Constitutive activation of epidermal growth factor receptor promotes tumorigenesis of Cr(VI)-transformed cells through decreased reactive oxygen species and apoptosis resistance development

Journal of Biological Chemistry

Volumn 290, Issue 4, 2015, Pages 2213-2224

  Kim, Donghern ^a   Dai, Jin ^a   Fai, Leonard Yenwong ^a   Yao, Hua ^b   Son, Young Ok ^a   Wang, Lei ^a   Pratheeshkumar, Poyil ^a   Kondo, Kazuya ^c   Shi, Xianglin ^a   Zhang, Zhuo ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b ZHEJIANG UNIVERSITY   (China)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ANTIOXIDANTS; BIOACTIVITY; BIOLOGICAL ORGANS; CELL DEATH; CHEMICAL ACTIVATION; ENZYMES; LIGANDS; MANGANESE COMPOUNDS; OXYGEN; REACTIVE OXYGEN SPECIES; TISSUE CULTURE; TUMORS;

BCL-2 AND BCL-XL; CHRONIC EXPOSURE; EPIDERMAL GROWTH FACTOR RECEPTORS; HEXAVALENT CHROMIUM; HUMAN LUNG TUMORS; MANGANESE SUPEROXIDE DISMUTASE; POLYMERASE CLEAVAGE; TRANSMEMBRANE RECEPTORS;

CHROMIUM COMPOUNDS;

AMPHIREGULIN; CHROMIUM; EPIDERMAL GROWTH FACTOR RECEPTOR; MANGANESE SUPEROXIDE DISMUTASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; ANTIOXIDANT; ARSENIC; BAX PROTEIN, HUMAN; CHROMIUM HEXAVALENT ION; EGFR PROTEIN, HUMAN; EGFR PROTEIN, MOUSE; LIGAND; NICKEL;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CARCINOGENESIS; CASE REPORT; CELL TRANSFORMATION; CONTROLLED STUDY; DNA SEQUENCE; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; LONG TERM EXPOSURE; MIDDLE AGED; MOUSE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; CANCER TRANSPLANTATION; CHEMISTRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENE SILENCING; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; NUDE MOUSE; SEQUENCE HOMOLOGY; TUMOR CELL LINE;

ANIMALIA;

AMPHIREGULIN; ANIMALS; ANTIOXIDANTS; APOPTOSIS; ARSENIC; BASE SEQUENCE; BCL-2-ASSOCIATED X PROTEIN; CELL LINE, TUMOR; CHROMIUM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; LIGANDS; MICE; MICE, INBRED BALB C; MICE, NUDE; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; NEOPLASM TRANSPLANTATION; NICKEL; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 84961289625     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.619783     Document Type: Article

References (51)

