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Research Paper

Epigenome-wide association studies of occupational exposure to benzene and formaldehyde

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Pages 2259-2277 | Received 25 Feb 2022, Accepted 17 Aug 2022, Published online: 25 Aug 2022

References

  • Kim KH, Jahan SA, Lee JT. Exposure to formaldehyde and its potential human health hazards. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2011;29:277–299.
  • Wallace LA. Major sources of benzene exposure. Environ Health Perspect. 1989;82:165–169.
  • Occupational Safety and Health Administration. Occupational exposure to formaldehyde. Federal Regulation. 1992.
  • Occupational Safety and Health Administration. Occupational exposure to benzene. Federal Regulation. 1987.
  • Weisel CP. Benzene exposure: an overview of monitoring methods and their findings. Chem Biol Interact. 2010;184:58–66.
  • Tang X, Bai Y, Duong A, et al. Formaldehyde in China: production, consumption, exposure levels, and health effects. Environ Int. 2009;35:1210–1224.
  • Zhang L, Steinmaus C, Eastmond DA, et al. Formaldehyde exposure and leukemia: a new meta-analysis and potential mechanisms. Mutat Res. 2009;681:150–168.
  • IARC. Formaldehyde, 2-butoxyethanol and 1-tert-butoxypropan-2-ol. IARC Monogr Eval Carcinog Risks Hum. 2006;88:1–478.
  • Stewart PA, Cubit DA, Blair A. Formaldehyde levels in seven industries. Appl Ind Hyg. 1987;2:231–236.
  • Benzene IARC. IARC monographs on the evaluation of carcinogenic risks to humans. Vol. 120. Lyons: France: International Agency for Research on Cancer; 2018.
  • Hayes RB, Songnian Y, Dosemeci M, et al. Benzene and lymphohematopoietic malignancies in humans. Am J Ind Med. 2001;40:117–126.
  • IARC. A review of human carcinogens – part F: chemical agents and related occupations, IARC monographs on the evaluation of carcinogenic risks to humans. Lyons: France: International Agency for Research on Cancer; 2012.
  • McHale CM, Zhang L, Smith MT. Current understanding of the mechanism of benzene-induced leukemia in humans: implications for risk assessment. Carcinogenesis. 2012;33:240–252.
  • National Toxicology Program. Report on carcinogens, fourteenth edition;https://ntp.niehs.nih.gov/go/roc14. U.S. Department of Health and Human Services; Research Triangle Park, NC; U.S., 2016. Accessed November 9, 2021.
  • Zhang L. Formaldehyde: exposure, toxicity and health effects. London, United Kingdom: Royal Society of Chemistry; 2018.
  • Smith MT, Guyton KZ, Gibbons CF, et al. Key characteristics of carcinogens as a basis for organizing data on mechanisms of carcinogenesis. Environ Health Perspect. 2016;124:713–721.
  • Chappell G, Pogribny IP, Guyton KZ, et al. Epigenetic alterations induced by genotoxic occupational and environmental human chemical carcinogens: a systematic literature review. Mutat Res Rev Mutat Res. 2016;768:27–45.
  • Bollati V, Baccarelli A, Hou L, et al. Changes in DNA methylation patterns in subjects exposed to low-dose benzene. Cancer Res. 2007;67:876–880.
  • Fustinoni S, Rossella F, Polledri E, et al. Global DNA methylation and low-level exposure to benzene. Med Lav. 2012;103:84–95.
  • Seow WJ, Pesatori AC, Dimont E, et al. Urinary benzene biomarkers and DNA methylation in Bulgarian petrochemical workers: study findings and comparison of linear and beta regression models. PLoS One. 2012;7:e50471.
  • Li J, Zhang X, He Z, et al. MGMT hypomethylation is associated with DNA damage in workers exposed to low-dose benzene. Biomarkers. 2017;22:470–475.
  • Jimenez-Garza O, Guo L, Byun HM, et al. Promoter methylation status in genes related with inflammation, nitrosative stress and xenobiotic metabolism in low-level benzene exposure: searching for biomarkers of oncogenesis. Food Chem Toxicol. 2017;109:669–676.
