Effects of 2,3′,4,4′,5-pentachlorobiphenyl exposure during pregnancy on DNA methylation in the testis of offspring in the mouse
Jian-Mei Zhang A * , Qiu-Yue Wang A * , Xiao-Ying Han A , Qi-Long He A , Li Liu A , Yong-Tao Zhang A , Xiao-Qian Meng A , Dong Cheng B , Tian-Liang Zhang B and Shu-Zhen Liu
A C
+ Author Affiliations
- Author Affiliations
A Shandong Provincial Key Laboratory of Animal Resistance Biology, College of Life Sciences, Shandong Normal University, Jinan 250014, China.
B Department of Toxicology, Shandong Center for Disease Control and Prevention, Jinan 250014, China.
C Corresponding author. Email: shuzhen26@163.com
Reproduction, Fertility and Development 32(12) 1048-1059 https://doi.org/10.1071/RD19412
Submitted: 29 October 2019 Accepted: 22 May 2020 Published: 31 July 2020
Abstract
Polychlorinated biphenyls (PCBs) are persistent organic pollutants, and the widespread use of PCBs has had adverse effects on human and animal health. This study experiment explored the effects of 2,3′,4,4′,5-pentachlorobiphenyl (PCB118) on the mammalian reproductive system. PCB118 was administered to pregnant mice from 7.5 to 12.5 days of gestation; F1 mice were obtained and the reproductive system of F1 male mice was examined. PCB118 damaged the reproductive system in male F1 mice, as evidenced by negative effects on the testicular organ coefficient (testes weight/bodyweight), a decrease in the diameter of seminiferous tubules and a significant reduction in the anogenital distance in 35-day-old F1 mice. In addition, methylation levels of genomic DNA were reduced, with reductions in the expression of the DNA methyltransferases DNMT1, DNMT3A and DNMT3B, as well as that of the epigenetic regulatory factor ubiquitin like with PHD and ring finger domains 1 (Uhrf1). Together, the results of this study provide compelling evidence that exposure of pregnant mice to PCB118 during primordial germ cell migration in the fetus affects the reproductive system of the offspring and decreases global methylation levels in the testis.
Additional keywords: DNA methyltransferase, PCB118.
References
Ahlborg, U. G., Brouwer, A., Fingerhut, M. A., Jacobson, J. L., Jacobson, S. W., Kennedy, S. W., Kettrup, A. A. F., Koeman, J. H., Poiger, H., and Rappe, C. (1992). Impact of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls on human and environmental health, with special emphasis on application of the toxic equivalency factor concept. Eur. J. Pharmacol. 228, 179–199.| 1335882PubMed |
Ambeskovic, M., Roseboom, T. J., and Metz, G. A. S. (2017). Transgenerational effects of early environmental insults on aging and disease incidence. Neurosci. Biobehav. Rev. , .
| Transgenerational effects of early environmental insults on aging and disease incidence.Crossref | GoogleScholarGoogle Scholar | 28807754PubMed |
Baccarelli, A., and Bollati, V. (2009). Epigenetics and environmental chemicals. Curr. Opin. Pediatr. 21, 243–251.
| Epigenetics and environmental chemicals.Crossref | GoogleScholarGoogle Scholar | 19663042PubMed |
Battershill, J. M. (1994). Review of the safety assessment of polychlorinated biphenyls (PCBs) with particular reference to reproductive toxicity. Hum. Exp. Toxicol. 13, 581–597.
| Review of the safety assessment of polychlorinated biphenyls (PCBs) with particular reference to reproductive toxicity.Crossref | GoogleScholarGoogle Scholar | 7986570PubMed |
Berg, V., Lyche, J. L., Gutleb, A. C., Lie, E., Skaare, J. U., Aleksandersen, M., and Ropstad, E. (2010). Distribution of PCB 118 and PCB 153 and hydroxylated PCB metabolites (OH-CBs) in maternal, fetal and lamb tissues of sheep exposed during gestation and lactation. Chemosphere 80, 1144–1150.
| Distribution of PCB 118 and PCB 153 and hydroxylated PCB metabolites (OH-CBs) in maternal, fetal and lamb tissues of sheep exposed during gestation and lactation.Crossref | GoogleScholarGoogle Scholar | 20605042PubMed |
Bonde, J. P., Flachs, E. M., Rimborg, S., Glazer, C. H., Giwercman, A., Ramlau-Hansen, C. H., Hougaard, K. S., Høyer, B. B., Hærvig, K. K., Petersen, S. B., Rylander, L., Specht, I. O., Toft, G., and Bräuner, E. V. (2016). The epidemiologic evidence linking prenatal and postnatal exposure to endocrine disrupting chemicals with male reproductive disorders: a systematic review and meta-analysis. Hum. Reprod. Update 23, 104–125.
