Perfluorooctanoic acid induces gene promoter hypermethylation of glutathione-S-transferase Pi in human liver L02 cells

Toxicology

Volumn 296, Issue 1-3, 2012, Pages 48-55

  Tian, Meiping ^a   Peng, Siyuan ^a   Martin, Francis L ^b   Zhang, Jie ^a   Liu, Liangpo ^a   Wang, Zhanlin ^a   Dong, Sijun ^a   Shen, Heqing ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

DNA methylation; Epigenetics; GSTP; L02 liver cells; PFOA

Indexed keywords

ACOX PROTEIN; BISULFITE; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DNA; DNA METHYLTRANSFERASE 3A; ESTROGEN RECEPTOR ALPHA; GLUTATHIONE TRANSFERASE P1; MESSENGER RNA; NUCLEIC ACID BINDING PROTEIN; PERFLUOROOCTANOIC ACID; PROGESTERONE RECEPTOR B; PROTEIN P16; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BINDING SITE; CELL LINE; CONTROLLED STUDY; CYTOTOXICITY; DNA METHYLATION; ELECTROSPRAY MASS SPECTROMETRY; EPIGENETICS; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; IN VITRO STUDY; LIPID METABOLISM; LIQUID CHROMATOGRAPHY; LIVER CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY;

ACYL-COA OXIDASE; CELL LINE; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; ENVIRONMENTAL POLLUTANTS; ESTROGEN RECEPTOR ALPHA; FLUOROCARBONS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GLUTATHIONE S-TRANSFERASE PI; HEPATOCYTES; HUMANS; OCTANOIC ACIDS; PROMOTER REGIONS, GENETIC; RECEPTORS, PROGESTERONE; RNA, MESSENGER;

EID: 84859966195     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2012.03.003     Document Type: Article

References (57)

