Organic extract contaminants from drinking water activate Nrf2-mediated antioxidant response in a human cell line

Environmental Science and Technology

Volumn 47, Issue 9, 2013, Pages 4768-4777

  Wang, Shu ^a   Zhang, Hao ^a,b   Zheng, Weiwei ^a   Wang, Xia ^a   Andersen, Melvin E ^b   Pi, Jingbo ^b   He, Gengsheng ^a   Qu, Weidong ^a  

^a FUDAN UNIVERSITY   (China)

^b HAMNER INSTITUTES FOR HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-OXIDANT RESPONSE; ANTIOXIDANT RESPONSE ELEMENTS; DRINKING WATER SOURCES; ENVIRONMENTAL EXPOSURE; OXIDATIVE STRESS RESPONSE; PROTEIN ACCUMULATION; REPORTER GENE ASSAYS; RISK ASSESSMENT METHODS;

CELL CULTURE; GENE EXPRESSION; MIXTURES; RISK ASSESSMENT; RISK PERCEPTION; TOXICITY;

CONTAMINATION;

ACETIC ACID; DRINKING WATER; ESTROGEN DERIVATIVE; GLUTAMATE CYSTEINE LIGASE; HEME OXYGENASE 1; LUCIFERASE; NITROSAMINE; ORGANIC COMPOUND; ORGANIC CONTAMINANT EXTRACT; ORGANOCHORIONIC PESTICIDE; PESTICIDE; PHENOL; POLYCHLORINATED BIPHENYL; POLYCYCLIC AROMATIC HYDROCARBON; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE QUINONE OXIDOREDUCTASE 1; TRANSCRIPTION FACTOR NRF2; TRIHALOMETHANE; UNCLASSIFIED DRUG; VOLATILE ORGANIC COMPOUND;

ANTIOXIDANT; BIOACCUMULATION; BIOASSAY; CELL ORGANELLE; DRINKING WATER; GENE EXPRESSION; MEASUREMENT METHOD; ORGANIC POLLUTANT; PROTEIN; RISK ASSESSMENT; TOXICITY;

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; BIOACCUMULATION; CELL STRAIN HEPG2; CONCENTRATION (PARAMETERS); CYTOTOXICITY; GENE ACTIVATION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PROTEIN EXPRESSION; REPORTER GENE; TOXICITY TESTING; TRANSCRIPTION INITIATION; WATER CONTAMINATION;

ANTIOXIDANTS; DRINKING WATER; HEP G2 CELLS; HUMANS; NF-E2-RELATED FACTOR 2; REAL-TIME POLYMERASE CHAIN REACTION; WATER POLLUTANTS, CHEMICAL;

EID: 84877593799     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es305133k     Document Type: Article

References (62)

