DOI QR코드

DOI QR Code

Influence of Toxicologically Relevant Metals on Human Epigenetic Regulation

  • Ryu, Hyun-Wook (College of Pharmacy, Yonsei Institute of Pharmaceutical Sciences, Yonsei University) ;
  • Lee, Dong Hoon (College of Pharmacy, Yonsei Institute of Pharmaceutical Sciences, Yonsei University) ;
  • Won, Hye-Rim (College of Pharmacy, Yonsei Institute of Pharmaceutical Sciences, Yonsei University) ;
  • Kim, Kyeong Hwan (College of Pharmacy, Yonsei Institute of Pharmaceutical Sciences, Yonsei University) ;
  • Seong, Yun Jeong (College of Pharmacy, Yonsei Institute of Pharmaceutical Sciences, Yonsei University) ;
  • Kwon, So Hee (College of Pharmacy, Yonsei Institute of Pharmaceutical Sciences, Yonsei University)
  • Received : 2015.02.23
  • Accepted : 2015.03.13
  • Published : 2015.03.31

Abstract

Environmental toxicants such as toxic metals can alter epigenetic regulatory features such as DNA methylation, histone modification, and non-coding RNA expression. Heavy metals influence gene expression by epigenetic mechanisms and by directly binding to various metal response elements in the target gene promoters. Given the role of epigenetic alterations in regulating genes, there is potential for the integration of toxic metal-induced epigenetic alterations as informative factors in the risk assessment process. Here, we focus on recent advances in understanding epigenetic changes, gene expression, and biological effects induced by toxic metals.

Keywords

References

  1. Baccarelli, A. and Bollati, V. (2009) Epigenetics and environmental chemicals. Curr. Opin. Pediatr., 21, 243-251. https://doi.org/10.1097/MOP.0b013e32832925cc
  2. Koturbash, I., Beland, F.A. and Pogribny, I.P. (2011) Role of epigenetic events in chemical carcinogenesis--a justification for incorporating epigenetic evaluations in cancer risk assessment. Toxicol. Mech. Methods, 21, 289-297. https://doi.org/10.3109/15376516.2011.557881
  3. Bird, A. (2002) DNA methylation patterns and epigenetic memory. Genes Dev., 16, 6-21. https://doi.org/10.1101/gad.947102
  4. Heyn, H. and Esteller, M. (2012) DNA methylation profiling in the clinic: applications and challenges. Nat. Rev. Genet., 13, 679-692. https://doi.org/10.1038/nrg3270
  5. De Carvalho, D.D., You, J.S. and Jones, P.A. (2010) DNA methylation and cellular reprogramming. Trends Cell Biol., 20, 609-617. https://doi.org/10.1016/j.tcb.2010.08.003
  6. Suganuma, T. and Workman, J.L. (2011) Signals and combinatorial functions of histone modifications. Annu. Rev. Biochem., 80, 473-499. https://doi.org/10.1146/annurev-biochem-061809-175347
  7. Hon, G.C., Hawkins, R.D. and Ren, B. (2009) Predictive chromatin signatures in the mammalian genome. Hum. Mol. Genet., 18, R195-201. https://doi.org/10.1093/hmg/ddp409
  8. Hawkins, R.D., Hon, G.C., Lee, L.K., Ngo, Q., Lister, R., Pelizzola, M., Edsall, L.E., Kuan, S., Luu, Y., Klugman, S., Antosiewicz-Bourget, J., Ye, Z., Espinoza, C., Agarwahl, S., Shen, L., Ruotti, V., Wang, W., Stewart, R., Thomson, J.A., Ecker, J.R. and Ren, B. (2010) Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell, 6, 479-491. https://doi.org/10.1016/j.stem.2010.03.018
