Reactive oxygen species mediate Cr(VI)-induced S phase arrest through p53 in human colon cancer cells

Journal of Environmental Pathology, Toxicology and Oncology

Volumn 31, Issue 2, 2012, Pages 95-107

  Sun, Lijuan ^a   Wang, Xin ^a   Yao, Hua ^b   Li, Wenqi ^a   Son, Young Ok ^a   Luo, Jia ^d   Liu, Jiankang ^c   Zhang, Zhuo ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b ZHEJIANG UNIVERSITY   (China)

^c XI'AN JIAOTONG UNIVERSITY   (China)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Cell cycle; Cell cycle checkpoints; Chromium (VI); Human colon cancer; p53; Reactive oxygen species

Indexed keywords

CATALASE; CHROMIC ACID; COPPER ZINC SUPEROXIDE DISMUTASE; CYCLIN A; CYCLIN D1; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN E; HYDROGEN PEROXIDE; HYDROXYL RADICAL; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SHORT HAIRPIN RNA; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR E2F1;

ARTICLE; CELL VIABILITY; COLON ADENOCARCINOMA; CYTOTOXICITY; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; S PHASE CELL CYCLE CHECKPOINT; WESTERN BLOTTING;

ADENOCARCINOMA; CATALASE; CELL LINE, TUMOR; CHROMATES; COLONIC NEOPLASMS; ELECTRON SPIN RESONANCE SPECTROSCOPY; HUMANS; HYDROGEN PEROXIDE; HYDROXIDES; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; S PHASE; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84871310462     PISSN: 07318898     EISSN: None     Source Type: Journal    
DOI: 10.1615/JEnvironPatholToxicolOncol.v31.i2.20     Document Type: Article

References (58)

