DNA methylation alterations in response to pesticide exposure in vitro
Although pesticides are subject to extensive carcinogenicity testing before regulatory approval, pesticide exposure has repeatedly been associated with various cancers. This suggests that pesticides may cause cancer via nonmutagenicity mechanisms. The present study provides evidence to support the h...
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Published in | Environmental and molecular mutagenesis Vol. 53; no. 7; pp. 542 - 549 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
Hoboken
Wiley Subscription Services, Inc., A Wiley Company
01.08.2012
Wiley-Liss |
Subjects | |
Online Access | Get full text |
ISSN | 0893-6692 1098-2280 1098-2280 |
DOI | 10.1002/em.21718 |
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Abstract | Although pesticides are subject to extensive carcinogenicity testing before regulatory approval, pesticide exposure has repeatedly been associated with various cancers. This suggests that pesticides may cause cancer via nonmutagenicity mechanisms. The present study provides evidence to support the hypothesis that pesticide‐induced cancer may be mediated in part by epigenetic mechanisms. We examined whether exposure to seven commonly used pesticides (i.e., fonofos, parathion, terbufos, chlorpyrifos, diazinon, malathion, and phorate) induces DNA methylation alterations in vitro. We conducted genome‐wide DNA methylation analyses on DNA samples obtained from the human hematopoietic K562 cell line exposed to ethanol (control) and several organophosphate pesticides (OPs) using the Illumina Infinium HumanMethylation27 BeadChip. Bayesian‐adjusted t‐tests were used to identify differentially methylated gene promoter CpG sites. In this report, we present our results on three pesticides (fonofos, parathion, and terbufos) that clustered together based on principle component analysis and hierarchical clustering. These three pesticides induced similar methylation changes in the promoter regions of 712 genes, while also exhibiting their own OP‐specific methylation alterations. Functional analysis of methylation changes specific to each OP, or common to all three OPs, revealed that differential methylation was associated with numerous genes that are involved in carcinogenesis‐related processes. Our results provide experimental evidence that pesticides may modify gene promoter DNA methylation levels, suggesting that epigenetic mechanisms may contribute to pesticide‐induced carcinogenesis. Further studies in other cell types and human samples are required, as well as determining the impact of these methylation changes on gene expression. Environ. Mol. Mutagen. 2012. © 2012 Wiley Periodicals, Inc. |
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AbstractList | Although pesticides are subject to extensive carcinogenicity testing before regulatory approval, pesticide exposure has repeatedly been associated with various cancers. This suggests that pesticides may cause cancer via nonmutagenicity mechanisms. The present study provides evidence to support the hypothesis that pesticide‐induced cancer may be mediated in part by epigenetic mechanisms. We examined whether exposure to seven commonly used pesticides (i.e., fonofos, parathion, terbufos, chlorpyrifos, diazinon, malathion, and phorate) induces DNA methylation alterations
in vitro.
We conducted genome‐wide DNA methylation analyses on DNA samples obtained from the human hematopoietic K562 cell line exposed to ethanol (control) and several organophosphate pesticides (OPs) using the Illumina Infinium HumanMethylation27 BeadChip. Bayesian‐adjusted t‐tests were used to identify differentially methylated gene promoter CpG sites. In this report, we present our results on three pesticides (fonofos, parathion, and terbufos) that clustered together based on principle component analysis and hierarchical clustering. These three pesticides induced similar methylation changes in the promoter regions of 712 genes, while also exhibiting their own OP‐specific methylation alterations. Functional analysis of methylation changes specific to each OP, or common to all three OPs, revealed that differential methylation was associated with numerous genes that are involved in carcinogenesis‐related processes. Our results provide experimental evidence that pesticides may modify gene promoter DNA methylation levels, suggesting that epigenetic mechanisms may contribute to pesticide‐induced carcinogenesis. Further studies in other cell types and human samples are required, as well as determining the impact of these methylation changes on gene expression. Environ. Mol. Mutagen. 