  9. Heyn, H., Carmona, F.J., Gomez, A., Ferreira, H.J., Bell, J.T., Sayols, S., Ward, K., Stefansson, O.A., Moran, S., Sandoval, J., Eyfjord, J.E., Spector, T.D. and Esteller, M. (2013) DNA methylation profiling in breast cancer discordant identical twins identifies DOK7 as novel epigenetic biomarker. Carcinogenesis, 34, 102-108. https://doi.org/10.1093/carcin/bgs321
  10. Choudhuri, S., Cui, Y. and Klaassen, C.D. (2010) Molecular targets of epigenetic regulation and effectors of environmental influences. Toxicol. Appl. Pharmacol., 245, 378-393. https://doi.org/10.1016/j.taap.2010.03.022
  11. Kozomara, A. and Griffiths-Jones, S. (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res., 39, D152-157. https://doi.org/10.1093/nar/gkq1027
  12. Mendell, J.T. and Olson, E.N. (2012) MicroRNAs in stress signaling and human disease. Cell, 148, 1172-1187. https://doi.org/10.1016/j.cell.2012.02.005
  13. Cheng, T.F., Choudhuri, S. and Muldoon-Jacobs, K. (2012) Epigenetic targets of some toxicologically relevant metals: a review of the literature. J. Appl. Toxicol., 32, 643-653. https://doi.org/10.1002/jat.2717
  14. Sengupta, S., McArthur, J.M., Sarkar, A., Leng, M.J., Ravenscroft, P., Howarth, R.J. and Banerjee, D.M. (2008) Do ponds cause arsenic-pollution of groundwater in the Bengal basin? An answer from West Bengal. Environ. Sci. Technol., 42, 5156-5164. https://doi.org/10.1021/es702988m
  15. Zhong, C.X. and Mass, M.J. (2001) Both hypomethylation and hypermethylation of DNA associated with arsenite exposure in cultures of human cells identified by methylation-sensitive arbitrarily-primed PCR. Toxicol. Lett., 122, 223-234. https://doi.org/10.1016/S0378-4274(01)00365-4
  16. Salnikow, K. and Zhitkovich, A. (2008) Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: nickel, arsenic, and chromium. Chem. Res. Toxicol., 21, 28-44. https://doi.org/10.1021/tx700198a
  17. Zhou, J., Ye, J., Zhao, X., Li, A. and Zhou, J. (2008) JWA is required for arsenic trioxide induced apoptosis in HeLa and MCF-7 cells via reactive oxygen species and mitochondria linked signal pathway. Toxicol. Appl. Pharmacol., 230, 33-40. https://doi.org/10.1016/j.taap.2008.01.041
  18. Zhou, L. Hou, J., Fu, W., Wang, D., Yuan, Z. and Jiang, H. (2008) Arsenic trioxide and 2-methoxyestradiol reduce betacatenin accumulation after proteasome inhibition and enhance the sensitivity of myeloma cells to Bortezomib. Leuk. Res., 32, 1674-1683. https://doi.org/10.1016/j.leukres.2008.03.039
  19. Benton, M.A., Rager, J.E., Smeester, L. and Fry, R.C. (2011) Comparative genomic analyses identify common molecular pathways modulated upon exposure to low doses of arsenic and cadmium. BMC Genomics, 12, 173. https://doi.org/10.1186/1471-2164-12-173
  20. Chervona, Y. Hall, M.N., Arita, A., Wu, F., Sun, H., Tseng, H.C., Ali, E., Uddin, M.N., Liu, X., Zoroddu, M.A., Gamble, M.V. and Costa, M. (2012) Associations between arsenic exposure and global posttranslational histone modifications among adults in Bangladesh. Cancer Epidemiol. Biomarkers Prev., 21, 2252-2260. https://doi.org/10.1158/1055-9965.EPI-12-0833