1. U.S.EPA (Environmental Protection Agency). Supplementary Guidance for Conducting Health Risk Assessment of Chemical Mixtures; EPA/630/R-00/002; U.S. Environmental Protection Agency: Washington, DC, 2000.
2. WHO (World Health Organization). Assessment of Combined Exposures to Multiple Chemicals: Report of a WHO/IPCS International Workshop on Aggregate/Cumulative Risk Assessment; WHO: Geneva, Switzerland, 2007.
3. Silva, E.; Rajapakse, N.; Kortenkamp, A. Something from "Nothing"-Eight Weak Estrogenic Chemicals Combined at Concentrations below NOECs Produce Significant Mixture Effects Environ. Sci. Technol. 2002, 36 (8) 1751-1756
4. Wang, S.; Tian, D.; Zheng, W.; Jiang, S.; Wang, X.; Andersen, M. E.; Zheng, Y.; He, G.; Qu, W. Combined exposure to 3-Chloro-4-dichloromethyl-5- hydroxy-2(5H)-furanone and Microsytin-LR Increases Genotoxicity in Chinese Hamster Ovary Cells through Oxidative Stress Environ. Sci. Technol. 2013, 47 (3) 1678-1687
5. National Research Council. Science and Decision: Advancing Risk Assessment; National Academy Press: Washington, D.C., 2008.
6. Hartung, T. Toxicology for the Twenty-First Century Nature 2009, 460 (7252) 208-212
7. Armstrong, D., Eds. Advanced Protocols in Oxidative Stress II; Humana Press: New York, 2010.
8. Committee on Toxicity Testing and Assessment of Environmental Agents, National Research Council. Toxicity Testing in the 21st Century: A Vision and a Strategy; The National Academies Press: Washington, D.C., 2007.
9. National Research Council staff. Cumulative Risk Assessment for Environmental Mixtures: New Approaches Based on Pathways. Emerging Science for Environmental Health Decisions, Newsletter, 2012.
10. Limón-Pacheco, J.; Gonsebatt, M. E. The Role of Antioxidants and Antioxidant-Related Enzymes in Protective Responses to Environmentally Induced Oxidative Stress Mutat. Res. 2009, 674 (1-2) 137-147
11. Itoh, K.; Ishii, T.; Wakabayashi, N.; Yamamoto, M. Regulatory Mechanisms of Cellular Response to Oxidative Stress Free Radic. Res. 1999, 31 (4) 319-24
12. Pi, J.; Bai, Y.; Reece, J. M.; Williams, J.; Liu, D.; Freeman, M. L.; Fahl, W. E.; Shugar, D.; Liu, J.; Qu, W.; Collins, S.; Waalkes, M. P. Molecular Mechanism of Human Nrf2 Activation and Degradation: Role of Sequential Phosphorylation by Protein Kinase CK2 Free Radic. Biol. Med. 2007, 42 (12) 1797-806
13. Kobayashi, M.; Yamamoto, M. Nrf2-Keap1 Regulation of Cellular Defense Mechanisms against Electrophiles and Reactive Oxygen Species Adv. Enzyme. Regul. 2006, 46, 113-140
14. Cho, H. Y.; Reddy, S. P.; Kleeberger, S. R. Nrf2 Defends the Lung from Oxidative Stress Antioxid. Redox. Signal. 2006, 8 (1-2) 76-87
15. Zeni, O.; Di Pietro, R.; d'Ambrosio, G.; Massa, R.; Capri, M.; Naarala, J.; Juutilainen, J.; Scarfì, M. R. Formation of Reactive Oxygen Species in L929 Cells after Exposure to 900 MHz RF Radiation with and without Co-Exposure to 3-Chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone Radiat. Res. 2007, 167 (3) 306-311
16. Zeni, O.; Salvemini, F.; Di Pietro, R.; Buonincontri, D.; Komulainen, H.; Romanò, M.; Scarfí, M. R. Induction of Oxidative Stress in Murine Cell Lines by 3-Chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone (MX) Toxicol. Lett. 2004, 147 (1) 79-85
17. Zhou, L.; Zou, Y.; Lai, R.; Fan, G. Oxidative Stress of Human Derived Fetal Hepatocytes Induced by Product of Chlorinated Drinking Water (MX) J. Hygiene. Res. 2007, 36 (2) 149-151
18. Ahmed, A. E.; Aronson, J.; Jacob, S. Induction of Oxidative Stress and TNF-alpha Secretion by Dichloroacetonitrile, A Water Disinfectant by-Product, As Possible Mediators of Apoptosis or Necrosis in a Murine Macrophage Cell Line (RAW) Toxicol. In Vitro 2000, 14 (3) 199-210