2012. © 2012 Wiley Periodicals, Inc. Although pesticides are subject to extensive carcinogenicity testing before regulatory approval, pesticide exposure has repeatedly been associated with various cancers. This suggests that pesticides may cause cancer via non-mutagenicity mechanisms. The present study provides evidence to support the hypothesis that pesticide-induced cancer may be mediated in part by epigenetic mechanisms. We examined whether exposure to 7 commonly used pesticides (i.e., fonofos, parathion, terbufos, chlorpyrifos, diazinon, malathion, and phorate) induces DNA methylation alterations in vitro. We conducted genome-wide DNA methylation analyses on DNA samples obtained from the human hematopoietic K562 cell line exposed to ethanol (control) and several OPs using the Illumina Infinium HumanMethylation27 BeadChip. Bayesian-adjusted t-tests were used to identify differentially methylated gene promoter CpG sites. In this report, we present our results on three pesticides (fonofos, parathion, and terbufos) that clustered together based on principle component analysis and hierarchical clustering. These three pesticides induced similar methylation changes in the promoter regions of 712 genes, while also exhibiting their own OP-specific methylation alterations. Functional analysis of methylation changes specific to each OP, or common to all three OPs, revealed that differential methylation was associated with numerous genes that are involved in carcinogenesis-related processes. Our results provide experimental evidence that pesticides may modify gene promoter DNA methylation levels, suggesting that epigenetic mechanisms may contribute to pesticide-induced carcinogenesis. Further studies in other cell types and human samples are required, as well as determining the impact of these methylation changes on gene expression. Although pesticides are subject to extensive carcinogenicity testing before regulatory approval, pesticide exposure has repeatedly been associated with various cancers. This suggests that pesticides may cause cancer via nonmutagenicity mechanisms. The present study provides evidence to support the hypothesis that pesticide‐induced cancer may be mediated in part by epigenetic mechanisms. We examined whether exposure to seven commonly used pesticides (i.e., fonofos, parathion, terbufos, chlorpyrifos, diazinon, malathion, and phorate) induces DNA methylation alterations in vitro. We conducted genome‐wide DNA methylation analyses on DNA samples obtained from the human hematopoietic K562 cell line exposed to ethanol (control) and several organophosphate pesticides (OPs) using the Illumina Infinium HumanMethylation27 BeadChip. Bayesian‐adjusted t‐tests were used to identify differentially methylated gene promoter CpG sites. In this report, we present our results on three pesticides (fonofos, parathion, and terbufos) that clustered together based on principle component analysis and hierarchical clustering. These three pesticides induced similar methylation changes in the promoter regions of 712 genes, while also exhibiting their own OP‐specific methylation alterations. Functional analysis of methylation changes specific to each OP, or common to all three OPs, revealed that differential methylation was associated with numerous genes that are involved in carcinogenesis‐related processes. Our results provide experimental evidence that pesticides may modify gene promoter DNA methylation levels, suggesting that epigenetic mechanisms may contribute to pesticide‐induced carcinogenesis. Further studies in other cell types and human samples are required, as well as determining the impact of these methylation changes on gene expression. Environ. Mol. Mutagen. 2012. © 2012 Wiley Periodicals, Inc. Although pesticides are subject to extensive carcinogenicity testing before regulatory approval, pesticide exposure has repeatedly been associated with various cancers. This suggests that pesticides may cause cancer via nonmutagenicity mechanisms. The present study provides evidence to support the hypothesis that pesticide-induced cancer may be mediated in part by epigenetic mechanisms. We examined whether exposure to seven commonly used pesticides (i.e., fonofos, parathion, terbufos, chlorpyrifos, diazinon, malathion, and phorate) induces DNA methylation alterations in vitro. We conducted genome-wide DNA methylation analyses on DNA samples obtained from the human hematopoietic K562 cell line exposed to ethanol (control) and several organophosphate pesticides (OPs) using the Illumina Infinium HumanMethylation27 BeadChip. Bayesian-adjusted t-tests were used to identify differentially methylated gene promoter CpG sites. In this report, we present our results on three pesticides (fonofos, parathion, and terbufos) that clustered together based on principle component analysis and hierarchical clustering. These three pesticides induced similar methylation changes in the promoter regions of 712 genes, while also exhibiting their own OP-specific methylation alterations. Functional analysis of methylation changes specific to each OP, or common to all three OPs, revealed that differential methylation was associated with numerous genes that are involved in carcinogenesis-related processes. Our results provide experimental evidence that pesticides may modify gene promoter DNA methylation levels, suggesting that epigenetic mechanisms may contribute to pesticide-induced carcinogenesis. Further studies in other cell types and human samples are required, as well as determining the impact of these methylation changes on gene expression. Although pesticides are subject to extensive carcinogenicity testing before regulatory approval, pesticide exposure has repeatedly been associated with various cancers. This suggests that pesticides may cause cancer via nonmutagenicity mechanisms. The present study provides evidence to support the hypothesis that pesticide-induced cancer may be mediated in part by epigenetic mechanisms. We examined