1. Hill, R., Leidal, A. M., Madureira, P. A., Gillis, L. D., Cochrane, H. K., Waisman, D. M., Chiu, A., and Lee, P. W. (2008) Hypersensitivity to chromium-induced DNA damage correlates with constitutive deregulation of upstream p53 kinases in p21-/- HCT116 colon cancer cells. DNA Repair 7, 239-252
2. International Agency for Research on Cancer (IARC) (1990) Chromium, nickel and welding. IARC Monogr. Eval. Carcinog Risks Hum. 49, 1-648
3. Langa˚rd, S. (1990) One hundred years of chromium and cancer: a review of epidemiological evidence and selected case reports. Am. J. Ind. Med. 17, 189-215
4. Pellerin, C., and Booker, S. M. (2000) Reflection on hexavalent chromium: health hazards of an industrial heavy weigh. Environ. Health Perspect. 108, A402-407
5. Schneider, M. R., and Wolf, E. (2009) The epidermal growth factor receptor ligands at a glance. J. Cell. Physiol. 218, 460-466
6. Engelman, J. A., Luo, J., and Cantley, L. C. (2006) The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 7, 606-619
7. Scagliotti, G. V., Selvaggi, G., Novello, S., and Hirsch, F. R. (2004) The biology of epidermal growth factor receptor in lung cancer. Clin. Cancer Res. 10, 4227s-4232s
8. Marinov, M., Ziogas, A., Pardo, O. E., Tan, L. T., Dhillon, T., Mauri, F. A., Lane, H. A., Lemoine, N. R., Zangemeister-Wittke, U., Seckl, M. J., and Arcaro, A. (2009) AKT/mTOR pathway activation and BCL-2 family proteins modulate the sensitivity of human small cell lung cancer cells to RAD001. Clin. Cancer Res. 15, 1277-1287
9. Santos, G., Shepherd, F. A., and Tsao, M. S. (2011) EGFR mutation and lung cancer. Annu. Rev. Pathol. Mech. Dis. 6, 49-69
10. Chiarugi, P., and Buricchi, F. (2007) Protein tyrosine phosphorylation and reversible oxidation: two cross-talking posttranslation modifications. Antioxid. Redox Signal 9, 1-24
11. Chen, C. H., Cheng, T. H., Lin, H., Shih, N. L., Chen, Y. L., Chen, Y. S., Cheng, C. F., Lian, W. S., Meng, T. C., Chiu, W. T., and Chen, J. J. (2006) Reactive oxygen species generation is involved in epidermal growth factor receptor transactivation through the transient oxidization of Src homology 2-containing tyrosine phosphatase in endothelin-1 signaling pathway in rat cardiac fibroblasts. Mol. Pharmacol. 69, 1347-1355
12. Trachootham, D., Alexandre, J., and Huang, P. (2009) Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat. Rev. Drug Discov. 8, 579-591
13. Irmer, D., Funk, J. O., and Blaukat, A. (2007) EGFR kinase domain mutations-functional impact and relevance for lung cancer therapy. Oncogene 26, 5693-5701
14. Rodrigues, C. F., Rodrigues, C. F., Urbano, A. M., Matoso, E., Carreira, I., Almeida, A., Santos, P., Botelho, F., Carvalho, L., Alves, M., Monteiro, C., Costa, A. N., Moreno, V., and Alpoim, M. C. (2009) Human bronchial epithelial cells malignantly transformed by hexavalent chromium exhibit an aneuploid phenotype but no microsatellite instability. Mutat. Res. 670, 42-52
15. Wang, B. J., Sheu, H. M., Guo, Y. L., Lee, Y. H., Lai, C. S., Pan, M. H., and Wang, Y. I. (2010) Hexavalent chromium induced ROS formation, Akt, NF-κB, and MAPK activation, and TNF-α and IL-1α production in keratinocytes. Toxicol. Lett. 198, 216-224
16. Beaver, L. M., Stemmy, E. J., Schwartz, A. M., Damsker, J. M., Constant, S. L., Ceryak, S. M., and Patierno, S. R. (2010) Lung Inflammation, Injury, and Proliferative Response after Repetitive Particulate Hexavalent Chromium Exposure. Environ. Health Perspec. 117, 1898-1902