1. De Flora S, Bagnasco M, Serra D, Zanacchi P. Genotoxicity of chromium compounds. A review. Mutat Res. 1990;238:99-172.
2. De Flora S, Serra D, Basso C, Zanacchi P. Mechanistic aspects of chromium carcinogenicity. Arch Toxicol Suppl. 1989;13:28-39.
3. Stout MD, Nyska A, Collins BJ, Witt KL, Kissling GE, Malarkey DE, Hooth MJ. Chronic toxicity and carcinogenicity studies of chromium picolinate monohydrate administered in feed to F344/N rats and B6C3F1 mice for 2 years. Food Chem Toxicol. 2009;47:729-733.
4. Gatto NM, Kelsh MA, Mai DH, Suh M, Proctor DM. Occupational exposure to hexavalent chromium and cancers of the gastrointestinal tract: a metaanalysis. Cancer Epidemiol. 2010;34:388-399.
5. Zhang Z, Leonard SS, Wang S, Vallyathan V, Castranova V, Shi X. Cr(VI) induces cell growth arrest through hydrogen peroxide-mediated reactions. Mol Cell Biochem. 2001;222:77-83.
6. Ha L, Ceryak S, Patierno SR. Chromium (VI) activates ataxia telangiectasia mutated (ATM) protein. Requirement of ATM for both apoptosis and recovery from terminal growth arrest. J Biol Chem. 2003;278:17885-17894.
7. Wakeman TP, Xu B. ATR regulates hexavalent chromium-induced S-phase checkpoint through phosphorylation of SMC1. Mutat Res. 2006;610:14-20.
8. Shackelford RE, Kaufmann WK, Paules RS. Cell cycle control, checkpoint mechanisms, and genotoxic stress. Environ Health Perspect. 1999;107(Suppl 1):5-24.
9. Hartwell LH, Kastan MB. Cell cycle control and cancer. Science. 1994;266:1821-1828.
10. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature. 2000;408:307-310.
11. Waldman T, Kinzler KW, Vogelstein B. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res. 1995;55:5187-5190.
12. Hill R, Leidal AM, Madureira PA, Gillis LD, Waisman DM, Chiu A, Lee PW. Chromium-mediated apoptosis: involvement of DNA-dependent protein kinase (DNA-PK) and differential induction of p53 target genes. DNA Repair (Amst). 2008;7:1484- 1499.
13. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP, Sedivy JM, Kinzler KW, Vogelstein B. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science. 1998;282:1497-1501.
14. Nicoletti I, Migliorati G, Pagliacci MC, Grignani F, Riccardi C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods. 1991;139:271-279.
15. Sgonc R, Wick G. Methods for the detection of apoptosis. Int Arch Allergy Immunol. 1994;105:327-332.
16. Bass DA, Parce JW, Dechatelet LR, Szejda P, Seeds MC, Thomas M. Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation. J Immunol. 1983;130:1910-1917.
17. LeBel CP, Ischiropoulos H, Bondy SC. Evaluation of the probe 2',7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol. 1992;5:227-231.
18. Ye J, Wang S, Leonard SS, Sun Y, Butterworth L, Antonini J,Ding M, Rojanasakul Y, Vallyathan V, Castranova V, Shi X. Role of reactive oxygen species and p53 in chromium(VI)-induced apoptosis. J Biol Chem. 1999;274:34974-34980.
19. Agarwal ML, Taylor WR, Chernov MV, Chernova OB, Stark GR. The p53 network. J Biol Chem. 1998;273:1-4.
20. Sorahan T, Burges DC, Hamilton L, Harrington JM. Lung cancer mortality in nickel/chromium platers, 1946-95. Occup Environ Med. 1998;55:236-242.
21. Langard S, Norseth T. A cohort study of bronchial carcinomas in workers producing chromate pigments. Br J Ind Med. 1975;32:62-65.
22. Norseth T. The carcinogenicity of chromium. Environ Health Perspect. 1981;40:121-30.
23. Enterline PE. Respiratory cancer among chromate workers. J Occup Med. 1974;16:523-526.
24. De Flora S, Serra D, Basso C, Zanacchi P. Mechanistic aspects of chromium carcinogenicity. Arch Toxicol Suppl. 1989;13:28-39.
25. Venitt S, Levy LS. Mutagenicity of chromates in bacteria and its relevance to chromate carcinogenesis. Nature. 1974;250:493-495.
26. Heichman KA, Roberts JM. Rules to replicate by. Cell. 1994;79:557-562.
27. Sherr CJ. Cancer cell cycles. Science. 1996;274:1672-1677.
28. Xu J, Bubley GJ, Detrick B, Blankenship LJ, Patierno SR. Chromium(VI) treatment of normal human lung cells results in guanine-specific DNA polymerase arrest, DNA-DNA cross-links and S-phase blockade of cell cycle. Carcinogenesis. 1996;17:1511-1517.