whether exposure to seven commonly used pesticides (i.e., fonofos, parathion, terbufos, chlorpyrifos, diazinon, malathion, and phorate) induces DNA methylation alterations in vitro. We conducted genome-wide DNA methylation analyses on DNA samples obtained from the human hematopoietic K562 cell line exposed to ethanol (control) and several organophosphate pesticides (OPs) using the Illumina Infinium HumanMethylation27 BeadChip. Bayesian-adjusted t-tests were used to identify differentially methylated gene promoter CpG sites. In this report, we present our results on three pesticides (fonofos, parathion, and terbufos) that clustered together based on principle component analysis and hierarchical clustering. These three pesticides induced similar methylation changes in the promoter regions of 712 genes, while also exhibiting their own OP-specific methylation alterations. Functional analysis of methylation changes specific to each OP, or common to all three OPs, revealed that differential methylation was associated with numerous genes that are involved in carcinogenesis-related processes. Our results provide experimental evidence that pesticides may modify gene promoter DNA methylation levels, suggesting that epigenetic mechanisms may contribute to pesticide-induced carcinogenesis. Further studies in other cell types and human samples are required, as well as determining the impact of these methylation changes on gene expression.Although pesticides are subject to extensive carcinogenicity testing before regulatory approval, pesticide exposure has repeatedly been associated with various cancers. This suggests that pesticides may cause cancer via nonmutagenicity mechanisms. The present study provides evidence to support the hypothesis that pesticide-induced cancer may be mediated in part by epigenetic mechanisms. We examined whether exposure to seven commonly used pesticides (i.e., fonofos, parathion, terbufos, chlorpyrifos, diazinon, malathion, and phorate) induces DNA methylation alterations in vitro. We conducted genome-wide DNA methylation analyses on DNA samples obtained from the human hematopoietic K562 cell line exposed to ethanol (control) and several organophosphate pesticides (OPs) using the Illumina Infinium HumanMethylation27 BeadChip. Bayesian-adjusted t-tests were used to identify differentially methylated gene promoter CpG sites. In this report, we present our results on three pesticides (fonofos, parathion, and terbufos) that clustered together based on principle component analysis and hierarchical clustering. These three pesticides induced similar methylation changes in the promoter regions of 712 genes, while also exhibiting their own OP-specific methylation alterations. Functional analysis of methylation changes specific to each OP, or common to all three OPs, revealed that differential methylation was associated with numerous genes that are involved in carcinogenesis-related processes. Our results provide experimental evidence that pesticides may modify gene promoter DNA methylation levels, suggesting that epigenetic mechanisms may contribute to pesticide-induced carcinogenesis. Further studies in other cell types and human samples are required, as well as determining the impact of these methylation changes on gene expression. |
Author | Zhang, Xiao Soares, Marcelo Bento Hou, Lifang Lin, Simon Wallace, Andrew D. Du, Pan Jafari, Nadereh Xie, Hehuang Kibbe, Warren A. Baccarelli, Andrea |
AuthorAffiliation | 5 Center for Genetic Medicine, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA 1 Department of Preventive Medicine, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA 2 Department of Environmental and Molecular Toxicology, North Carolina State University, Raleigh, North Carolina, USA 7 Biomedical Informatics Research Center, Marshfield Clinic Research Foundation, Marshfield, Wisconsin, USA 8 Exposure, Epidemiology and Risk Program, Department of Environmental Health, Harvard School of Public Health, Boston, Massachusetts, USA 3 Department of Bioinformatics and Computational Biology, Genentech Inc., South San Francisco, California, USA 9 The Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA 4 Northwestern University Biomedical Informatics Center (NUBIC), Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA 6 Falk Brain Tumor Center, Cancer Biolog |
AuthorAffiliation_xml | – name: 9 The Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA – name: 5 Center for Genetic Medicine, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA – name: 7 Biomedical Informatics Research Center, Marshfield Clinic Research Foundation, Marshfield, Wisconsin, USA – name: 2 Department of Environmental and Molecular Toxicology, North Carolina State University, Raleigh, North Carolina, USA – name: 4 Northwestern University Biomedical Informatics Center (NUBIC), Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA – name: 6 Falk Brain Tumor Center, Cancer Biology and Epigenomics Program, Children’s Memorial Research Center, Department of Pediatrics, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA – name: 8 Exposure, Epidemiology and Risk Program, Department of Environmental Health, Harvard School of Public Health, Boston, Massachusetts, USA – name: 3 Department of Bioinformatics and Computational Biology, Genentech Inc., South San Francisco, California, USA – name: 1 Department of Preventive Medicine, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA |
Author_xml | – sequence: 1 givenname: Xiao surname: Zhang fullname: Zhang, Xiao organization: Department of Preventive Medicine, Feinberg School of Medicine, Northwestern University, Chicago, Illinois – sequence: 2 givenname: Andrew D. surname: Wallace fullname: Wallace, Andrew D. organization: Department of Environmental and Molecular Toxicology, North Carolina State University, Raleigh, North Carolina – sequence: 3 givenname: Pan surname: Du fullname: Du, Pan organization: Department of Bioinformatics and Computational Biology, Genentech Inc., South San Francisco, California – sequence: 4 givenname: Warren A. surname: Kibbe fullname: Kibbe, Warren A. organization: Northwestern University Biomedical Informatics Center (NUBIC), Feinberg School of Medicine, Northwestern University, Chicago, Illinois – sequence: 5 givenname: Nadereh surname: Jafari fullname: Jafari, Nadereh organization: Center for Genetic Medicine, Feinberg School of Medicine, Northwestern University, Chicago, Illinois – sequence: 6 givenname: Hehuang surname: Xie fullname: Xie, Hehuang organization: Falk Brain Tumor Center, Cancer Biology and Epigenomics Program, Children's Memorial Research Center, Department of Pediatrics, Feinberg School of Medicine, Northwestern University, Chicago, Illinois – sequence: 7 givenname: Simon surname: Lin fullname: Lin, Simon organization: Biomedical Informatics Research Center, Marshfield Clinic Research Foundation, Marshfield, Wisconsin – sequence: 8 givenname: Andrea surname: Baccarelli fullname: Baccarelli, Andrea organization: Exposure, Epidemiology and Risk Program, Department of Environmental Health, Harvard School of Public Health, Boston, Massachusetts – sequence: 9 givenname: Marcelo Bento surname: Soares fullname: Soares, Marcelo Bento organization: Falk Brain Tumor Center, Cancer Biology and Epigenomics Program, Children's Memorial Research Center, Department of Pediatrics, Feinberg School of Medicine, Northwestern University, Chicago, Illinois – sequence: 10 givenname: Lifang surname: Hou fullname: Hou, Lifang email: l-hou@northwestern.edu organization: Department of Preventive Medicine, Feinberg School of Medicine, Northwestern University, Chicago, Illinois |
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Keywords | Toxicology DNA methylation alteration DNA pesticide exposure Pesticides Genetics Exposure Methylation Carcinogenesis In vitro |
Language | English |
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Notes | ArticleID:EM21718 istex:6EBA586ABDB6A52B53B47560DCDB285AB26A89C9 NIH - No. 1RC1ES018461-01 ark:/67375/WNG-LS2RVSDX-8 ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Authors’ contributions Wallace, Jafari, Xie and Soares performed the laboratory analyses. Zhang, Lin, Baccarelli, and Hou generated the study concept, study design, and prepared manuscript. All authors read and approved the final manuscript. Conflict of Interest statement: The authors declare that there are no conflicts of interest Du, Lin, Kibbe performed bioinformatics analyses. |
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References | Galloway T,Handy R. 2003. Immunotoxicity of organophosphorous pesticides. Ecotoxicology 12: 345-363. Pasquini R,Scassellati-Sforzolini G,Dolara P,Pampanella L,Villarini M,Caderni G,Fazi M,Fatigoni C. 1994. Assay of linuron and a pesticide mixture commonly found in the Italian diet, for promoting activity in rat liver carcinogenesis. Pharmacol Toxicol 75: 170-176. Phillips TM. 2000. Assessing environmental exposure in children: Immunotoxicology screening. J Expo Anal Environ Epidemiol 10(6 Pt 2): 769-775. Skinner MK,Anway MD. 2007. Epigenetic transgenerational actions of vinclozolin on the development of disease and cancer. Crit Rev Oncog 13: 75-82. Fratelli M,Goodwin LO,Orom UA,Lombardi S,Tonelli R,Mengozzi M,Ghezzi P. 2005. Gene expression profiling reveals a signaling role of glutathione in redox regulation. Proc Natl Acad Sci U S A 102: 13998-14003. Gupta SC,Siddique HR,Mathur N,Vishwakarma AL,Mishra RK,Saxena DK,Chowdhuri DK. 2007. Induction of hsp70, alterations in oxidative stress markers and apoptosis against dichlorvos exposure in transgenic Drosophila melanogaster: Modulation by reactive oxygen species. Biochim Biophys Acta 1770: 1382-1394. Du P,Kibbe WA,Lin SM. 2008. Lumi: A pipeline for processing Illumina microarray. Bioinformatics 24: 1547-1548. Andersson LC,Jokinen M,Klein E,Klein G,Nilsson K. 1979. Presence of erythrocytic components in the K562 cell line. Int J Cancer 24: 514. Hodge DR,Xiao W,Clausen PA,Heidecker G,Szyf M,Farrar WL. 2001. Interleukin-6 regulation of the human DNA methyltransferase (HDNMT) gene in human erythroleukemia cells. J Biol Chem 276: 39508-39511. Arcury TA,Grzywacz JG,Chen H,Vallejos QM,Galvan L,Whalley LE,Isom S,Barr DB,Quandt SA. 2009. Variation across the agricultural season in organophosphorus pesticide urinary metabolite levels for Latino farmworkers in eastern North Carolina: Project design and descriptive results. Am J Ind Med 52: 539-550. Bassil KL,Vakil C,Sanborn M,Cole DC,Kaur JS,Kerr KJ. 2007. Cancer health effects of pesticides: Systematic review. Can Fam Physician 53: 1704-1711. Baker EJ,Ichiki AT,Day NE,Andrews RB,Bamberger EG,Lozzio