19. Jung, K. H.; Hong, S. W.; Zheng, H. M.; Lee, D. H.; Hong, S. S. Melatonin Downregulates Nuclear Erythroid 2-Related Factor 2 and Nuclear Factor-kappaB during Prevention of Oxidative Liver Injury in a Dimethylnitrosamine Model J. Pineal. Res. 2009, 47 (2) 173-83
20. Woods, C. G.; Fu, J.; Xue, P.; Hou, Y.; Pluta, L. J.; Yang, L.; Zhang, Q.; Thomas, R. S.; Andersen, M. E.; Pi, J. Dose-Dependent Transitions in Nrf2-Mediated Adaptive Response and Related Stress Responses to Hypochlorous Acid in Mouse Macrophages Toxicol. Appl. Pharmacol. 2009, 238 (1) 27-36
21. Zhao, S.; Xie, P.; Li, G.; Jun, C.; Cai, Y.; Xiong, Q.; Zhao, Y. The Proteomic Study on Cellular Responses of the Testes of Zebrash (Danio rerio) Exposed to Microcystin-RR Proteomics 2012, 12 (2) 300-312
22. Jiang, J.; Gu, X.; Song, R.; Zhang, Q.; Geng, J.; Wang, X.; Yang, L. Time-Dependent Oxidative Stress and Histopathological Changes in Cyprinus carpio L. Exposed to Microcystin-LR Ecotoxicology 2011, 20 (5) 1000-1009
23. Hassan, H. M.; Fridovich, I. Superoxide Radical and the Oxygen Enhancement of the Toxicity of Paraquat in Escherichia coli J. Biol. Chem. 1978, 253 (22) 8143-8148
24. Rhodes, M. L.; Zavala, D. C.; Brown, D. Hypoxic Protection in Paraquat Poisoning Lab Invest. 1976, 35 (5) 496-500
25. Stancliffe, T. C.; Pirie, A. The Production of Superoxide Radicals in Reactions of the Herbicide Diquat FEBS Lett. 1971, 17 (2) 297-299
26. Osburn, W. O.; Wakabayashi, N.; Misra, V.; Nilles, T.; Biswal, S.; Trush, M. A.; Kensler, T. W. Nrf2 Regulates an Adaptive Response Protecting against Oxidative Damage Following Diquat-Mediated Formation of Superoxide Anion Arch. Biochem. Biophys. 2006, 454 (1) 7-15
27. Li, H. Y.; Wu, S. Y.; Ma, Q.; Shi, N. The Pesticide Deltamethrin Increases Free Radical Production and Promotes Nuclear Translocation of the Stress Response Transcription Factor Nrf2 in Rat Brain Toxicol. Ind. Health. 2011, 27 (7) 579-590
28. Li, H. Y.; Wu, S. Y.; Shi, N. Transcription Factor Nrf2 Activation by Deltamethrin in PC12 Cells: Involvement of ROS Toxicol. Lett. 2007, 171 (1-2) 87-98
29. Klaunig, J. E.; Xu, Y.; Isenberg, J. S.; Bachowski, S.; Kolaja, K. L.; Jiang, J.; Stevenson, D. E.; Walborg, E. F., Jr. the Role of Oxidative Stress in Chemical Carcinogenesis Environ. Health Perspect. 1998, 106 (Suppl 1) 289-295
30. Morio, L. A.; Leone, A.; Sawant, S. P.; Nie, A. Y.; Parker, J. B.; Taggart, P.; Barron, A. M.; McMillian, M. K.; Lord, P. Hepatic Expression of Heme Oxygenase-1 and Antioxidant Response Element-Mediated Genes Following Administration of Ethinyl Estradiol to Rats Toxicol. Appl. Pharmacol. 2006, 216 (3) 416-425
31. Ulas, M.; Cay, M. The Effects of 17beta-Estradiol and Vitamin E Treatments on Oxidative Stress and Antioxidant Levels in Brain Cortex of Diabetic Ovari-ectomized Rats Acta Physiol. Hung. 2010, 97 (2) 208-215
32. Lucarini, M.; Pedulli, G. F.; Valgimigli, L.; Amorati, R.; Minisci, F. Thermo-Chemical and Kinetic Studies of a Bisphenol Antioxidant J. Org. Chem. 2001, 66 (16) 5456-5462
33. Chitra, K. C.; Latchoumycandane, C.; Mathur, P. P. Effect of Nonylphenol on the Antioxidant System in Epididymal Sperm of Rats Arch. Toxicol. 2002, 76 (9) 5455-5451
34. Xiao, Q.; Zhang, S.; Guo, H.; Su, F.; Xu, Y. Nonylphenol Causes Decrease in Antioxidant Enzyme Activities, Increase in O(2)(-) Content, And Alteration in Ultrastructures of FG Cells, A Flounder (Paralichthys olivaceus) Gill Cell Line Toxiol. Mech. Methods. 2007, 17 (3) 127-134