29. Sherr CJ, McCormick F. The RB and p53 pathways in cancer. Cancer Cell. 2002;2:103-112.
30. Sheaff RJ, Groudine M, Gordon M, Roberts JM, Clurman BE. Cyclin E-CDK2 is a regulator of p27Kip1. Genes Dev. 1997;11:1464-1478.
31. Inoshita S, Terada Y, Nakashima O, Kuwahara M, Sasaki S, Marumo F. Roles of E2F1 in mesangial cell proliferation in vitro. Kidney Int. 1999;56:2085-2095.
32. Lees JA, Saito M, Vidal M, Valentine M, Look T, Harlow E, Dyson N, Helin K. The retinoblastoma protein binds to a family of E2F transcription factors. Mol Cell Biol. 1993;13:7813-7825.
33. Ikeda MA, Jakoi L, Nevins JR. A unique role for the Rb protein in controlling E2F accumulation during cell growth and differentiation. Proc Natl Acad Sci U S A. 1996;93:3215-3220.
34. Moberg K, Starz MA, Lees JA. E2F-4 switches from p130 to p107 and pRB in response to cell cycle reentry. Mol Cell Biol. 1996;16:1436-1449.
35. Helin K. Regulation of cell proliferation by the E2F transcription factors. Curr Opin Genet Dev. 1998;8:28-35.
36. DeGregori J, Leone G, Miron A, Jakoi L, Nevins JR. Distinct roles for E2F proteins in cell growth control and apoptosis. Proc Natl Acad Sci U S A. 1997;94:7245-7250.
37. Cam H, Dynlacht BD. Emerging roles for E2F: beyond the G1/S transition and DNA replication. Cancer Cell. 2003;3:311-316.
38. DeGregori J, Kowalik T, Nevins JR. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/S-regulatorygenes. Mol Cell Biol. 1995;15:4215-4224.
39. Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB. Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med. 2010;49:1603-1616.
40. Trush MA, Kensler TW. An overview of the relationship between oxidative stress and chemical carcinogenesis. Free Radic Biol Med. 1991;10:201-209.
41. Cerutti PA. Prooxidant states and tumor promotion. Science. 1985;227:375-381.
42. Slaga TJ, Klein-Szanto AJ, Triplett LL, Yotti LP, Trosko KE. Skin tumor-promoting activity of benzoyl peroxide, a widely used free radical-generating compound. Science. 1981;213:1023-1025.
43. Kamata T. Roles of Nox1 and other Nox isoforms in cancer development. Cancer Sci. 2009;100:1382-1388.
44. Zhang Z, Wang X, Cheng S, Sun L, Son YO, Yao H, Li W, Budhraja A, Li L, Shelton BJ, Tucker T, Arnold SM, 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.
45. Ozaki T, Nakagawara A. p53: the attractive tumor suppressor in the cancer research field. J Biomed Biotechnol. 2011;2011:603925.
46. Vousden KH, Lu X. Live or let die: the cell's response to p53. Nat Rev Cancer. 2002;2:594-604.
47. Sionov RV, Haupt Y. The cellular response to p53: the decision between life and death. Oncogene. 1999;18:6145-6157.
48. El-Deiry WS. The role of p53 in chemosensitivity and radiosensitivity. Oncogene. 2003;22:7486-7495.
49. Kim DH, Kundu JK, Surh YJ. Redox modulation of p53: mechanisms and functional significance. Mol Carcinog. 2011;50:222-234.
50. Lacroix M, Toillon RA, Leclercq G. p53 and breast cancer, an update. Endocr Relat Cancer. 2006;13:293-325.
51. Yao H, Guo L, Jiang BH, Luo J, Shi X. Oxidative stress and chromium(VI) carcinogenesis. J Environ Pathol Toxicol Oncol. 2008;27:77-88.
52. Shi X, Chiu A, Chen CT, Halliwell B, Castranova V, Vallyathan V. Reduction of chromium(VI) and its relationship to carcinogenesis. J Toxicol Environ Health B Crit Rev. 1999;2:87-104.
53. Harris GK, Shi X. Signaling by carcinogenic metals and metal-induced reactive oxygen species. Mutat Res. 2003;533:183-200.
54. Leonard SS, Bower JJ, Shi X. Metal-induced toxicity, carcinogenesis, mechanisms and cellular responses. Mol Cell Biochem. 2004;255:3-10.
55. Wang S, Shi X. Molecular mechanisms of metal toxicity and carcinogenesis. Mol Cell Biochem. 2001;222:3-9.
56. Pernin D, Uhrhammer N, Verrelle P, Bignon YJ, Bay JO. p53 activation by PI-3K family kinases after DNA double-strand breaks. Bull Cancer. 2000;87:635-641.
57. Wang S, Shi X. Mechanisms of Cr(VI)-induced p53 activation: the role of phosphorylation, mdm2 and ERK. Carcinogenesis. 2001;22:757-762.
58. Carlisle DL, Pritchard DE, Singh J, Patierno SR. Chromium(VI) induces p53-dependent apoptosis in diploid human lung and mouse dermal fibroblasts. Mol Carcinog. 2000;28:111-118.