1. Aniagu S.O., Williams T.D., Chipman J.K. Changes in gene expression and assessment of DNA methylation in primary human hepatocytes and HepG2 cells exposed to environmental contaminants - hexabromocyclododecane and 17-β oestradiol. Toxicology 2009, 256:143-151.
2. Bauer M., Herbarth O., Aust G., Hengstler J.G., Dotzauer A., Graebsch C., Schmuecking E. Expression patterns and novel splicing variants of glutathione-S-transferase isoenzymes of human lung and hepatocyte cell lines. Cell Tissue Res. 2006, 324:423-432.
3. Biegel L.B., Hurtt M.E., Frame S.R., O'Connor J.C., Cook J.C. Mechanisms of extrahepatic tumor induction by peroxisome proliferators in male Cd rats. Toxicol. Sci. 2001, 60:44-55.
4. Brandeis M., Frank D., Keshet I., Siegfried Z., Mendelsohn M., Nemes A., Temper V., Razin A., Cedar H. Sp1 elements protect a CpG island from de novo methylation. Nature 1994, 371:435-438.
5. Corsini E., Avogadro A., Galbiati V., dell'Agli M., Marinovich M., Galli C.L., Germolec D.R. In vitro evaluation of the immunotoxic potential of perfluorinated compounds (PFCs). Toxicol. Appl. Pharmacol. 2010, 250:108-116.
6. Dewitt J.C., Copeland C.B., Strynar M.J., Luebke R.W. Perfluorooctanoic acid-induced immunomodulation in adult C57BL/6J or C57BL/6N female mice. Environ. Health Perspect. 2008, 116:644-650.
7. Esteller M., Corn P.G., Urena J.M., Cabrielson E., Baylin S.B., Herman J.G. Inactivation of glutathione-S-transferase P1 gene by promoter hypermethylation in human neoplasia. Cancer Res. 1998, 58:4515-4518.
8. Foley D.L., Craig J.M., Morley R., Olsson C.J., Dwyer T., Smith K., Saffery R. Prospects for epigenetic epidemiology. Am. J. Epidemiol. 2009, 169:389-400.
9. Friso S., Choi S.W., Dolnikowski G.G., Selhub J. A method to assess genomic DNA methylation using high-performance liquid chromatography/electrospray ionization mass spectrometry. Anal. Chem. 2002, 74:4526-4531.
10. Giesy J.P., Kannan K. Global distribution of perfluorooctane sulfonate in wildlife. Environ. Sci. Technol. 2001, 35:1339-1342.
11. Girault I., Tozlu S., Lidereau R., Bièche I. Expression analysis of DNA methyltransferases 1, 3A, 3B in sporadic breast carcinomas. Clin. Cancer Res. 2003, 9:4415-4422.
12. Guerrero-Preston R., Goldman L.R., Brebi-Mieville P., Lli-Gangas C., Lebron C., Witter F.R., Apelberg B.J., Hernández-Roystacher M., Jaffe A., Halden R.U., Sidransky D. Global DNA hyomethylation is associated with in utero exposure to cotinine and perfluorinated alkyl compounds. Epigenetics 2010, 5:539-546.
13. Guruge K.S., Yeung L.W., Yamanaka N., Miyazaki S., Lam P.K., Giesy J.P., Jones P.D., Yamashita N. Gene expression profiles in rat liver treated with perfluorooctanoic acid (PFOA). Toxicol. Sci. 2006, 89:93-107.
14. Hu J., Ma H., Zhang W., Yu Z., Sheng G., Fu J. Effects of benzene and its metabolites on global DNA methylation in human normal hepatic L02 cells. Environ. Toxicol. 2011, doi:10.1002/tox.20777.
15. Jones P.A., Baylin S.B. The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 2002, 3:415-428.
16. Karius T., Schnekenburger M., Ghelfi J., Walter J., Dicato M., Diederich M. Reversible epigenetic fingerprint-mediated glutathione-S-transferase P1 gene silencing in human leukemia cell lines. Biochem. Pharmacol. 2011, 81:1329-1342.
17. Kennedy G.L., Butenhoff J.L., Olsen G.W., O'Connor J.C., Seacat A.M., Perkins R.G., Biegel L.B., Murphy S.R., Farrar D.G. The toxicology of perfluorooctanoate. Crit. Rev. Toxicol. 2004, 34:351-384.
18. Key B.D., Howell R.D., Criddle C.S. Fluorinated organics in the biosphere. Environ. Sci. Technol. 1997, 31:2445-2454.
19. Kim K.Y., Kim D.S., Lee S.K., Lee I.K., Kang J.H., Chang Y.S., Jacobs D.R., Steffes M., Lee D.H. Association of low-dose exposure to persistent organic pollutants with global DNA hypomethylation in healthy Koreans. Environ. Health Perspect. 2010, 118:370-374.