| The epidemiologic evidence linking prenatal and postnatal exposure to endocrine disrupting chemicals with male reproductive disorders: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 27655588PubMed |
Bostick, M., Kim, J. K., Esteve, P. O., Clark, A., Pradhan, S., and Jacobsen, S. E. (2007). UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317, 1760–1764.
| UHRF1 plays a role in maintaining DNA methylation in mammalian cells.Crossref | GoogleScholarGoogle Scholar | 17673620PubMed |
Bush, B., Bennett, A. H., and Snow, J. T. (1986). Polychlorobiphenyl congeners, p,p′-DDE, and sperm function in humans. Arch. Environ. Contam. Toxicol. 15, 333–341.
| Polychlorobiphenyl congeners, p,p′-DDE, and sperm function in humans.Crossref | GoogleScholarGoogle Scholar | 3090950PubMed |
Chen, C. C., Wang, K. Y., and Shen, C. K. (2012). The mammalian de novo DNA methyltransferases DNMT3A and DNMT3B are also DNA 5-hydroxymethylcytosine dehydroxymethylases. J. Biol. Chem. 287, 33116–33121.
| The mammalian de novo DNA methyltransferases DNMT3A and DNMT3B are also DNA 5-hydroxymethylcytosine dehydroxymethylases.Crossref | GoogleScholarGoogle Scholar | 22898819PubMed |
Cui, L. L., Yang, G., Pan, J., and Zhang, C. (2011). Tumor necrosis factor alpha knockout increases fertility of mice. Theriogenology 75, 867–876.
| Tumor necrosis factor alpha knockout increases fertility of mice.Crossref | GoogleScholarGoogle Scholar | 21211832PubMed |
Dada, R., Kumar, M., Jesudasan, R., Fernández, J. L., Gosálvez, J., and Agarwal, A. (2012). Epigenetics and its role in male infertility. J. Assist. Reprod. Genet. 29, 213–223.
| Epigenetics and its role in male infertility.Crossref | GoogleScholarGoogle Scholar | 22290605PubMed |
Dallinga, J. W., Moonen, E. J. C., Dumoulin, J. C. M., Evers, J. L. H., Geraedts, J. P. M., and Kleinjans, J. C. S. (2002). Decreased human semen quality and organochlorine compounds in blood. Hum. Reprod. 17, 1973–1979.
| Decreased human semen quality and organochlorine compounds in blood.Crossref | GoogleScholarGoogle Scholar | 12151423PubMed |
del Mazo, J., Prantera, G., Torres, M., and Ferraro, M. (1994). DNA methylation changes during mouse spermatogenesis. Chromosome Res. 2, 147–152.
| DNA methylation changes during mouse spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 8032673PubMed |
Desaulniers, D., Xiao, G.-h., Lian, H., Feng, Y.-L., Zhu, J., Nakai, J., and Bowers, W. J. (2009). Effects of mixtures of polychlorinated biphenyls, methylmercury, and organochlorine pesticides on hepatic DNA methylation in prepubertal female Sprague-Dawley rats. Int. J. Toxicol. 28, 294–307.
| Effects of mixtures of polychlorinated biphenyls, methylmercury, and organochlorine pesticides on hepatic DNA methylation in prepubertal female Sprague-Dawley rats.Crossref | GoogleScholarGoogle Scholar | 19636072PubMed |
Dickerson, S. M., Cunningham, S. L., and Gore, A. C. (2011). Prenatal PCBs disrupt early neuroendocrine development of the rat hypothalamus. Toxicol App Pharmacol 252, 36–46.
Euling, S., Kimmel, C., and Kimmel, G. (2005). Developmental and reproductive toxicity risk assessment for environmental agents. In ‘Developmental and Reproductive Toxicology’. (Ed. R. D. Hood.) pp. 841–875. (CRC Press: Boca Raton, FL.).