  • Zhang GH, Lu Y, Ji BQ, et al. Do mutations in DNMT3A/3B affect global DNA hypomethylation among benzene-exposed workers in Southeast China?: effects of mutations in DNMT3A/3B on global DNA hypomethylation. Environ Mol Mutagen. 2017;58:678–687.
  • Agency for Toxic Substances and Disease Registry (ATSDR). Toxicological profile for benzene. Atlanta: GA: U.S. Department of Health and Human Services, Public Health Service; 2007.
  • Kalasz H. Biological role of formaldehyde, and cycles related to methylation, demethylation, and formaldehyde production. Mini Rev Med Chem. 2003;3:175–192.
  • Liu Q, Yang L, Gong C, et al. Effects of long-term low-dose formaldehyde exposure on global genomic hypomethylation in 16HBE cells. Toxicol Lett. 2011;205:235–240.
  • Barbosa E, Dos Santos ALA, Peteffi GP, et al. Increase of global DNA methylation patterns in beauty salon workers exposed to low levels of formaldehyde. Environ Sci Pollut Res Int. 2019;26:1304–1314.
  • Bassig BA, Zhang L, Vermeulen R, et al. Comparison of hematological alterations and markers of B-cell activation in workers exposed to benzene, formaldehyde and trichloroethylene. Carcinogenesis. 2016;37:692–700.
  • Hosgood HDs3rd, Zhang L, Tang X, et al. Occupational exposure to formaldehyde and alterations in lymphocyte subsets. Am J Ind Med. 2013;56:252–257.
  • Lan Q, Zhang L, Li G, et al. Hematotoxicity in workers exposed to low levels of benzene. Science. 2004;306:1774–1776.
  • Zhang L, Tang X, Rothman N, et al. Occupational exposure to formaldehyde, hematotoxicity, and leukemia-specific chromosome changes in cultured myeloid progenitor cells. Cancer Epidemiol Biomarkers Prev. 2010;19:80–88.
  • McHale CM, Zhang L, Lan Q, et al. Global gene expression profiling of a population exposed to a range of benzene levels. Environ Health Perspect. 2011;119:628–634.
  • Schiffman C, McHale CM, Hubbard AE, et al. Identification of gene expression predictors of occupational benzene exposure. PLoS One. 2018;13:e0205427.
  • Thomas R, Hubbard AE, McHale CM, et al. Characterization of changes in gene expression and biochemical pathways at low levels of benzene exposure. PLoS One. 2014;9:e91828.
  • Thomas R, McHale CM, Lan Q, et al. Global gene expression response of a population exposed to benzene: a pilot study exploring the use of RNA-sequencing technology. Environ Mol Mutagen. 2013;54:566–573.
  • Chung FF, Herceg Z. The promises and challenges of toxico-epigenomics: environmental chemicals and their impacts on the epigenome. Environ Health Perspect. 2020;128:15001.
  • Teschendorff AE, Gao Y, Jones A, et al. DNA methylation outliers in normal breast tissue identify field defects that are enriched in cancer. Nat Commun. 2016;7:10478.
  • Paul DS, Teschendorff AE, Dang MA, et al. Increased DNA methylation variability in type 1 diabetes across three immune effector cell types. Nat Commun. 2016;7:13555.
  • Clifford RL, Fishbane N, Patel J, et al. Altered DNA methylation is associated with aberrant gene expression in parenchymal but not airway fibroblasts isolated from individuals with COPD. Clin Epigenetics. 2018;10:32.
  • Morris TJ, Beck S. Analysis pipelines and packages for infinium humanMethylation450 beadchip (450k) data. Methods. 2015;72:3–8.
  • Aryee MJ, Jaffe AE, Corrada-Bravo H, et al. Minfi: a flexible and comprehensive bioconductor package for the analysis of Infinium DNA methylation microarrays. Vol. 30. Oxford: England: Bioinformatics; 2014. p. 1363–1369.
  • Gentleman RC, Carey VJ, Bates DM, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5:R80.
  • Houseman EA, Accomando WP, Koestler DC, et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics. 2012;13:86.