  21. Cantone, L. Nordio, F., Hou, L., Apostoli, P., Bonzin, M., Tarantini, L., Angelici, L., Bollati, V., Zanobetti, A., Schwartz, J., Bertazzi, P.A. and Baccarelli, A. (2011) Inhalable metalrich air particles and histone H3K4 dimethylation and H3K9 acetylation in a cross-sectional study of steel workers. Environ. Health Perspect., 119, 964-969. https://doi.org/10.1289/ehp.1002955
  22. Li, J., Gorospe, M., Barnes, J. and Liu, Y. (2003) Tumor promoter arsenite stimulates histone H3 phosphoacetylation of proto-oncogenes c-fos and c-jun chromatin in human diploid fibroblasts. J. Biol. Chem., 278, 13183-13191. https://doi.org/10.1074/jbc.M300269200
  23. Huang, B.W., Ray, P.D., Iwasaki, K. and Tsuji, Y. (2013) Transcriptional regulation of the human ferritin gene by coordinated regulation of Nrf2 and protein arginine methyltransferases PRMT1 and PRMT4. FASEB J., 27, 3763-3774. https://doi.org/10.1096/fj.12-226043
  24. Ramirez, T., Brocher, J., Stopper, H. and Hock, R. (2008) Sodium arsenite modulates histone acetylation, histone deacetylase activity and HMGN protein dynamics in human cells. Chromosoma, 117, 147-157. https://doi.org/10.1007/s00412-007-0133-5
  25. Zhou, X., Sun, H., Ellen, T.P., Chen, H. and Costa, M. (2008) Arsenite alters global histone H3 methylation. Carcinogenesis, 29, 1831-1836. https://doi.org/10.1093/carcin/bgn063
  26. Marsit, C.J., Eddy, K. and Kelsey, K.T. (2006) MicroRNA responses to cellular stress. Cancer Res., 66, 10843-10848. https://doi.org/10.1158/0008-5472.CAN-06-1894
  27. Wang, Z., Zhao, Y., Smith, E., Goodall, G.J., Drew, P.A., Brabletz, T. and Yang, C. (2011) Reversal and prevention of arsenic-induced human bronchial epithelial cell malignant transformation by microRNA-200b. Toxicol. Sci., 121, 110-122. https://doi.org/10.1093/toxsci/kfr029
  28. Tellez-Plaza, M., Navas-Acien, A., Menke, A., Crainiceanu, C.M., Pastor-Barriuso, R. and Guallar, E. (2012) Cadmium exposure and all-cause and cardiovascular mortality in the U.S. general population. Environ. Health Perspect., 120, 1017-1022. https://doi.org/10.1289/ehp.1104352
  29. Jarup, L. and Akesson, A. (2009) Current status of cadmium as an environmental health problem. Toxicol. Appl. Pharmacol., 238, 201-208. https://doi.org/10.1016/j.taap.2009.04.020
  30. Takiguchi, M., Achanzar, W.E., Qu, W., Li, G. and Waalkes, M.P. (2003) Effects of cadmium on DNA-(Cytosine-5) methyltransferase activity and DNA methylation status during cadmium-induced cellular transformation. Exp. Cell Res., 286, 355-365. https://doi.org/10.1016/S0014-4827(03)00062-4
  31. Benbrahim-Tallaa, L., Waterland, R.A., Dill, A.L., Webber, M.M. and Waalkes, M.P. (2007) Tumor suppressor gene inactivation during cadmium-induced malignant transformation of human prostate cells correlates with overexpression of de novo DNA methyltransferase. Environ. Health Perspect., 115, 1454-1459.