Fängström, B., Hovander, L., Bignert, A., Athanassiadis, I., Linderholm, L., Grandjean, P., Weihe, P., and Bergman, A. (2005). Concentrations of polybrominated diphenyl ethers, polychlonnated biphenyls, and polychlorobiphenylols in serum from pregnant Faroese women and their children 7 years later. Environ. Sci. Technol. 39, 9457–9463.
| Concentrations of polybrominated diphenyl ethers, polychlonnated biphenyls, and polychlorobiphenylols in serum from pregnant Faroese women and their children 7 years later.Crossref | GoogleScholarGoogle Scholar | 16475322PubMed |
Feil, R., and Fraga, M. F. (2012). Epigenetics and the environment: emerging patterns and implications. Nat. Rev. Genet. 13, 97–109.
| Epigenetics and the environment: emerging patterns and implications.Crossref | GoogleScholarGoogle Scholar | 22215131PubMed |
Fowler, P. A., Dora, N. J., McFerran, H., Amezaga, M. R., Miller, D. W., Lea, R. G., Cash, P., McNeilly, A. S., Evans, N. P., and Cotinot, C. (2008). In utero exposure to low doses of environmental pollutants disrupts fetal ovarian development in sheep. Mol. Hum. Reprod. 14, 269–280.
| In utero exposure to low doses of environmental pollutants disrupts fetal ovarian development in sheep.Crossref | GoogleScholarGoogle Scholar | 18436539PubMed |
Fudvoye, J., Bourguignon, J. P., and Parent, A. S. (2014). Endocrine-disrupting chemicals and human growth and maturation: a focus on early critical windows of exposure. Vitam. Horm. 94, 1–25.
| 24388185PubMed |
Gao, Y., Wang, Z. X., Chang, C., Liu, J., Gao, X. Q., and Deng, J. B. (2017). Reproduction toxicity in male mice after nitrite exposure. Acta Anatomica Sinica 48, 576–584.
Grandjean, P., Weihe, P., Nielsen, F., Heinzow, B., Debes, F., and Budtzjørgensen, E. (2012). Neurobehavioral deficits at age 7 years associated with prenatal exposure to toxicants from maternal seafood diet. Neurotoxicol. Teratol. 34, 466–472.
| Neurobehavioral deficits at age 7 years associated with prenatal exposure to toxicants from maternal seafood diet.Crossref | GoogleScholarGoogle Scholar | 22705177PubMed |
Grimm, F. A., Hu, D., Kania-Korwel, I., Lehmler, H.-J., Ludewig, G., Hornbuckle, K. C., Duffel, M. W., Bergman, Å., and Robertson, L. W. (2015). Metabolism and metabolites of polychlorinated biphenyls. Crit. Rev. Toxicol. 45, 245–272.
| Metabolism and metabolites of polychlorinated biphenyls.Crossref | GoogleScholarGoogle Scholar | 25629923PubMed |
Guerrero-Bosagna, C., Settles, M., Lucker, B., and Skinner, M. K. (2010). Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS One 5, e13100.
| Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome.Crossref | GoogleScholarGoogle Scholar | 20927350PubMed |
Guibert, S., Forne, T., and Weber, M. (2012). Global profiling of DNA methylation erasure in mouse primordial germ cells. Genome Res. 22, 633–641.
| Global profiling of DNA methylation erasure in mouse primordial germ cells.Crossref | GoogleScholarGoogle Scholar | 22357612PubMed |
Hajkova, P., Erhardt, S., Lane, N., Haaf, T., El-Maarri, O., Reik, W., Walter, J. r., and Surani, M. A. (2002). Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev. 117, 15–23.
| Epigenetic reprogramming in mouse primordial germ cells.Crossref | GoogleScholarGoogle Scholar | 12204247PubMed |
Hartmann, S., Bergmann, M., Bohle, R. M., Weidner, W., and Steger, K. (2006). Genetic imprinting during impaired spermatogenesis. Mol. Hum. Reprod. 12, 407–411.
| Genetic imprinting during impaired spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 16608903PubMed |
Hashimoto, H., Horton, J. R., Zhang, X., Bostick, M., Jacobsen, S. E., and Cheng, X. (2008). The SRA domain of UHRF1 flips 5-methylcytosine out of the DNA helix. Nature 455, 826–829.
| The SRA domain of UHRF1 flips 5-methylcytosine out of the DNA helix.Crossref | GoogleScholarGoogle Scholar | 18772888PubMed |
Hata, K., Okano, M., Lei, H., and Li, E. (2002). Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129, 1983–1993.
| 11934864PubMed |
Hauser, R., Chen, Z., Pothier, L., Ryan, L., and Altshul, L. (2003). The relationship between human semen parameters and environmental exposure to polychlorinated biphenyls and p,p′-DDE. Environ. Health Perspect. 111, 1505–1511.
| The relationship between human semen parameters and environmental exposure to polychlorinated biphenyls and p,p′-DDE.Crossref | GoogleScholarGoogle Scholar | 12948891PubMed |
He, Q. L., Wei, X. Y., Han, X. Y., Zhou, Q., Wang, H. Q., Ding, N. Z., Meng, X. Q., Schatten, H., Sun, Q. Y., and Liu, S. Z. (2019). Effects of 2,3′,4,4′5-pentachlorobiphenyl exposure during pregnancy on epigenetic imprinting and maturation of offspring’s oocytes in mice. Arch. Toxicol. 93, 2575–2592.