20. Koch H.M., Preuss R., Angerer J. Di (2-ethylhexyl) phthalate (DEHP): human metabolism and internal exposure - an update and latest results. Int. J. Androl. 2006, 29:155-165.
21. Kovalenko V.M., Bagnyukova T.V., Sergienko O.V., Bondarenko L.B., Shayakhmetova G.M., Matvienko A.V., Pogribny I.P. Epigenetic changes in the rat livers induced by pyrazinamide treatment. Toxicol. Appl. Pharmacol. 2007, 225:293-299.
22. Krøvel A.V., Søfteland L., Torstensen B., Olsvik P.A. Transcriptional effects of PFOS in isolated hepatocytes from Atlantic salmon Salmo salar L. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2008, 148:14-22.
23. Kumaki Y., Oda M., Okano M. Quantification tool for methylation analysis. Nucleic Acids Res. 2008, 36:170-175.
24. Lau C., Anitole K., Hodes C., Lai D., Pfahles-Hutchens A., Seed J. Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicol. Sci. 2007, 99:366-394.
25. Lee Y.W., Broday L., Costa M. Effects of nickel on DNA methyltransferase activity and genomic DNA methylation levels. Mutat. Res. 1998, 415:213-218.
26. Lee D.H., Jacobs D.J., Porta M. Hypothesis: a unifying mechanism for nutrition and chemicals as lifelong modulators of DNA hypomethylation. Environ. Health Perspect. 2009, 117:1799-1802.
27. Li C., Xu M., Wang S., Yang X., Zhou S., Zhang J., Liu Q., Sun Y. Lead exposure suppressed ALAD transcription by increasing methylation level of promoter CpG islands. Toxicol. Lett. 2011, 203:48-53.
28. Liu C., Yu K., Shi X., Wang J., Lam P.K., Wu R.S., Zhou B. Induction of oxidative stress and apoptosis by PFOS and PFOA in primary cultured hepatocytes of freshwater tilapia (Oreochromis niloticus). Aquat. Toxicol. 2007, 82:135-143.
29. Liu Z., Maekawa M., Horii T., Morita M. The multiple promoter methylation profile of PR gene and ERα gene in tumor cell lines. Life Sci. 2003, 73:1963-1972.
30. Llabjani V., Jones K.C., Thomas G.O., Walker L.A., Shore R.F., Martin F.L. Polybrominated diphenyl ether-associated alterations in cell biochemistry as determined by attenuated total reflection Fourier-transform infrared spectroscopy: a comparison with DNA-reactive and/or endocrine-disrupting agents. Environ. Sci. Technol. 2009, 43:3356-3364.
31. Llabjani V., Trevisan J., Jones K.C., Shore R.F., Martin F.L. Binary mixture effects of PBDE congeners (47, 153, 183, or 209) and PCB congeners (126 or 153) in MCF-7 cells: biochemical alterations assessed by IR spectroscopy and multivariate analysis. Environ. Sci. Technol. 2010, 44:3992-3998.
32. Minami R., Muta K., Umemura T., Motomura S., Abe Y., Nishimura J., Nawata H. p16 (INK4a) induces differentiation and apoptosis in erythroid lineage cells. Exp. Hematol. 2003, 31:355-362.
33. Moffat G.J., McLaren A.W., Wolf C.R. Sp1-mediated transcriptional activation of the human Pi class glutathione S-transferase promoter. J. Biol. Chem. 1996, 271:1054-1060.
34. Murai Y., Hayashi S., Takahashi H., Tsuneyama K., Takano Y. Correlation between DNA alterations and p53 and p16 protein expression in cancer cell lines. Pathol. Res. Pract. 2005, 201:109-115.
35. Nakayama M., Gonzalgo M.L., Yegnasubramanian S., Lin X., De Marzo A.M., Nelson W.G. GSTP1 CpG island hypermethylation as a molecular biomarker for prostate cancer. J. Cell. Biochem. 2004, 91:540-552.
36. Nelson J.W., Hatch E.E., Webster T.F. Exposure to polyfluoroalkyl chemicals and cholesterol, body weight, and insulin resistance in the general U.S. population. Environ. Health Perspect. 2010, 118:197-202.
37. Olsen G.W., Hansen K.J., Stevenson L.A., Burris J.M., Mandel J.H. Human donor liver and serum concentrations of perfluorooctanesulfonate and other perfluorochemicals. Environ. Sci. Technol. 2003, 37:888-891.
38. Pathak S., Kedia-Mokashi N., Saxena M., D'Souza R., Maitra R., Parte A., Gill-Sharma P., Balasinor M.N. Effect of tamoxifen treatment on global and insulin-like growth factor 2-H19 locus-specific DNA methylation in rat spermatozoa and its association with embryo loss. Fertil. Steril. 2009, 91:2253-2263.