  32. Somji, S., Garrett, S.H., Toni, C., Zhou, X.D., Zheng, Y., Ajjimaporn, A., Sens, M.A. and Sens, D.A. (2011) Differences in the epigenetic regulation of MT-3 gene expression between parental and Cd+2 or As+3 transformed human urothelial cells. Cancer Cell Int., 11, 2. https://doi.org/10.1186/1475-2867-11-2
  33. Barcia-Sanjurjo, I., Vazquez-Cedeira, M., Barcia, R. and Lazo, P.A. (2013) Sensitivity of the kinase activity of human vaccinia-related kinase proteins to toxic metals. J. Biol. Inorg. Chem., 18, 473-482. https://doi.org/10.1007/s00775-013-0992-6
  34. Hassan, F., Nuovo, G.J., Crawford, M., Boyaka, P.N., Kirkby, S., Nana-Sinkam, S.P. and Cormet-Boyaka, E. (2012) MiR-101 and miR-144 regulate the expression of the CFTR chloride channel in the lung. PloS One, 7, e50837. https://doi.org/10.1371/journal.pone.0050837
  35. Langavdrd, 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. https://doi.org/10.1002/ajim.4700170205
  36. Nickens, K.P., Patierno, S.R. and Ceryak, S. (2010) Chromium genotoxicity: A double-edged sword. Chem. Biol. Interact., 188, 276-288. https://doi.org/10.1016/j.cbi.2010.04.018
  37. Shi, X., Mao, Y., Knapton, A.D., Ding, M., Rojanasakul, Y., Gannett, P.M., Dalal, N. and Liu, K. (1994) Reaction of Cr(VI) with ascorbate and hydrogen peroxide generates hydroxyl radicals and causes DNA damage: role of a Cr(IV)-mediated Fenton-like reaction. Carcinogenesis, 15, 2475-2478. https://doi.org/10.1093/carcin/15.11.2475
  38. Zhitkovich, A. (2005) Importance of chromium-DNA adducts in mutagenicity and toxicity of chromium(VI). Chem. Res. Toxicol., 18, 3-11. https://doi.org/10.1021/tx049774+
  39. Kondo, K., Takahashi, Y., Hirose, Y., Nagao, T., Tsuyuguchi, M., Hashimoto, M., Ochiai, A., Monden, Y. and Tangoku, A. (2006) The reduced expression and aberrant methylation of p16(INK4a) in chromate workers with lung cancer. Lung Cancer, 53, 295-302. https://doi.org/10.1016/j.lungcan.2006.05.022
  40. Ali, A.H., Kondo, K., Namura, T., Senba, Y., Takizawa, H., Nakagawa, Y., Toba, H., Kenzaki, K., Sakiyama, S. and Tangoku, A. (2011) Aberrant DNA methylation of some tumor suppressor genes in lung cancers from workers with chromate exposure. Mol. Carcinog., 50, 89-99. https://doi.org/10.1002/mc.20697
  41. Schnekenburger, M., Peng, L. and Puga, A. (2007) HDAC1 bound to the Cyp1a1 promoter blocks histone acetylation associated with Ah receptor-mediated trans-activation. Biochim. Biophys. Acta, 1769, 569-578. https://doi.org/10.1016/j.bbaexp.2007.07.002
  42. Schnekenburger, M., Talaska, G. and Puga, A. (2007) Chromium cross-links histone deacetylase 1-DNA methyltransferase 1 complexes to chromatin, inhibiting histone-remodeling marks critical for transcriptional activation. Mol. Cell. Biol., 27, 7089-7101. https://doi.org/10.1128/MCB.00838-07
  43. Levina, A., Harris, H.H. and Lay, P.A. (2006) Binding of chromium(VI) to histones: implications for chromium(VI)-induced genotoxicity. J. Biol. Inorg. Chem., 11, 225-234. https://doi.org/10.1007/s00775-005-0068-3
  44. Fan, J., Sun, Y., Wang, J. and Fan, M. (2009) An organicreagent-free method for determination of chromium(VI) in steel alloys, sewage sludge and wastewater. Anal. Chim. Acta, 640, 58-62. https://doi.org/10.1016/j.aca.2009.03.007