| Effects of 2,3′,4,4′5-pentachlorobiphenyl exposure during pregnancy on epigenetic imprinting and maturation of offspring’s oocytes in mice.Crossref | GoogleScholarGoogle Scholar | 31388691PubMed |
Heijmans, B. T., Tobi, E. W., Stein, A. D., Putter, H., Blauw, G. J., Susser, E. S., Slagboom, P. E., and Lumey, L. H. (2008). Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl Acad. Sci. U. S. A. 105, 17046–17049.
| 18955703PubMed |
Islam, M. N., Zhu, X. B., Aoyama, M., and Sugita, S. (2010). Histological and morphometric analyses of seasonal testicular variations in the Jungle Crow (Corvus macrorhynchos). Anat Sci Int 85, 121–129.
| 19937424PubMed |
Kato, Y., and Nozaki, M. (2012). Distinct DNA methylation dynamics of spermatogenic cell-specific intronless genes is associated with CpG content. PLoS One 7, e43658.
| Distinct DNA methylation dynamics of spermatogenic cell-specific intronless genes is associated with CpG content.Crossref | GoogleScholarGoogle Scholar | 23251698PubMed |
Kim, K. Y., Kim, D. S., Lee, S. K., Lee, I. K., Kang, J. H., Chang, Y. S., Jacobs, J., David, R., Steffes, M., and Lee, D. H. (2010). Association of low-dose exposure to persistent organic pollutants with global DNA hypomethylation in healthy Koreans. Environ. Health Perspect. 118, 370–374.
| Association of low-dose exposure to persistent organic pollutants with global DNA hypomethylation in healthy Koreans.Crossref | GoogleScholarGoogle Scholar | 20064773PubMed |
Kobayashi, H., Sato, A., Otsu, E., Hiura, H., Tomatsu, C., Utsunomiya, T., Sasaki, H., Yaegashi, N., and Arima, T. (2007). Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum. Mol. Genet. 16, 2542–2551.
| Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients.Crossref | GoogleScholarGoogle Scholar | 17636251PubMed |
Kožul, D., and Romanić, S. H. (2010). Levels and distribution of PCBs and organochlorine pesticides in the air, pine needles, and human milk. Arch. Ind. Hyg. Toxicol. 61, 339–356.
| Levels and distribution of PCBs and organochlorine pesticides in the air, pine needles, and human milk.Crossref | GoogleScholarGoogle Scholar |
Kristensen, S. L., Ramlau-Hansen, C. H. s., Ernst, E., Olsen, S. F., Bonde, J. P., Vested, A., Halldorsson, T. I., Rantakokko, P., Kiviranta, H., and Toft, G. (2016). Prenatal exposure to persistent organochlorine pollutants and female reproductive function in young adulthood. Environ. Int. 92–93, 366–372.
| Prenatal exposure to persistent organochlorine pollutants and female reproductive function in young adulthood.Crossref | GoogleScholarGoogle Scholar | 27132162PubMed |
Kuriyama, S. N., and Chahoud, I. (2004). In utero exposure to low-dose 2,3′,4,4’,5-pentachlorobiphenyl (PCB 118) impairs male fertility and alters neurobehavior in rat offspring. Toxicology 202, 185–197.
| In utero exposure to low-dose 2,3′,4,4’,5-pentachlorobiphenyl (PCB 118) impairs male fertility and alters neurobehavior in rat offspring.Crossref | GoogleScholarGoogle Scholar | 15337582PubMed |
La Rocca, C., and Mantovani, A. (2006). From environment to food: the case of PCB. Ann. Ist. Super. Sanita 42, 410–416.
| 17361063PubMed |
Leeuwen, F., and Malisch, R. (2002). Results of the third round of the WHO-coordinated exposure study on the levels of PCBs, PCDDs and PCDFs in human milk. Organohalogen Comp 56, 311–316.