35. Park, S. H.; Jang, J. H.; Chen, C. Y.; Na, H. K.; Surh, Y. J. A Formulated Red Ginseng Extract Rescues PC12 Cells from PCB-Induced Oxidative Cell Death through Nrf2-Mediated Upregulation of Heme Oxygenase-1 and Glutamate Cysteine Ligase Toxicology 2010, 278 (1) 131-139
36. Majkova, Z.; Layne, J.; Sunkara, M.; Morris, A. J.; Toborek, M.; Hennig, B. Omega-3 Fatty Acid Oxidation Products Prevent Vascular Endothelial Cell Activation by Coplanar Polychlorinated Biphenyls Toxicol. Appl. Pharmacol. 2011, 251 (1) 41-49
37. Claxton, L. D.; Pegram, R.; Schenck, K. M.; Simmons, J. E.; Warren, S. H. Integrated Disinfection by-Products Research: Salmonella Mutagenicity of Water Concentrates Disinfected by Chlorination and Ozonation/ Postchlorination J. Toxicol. Environ. Health A. 2008, 71 (17) 1187-1194
38. Buschini, A.; Giordani, F.; Pellacani, C.; Rossi, C.; Poli, P. Cytotoxic and Genotoxic Potential of Drinking Water: A Comparison between Two Different Concentration Methods Water Res. 2008, 42 (8-9) 1999-2006
39. Constan, A. A.; Yang, R. S.; Baker, D. C.; Benjamin, S. A. A Unique Pattern of Hepatocyte Proliferation in F344 Rats Following Long-Term Exposures to Low Levels of a Chemical Mixture of Groundwater Contaminants Carcinogenesis 1995, 16 (2) 303-310
40. Loper, J. C.; Lang, D. R.; Schoeny, R. S.; Richmond, B. B.; Gallagher, P. M.; Smith, C. C. Residue Organic Mixture from Drinking Water Show in Vitro Mutagenic and Transforming Activity J. Toxicol. Environ. Health. 1978, 4 (5-6) 919-938
41. Zheng, W.; Wang, X.; Tian, D.; Jiang, S.; Andersen, M. E.; He, G.; Crabbe, M. J. C. C.; Zheng, Y.; Zhong, Y.; Qu, W. Water Pollutant Fingerprinting Tracks Recent Industrial Transfer from Coastal to Inland China: A Case Study Sci. Rep. 2013, 3, 1031
42. Zheng, W.; Tian, D.; Wang, X.; Tian, W.; Zhang, H.; Jiang, S.; He, G.; Zheng, Y.; Qu, W. Support Vector Machine: Classifying and Predicting Mutagenicity of Complex Mixtures Based on Pollution Profiles Toxicology 2013, 10.1016/j.tox.2013.01.016
43. U.S.EPA (Environmental Protection Agency). Method 525.2: Determination of Organic Compounds in Drinking Water by Liquid-Solid Extraction and Capillary Column Gas Chromatography/Mass Spectrometry; EPA/600/R-95-131; U.S. Environmental Protection Agency: OH, 1995.
44. Chen, L.; Zhou, Y.; Wu, Y. L.; Zhang, H.; Wang, X.; Zheng, W. W.; Liu, L.; Jiang, S. H.; Qu, W. D.; Zhao, J. W. Status of Trace Organic Pollution in the Network Water Came from Huangpu River [in Chinese] J. Hygiene Res. 2008, 37 (2) 137-143
45. Pi, J.; Bai, Y.; Reece, J. M.; William, J.; Liu, D.; Freeman, M. L.; Fahl, W. E.; Shugar, D.; Liu, J.; Qu, W.; Collins, S.; Waalkes, M. P. Molecular Mechanism of Nrf2 Activation and Degradation: Role of Sequential Phosphorylation by Protein Kinase CK2 Free Radic. Biol. Med. 2007, 42 (12) 1797-1806
46. Pi, J.; Zhang, Q.; Wong, V.; Woods, C.; Collins, S.; Andersen, M. E. Activation of Nrf2-Mediated Oxidative Stress Response in Macrophages by Hypochlorous Acid Toxicol. Appl. Pharmacol. 2008, 226, 236-243
47. Pi, J.; Qu, W.; Reece, J. M.; Kumagai, Y.; Waalkes, M. P. Transcription Factor Nrf2 Activation by Inorganic Arsenic in Cultured Keratinocytes: Involvement of Hydrogen Peroxide Exp. Cell Res. 2003, 290 (2) 234-245
48. Dupuis, A.; Migeot, V.; Cariot, A.; Albouy-Llaty, M.; Legube, B.; Rabouan, S. Quantification of Bisphenol a, 353-Nonylphenol and Their Chlorinated Derivatives in Drinking Water Treatment Plants Environ. Sci. Pollut. Res. Int. 2012, 10.1007/s11356-012-0972-3
