 177:253-265.
13. Galan A., Garcia-Bermejo L., Troyano A., Vilaboa N.E., Fernandez C., de Blas E., Aller P. The role of intracellular oxidation in death induction (apoptosis and necrosis) in human promonocytic cells treated with stress inducers (cadmium, heat, X-rays). Eur. J. Cell Biol. 2001, 80:312-320.
14. Glahn F., Schmidt-Heck W., Zellmer S., Guthke R., Wiese J., Golka K., Hergenroder R., Degen G.H., Lehmann T., Hermes M., Schormann W., Brulport M., Bauer A., Bedawy E., Gebhardt R., Hengstler J.G., Foth H. Cadmium, cobalt and lead cause stress response, cell cycle deregulation and increased steroid as well as xenobiotic metabolism in primary normal human bronchial epithelial cells which is coordinated by at least nine transcription factors. Arch. Toxicol. 2008, 82:513-524.
15. Harris C.C. Chemical and physical carcinogenesis: advances and perspectives for the 1990s. Cancer Res. 1991, 51:5023s-5044s.
16. Henson M.C., Chedrese P.J. Endocrine disruption by cadmium, a common environmental toxicant with paradoxical effects on reproduction. Exp. Biol. Med. (Maywood) 2004, 229:383-392.
17. Heo J.S., Lee J.C. beta-Catenin mediates cyclic strain-stimulated cardiomyogenesis in mouse embryonic stem cells through ROS-dependent and integrin-mediated PI3K/Akt pathways. J. Cell. Biochem. 2011, 112:1880-1889.
18. Howe L.R., Crawford H.C., Subbaramaiah K., Hassell J.A., Dannenberg A.J., Brown A.M. PEA3 is up-regulated in response to Wnt1 and activates the expression of cyclooxygenase-2. J. Biol. Chem. 2001, 276:20108-20115.
19. Huang C., Li J., Ma W.Y., Dong Z. JNK activation is required for JB6 cell transformation induced by tumor necrosis factor-alpha but not by 12-O-tetradecanoylphorbol-13-acetate. J. Biol. Chem. 1999, 274:29672-29676.
20. IARC Beyllium, cadmium, Hg, and exposure in the glass manufacturing industry. IARC Monogr. Eval. Carcinog. Risks Hum. 1993, 58:119-237.
21. Jang Y.Y., Sharkis S.J. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 2007, 110:3056-3063.
22. Jarup L. Hazards of heavy metal contamination. Br. Med. Bull. 2003, 68:167-182.
23. Jin P., Ringertz N.R. Cadmium induces transcription of proto-oncogenes c-jun and c-myc in rat L6 myoblasts. J. Biol. Chem. 1990, 265:14061-14064.
24. Jing Y., Liu L.Z., Jiang Y., Zhu Y., Guo N.L., Barnett J., Rojanasakul Y., Agani F., Jiang B.H. Cadmium increases HIF-1 and VEGF expression through ROS, ERK, and AKT signaling pathways and induces malignant transformation of human bronchial epithelial cells. Toxicol. Sci. 2012, 125:10-19.
25. Klaus A., Birchmeier W. Wnt signalling and its impact on development and cancer. Nat. Rev. Cancer 2008, 8:387-398.
26. 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, 15:1749-1761.
27. Lustig B., Behrens J. The Wnt signaling pathway and its role in tumor development. J. Cancer Res. Clin. Oncol. 2003, 129:199-221.
28. MacDonald B.T., Tamai K., He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 2009, 17:9-26.
29. Marchenko G.N., Marchenko N.D., Leng J., Strongin A.Y. Promoter characterization of the novel human matrix metalloproteinase-26 gene: regulation by the T-cell factor-4 implies specific expression of the gene in cancer cells of epithelial origin. Biochem. J. 2002, 363:253-262.
30. Meng D., Lv D.D., Zhuang X., Sun H., Fan L., Shi X.L., Fang J. Benzo[a]pyrene induces expression of matrix metalloproteinases and cell migration and invasion of vascular smooth muscle cells. Toxicol. Lett. 2009, 184:44-49.