CB. 2001. Simultaneous flow cytometric measurement of K-562 megakaryocytic differentiation and CD56+ large granular lymphocyte cytotoxicity. J Immunol Methods 253: 37-44. Dennis LK,Lynch CF,Sandler DP,Alavanja MC. 2010. Pesticide use and cutaneous melanoma in pesticide applicators in the agricultural heath study. Environ Health Perspect 118: 812-817. EPH. 1997. Environmental Protection Agency. Notice to manufacturers, producers and registrants of pesticide products. Washington, DC: Environmental Protection Agency. Issa JP. 2004. CpG island methylator phenotype in cancer. Nat Rev Cancer 4: 988-993. Bonner MR,Williams BA,Rusiecki JA,Blair A,Beane Freeman LE,Hoppin JA,Dosemeci M,Lubin J,Sandler DP,Alavanja MC. 2010. Occupational exposure to terbufos and the incidence of cancer in the Agricultural Health Study. Cancer Causes Control 21: 871-877. Lee WJ,Sandler DP,Blair A,Samanic C,Cross AJ,Alavanja MC. 2007. Pesticide use and colorectal cancer risk in the Agricultural Health Study. Int J Cancer 121: 339-346. Hathaway G,Proctor N,Hughes J,Fischman M. 1991. Proctor and Hughes' Chemical Hazards of the Workplace. New York: Van Nostrand Reinhold. Arcury TA,Grzywacz JG,Barr DB,Tapia J,Chen H,Quandt SA. 2007. Pesticide urinary metabolite levels of children in eastern North Carolina farmworker households. Environ Health Perspect 115: 1254-1260. Watson RE,McKim JM,Cockerell GL,Goodman JI. 2004. The value of DNA methylation analysis in basic, initial toxicity assessments. Toxicol Sci 79: 178-188. Veraldi A,Costantini AS,Bolejack V,Miligi L,Vineis P,van Loveren H. 2006. Immunotoxic effects of chemicals: A matrix for occupational and environmental epidemiological studies. Am J Ind Med 49: 1046-1055. Waggoner JK,Kullman GJ,Henneberger PK,Umbach DM,Blair A,Alavanja MC,Kamel F,Lynch CF,Knott C,London SJ,Hines CJ,Thomas KW,Sandler DP,Lubin JH,Beane Freeman LE,Hoppin JA. 2011. Mortality in the agricultural health study, 1993-2007. Am J Epidemiol 173(1): 71-83. Baccarelli A,Bollati V. 2009. Epigenetics and environmental chemicals. Curr Opin Pediatr 21: 243-251. Mahajan R,Blair A,Lynch CF,Schroeder P,Hoppin JA,Sandler DP,Alavanja MC. 2006. Fonofos exposure and cancer incidence in the agricultural health study. Environ Health Perspect 114: 1838-1842. Soltaninejad K,Abdollahi M. 2009. Current opinion on the science of organophosphate pesticides and toxic stress: A systematic review. Med Sci Monit 15(3): RA75-RA90. Calaf GM,Echiburu-Chau C,Roy D. 2009. Organophosphorous pesticides and estrogen induce transformation of breast cells affecting p53 and c-Ha-ras genes. Int J Oncol 35: 1061-1068. Koutros S,Alavanja MC,Lubin JH,Sandler DP,Hoppin JA,Lynch CF,Knott C,Blair A,Freeman LE. 2010. An update of cancer incidence in the Agricultural Health Study. J Occup Environ Med 52: 1098-1105. Daniel V,Huber W,Bauer K,Suesal C,Mytilineos J,Melk A,Conradt C,Opelz G. 2001. Association of elevated blood levels of pentachlorophenol (PCP) with cellular and humoral immunodeficiencies. Arch Environ Health 56: 77-83. Huang D,Zhang Y,Qi Y,Chen C,Ji W. 2008. Global DNA hypomethylation, rather than reactive oxygen species (ROS), a potential facilitator of cadmium-stimulated K562 cell proliferation. Toxicol Lett 179: 43-47. Alavanja MC. 2009. Introduction: Pesticides use and exposure extensive worldwide. Rev Environ Health 24: 303-309. Rusiecki JA,Baccarelli A,Bollati V,Tarantini L,Moore LE,Bonefeld-Jorgensen EC. 2008. Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic Inuit. Environ Health Perspect 116: 1547-1552. Yu F,Wang Z,Ju B,Wang Y,Wang J,Bai D. 2008. Apoptotic effect of organophosphorus insecticide chlorpyrifos on mouse retina in vivo via oxidative stress and protection of combination of vitamins C and E. Exp Toxicol Pathol 59: 415-423. Kim KY,Kim DS,Lee SK,Lee IK,Kang JH,Chang YS,Jacobs DR,Steffes M,Lee DH. 2010. Association of low-dose exposure to persistent organic pollutants with global DNA hypomethylation in healthy Koreans. Environ Health Perspect 118: 370-374. Fenske RA,Lu C,Barr D,Needham L. 2002. Children's exposure to chlorpyrifos and parathion in an agricultural community in central Washington State. Environ Health Perspect 110: 549-553. Smyth GK. 2004. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3. De Roos AJ,Zahm SH,Cantor KP,Weisenburger DD,Holmes FF,Burmeister LF,Blair A. 2003. Integrative assessment of multiple pesticides as risk factors for non-Hodgkin's lymphoma among men. Occup Environ Med 60: E11. Bibikova M,Lin Z,Zhou L,Chudin E,Garcia EW,Wu B,Doucet D,Thomas NJ,Wang Y,Vollmer E,Goldmann T,Seifart C,Jiang W,Barker DL,Chee MS,Floros J,Fan JB. 2006. High-throughput DNA methylation profiling using universal bead arrays. Genome Res 16: 383-393. Coral MN,Ucman S,Yildiz H,Oztas H,Dalkilic S. 2009. Potential neoplastic effects of parathion-methyl on rat liver. J Environ Sci (China) 21: 696-699. Cabello G,Juarranz A,Botella LM,Calaf GM. 2003. Organophosphorous pesticides in breast cancer progression. J Submicrosc Cytol Pathol 35: 1-9. Wong PS,Matsumura F. 2007. Promotion of breast cancer by beta-hexachlorocyclohexane in MCF10AT1 cells and MMTV-neu mice. BMC Cancer 7: 130. Weichenthal S,Moase C,Chan P. 2010. A review of pesticide exposure and cancer incidence in the Agricultural Health Study cohort. Environ Health Perspect 118: 1117-1125. Guerrero-Bosagna C,Settles M,Lucker B,Skinner MK. 2010. Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS One 5(9). Lozzio BB,Lozzio CB,Bamberger EG,Feliu AS. 1981. A multipotential leukemia cell line (K-562) of human origin. Proc Soc Exp Biol Med 166: 546-550. Cabello G,Valenzuela M,Vilaxa A,Duran V,Rudolph I,Hrepic N,Calaf G. 2001. A rat mammary tumor model induced by the organophosphorous pesticides parathion and malathion, possibly through acetylcholinesterase inhibition. Environ Health Perspect 109: 471-479. Du P,Zhang X,Huang CC,Jafari N,Kibbe WA,Hou L,Lin SM. 2010. Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics 11: 587. Alavanja MC,Ward MH,Reynolds P. 2007. Carcinogenicity of agricultural pesticides in adults and children. J Agromedicine 12: 39-56. Bachman AN,Kamendulis LM,Goodman JI. 2006. Diethanolamine and phenobarbital produce an altered pattern of methylation in GC-rich regions of DNA in B6C3F1 mouse hepatocytes similar to that resulting from choline deficiency. Toxicol Sci 90: 317-325. Shepherd KR,Lee ES,Schmued L,Jiao Y,Ali SF,Oriaku ET,Lamango NS,Soliman KF,Charlton CG. 2006. The potentiating effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) on paraquat-induced neurochemical and behavioral changes in mice. Pharmacol Biochem Behav 83: 349-359. Feng G,Du P,Krett NL,Tessel M,Rosen S,Kibbe WA,Lin SM. 2010. A collection of bioconductor methods to visualize gene-list annotations. BMC Res Notes 3: 10. Mena S,Ortega A,Estrela JM. 2009. Oxidative stress in environmental-induced carcinogenesis. Mutat Res 674: 36-44. Reuber MD. 1981. Carcinogenicity of dichlorvos. Clin Toxicol 18: 47-84. Anway MD,Skinner MK. 2006. Epigenetic transgenerational actions of endocrine disruptors. Endocrinology 147( 6 Suppl): S43-S49. Barr DB,Allen R,Olsson AO,Bravo R,Caltabiano LM,Montesano A,Nguyen J,Udunka S,Walden D,Walker RD,Weerasekera G,Whitehead RDJr,Schober SE,Needham LL. 2005. Concentrations of selective metabolites of organophosphorus pesticides in the United States population. Environ Res 99: 314-326. Alavanja MC,Bonner MR. 2005. Pesticides and human cancers. Cancer Invest 23: 700-711. Xie H,Wang M,Bonaldo Mde F,Smith C,Rajaram V,Goldman S,Tomita T,Soares MB. 2009. High-throughput sequence-based epigenomic analysis of Alu repeats in human cerebellum. Nucleic Acids Res 37: 4331-4340. 2010; 11 2002; 110 2004; 4 2004; 3 2009; 674 2001; 109 2005; 23 2003; 12 2001; 253 2010; 21 1979; 24 2009; 52 2010; 118 2005; 102 2000; 10 2007; 1770 2004; 79 2008; 24 2007; 7 2008; 116 2010; 3 2001; 56 2010; 5 2009; 15 1994; 75 2006; 90 2009; 24 2009; 21 2006; 16 2007; 121 1981; 166 2003; 35 1997 2008; 59 1991 2007; 53 2011; 173 2007; 12 2007; 13 2006; 114 2001; 276 2007; 115 2009; 35 2006; 83 2006; 49 1981; 18 2008; 179 2003; 60 2005; 99 2010; 52 2009; 37 2006; 147 e_1_2_6_51_1 e_1_2_6_53_1 e_1_2_6_30_1 e_1_2_6_19_1 e_1_2_6_36_1 e_1_2_6_11_1 e_1_2_6_34_1 e_1_2_6_17_1 e_1_2_6_55_1 e_1_2_6_15_1 e_1_2_6_38_1 e_1_2_6_57_1 e_1_2_6_43_1 e_1_2_6_20_1 e_1_2_6_41_1 e_1_2_6_9_1 Soltaninejad K (e_1_2_6_50_1) 2009; 15 e_1_2_6_5_1 e_1_2_6_7_1 e_1_2_6_24_1 e_1_2_6_49_1 e_1_2_6_3_1 e_1_2_6_22_1 e_1_2_6_28_1 e_1_2_6_45_1 e_1_2_6_26_1 e_1_2_6_47_1 e_1_2_6_52_1 e_1_2_6_54_1 e_1_2_6_10_1 e_1_2_6_31_1 e_1_2_6_14_1 e_1_2_6_35_1 Cabello G (e_1_2_6_16_1) 2003; 35 e_1_2_6_12_1 e_1_2_6_33_1 e_1_2_6_18_1 e_1_2_6_39_1 e_1_2_6_56_1 e_1_2_6_37_1 EPH (e_1_2_6_25_1) 1997 e_1_2_6_42_1 e_1_2_6_21_1 Hathaway G (e_1_2_6_32_1) 1991 e_1_2_6_40_1 Bassil KL (e_1_2_6_13_1) 2007; 53 e_1_2_6_8_1 e_1_2_6_4_1 e_1_2_6_6_1 e_1_2_6_48_1 e_1_2_6_23_1 e_1_2_6_2_1 e_1_2_6_29_1 e_1_2_6_44_1 e_1_2_6_27_1 e_1_2_6_46_1 16307973 - Environ Res. 2005 Nov;99(3):314-26 18222074 - Exp Toxicol Pathol. 2008 Apr;59(6):415-23 15573120 - Nat Rev Cancer. 2004 Dec;4(12):988-93 17640349 - BMC Cancer. 2007;7:130 18032335 - J Agromedicine. 2007;12(1):39-56 18467348 - Bioinformatics. 2008 Jul 1;24(13):1547-8 18977455 - Mutat Res. 2009 Mar 31;674(1-2):36-44 7194480 - Proc Soc Exp Biol Med. 1981 Apr;166(4):546-50 17687456 - Environ Health Perspect. 2007 Aug;115(8):1254-60 15103049 - Toxicol Sci. 2004 May;79(1):178-88 17390374 - Int J Cancer. 2007 Jul 15;121(2):339-46 16580056 - Pharmacol Biochem Behav. 2006 Mar;83(3):349-59 21118553 - BMC Bioinformatics. 2010;11:587 20064773 - Environ Health Perspect. 2010 Mar;118(3):370-4 20164001 - Environ Health Perspect. 2010 Jun;118(6):812-7 12739880 - Ecotoxicology. 2003 Feb-Aug;12(1-4):345-63 11256860 - Arch Environ Health. 2001 Jan-Feb;56(1):77-83 17934034 - Can Fam Physician. 2007 Oct;53(10):1704-11 16377589 - Cancer Invest. 2005;23(8):700-11 17640809 - Biochim Biophys Acta. 2007 Sep;1770(9):1382-94 20180973 - BMC Res Notes. 2010 Jan 19;3:10 16690803 - Endocrinology. 2006 Jun;147(6 Suppl):S43-9 16396840 - Toxicol Sci. 2006 Apr;90(2):317-25 16449502 - Genome Res. 2006 Mar;16(3):383-93 20444670 - Environ Health Perspect. 2010 Aug;118(8):1117-25 19663042 - Curr Opin Pediatr. 2009 Apr;21(2):243-51 16646809 - Stat Appl Genet Mol Biol. 2004;3:Article3 16172407 - Proc Natl Acad Sci U S A. 2005 Sep 27;102(39):13998-4003 11138669 - J Expo Anal Environ Epidemiol. 2000 Nov-Dec;10(6 Pt 2):769-75 528075 - Int J Cancer. 1979 Oct 15;24(4):514 19517490 - Am J Ind Med. 2009 Jul;52(7):539-50 17956218 - Crit Rev Oncog. 2007 Aug;13(1):75-82 21084556 - Am J Epidemiol. 