49. Wang, W.; Ren, S.; Zhang, H.; Yu, J.; An, W.; Hu, J.; Yang, M. Occurrence of Nine Nitrosamines and Secondary Amines in Source Water and Drinking Water: Potential of Secondary Amines As Nitrosamine Precursors Water Res. 2011, 45 (16) 4930-4938
50. Pi, J.; Bai, Y.; Reece, J. M.; William, J.; Liu, D.; Freeman, M. L.; Fahl, W. E.; Shugar, D.; Liu, J.; Qu, W.; Collins, S.; Waalkes, M. P. Molecular Mechanism of Nrf2 Activation and Degradation: Role of Sequential Phosphorylation by Protein Kinase CK2 Free Radic. Biol. Med. 2007, 42 (12) 1797-1806
51. Gharavi, N.; Haggarty, S.; El-Kadi, A. O. Chemoprotective and Carcinogenic Effects of tert -Butylhydroquinone and its metabolites Curr. Drug Metab. 2007, 8 (1) 1-7
52. el-Masri, H. A.; Thomas, R. S.; Benjamin, S. A.; Yang, R. S. Physiologically Based Pharmacokinetic/Pharmacodynamic Modeling of Chemical Mixtures and Possible Applications in Risk Assessment Toxicology 1995, 105 (2-3) 275-282
53. Vollmer, C. M.; Ribas, A.; Butterfield, L. H.; Dissette, V. B.; Andrews, K. J.; Eilber, F. C.; Montejo, L. D.; Chen, A. Y.; Hu, B.; Glaspy, J. A.; McBride, W. H.; Economou, J. S. p53 Selective and Nonselective Replication of an E1B-Deleted Adenovirus in Hepatocellular Carcinoma Cancer Res. 1999, 59 (17) 4369-4374
54. Adachi, T.; Nakagawa, H.; Chung, I.; Hagiya, Y.; Hoshijima, K.; Noguchi, N.; Kuo, M. T.; Ishikawa, T. Nrf2-Dependent and -Independent Induction of ABC Transporters ABCC1, ABCC2, and ABCG2 in HepG2 Cells under Oxidative Stress J. Exp. Ther. Oncol. 2007, 6 (4) 335-348
55. Westerink, W. M.; Schoonen, W. G. Phase II Enzyme Levels in HepG2 Cells and Cryopreserved Primary Human Hepatocytes and Their Induction in HepG2 Cells Toxicol. In Vitro 2007, 21 (8) 1592-1602
56. Westerink, W. M.; Schoonen, W. G. Cytochrome P450 Enzyme Levels in HepG2 Cells and Cryopreserved Primary Human Hepatocytes and Their Induction in HepG2 Cells Toxicol. In Vitro 2007, 21 (8) 1581-1591
57. Lou, H.; Du, S.; Ji, Q.; Stolz, A. Induction of AKR1C2 by Phase II Inducers: Identification of a Distal Consensus Antioxidant Response Element Regulated by NRF2 Mol. Pharmacol. 2006, 69 (5) 1662-1672
58. Zhang, Q.; Pi, J.; Woods, C. G.; Andersen, M. E. A Systems Biology Perspective on Nrf2-Mediated Antioxidant Response Toxicol. Appl. Pharmacol. 2010, 244 (1) 84-97
59. Wang, X. J.; Hayes, J. D.; Wolf, C. R. Generation of a Stable Antioxidant Response Element-Driven Reporter Gene Cell Line and Its Use to Show Redox-Dependent Activation of Nrf2 by Cancer Chemotherapeutic Agents Cancer Res. 2006, 66 (22) 10983-10994
60. Richardson, S. D.; Thruston, A. D., Jr.; Krasner, S. W.; Weinberg, H. S.; Miltner, R. J.; Schenck, K. M.; Narotsky, M. G.; McKague, A. B.; Simmons, J. E. Integrated Disinfection by-Products Mixtures Research: Comprehensive Characterization of Water Concentrates Prepared from Chlorinated and Ozonated/Postchlorinated Drinking Water J. Toxicol. Environ. Health A. 2008, 71 (17) 1165-1186
61. Chen, X.; Zhang, D.; Lu, Y. H.; Zheng, W. W.; Wu, Y. X.; Wei, X.; Tian, D. J.; Wang, X.; Zhang, H.; Guo, S.; Jiang, S. H.; Qu, W. D. Formation and Changes of Regulated Trihalomethanes and Haloacetic Acids in Raw Water of Yangtze River, Huangpu River and Different Treatment Processes and Pipelines Network [in Chinese] Chin. J. Prev. Med. 2010, 44 (10) 893-898
62. Yuan, J.; Liu, H.; Zhou, L. H.; Zou, Y. L.; Lu, W. Q. Oxidative Stress and DNA Damage Induced by a Drinking-Water Chlorination Disinfection by-Product 3-Chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone (MX) in Mice Mutat. Res. 2006, 609 (2) 129-136