  45. Bollati, V., Marinelli, B., Apostoli, P., Bonzini, M., Nordio, F., Hoxha, M., Pegoraro, V., Motta, V., Tarantini, L., Cantone, L., Schwartz, J., Bertazzi, P.A. and Baccarelli, A. (2010) Exposure to metal-rich particulate matter modifies the expression of candidate microRNAs in peripheral blood leukocytes. Environ. Health Perspect., 118, 763-768. https://doi.org/10.1289/ehp.0901300
  46. He, J., Qian, X., Carpenter, R., Xu, Q., Wang, L., Qi, Y., Wang, Z.X., Liu, L.Z. and Jiang, B.H. (2013) Repression of miR-143 mediates Cr (VI)-induced tumor angiogenesis via IGF-IR/IRS1/ERK/IL-8 pathway. Toxicol. Sci., 134, 26-38. https://doi.org/10.1093/toxsci/kft101
  47. Li, Y., Li, P., Yu, S., Zhang, J., Wang, T. and Jia, G. (2014) miR-3940-5p associated with genetic damage in workers exposed to hexavalent chromium. Toxicol. Lett., 229, 319-326. https://doi.org/10.1016/j.toxlet.2014.06.033
  48. De Olivera, J.V., Boufleur, L.A., Dos Santos, C.E., Dias, J.F., Squeff, C.H., Silva, G.R., Ianistcki, M., Benvegnu, V.C. and Da Silva, J. (2012) Occupational genotoxicity among copper smelters. Toxicol. Ind. Health, 28, 789-795. https://doi.org/10.1177/0748233711422735
  49. Kang, J., Lin, C., Chen, J. and Liu, Q. (2004) Copper induces histone hypoacetylation through directly inhibiting histone acetyltransferase activity. Chem. Biol. Interact., 148, 115-123. https://doi.org/10.1016/j.cbi.2004.05.003
  50. Zoroddu, M.A., Kowalik-Jankowska, T., Kozlowski, H., Molinari, H., Salnikow, K., Broday, L. and Costa, M. (2000) Interaction of Ni(II) and Cu(II) with a metal binding sequence of histone H4: AKRHRK, a model of the H4 tail. Biochim. Biophys. Acta, 1475, 163-168. https://doi.org/10.1016/S0304-4165(00)00066-0
  51. Karavelas, T., Mylonas, M., Malandrinos, G., Plakatouras, J.C., Hadjiliadis, N., Mlynarz, P. and Kozlowski, H. (2005) Coordination properties of Cu(II) and Ni(II) ions towards the C-terminal peptide fragment-ELAKHA-of histone H2B. J. Inorg. Biochem., 99, 606-615. https://doi.org/10.1016/j.jinorgbio.2004.11.012
  52. Zavitsanos, K., Nunes, A.M., Malandrinos, G. and Hadjiliadis, N. (2011) Copper effective binding with 32-62 and 94-125 peptide fragments of histone H2B. J. Inorg. Biochem., 105, 102-110. https://doi.org/10.1016/j.jinorgbio.2010.09.002
  53. Nunes, A.M., Zavitsanos, K., Malandrinos, G. and Hadjiliadis, N. (2010) Coordination of Cu(2+) and Ni(2+) with the histone model peptide of H2B N-terminal tail (1-31 residues):A spectroscopic study. Dalton Trans., 39, 4369-4381. https://doi.org/10.1039/b927157k
  54. Bonnet, E., Wuyts, J., Rouze, P. and Van de Peer, Y. (2004) Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes. Proc. Natl. Acad. Sci. U.S.A., 101, 11511-11516. https://doi.org/10.1073/pnas.0404025101
  55. Naya, L., Paul, S., Valdes-Lopez, O., Mendoza-Soto, A.B., Nova-Franco, B., Sosa-Valencia, G., Reyes, J.L. and Hernandez, G. (2014) Regulation of copper homeostasis and biotic interactions by microRNA 398b in common bean. PloS One, 9, e84416. https://doi.org/10.1371/journal.pone.0084416
  56. Kasuba, V., Rozgaj, R., Milic, M., Zeljezic, D., Kopjar, N., Pizent, A. and Kljakovic-Gaspic, Z. (2010) Evaluation of lead exposure in battery-manufacturing workers with focus on different biomarkers. J. Appl. Toxicol., 30, 321-328.