2011 Jan 1;173(1):71-83 19458156 - Nucleic Acids Res. 2009 Jul;37(13):4331-40 18482805 - Toxicol Lett. 2008 Jun 10;179(1):43-7 12003762 - Environ Health Perspect. 2002 May;110(5):549-53 20927350 - PLoS One. 2010;5(9). pii: e13100. doi: 10.1371/journal.pone.0013100 20384038 - Rev Environ Health. 2009 Oct-Dec;24(4):303-9 20155313 - Cancer Causes Control. 2010 Jun;21(6):871-7 12762645 - J Submicrosc Cytol Pathol. 2003 Jan;35(1):1-9 11401758 - Environ Health Perspect. 2001 May;109(5):471-9 17036363 - Am J Ind Med. 2006 Dec;49(12):1046-55 19247260 - Med Sci Monit. 2009 Mar;15(3):RA75-90 7009035 - Clin Toxicol. 1981 Jan;18(1):47-84 21063187 - J Occup Environ Med. 2010 Nov;52(11):1098-105 11551897 - J Biol Chem. 2001 Oct 26;276(43):39508-11 11384667 - J Immunol Methods. 2001 Jul 1;253(1-2):37-44 19057709 - Environ Health Perspect. 2008 Nov;116(11):1547-52 19787260 - Int J Oncol. 2009 Nov;35(5):1061-8 |
References_xml | – reference: Baccarelli A,Bollati V. 2009. Epigenetics and environmental chemicals. Curr Opin Pediatr 21: 243-251. – reference: Andersson LC,Jokinen M,Klein E,Klein G,Nilsson K. 1979. Presence of erythrocytic components in the K562 cell line. Int J Cancer 24: 514. – reference: De Roos AJ,Zahm SH,Cantor KP,Weisenburger DD,Holmes FF,Burmeister LF,Blair A. 2003. Integrative assessment of multiple pesticides as risk factors for non-Hodgkin's lymphoma among men. Occup Environ Med 60: E11. – reference: Bachman AN,Kamendulis LM,Goodman JI. 2006. Diethanolamine and phenobarbital produce an altered pattern of methylation in GC-rich regions of DNA in B6C3F1 mouse hepatocytes similar to that resulting from choline deficiency. Toxicol Sci 90: 317-325. – reference: Alavanja MC,Bonner MR. 2005. Pesticides and human cancers. Cancer Invest 23: 700-711. – reference: Watson RE,McKim JM,Cockerell GL,Goodman JI. 2004. The value of DNA methylation analysis in basic, initial toxicity assessments. Toxicol Sci 79: 178-188. – reference: Bassil KL,Vakil C,Sanborn M,Cole DC,Kaur JS,Kerr KJ. 2007. Cancer health effects of pesticides: Systematic review. Can Fam Physician 53: 1704-1711. – reference: Lozzio BB,Lozzio CB,Bamberger EG,Feliu AS. 1981. A multipotential leukemia cell line (K-562) of human origin. Proc Soc Exp Biol Med 166: 546-550. – reference: Anway MD,Skinner MK. 2006. Epigenetic transgenerational actions of endocrine disruptors. Endocrinology 147( 6 Suppl): S43-S49. – reference: Arcury TA,Grzywacz JG,Barr DB,Tapia J,Chen H,Quandt SA. 2007. Pesticide urinary metabolite levels of children in eastern North Carolina farmworker households. Environ Health Perspect 115: 1254-1260. – reference: Arcury TA,Grzywacz JG,Chen H,Vallejos QM,Galvan L,Whalley LE,Isom S,Barr DB,Quandt SA. 2009. Variation across the agricultural season in organophosphorus pesticide urinary metabolite levels for Latino farmworkers in eastern North Carolina: Project design and descriptive results. Am J Ind Med 52: 539-550. – reference: Calaf GM,Echiburu-Chau C,Roy D. 2009. Organophosphorous pesticides and estrogen induce transformation of breast cells affecting p53 and c-Ha-ras genes. Int J Oncol 35: 1061-1068. – reference: Rusiecki JA,Baccarelli A,Bollati V,Tarantini L,Moore LE,Bonefeld-Jorgensen EC. 2008. Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic Inuit. Environ Health Perspect 116: 1547-1552. – reference: Coral MN,Ucman S,Yildiz H,Oztas H,Dalkilic S. 2009. Potential neoplastic effects of parathion-methyl on rat liver. J Environ Sci (China) 21: 696-699. – reference: Hathaway G,Proctor N,Hughes J,Fischman M. 1991. Proctor and Hughes' Chemical Hazards of the Workplace. New York: Van Nostrand Reinhold. – reference: Shepherd KR,Lee ES,Schmued L,Jiao Y,Ali SF,Oriaku ET,Lamango NS,Soliman KF,Charlton CG. 2006. The potentiating effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) on paraquat-induced neurochemical and behavioral changes in mice. Pharmacol Biochem Behav 83: 349-359. – reference: Gupta SC,Siddique HR,Mathur N,Vishwakarma AL,Mishra RK,Saxena DK,Chowdhuri DK. 2007. Induction of hsp70, alterations in oxidative stress markers and apoptosis against dichlorvos exposure in transgenic Drosophila melanogaster: Modulation by reactive oxygen species. Biochim Biophys Acta 1770: 1382-1394. – reference: Smyth GK. 2004. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3. – reference: Yu F,Wang Z,Ju B,Wang Y,Wang J,Bai D. 2008. Apoptotic effect of organophosphorus insecticide chlorpyrifos on mouse retina in vivo via oxidative stress and protection of combination of vitamins C and E. Exp Toxicol Pathol 59: 415-423. – reference: Waggoner JK,Kullman GJ,Henneberger PK,Umbach DM,Blair A,Alavanja MC,Kamel F,Lynch CF,Knott C,London SJ,Hines CJ,Thomas KW,Sandler DP,Lubin JH,Beane Freeman LE,Hoppin JA. 2011. Mortality in the agricultural health study, 1993-2007. Am J Epidemiol 173(1): 71-83. – reference: Xie H,Wang M,Bonaldo Mde F,Smith C,Rajaram V,Goldman S,Tomita T,Soares MB. 2009. High-throughput sequence-based epigenomic analysis of Alu repeats in human cerebellum. Nucleic Acids Res 37: 4331-4340. – reference: Galloway T,Handy R. 2003. Immunotoxicity of organophosphorous pesticides. Ecotoxicology 12: 345-363. – reference: Cabello G,Valenzuela M,Vilaxa A,Duran V,Rudolph I,Hrepic N,Calaf G. 2001. A rat mammary tumor model induced by the organophosphorous pesticides parathion and malathion, possibly through acetylcholinesterase inhibition. Environ Health