39. Rosen M.B., Thibodeaux J.R., Wood C.R., Zehr R.D., Schmida J.E., Lau C. Gene expression profiling in the lung and liver of PFOA-exposed mouse fetuses. Toxicology 2007, 239:15-33.
40. Rusiecki J.A., Baccarelli A., Bollati V., Tarantini L., Moore L.E., Bonefeld-Jorgensen E.C. Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic Inuit. Environ. Health Perspect. 2008, 116:1547-1552.
41. Seacat A.M., Thomford P.J., Hansen K.J., Olsen G.W., Case M.T., Butenhoff J.L. Subchronic toxicity studies on perfluoroctanesulfonate potassium salt in cynomolgus monkeys. Toxicol. Sci. 2002, 68:249-264.
42. Shi D.Y., Xie F.Z., Zhai C., Stern J.S., Liu Y., Liu S.L. The role of cellular oxidative stress in regulating glycolysis energy metabolism in hepatoma cells. Mol. Cancer 2009, 8:32.
43. Shi X., Du Y., Lam P.K., Wu R.S., Zhou B. Development toxicity and alteration of gene expression in zebrafish embryos expose to PFOS. Toxicol. Appl. Pharmacol. 2008, 230:23-32.
44. Slotkin T.A., MacKillop E.A., Melnick R.L., Thayer K.A., Seidler F.J. Development neurotoxicity of perfluorinated chemicals modeled in vitro. Environ. Health Perspect. 2008, 116:716-722.
45. Smithwick M., Muir D.C., Mabury S.A., Solomon K.R., Martin J.W., Sonne C., Born E.W., Letcher R.J., Dietz R. Perflouroalkyl contaminants in liver tissue from East Greenland polar bears (Ursus maritimus). Environ. Toxicol. Chem. 2005, 24:981-986.
46. So M.K., Yamashita N., Taniyasu S., Jiang Q., Giesy J.P., Chen K., Lam P.K. Health risks in infants associated with exposure to perfluorinated compounds in human breast milk from Zhoushan, China. Environ. Sci. Technol. 2006, 40:2924-2929.
47. Steenland K., Fletcher T., Savitz D.A. Epidemiologic evidence on the health effects of perfluorooctanoic acid (PFOA). Environ. Health Perspect. 2010, 118:1100-1108.
48. Takiguchi M., Achanzar W.E., Qu W., Li G., Waalkes M.P. Effects of cadmium on DNA-(cytosine-5) methyltransferase activity and DNA methylation status during cadmium-induced cellular transformation. Exp. Cell Res. 2003, 286:353-365.
49. U.S.EPA (Environmental Protection Agency) Scientific Advisory Board's Response to EPA's Draft Risk Assessment 2006, (letter).
50. Wan Y.J., Li Y.Y., Xia W., Chen J., Lv Z.Q., Zeng H.C., Zhang L., Yang W.J., Chen T., Lin Y., Wei J., Xu S.Q. Alterations in tumor biomarker GSTP gene methylation patterns induced by prenatal exposure to PFOS. Toxicology 2010, 274:57-64.
51. Watson R.E., McKim J.M., Cockerell G.L., Goodman J.I. The value of DNA methylation analysis in basic initial toxicity assessments. Toxicol. Sci. 2004, 79:178-188.
52. Xie Y., Liu J., Benbrahim-Tallaa L., Ward J.M., Logsdon D., Diwan B.A., Waalkes M.P. Aberrant DNA methylation and gene expression in livers of newborn mice transplacentally exposed to a hepatocarcinogenic dose of inorganic arsenic. Toxicology 2007, 236:7-15.
53. Yeung L.W., Guruge K.S., Yamanaka N., Miyazaki S., Lam P.K. Differential expression of chicken hepatic genes responsive to PFOA and PFOS. Toxicology 2007, 237:111-125.
54. Zhang D., Ai D., Tanaka H., Hammock B.D., Zhu Y. DNA methylation of the promoter of soluble epoxide hydrolase silences its expression by an SP-1-dependent mechanism. Biochim. Biophys. Acta 2010, 1799:659-667.
55. Zhang H., Rosdahl I. Expression profiles of Id1 and p16 proteins in all-trans-retinoic acid-induced apoptosis and cell cycle re-distribution in melanoma. Cancer Lett. 2005, 217:33-41.
56. Zhong S., Tang M.W., Yeo W., Liu C., Lo Y.M., Johnson P.J. Silencing of GSTP1 gene by CpG island DNA hypermethylation in HBV-associated hepatocellular carcinomas. Clin. Cancer Res. 2002, 8:1087-1092.
57. Zhang W., Liu Y., Zhang H., Dai J. Proteomic analysis of male zebrafish livers chronically exposed to perfluorononanoic acid. Environ. Int. 2011, 10.1016/j.envint.2011.03.002.