  57. Wu, J., Basha, M.R., Brock, B., Cox, D.P., Cardozo-Pelaez, F., McPherson, C.A., Harry, J., Rice, D.C., Maloney, B., Chen, D., Lahiri, D.K. and Zawia, N.H. (2008) Alzheimer's disease (AD)-like pathology in aged monkeys after infantile exposure to environmental metal lead (Pb): evidence for a developmental origin and environmental link for AD. J. Neurosci., 28, 3-9. https://doi.org/10.1523/JNEUROSCI.4405-07.2008
  58. Bihaqi, S.W., Huang, H., Wu, J. and Zawia, N.H. (2011) Infant exposure to lead (Pb) and epigenetic modifications in the aging primate brain: implications for Alzheimer's disease. J. Alzheimers Dis., 27, 819-833.
  59. Wright, R.O., Schwartz, J., Wright, R.J., Bollati, V., Tarantini, L., Park, S.K., Hu, H., Sparrow, D., Vokonas, P. and Baccarelli, A. (2010) Biomarkers of lead exposure and DNA methylation within retrotransposons. Environ. Health Perspect., 118, 790-795. https://doi.org/10.1289/ehp.0901429
  60. le Sage, C., Nagel, R., Egan, D.A., Schrier, M., Mesman, E., Mangiola, A., Anile, C., Mercatelli, N., Ciafre, S.A., Farace, M.G. and Agami, R. (2007) Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J., 26, 3699-3708. https://doi.org/10.1038/sj.emboj.7601790
  61. Tchounwou, P.B., Ayensu, W.K., Ninashvili, N. and Sutton, D. (2003) Environmental exposure to mercury and its toxicopathologic implications for public health. Environ. Toxicol., 18, 149-175. https://doi.org/10.1002/tox.10116
  62. Spiegel, S.J. (2009) Occupational health, mercury exposure, and environmental justice: learning from experiences in Tanzania. Am. J. Public Health, 99 Suppl 3, S550-558.
  63. Grotto, D., Valentini, J., Fillion, M., Passos, C.J., Garcia, S.C., Mergler, D. and Barbosa, F. Jr. (2010) Mercury exposure and oxidative stress in communities of the Brazilian Amazon. Sci. Total Environ., 408, 806-811. https://doi.org/10.1016/j.scitotenv.2009.10.053
  64. Hanna, C.W., Bloom, M.S., Robinson, W.P., Kim, D., Parsons, P.J., vom Saal, F.S., Taylor, J.A., Steuerwald, A.J. and Fujimoto, V.Y. (2012) DNA methylation changes in whole blood is associated with exposure to the environmental contaminants, mercury, lead, cadmium and bisphenol A, in women undergoing ovarian stimulation for IVF. Hum. Reprod., 27, 1401-1410. https://doi.org/10.1093/humrep/des038
  65. Goodrich, J.M., Basu, N., Franzblau, A. and Dolinoy, D.C. (2013) Mercury biomarkers and DNA methylation among Michigan dental professionals. Environ. Mol. Mutagen., 54, 195-203. https://doi.org/10.1002/em.21763
  66. Onishchenko, N., Karpova, N., Sabri, F., Castren, E. and Ceccatelli, S. (2008) Long-lasting depression-like behavior and epigenetic changes of BDNF gene expression induced by perinatal exposure to methylmercury. J. Neurochem., 106, 1378-1387. https://doi.org/10.1111/j.1471-4159.2008.05484.x
  67. Pallocca, G., Fabbri, M., Sacco, M.G., Gribaldo, L., Pamies, D., Laurenza, I. and Bal-Price, A. (2013) miRNA expression profiling in a human stem cell-based model as a tool for developmental neurotoxicity testing. Cell Biol. Toxicol., 29, 239-257. https://doi.org/10.1007/s10565-013-9250-5
