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Anway MD, Cupp AS, Uzumcu M, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science. 2005;308:1466\u20139. https:\/\/doi.org\/10.1126\/science.1108190.","DOI":"10.1126\/science.1108190"},{"key":"2","doi-asserted-by":"publisher","unstructured":"2. Barouki R, Melen E, Herceg Z, Beckers J, Chen J, Karagas M, et al. Epigenetics as a mechanism linking developmental exposures to long-term toxicity. Environ Int. 2018;114:77\u201386. https:\/\/doi.org\/10.1016\/j.envint.2018.02.014.","DOI":"10.1016\/j.envint.2018.02.014"},{"key":"3","doi-asserted-by":"publisher","unstructured":"3. Cavalli G, Heard E. Advances in epigenetics link genetics to the environment and disease. Nature. 2019;571:489\u201399. https:\/\/doi.org\/10.1038\/s41586-019-1411-0.","DOI":"10.1038\/s41586-019-1411-0"},{"key":"4","doi-asserted-by":"publisher","unstructured":"4. Radford EJ, Ito M, Shi H, Corish JA, Yamazawa K, Isganaitis E, et al. In utero effects. 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Emerging evidence that the mammalian sperm epigenome serves as a template for embryo development. Nat Commun. 2023;14:2142. https:\/\/doi.org\/10.1038\/s41467-023-37820-2.","DOI":"10.1038\/s41467-023-37820-2"},{"key":"8","doi-asserted-by":"publisher","unstructured":"8. Wang S, Wu J, Chen Z, Wu W, Lu L, Cheng Y, et al. DNA methylation reprogramming mediates transgenerational diabetogenic effect induced by early-life p,p\u2032-DDE exposure. Chemosphere. 2024;349:140907. https:\/\/doi.org\/10.1016\/j.chemosphere.2023.140907.","DOI":"10.1016\/j.chemosphere.2023.140907"},{"key":"9","doi-asserted-by":"publisher","unstructured":"9. Hughes MF, Beck BD, Chen Y, Lewis AS, Thomas DJ. Arsenic exposure and toxicology: a historical perspective. Toxicol Sci. 2011;123:305\u201332. https:\/\/doi.org\/10.1093\/toxsci\/kfr184.","DOI":"10.1093\/toxsci\/kfr184"},{"key":"10","doi-asserted-by":"publisher","unstructured":"10. Young JL, Cai L, States JC. Impact of prenatal arsenic exposure on chronic adult diseases. Syst Biol Reprod Med. 2018;64:469\u201383. https:\/\/doi.org\/10.1080\/19396368.2018.1480076.","DOI":"10.1080\/19396368.2018.1480076"},{"key":"11","doi-asserted-by":"publisher","unstructured":"11. Martinez VD, Lam WL. Health Effects Associated With Pre- and Perinatal Exposure to Arsenic. Front Genet. 2021;12:664717. https:\/\/doi.org\/10.3389\/fgene.2021.664717.","DOI":"10.3389\/fgene.2021.664717"},{"key":"12","doi-asserted-by":"publisher","unstructured":"12. Smith AH, Marshall G, Yuan Y, Ferreccio C, Liaw J, von Ehrenstein O, et al. Increased mortality from lung cancer and bronchiectasis in young adults after exposure to arsenic in utero and in early childhood. Environ Health Perspect. 2006;114:1293\u20136. https:\/\/doi.org\/10.1289\/ehp.8832.","DOI":"10.1289\/ehp.8832"},{"key":"13","doi-asserted-by":"publisher","unstructured":"13. Smith AH, Marshall G, Liaw J, Yuan Y, Ferreccio C, Steinmaus C. Mortality in young adults following in utero and childhood exposure to arsenic in drinking water. Environ Health Perspect. 2012;120:1527\u201331. https:\/\/doi.org\/10.1289\/ehp.1104867.","DOI":"10.1289\/ehp.1104867"},{"key":"14","doi-asserted-by":"publisher","unstructured":"14. Nohara K, Okamura K, Suzuki T, Murai H, Ito T, Shinjo K, et al. Augmenting effects of gestational arsenite exposure of C3H mice on the hepatic tumors of the F(2) male offspring via the F(1) male offspring. J Appl Toxicol. 2016;36:105\u201312. https:\/\/doi.org\/10.1002\/jat.3149.","DOI":"10.1002\/jat.3149"},{"key":"15","doi-asserted-by":"publisher","unstructured":"15. Nohara K, Nakabayashi K, Okamura K, Suzuki T, Suzuki S, Hata K. Gestational arsenic exposure induces site-specific DNA hypomethylation in active retrotransposon subfamilies in offspring sperm in mice. 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A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell. 2008;31:785\u201399. https:\/\/doi.org\/10.1016\/j.molcel.2008.09.003.","DOI":"10.1016\/j.molcel.2008.09.003"},{"key":"37","doi-asserted-by":"publisher","unstructured":"37. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 2008;22:908\u201317. https:\/\/doi.org\/10.1101\/gad.1640708.","DOI":"10.1101\/gad.1640708"},{"key":"38","doi-asserted-by":"publisher","unstructured":"38. Inoue K, Ichiyanagi K, Fukuda K, Glinka M, Sasaki H. Switching of dominant retrotransposon silencing strategies from posttranscriptional to transcriptional mechanisms during male germ-cell development in mice. PLoS Genet. 2017;13:e1006926. https:\/\/doi.org\/10.1371\/journal.pgen.1006926.","DOI":"10.1371\/journal.pgen.1006926"},{"key":"39","doi-asserted-by":"publisher","unstructured":"39. Molaro A, Falciatori I, Hodges E, Aravin AA, Marran K, Rafii S, et al. Two waves of de novo methylation during mouse germ cell development. Genes Dev. 2014;28:1544\u20139. https:\/\/doi.org\/10.1101\/gad.244350.114.","DOI":"10.1101\/gad.244350.114"},{"key":"40","doi-asserted-by":"publisher","unstructured":"40. Waalkes MP, Liu J, Ward JM, et al. Transplacental carcinogenicity of inorganic arsenic in mice. Toxicol Appl Pharmacol. 2003;186:7\u201317. https:\/\/doi.org\/10.1016\/S0041-008X(02)00022-4.","DOI":"10.1016\/S0041-008X(02)00022-4"},{"key":"41","doi-asserted-by":"crossref","unstructured":"41. Li S, Garrett-Bakelman FE, Chung SS, Sanders MA, Hricik T, Rapaport F, et al. An optimized algorithm for detecting and annotating regional differential methylation. 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