31. Nakamura T., Hamada F., Ishidate T., Anai K., Kawahara K., Toyoshima K., Akiyama T. Axin, an inhibitor of the Wnt signalling pathway, interacts with beta-catenin, GSK-3beta and APC and reduces the beta-catenin level. Genes Cells 1998, 3:395-403.
32. O'Brien P., Salacinski H.J. Evidence that the reactions of cadmium in the presence of metallothionein can produce hydroxyl radicals. Arch. Toxicol. 1998, 72:690-700.
33. Plaisant M., Giorgetti-Peraldi S., Gabrielson M., Loubat A., Dani C., Peraldi P. Inhibition of hedgehog signaling decreases proliferation and clonogenicity of human mesenchymal stem cells. PLoS One 2011, 6:e16798.
34. Qian Y., Luo J., Leonard S.S., Harris G.K., Millecchia L., Flynn D.C., Shi X. Hydrogen peroxide formation and actin filament reorganization by Cdc42 are essential for ethanol-induced in vitro angiogenesis. J. Biol. Chem. 2003, 278:16189-16197.
35. Shaikh Z.A., Vu T.T., Zaman K. Oxidative stress as a mechanism of chronic cadmium-induced hepatotoxicity and renal toxicity and protection by antioxidants. Toxicol. Appl. Pharmacol. 1999, 154:256-263.
36. Son Y.O., Lee J.C., Hitron J.A., Pan J., Zhang Z., Shi X. Cadmium induces intracellular Ca2+- and H2O2-dependent apoptosis through JNK- and p53-mediated pathways in skin epidermal cell line. Toxicol. Sci. 2010, 113:127-137.
37. Stohs S.J., Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 1995, 18:321-336.
38. Stohs S.J., Bagchi D., Hassoun E., Bagchi M. Oxidative mechanisms in the toxicity of chromium and cadmium ions. J. Environ. Pathol. Toxicol. Oncol. 2001, 20:77-88.
39. Szuster-Ciesielska A., Stachura A., Slotwinska M., Kaminska T., Sniezko R., Paduch R., Abramczyk D., Filar J., Kandefer-Szerszen M. The inhibitory effect of zinc on cadmium-induced cell apoptosis and reactive oxygen species (ROS) production in cell cultures. Toxicology 2000, 145:159-171.
40. Trachootham D., Alexandre J., Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach?. Nat. Rev. Drug Discov. 2009, 8:579-591.
41. Waalkes M.P. Cadmium carcinogenesis in review. J. Inorg. Biochem. 2000, 79:241-244.
42. Waalkes M.P. Cadmium carcinogenesis. Mutat. Res. 2003, 533:107-120.
43. Waalkes M.P., Anver M.R., Diwan B.A. Chronic toxic and carcinogenic effects of oral cadmium in the Noble (NBL/Cr) rat: induction of neoplastic and proliferative lesions of the adrenal, kidney, prostate, and testes. J. Toxicol. Environ. Health A 1999, 58:199-214.
44. Waisberg M., Joseph P., Hale B., Beyersmann D. Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 2003, 192:95-117.
45. Wang Y., Fang J., Leonard S.S., Rao K.M. Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic. Biol. Med. 2004, 36:1434-1443.
46. Wang Y., Krivtsov A.V., Sinha A.U., North T.E., Goessling W., Feng Z., Zon L.I., Armstrong S.A. The Wnt/beta-catenin pathway is required for the development of leukemia stem cells in AML. Science 2010, 327:1650-1653.
47. Zhang X., Gaspard J.P., Chung D.C. Regulation of vascular endothelial growth factor by the Wnt and K-ras pathways in colonic neoplasia. Cancer Res. 2001, 61:6050-6054.
48. Zhang Z., Wang X., Cheng S., Sun L., Son Y.O., Yao H., Li W., Budhraja A., Li L., Shelton B.J., Tucker T., Arnold S.M., Shi X. Reactive oxygen species mediate arsenic induced cell transformation and tumorigenesis through Wnt/beta-catenin pathway in human colorectal adenocarcinoma DLD1 cells. Toxicol. Appl. Pharmacol. 2011, 256:114-121.