  68. Sutherland, J.E. and Costa, M. (2003) Epigenetics and the environment. Ann. N. Y. Acad. Sci., 983, 151-160. https://doi.org/10.1111/j.1749-6632.2003.tb05970.x
  69. Arita, A. and Costa, M. (2009) Epigenetics in metal carcinogenesis: nickel, arsenic, chromium and cadmium. Metallomics, 1, 222-228. https://doi.org/10.1039/b903049b
  70. Ellen, T.P., Kluz, T., Harder, M.E., Xiong, J. and Costa, M. (2009) Heterochromatinization as a potential mechanism of nickel-induced carcinogenesis. Biochemistry, 48, 4626-4632. https://doi.org/10.1021/bi900246h
  71. Govindarajan, B., Klafter, R., Miller, M.S., Mansur, C., Mizesko, M., Bai, X., LaMontagne, K. Jr. and Arbiser, J.L. (2002) Reactive oxygen-induced carcinogenesis causes hypermethylation of p16(Ink4a) and activation of MAP kinase. Mol. Med., 8, 1-8. https://doi.org/10.1007/s00894-001-0054-9
  72. Kowara, R., Salnikow, K., Diwan, B.A., Bare, R.M., Waalkes, M.O. and Kasprzak, K.S. (2004) Reduced Fhit protein expression in nickel-transformed mouse cells and in nickelinduced murine sarcomas. Mol. Cell. Biochem., 255, 195-202. https://doi.org/10.1023/B:MCBI.0000007275.22785.91
  73. Ji, W., Yang, L., Yu, L., Yuan, J., Hu, D., Zhang, W., Yang, J., Pang, Y., Li, W., Lu, J., Fu, J., Chen, J., Lin, Z., Chen, W. and Zhuang, Z. (2008) Epigenetic silencing of O6-methylguanine DNA methyltransferase gene in NiS-transformed cells. Carcinogenesis, 29, 1267-1275. https://doi.org/10.1093/carcin/bgn012
  74. Chen, H., Ke, Q., Kluz, T., Yan, Y. and Costa, M. (2006) Nickel ions increase histone H3 lysine 9 dimethylation and induce transgene silencing. Mol. Cell. Biol., 26, 3728-3737. https://doi.org/10.1128/MCB.26.10.3728-3737.2006
  75. Chen, X., Fan, Y., Long, X. and Sun, X. (2010) Similar DNA methylation and histone H3 lysine 9 dimethylation patterns in tripronuclear and corrected bipronuclear human zygotes. J. Reprod. Dev., 56, 324-329. https://doi.org/10.1262/jrd.09-170A
  76. Ke, Q., Ellen, T.P. and Costa, M. (2008) Nickel compounds induce histone ubiquitination by inhibiting histone deubiquitinating enzyme activity. Toxicol. Appl. Pharmacol., 228, 190-199. https://doi.org/10.1016/j.taap.2007.12.015
  77. Ke, Q., Li, Q., Ellen, T.P., Sun, H. and Costa, M. (2008) Nickel compounds induce phosphorylation of histone H3 at serine 10 by activating JNK-MAPK pathway. Carcinogenesis, 29, 1276-1281. https://doi.org/10.1093/carcin/bgn084
  78. Karaczyn, A.A., Bal, W., North, S.L., Bare, R.M., Hoang, V.M., Fisher, R.J. and Kasprzak, K.S. (2003) The octapeptidic end of the C-terminal tail of histone H2A is cleaved off in cells exposed to carcinogenic nickel(II). Chem. Res. Toxicol., 16, 1555-1559. https://doi.org/10.1021/tx0300277
  79. Karaczyn, A.A., Golebiowski, F. and Kasprzak, K.S. (2005) Truncation, deamidation, and oxidation of histone H2B in cells cultured with nickel(II). Chem. Res. Toxicol., 18, 1934-1942. https://doi.org/10.1021/tx050122a
  80. Zhang, J., Zhou, Y., Ma, L., Huang, S., Wang, R., Gao, R., Wu, Y., Shi, H. and Zhang, J. (2013) The alteration of miR-222 and its target genes in nickel-induced tumor. Biol. Trace Elem. Res., 152, 267-274. https://doi.org/10.1007/s12011-013-9619-6