  • Touleimat N, Tost J. Complete pipeline for Infinium((R)) human methylation 450K beadchip data processing using subset quantile normalization for accurate DNA methylation estimation. Epigenomics. 2012;4:325–341.
  • Zhou W, Laird PW, Shen H. Comprehensive characterization, annotation and innovative use of Infinium DNA methylation BeadChip probes. Nucleic Acids Res. 2017;45:e22.
  • Leek JT, Johnson WE, Parker HS, et al. The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Vol. 28. Oxford: England: Bioinformatics; 2012. p. 882–883.
  • Ritchie ME, Phipson B, Wu D, et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43:e47.
  • Phipson B, Maksimovic J, Oshlack A. missMethyl: an R package for analyzing data from Illumina’s HUMANMETHYLATION450 platform. Vol. 32. Oxford: England: Bioinformatics; 2016. p. 286–288.
  • Phipson B, Oshlack A. DiffVar: a new method for detecting differential variability with application to methylation in cancer and aging. Genome Biol. 2014;15:465.
  • Phipson B, Lee S, Majewski IJ, et al. Robust hyperparameter estimation protects against hypervariable genes and improves power to detect differential expression. Ann Appl Stat. 2016;10:946–963.
  • van Iterson M, Cats D, Hop P, et al. omicsPrint: detection of data linkage errors in multiple omics studies. Bioinformatics. 2018;34:2142–2143.
  • Devlin B, Roeder K. Genomic control for association studies. Biometrics. 1999;55:997–1004.
  • Jaffe AE, Murakami P, Lee H, et al. Bump hunting to identify differentially methylated regions in epigenetic epidemiology studies. Int J Epidemiol. 2012;41:200–209.
  • Kuleshov MV, Jones MR, Rouillard AD, et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 2016;44:W90–7.
  • Wu MF, Chen ST, Yang AH, et al. CLEC5A is critical for dengue virus-induced inflammasome activation in human macrophages. Blood. 2013;121:95–106.
  • Geeleher P, Hartnett L, Egan LJ, et al. Gene-set analysis is severely biased when applied to genome-wide methylation data. Bioinformatics. 2013;29:1851–1857.
  • Kim S, Vermeulen R, Waidyanatha S, et al. Using urinary biomarkers to elucidate dose-related patterns of human benzene metabolism. Carcinogenesis. 2006;27:772–781.
  • Steinmaus C, Smith AH, Jones RM, et al. Meta-analysis of benzene exposure and non-Hodgkin lymphoma: biases could mask an important association. Occup Environ Med. 2008;65:371–378.
  • Hansen KD, Timp W, Bravo HC, et al. Increased methylation variation in epigenetic domains across cancer types. Nat Genet. 2011;43:768–775.
  • Teschendorff AE, Widschwendter M. Differential variability improves the identification of cancer risk markers in DNA methylation studies profiling precursor cancer lesions. Bioinformatics. 2012;28:1487–1494.
  • Webster AP, Plant D, Ecker S, et al. Increased DNA methylation variability in rheumatoid arthritis-discordant monozygotic twins. Genome Med. 2018;10:64.
  • Phillips RV, Rieswijk L, Hubbard AE, et al. Human exposure to trichloroethylene is associated with increased variability of blood DNA methylation that is enriched in genes and pathways related to autoimmune disease and cancer. Epigenetics. 2019;14:1112–1124.
  • McHale CM, Zhang L, Lan Q, et al. Changes in the peripheral blood transcriptome associated with occupational benzene exposure identified by cross-comparison on two microarray platforms. Genomics. 2009;93:343–349.
  • Hou Y, Ding M, Wang C, et al. TRIM11 promotes lymphomas by activating the beta-catenin signaling and Axin1 ubiquitination degradation. Exp Cell Res. 2020;387:111750.
  • Agarwal NK, Zhu X, Gagea M, et al. PHLPP2 suppresses the NF-kappaB pathway by inactivating IKKbeta kinase. Oncotarget. 2014;5:815–823.
  • Yan Y, Hanse EA, Stedman K, et al. Transcription factor C/EBP-beta induces tumor-suppressor phosphatase PHLPP2 through repression of the miR-17-92 cluster in differentiating AML cells. Cell Death Differ. 2016;23:1232–1242.