17. Wang, X., Son, Y. O., Chang, Q., Sun, L., Hitron, J. A., Budhraja, A., Zhang, Z., Ke, Z., Chen, F., Luo, J., and Shi, X. (2011) NADPH oxidase activation is required in reactive oxygen species generation and cell transformation induced by hexavalent chromium. Toxicol. Sci. 123, 399-410
18. Sun, Y., Ren, Y., Fang, Z., Li, C., Fang, R., Gao, B., Han, X., Tian, W., Pao, W., Chen, H., and Ji, H. (2010) Lung adenocarcinoma from East Asian never-smokers is a disease largely defined by targetable oncogenic mutant kinases. J. Clin. Oncol. 28, 4616-4620
19. Harris, R. C., Chung, E., and Coffey, R. J. (2003) EGF receptor ligands. Exp. Cell Res. 284, 2-13
20. Portt, L., Norman, G., Clapp, C., Greenwood, M., and Greenwood, M. T. (2011) Anti-apoptosis and cell survival: a review. Biochim. Biophys. Acta 1813, 238-259
21. Shi, X., and Dalal, N. S. (1989) Chromium (V) and hydroxyl radical formation during the glutathione reductase-catalyzed reduction of chromium (VI). Biochem. Biophys. Res. Commun. 163, 627-634
22. Yao, H., Guo, L., Jiang, B., Luo, J., Zhang, Z., and Shi, X. (2008) Oxidative stress and chromium carcinogenesis. J. Environ. Pathol. Toxicol. Oncol. 27, 77-88
23. Leonard, S. S., Harris, G. K., and Shi, X. (2004) Metal-induced oxidative stress and signal transduction. Free Radic. Biol. Med. 37, 1921-1942
24. Ye, J., Wang, S., Leonard, S. S., Sun, Y., Butterworth, L., Antonini, J., Ding, M., Rojanasakul, Y., Vallyathan, V., Castranova, V., and Shi, X. (1999) Role of reactive oxygen species and p53 in chromium (VI)-induced apoptosis. J. Biol. Chem. 274, 34974-34980
25. Lee, D. H., Szczepanski, M. J., and Lee, Y. J. (2009) Magnolol induces apoptosis via inhibiting the EGFR/PI3K/Akt signaling pathway in human prostate cancer cells. J. Cell. Biochem. 106, 1113-1122
26. Zhou, C., Qiu, L., Sun, Y., Healey, S., Wanebo, H., Kouttab, N., Di, W., Yan, B., and Wan, Y. (2006) Inhibition of EGFR/PI3K/AKT cell survival pathway promotes TSA's effect on cell death and migration in human ovarian cancer cells. Int. J. Oncol. 29, 269-278
27. Greulich, H., Chen, T. H., Feng, W., Jänne, P. A., Alvarez, J. V., Zappaterra, M., Bulmer, S. E., Frank, D. A., Hahn, W. C., Sellers, W. R., and Meyerson, M. (2005) Oncogenic transformation by inhibitor-sensitive and -resistant EGFR mutants. PLOS Med. 2, e313
28. Yun, C. H., Boggon, T. J., Li, Y., Woo, M. S., Greulich, H., Meyerson, M., and Eck, M. J. (2007) Structures of lung cancer-derived EGFR mutants and inhibitor complexes: mechanism of activation and insights into differential inhibitor sensitivity. Cancer Cell 11, 217-227
29. Zhou, B. B., Peyton, M., He, B., Liu, C., Girard, L., Caudler, E., Lo, Y., Baribaud, F., Mikami, I., Reguart, N., Yang, G., Li, Y., Yao, W., Vaddi, K., Gazdar, A. F., Friedman, S. M., Jablons, D. M., Newton, R. C., Fridman, J. S., Minna, J. D., and Scherle, P. A. (2006) Targeting ADAM-mediated ligand cleavage to inhibit HER3 and EGFR pathways in non-small cell lung cancer. Cancer Cell 10, 39-50
30. Truong, T. H., and Carroll, K. S. (2013) Redox regulation of protein kinases. Crit. Rev. Biochem. Mol. Biol. 48, 332-356
31. Knebel, A., Rahmsdorf, H. J., Ullrich, A., and Herrlich, P. (1996) Dephosphorylation of receptor tyrosine kinases as target of regulation by radiation, oxidants or alkylating agents. EMBO J. 15, 5314-5325
32. Sancho, P., and Fabregat, I. (2010) NADPH oxidase NOX1 controls autocrine growth of liver tumor cells through up-regulation of the epidermal growth factor receptor pathway. J. Biol. Chem. 285, 24815-24824
33. Mesquita, F. S., Dyer, S. N., Heinrich, D. A., Bulun, S. E., Marsh, E. E., and Nowak, R. A. (2010) Reactive oxygen species mediate mitogenic growth factor signaling pathways in human leiomyoma smooth muscle cells. Biol. Reprod. 82, 341-351