  81. Boyer, I.J. (1989) Toxicity of dibutyltin, tributyltin and other organotin compounds to humans and to experimental animals. Toxicology, 55, 253-298. https://doi.org/10.1016/0300-483X(89)90018-8
  82. Osada, S., Nishikawa, J., Nakanishi, T., Tanaka, K. and Nishihara, T. (2005) Some organotin compounds enhance histone acetyltransferase activity. Toxicol. Lett., 155, 329-335. https://doi.org/10.1016/j.toxlet.2004.10.009
  83. Wang, Y., Wang, C., Zhang, J., Chen, Y. and Zuo, Z. (2009) DNA hypomethylation induced by tributyltin, triphenyltin, and a mixture of these in Sebastiscus marmoratus liver. Aquat. Toxicol., 95, 93-98. https://doi.org/10.1016/j.aquatox.2009.06.008
  84. Fragou, D., Fragou, A., Kouidou, S., Njau, S. and Kovatsi, L. (2011) Epigenetic mechanisms in metal toxicity. Toxicol. Mech. Methods, 21, 343-352. https://doi.org/10.3109/15376516.2011.557878
  85. Coppin, J.F., Qu, W. and Waalkes, M.P. (2008) Interplay between cellular methyl metabolism and adaptive efflux during oncogenic transformation from chronic arsenic exposure in human cells. J. Biol. Chem., 283, 19342-19350. https://doi.org/10.1074/jbc.M802942200
  86. Franco, R., Schoneveld, O., Georgakilas, A.G. and Panayiotidis, M.I. (2008) Oxidative stress, DNA methylation and carcinogenesis. Cancer Lett., 266, 6-11. https://doi.org/10.1016/j.canlet.2008.02.026

Cited by

  1. Titanium and Zirconium Levels Are Associated with Changes in MicroRNAs Expression: Results from a Human Cross-Sectional Study on Obese Population vol.11, pp.9, 2016, https://doi.org/10.1371/journal.pone.0161916
  2. Cadmium Exposure and Potential Health Risk from Foods in Contaminated Area, Thailand vol.32, pp.1, 2016, https://doi.org/10.5487/TR.2016.32.1.065
  3. “He Beat You in the Blood”: Knowledge and Beliefs About the Transmission of Traits Among Latinos from Mexico and Central America vol.19, pp.1, 2017, https://doi.org/10.1007/s10903-015-0311-0
  4. Determination of total arsenic content and arsenic speciation in different types of rice vol.26, pp.1, 2017, https://doi.org/10.1007/s10068-017-0039-9
  5. Detection of Toxic Heavy Metal, Co(II) Trace via Voltammetry with Semiconductor Microelectrodes vol.33, pp.2, 2017, https://doi.org/10.5487/TR.2017.33.2.135
  6. Chelation of Thallium (III) in Rats Using Combined Deferasirox and Deferiprone Therapy vol.33, pp.4, 2017, https://doi.org/10.5487/TR.2017.33.4.299
  7. Systematic Investigation of the Reduction of Inorganic Arsenic and Bioactive Nutrients in Rice with Various Cooking Techniques vol.80, pp.11, 2017, https://doi.org/10.4315/0362-028X.JFP-17-095
  8. Epigenetics and Its Clinical Applications vol.21, pp.6, 2015, https://doi.org/10.1089/act.2015.29027.sho
  9. An Assessment of Dietary Exposure to Cadmium in Residents of Guangzhou, China vol.15, pp.3, 2018, https://doi.org/10.3390/ijerph15030556
  10. Seed priming with Se mitigates As-induced phytotoxicity in rice seedlings by enhancing essential micronutrient uptake and translocation and reducing As translocation vol.25, pp.27, 2018, https://doi.org/10.1007/s11356-018-2711-x