  • Kuo YH, Zaidi SK, Gornostaeva S, et al. Runx2 induces acute myeloid leukemia in cooperation with Cbfbeta-SMMHC in mice. Blood. 2009;113:3323–3332.
  • Zolghadr F, Sadeghizadeh M, Amirizadeh N, et al. How benzene and its metabolites affect human marrow derived mesenchymal stem cells. Toxicol Lett. 2012;214:145–153.
  • Hartmann L, Dutta S, Opatz S, et al. ZBTB7A mutations in acute myeloid leukaemia with t(8;21) translocation. Nat Commun. 2016;7:11733.
  • Redondo Monte E, Wilding A, Leubolt G, et al. ZBTB7A prevents RUNX1-RUNX1T1-dependent clonal expansion of human hematopoietic stem and progenitor cells. Oncogene. 2020;39:3195–3205.
  • Herzig S, Shaw RJ. AMPK: guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol. 2018;19:121–135.
  • Mihaylova MM, Shaw RJ. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol. 2011;13:1016–1023.
  • Greer EL, Dowlatshahi D, Banko MR, et al. An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol. 2007;17:1646–1656.
  • Templeman NM, Murphy CT. Regulation of reproduction and longevity by nutrient-sensing pathways. J Cell Biol. 2018;217:93–106.
  • Jacquel A, Luciano F, Robert G, et al. Implication and regulation of AMPK during physiological and pathological myeloid differentiation. Int J Mol Sci. 2018;19:2991.
  • Visnjic D, Dembitz V, Lalic H. The role of AMPK/mTOR modulators in the therapy of acute myeloid leukemia. Curr Med Chem. 2019;26:2208–2229.
  • Li Z, Wang C, Zhu J, et al. The possible role of liver kinase B1 in hydroquinone-induced toxicity of murine fetal liver and bone marrow hematopoietic stem cells. Environ Toxicol. 2016;31:830–841.
  • Patterson KI, Brummer T, O’Brien PM, et al. Dual-specificity phosphatases: critical regulators with diverse cellular targets. Biochem J. 2009;418:475–489.
  • Li JP, Yang CY, Chuang HC, et al. The phosphatase JKAP/DUSP22 inhibits T-cell receptor signalling and autoimmunity by inactivating Lck. Nat Commun. 2014;5:3618.
  • Huang CY, Tan TH. DUSPs, to MAP kinases and beyond. Cell Biosci. 2012;2:24.
  • Li JP, Fu YN, Chen YR, et al. JNK pathway-associated phosphatase dephosphorylates focal adhesion kinase and suppresses cell migration. J Biol Chem. 2010;285:5472–5478.
  • Sekine Y, Ikeda O, Hayakawa Y, et al. DUSP22/LMW-DSP2 regulates estrogen receptor-alpha-mediated signaling through dephosphorylation of Ser-118. Oncogene. 2007;26:6038–6049.
  • Sekine Y, Tsuji S, Ikeda O, et al. Regulation of STAT3-mediated signaling by LMW-DSP2. Oncogene. 2006;25:5801–5806.
  • Chen AJ, Zhou G, Juan T, et al. The dual specificity JKAP specifically activates the c-Jun N-terminal kinase pathway. J Biol Chem. 2002;277:36592–36601.
  • Alonso A, Merlo JJ, Na S, et al. Inhibition of T cell antigen receptor signaling by VHR-related MKPX (VHX), a new dual specificity phosphatase related to VH1 related (VHR). J Biol Chem. 2002;277:5524–5528.
  • Chuang HC, Tan TH. MAP4K family kinases and DUSP family phosphatases in t-cell signaling and systemic lupus erythematosus. Cells. 2019;8(11):1433. https://doi.org/10.3390/cells8111433.
  • Lin HP, Ho HM, Chang CW, et al. DUSP22 suppresses prostate cancer proliferation by targeting the EGFR-AR axis. FASEB J. 2019;33:14653–14667.