34. Paletta-Silva, R., Rocco-Machado, N., and Meyer-Fernandes, J. R. (2013) NADPH oxidase biology and the regulation of tyrosine kinase receptor signaling and cancer drug cytotoxicity. Int. J. Mol. Sci. 14, 3683-3704
35. Ellis, R. E., Yuan, J., and Horvitz, H. R. (1991) Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7, 663-698
36. Hanahan, D., and Weinberg, R. A. (2000) The hallmarks of cancer. Cell 100, 57-70
37. Wyllie, A. H., Bellamy, C. O., Bubb, V. J., Clarke, A. R., Corbet, S., Curtis, L., Harrison, D. J., Hooper, M. L., Toft, N., Webb, S., and Bird, C. C. (1999) Apoptosis and carcinogenesis. Br. J. Cancer 80, 34-37
38. Medan, D., Luanpitpong, S., Azad, N., Wang, L., Jiang, B., Davis, M. E., Barnett, J. B., Guo, L., and Rojanasakul, Y. (2012) Multifunctional Role of Bcl-2 in Malignant Transformation and Tumorigenesis of Cr(VI)-Transformed Lung Cells. PLOS One 7, e37045
39. Zinkel, S., Gross, A., and Yang, E. (2006) BCL2 family in DNA damage and cell cycle control. Cell Death Differ. 13, 1351-1359
40. Faber, A. C., Li, D., Song, Y., Liang, M. C., Yeap, B. Y., Bronson, R. T., Lifshits, E., Chen, Z., Maira, S. M., García-Echeverría, C., Wong, K. K., and Engelman, J. A. (2009) Differential induction of apoptosis in HER2 and EGFR addicted cancers following PI3K inhibition. Proc. Natl. Acad. Sci. U.S.A. 106, 19503-19508
41. Kagan, V., Bakalova, R., and Karakashev, P. (1990) Lipid peroxidation in tumor cells and tissues of tumor-bearing animals, in: "Membrane Lipid Oxidation", Vigo-Pelfrey, C. (ed), CRC Press, Boca-Raton, Florida 3, 192-208
42. Ivanova, D., Bakalova, R., Lazarova, D., Gadjeva, V., and Zhelev, Z. (2013) The impact of reactive oxygen species on anticancer therapeutic strategies. Adv. Clin. Exp. Med. 22, 899-908
43. Chen, F., Vallyathan, V., Castranova, V., and Shi, X. (2001) Cell apoptosis induced by carcinogenic metals. Mol. Cell Biochem. 222, 183-188
44. Wang, X., McCullough, K. D., Franke, T. F., and Holbrook, N. J. (2000) Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J. Biol. Chem. 275, 14624-14631
45. Fischer, O. M., Hart, S., Gschwind, A., Prenzel, N., and Ullrich, A. (2004) Oxidative and osmotic stress signaling in tumor cells is mediated by ADAM proteases and heparin-binding epidermal growth factor. Mol. Cell. Biol. 24, 5172-5183
46. Peus, D., Vasa, R. A., Meves, A., Beyerle, A., and Pittelkow, M. R. (2000) UVB-induced epidermal growth factor receptor phosphorylation is critical for downstream signaling and keratinocyte survival. Photochem. Photobiol. 72, 135-140
47. Orcutt, K. P., Parsons, A. D., Sibenaller, Z. A., Scarbrough, P. M., Zhu, Y., Sobhakumari, A., Wilke, W. W., Kalen, A. L., Goswami, P., Miller, F. J., Jr., Spitz, D. R., and Simons, A. L. (2011) Erlotinib-mediated inhibition of EGFR signaling induces metabolic oxidative stress through NOX4. Cancer Res. 71, 3932-3940
48. Yarden, Y., and Sliwkowski, M. X. (2001) Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2, 127-137
49. Sordella, R., Bell, D. W., Haber, D. A., and Settleman, J. (2004) Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science 305, 1163-1167
50. Fumarola, C., Bonelli, M. A., Petronini, P. G., and Alfieri, R. R. (2014) Targeting PI3K/AKT/mTOR pathway in non-small cell lung cancer. Biochem. Pharmacol. 90, 197-207
51. Pugazhenthi, S., Nesterova, A., Sable, C., Heidenreich, K. A., Boxer, L. M., Heasley, L. E., and Reusch, J. E. (2000) Akt/protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein. J. Biol. Chem. 275, 10761-10766