Perspect 109: 471-479. – reference: Hodge DR,Xiao W,Clausen PA,Heidecker G,Szyf M,Farrar WL. 2001. Interleukin-6 regulation of the human DNA methyltransferase (HDNMT) gene in human erythroleukemia cells. J Biol Chem 276: 39508-39511. – reference: Weichenthal S,Moase C,Chan P. 2010. A review of pesticide exposure and cancer incidence in the Agricultural Health Study cohort. Environ Health Perspect 118: 1117-1125. – reference: Bonner MR,Williams BA,Rusiecki JA,Blair A,Beane Freeman LE,Hoppin JA,Dosemeci M,Lubin J,Sandler DP,Alavanja MC. 2010. Occupational exposure to terbufos and the incidence of cancer in the Agricultural Health Study. Cancer Causes Control 21: 871-877. – reference: Reuber MD. 1981. Carcinogenicity of dichlorvos. Clin Toxicol 18: 47-84. – reference: Alavanja MC,Ward MH,Reynolds P. 2007. Carcinogenicity of agricultural pesticides in adults and children. J Agromedicine 12: 39-56. – reference: Dennis LK,Lynch CF,Sandler DP,Alavanja MC. 2010. Pesticide use and cutaneous melanoma in pesticide applicators in the agricultural heath study. Environ Health Perspect 118: 812-817. – reference: Lee WJ,Sandler DP,Blair A,Samanic C,Cross AJ,Alavanja MC. 2007. Pesticide use and colorectal cancer risk in the Agricultural Health Study. Int J Cancer 121: 339-346. – reference: Koutros S,Alavanja MC,Lubin JH,Sandler DP,Hoppin JA,Lynch CF,Knott C,Blair A,Freeman LE. 2010. An update of cancer incidence in the Agricultural Health Study. J Occup Environ Med 52: 1098-1105. – reference: Barr DB,Allen R,Olsson AO,Bravo R,Caltabiano LM,Montesano A,Nguyen J,Udunka S,Walden D,Walker RD,Weerasekera G,Whitehead RDJr,Schober SE,Needham LL. 2005. Concentrations of selective metabolites of organophosphorus pesticides in the United States population. Environ Res 99: 314-326. – reference: Feng G,Du P,Krett NL,Tessel M,Rosen S,Kibbe WA,Lin SM. 2010. A collection of bioconductor methods to visualize gene-list annotations. BMC Res Notes 3: 10. – reference: Kim KY,Kim DS,Lee SK,Lee IK,Kang JH,Chang YS,Jacobs DR,Steffes M,Lee DH. 2010. Association of low-dose exposure to persistent organic pollutants with global DNA hypomethylation in healthy Koreans. Environ Health Perspect 118: 370-374. – reference: Issa JP. 2004. CpG island methylator phenotype in cancer. Nat Rev Cancer 4: 988-993. – reference: Wong PS,Matsumura F. 2007. Promotion of breast cancer by beta-hexachlorocyclohexane in MCF10AT1 cells and MMTV-neu mice. BMC Cancer 7: 130. – reference: Skinner MK,Anway MD. 2007. Epigenetic transgenerational actions of vinclozolin on the development of disease and cancer. Crit Rev Oncog 13: 75-82. – reference: Fratelli M,Goodwin LO,Orom UA,Lombardi S,Tonelli R,Mengozzi M,Ghezzi P. 2005. Gene expression profiling reveals a signaling role of glutathione in redox regulation. Proc Natl Acad Sci U S A 102: 13998-14003. – reference: Fenske RA,Lu C,Barr D,Needham L. 2002. Children's exposure to chlorpyrifos and parathion in an agricultural community in central Washington State. Environ Health Perspect 110: 549-553. – reference: Daniel V,Huber W,Bauer K,Suesal C,Mytilineos J,Melk A,Conradt C,Opelz G. 2001. Association of elevated blood levels of pentachlorophenol (PCP) with cellular and humoral immunodeficiencies. Arch Environ Health 56: 77-83. – reference: Du P,Kibbe WA,Lin SM. 2008. Lumi: A pipeline for processing Illumina microarray. Bioinformatics 24: 1547-1548. – reference: Baker EJ,Ichiki AT,Day NE,Andrews RB,Bamberger EG,Lozzio CB. 2001. Simultaneous flow cytometric measurement of K-562 megakaryocytic differentiation and CD56+ large granular lymphocyte cytotoxicity. J Immunol Methods 253: 37-44. – reference: EPH. 1997. Environmental Protection Agency. Notice to manufacturers, producers and registrants of pesticide products. Washington, DC: Environmental Protection Agency. – reference: Du P,Zhang X,Huang CC,Jafari N,Kibbe WA,Hou L,Lin SM. 2010. Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics 11: 587. – reference: Bibikova M,Lin Z,Zhou L,Chudin E,Garcia EW,Wu B,Doucet D,Thomas NJ,Wang Y,Vollmer E,Goldmann T,Seifart C,Jiang W,Barker DL,Chee MS,Floros J,Fan JB. 2006. High-throughput DNA methylation profiling using universal bead arrays. Genome Res 16: 383-393. – reference: Huang D,Zhang Y,Qi Y,Chen C,Ji W. 2008. Global DNA hypomethylation, rather than reactive oxygen species (ROS), a potential facilitator of cadmium-stimulated K562 cell proliferation. Toxicol Lett 179: 43-47. – reference: Mahajan R,Blair A,Lynch CF,Schroeder P,Hoppin JA,Sandler DP,Alavanja MC. 2006. Fonofos exposure and cancer incidence in the agricultural health study. 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SubjectTerms | Bayes Theorem Biological and medical sciences carcinogenesis Cell physiology Cell transformation and carcinogenesis. Action of oncogenes and antioncogenes Cluster Analysis Computational Biology DNA Methylation - drug effects DNA methylation alteration Fundamental and applied biological sciences. Psychology Genetics of eukaryotes. Biological and molecular evolution Humans In Vitro Techniques K562 Cells Medical sciences Molecular and cellular biology pesticide exposure Pesticides - toxicity Principal Component Analysis Sequence Analysis, DNA Toxicology |
Title | DNA methylation alterations in response to pesticide exposure in vitro |
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