  • Lim MS, Bailey NG, King RL, et al. Molecular genetics in the diagnosis and biology of lymphoid neoplasms. Am J Clin Pathol. 2019;152:277–301.
  • Parrilla Castellar ER, Jaffe ES, Said JW, et al. ALK-negative anaplastic large cell lymphoma is a genetically heterogeneous disease with widely disparate clinical outcomes. Blood. 2014;124:1473–1480.
  • Boks MP, Houtepen LC, Xu Z, et al. Genetic vulnerability to DUSP22 promoter hypermethylation is involved in the relation between in utero famine exposure and schizophrenia. NPJ Schizophr. 2018;4:16.
  • Mok A, Rhead B, Holingue C, et al. Hypomethylation of CYP2E1 and DUSP22 promoters associated with disease activity and erosive disease among rheumatoid arthritis patients. Arthritis Rheumatol. 2018;70:528–536.
  • Rutten BPF, Vermetten E, Vinkers CH, et al. Longitudinal analyses of the DNA methylome in deployed military servicemen identify susceptibility loci for post-traumatic stress disorder. Mol Psychiatry. 2018;23:1145–1156.
  • Ouyang B, Baxter CS, Lam HM, et al. Hypomethylation of dual specificity phosphatase 22 promoter correlates with duration of service in firefighters and is inducible by low-dose benzo[a]pyrene. J Occup Environ Med. 2012;54:774–780.
  • Miura R, Araki A, Miyashita C, et al. An epigenome-wide study of cord blood DNA methylations in relation to prenatal perfluoroalkyl substance exposure: the Hokkaido study. Environ Int. 2018;115:21–28.
  • Rizzo HE, Escaname EN, Alana NB, et al. Maternal diabetes and obesity influence the fetal epigenome in a largely Hispanic population. Clin Epigenetics. 2020;12:34.
  • Crooks GM, Fuller J, Petersen D, et al. Constitutive HOXA5 expression inhibits erythropoiesis and increases myelopoiesis from human hematopoietic progenitors. Blood. 1999;94:519–528.
  • Fuller JF, McAdara J, Yaron Y, et al. Characterization of HOX gene expression during myelopoiesis: role of HOX A5 in lineage commitment and maturation. Blood. 1999;93:3391–3400.
  • Shah N, Sukumar S. The Hox genes and their roles in oncogenesis. Nat Rev Cancer. 2010;10(5):361–371.
  • Kim SY, Hwang SH, Song EJ, et al. Level of HOXA5 hypermethylation in acute myeloid leukemia is associated with short-term outcome. Korean J Lab Med. 2010;30:469–473.
  • Strathdee G, Holyoake TL, Sim A, et al. Inactivation of HOXA genes by hypermethylation in myeloid and lymphoid malignancy is frequent and associated with poor prognosis. Clin Cancer Res. 2007;13:5048–5055.
  • Nagy A, Osz A, Budczies J, et al. Elevated HOX gene expression in acute myeloid leukemia is associated with NPM1 mutations and poor survival. J Adv Res. 2019;20:105–116.
  • Musialik E, Bujko M, Kober P, et al. Promoter DNA methylation and expression levels of HOXA4, HOXA5 and MEIS1 in acute myeloid leukemia. Mol Med Rep. 2015;11:3948–3954.
  • Godish T. Formaldehyde exposures from tobacco smoke: a review. Am J Public Health. 1989;79:1044–1045.
  • Wallace L, Pellizzari E, Hartwell TD, et al. Exposures to benzene and other volatile compounds from active and passive smoking. Arch Environ Health. 1987;42:272–279.
  • Jacoby M, Gohrbandt S, Clausse V, et al. Interindividual variability and co-regulation of DNA methylation differ among blood cell populations. Epigenetics. 2012;7:1421–1434.
  • Heiss JA, Breitling LP, Lehne B, et al. Training a model for estimating leukocyte composition using whole-blood DNA methylation and cell counts as reference. Epigenomics. 2017;9:13–20.
  • Cardenas A, Allard C, Doyon M, et al. Validation of a DNA methylation reference panel for the estimation of nucleated cells types in cord blood. Epigenetics. 2016;11:773–779.

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