Li, E., Bestor, T. H., and Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915–926.
| Targeted mutation of the DNA methyltransferase gene results in embryonic lethality.Crossref | GoogleScholarGoogle Scholar | 1606615PubMed |
Lignell, S., Aune, M., Darnerud, P. O., Stridsberg, M., Hanberg, A., Larsson, S. C., and Glynn, A. (2016). Maternal body burdens of PCDD/Fs and PBDEs are associated with maternal serum levels of thyroid hormones in early pregnancy: a cross-sectional study. Environ. Health 15, 55.
| Maternal body burdens of PCDD/Fs and PBDEs are associated with maternal serum levels of thyroid hormones in early pregnancy: a cross-sectional study.Crossref | GoogleScholarGoogle Scholar | 27114094PubMed |
Linder, R. E., Gaines, T. B., and Kimbrough, R. D. (1974). The effect of polychlorinated biphenyls on rat reproduction. Food Cosmet. Toxicol. 12, 63–77.
| The effect of polychlorinated biphenyls on rat reproduction.Crossref | GoogleScholarGoogle Scholar | 4218577PubMed |
Margot, J. B., Cardoso, M. C., and Leonhardt, H. (2001). Mammalian DNA methyltransferases show different subnuclear distributions. J. Cell. Biochem. 83, 373–379.
| Mammalian DNA methyltransferases show different subnuclear distributions.Crossref | GoogleScholarGoogle Scholar | 11596106PubMed |
Okano, M., Bell, D. W., Haber, D. A., and Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247–257.
| DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development.Crossref | GoogleScholarGoogle Scholar | 10555141PubMed |
Omisanjo, O. A., Biermann, K., Hartmann, S., Heukamp, L. C., Sonnack, V., Hild, A., Brehm, R., Bergmann, M., Weidner, W., and Steger, K. (2007). DNMT1 and HDAC1 gene expression in impaired spermatogenesis and testicular cancer. Histochem. Cell Biol. 127, 175–181.
| DNMT1 and HDAC1 gene expression in impaired spermatogenesis and testicular cancer.Crossref | GoogleScholarGoogle Scholar | 16960727PubMed |
Park, J. S., Bergman, K., Linderholm, L., Athanasiadou, M., Kocan, A., Petrik, J., Drobna, B., Trnovec, T., Charles, M. J., and Hertz-Picciotto, I. (2008). Placental transfer of polychlorinated biphenyls, their hydroxylated metabolites and pentachlorophenol in pregnant women from eastern Slovakia. Chemosphere 70, 1676–1684.
| Placental transfer of polychlorinated biphenyls, their hydroxylated metabolites and pentachlorophenol in pregnant women from eastern Slovakia.Crossref | GoogleScholarGoogle Scholar | 17764717PubMed |
Raman, R., and Narayan, G. (1995). 5-Aza deoxycytidine-induced inhibition of differentiation of spermatogonia into spermatocytes in the mouse. Mol. Reprod. Dev. 42, 284–290.
| 5-Aza deoxycytidine-induced inhibition of differentiation of spermatogonia into spermatocytes in the mouse.Crossref | GoogleScholarGoogle Scholar | 8579841PubMed |
Reichard, J. F., Schnekenburger, M., and Puga, A. (2007). Long term low-dose arsenic exposure induces loss of DNA methylation. Biochem. Biophys. Res. Commun. 352, 188–192.
| Long term low-dose arsenic exposure induces loss of DNA methylation.Crossref | GoogleScholarGoogle Scholar | 17107663PubMed |
Santos, F., Hendrich, B., Reik, W., and Dean, W. (2002). Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev. Biol. 241, 172–182.
| Dynamic reprogramming of DNA methylation in the early mouse embryo.Crossref | GoogleScholarGoogle Scholar | 11784103PubMed |
Schantz, S. L., Widholm, J. J., and Rice, D. C. (2003). Effects of PCB exposure on neuropsychological function in children. Environ. Health Perspect. 111, 357–376.
| Effects of PCB exposure on neuropsychological function in children.Crossref | GoogleScholarGoogle Scholar | 12611666PubMed |
Schübeler, D. (2015). Function and information content of DNA methylation. Nature 517, 321–326.
| Function and information content of DNA methylation.Crossref | GoogleScholarGoogle Scholar | 25592537PubMed |
Soechitram, S. D., Athanasiadou, M., Hovander, L., Bergman, Å., and Sauer, P. J. J. (2004). Fetal exposure to PCBs and their hydroxylated metabolites in a Dutch cohort. Environ. Health Perspect. 112, 1208–1212.
| Fetal exposure to PCBs and their hydroxylated metabolites in a Dutch cohort.Crossref | GoogleScholarGoogle Scholar | 15289169PubMed |
Song, Y., and Yang, L. (2018). Transgenerational impaired spermatogenesis with sperm H19 and Gtl2 hypomethylation induced by the endocrine disruptor p,p′-DDE. Toxicol. Lett. 297, 34–41.
| Transgenerational impaired spermatogenesis with sperm H19 and Gtl2 hypomethylation induced by the endocrine disruptor p,p′-DDE.Crossref | GoogleScholarGoogle Scholar | 30153481PubMed |
Song, N., Endo, D., Song, B., Shibata, Y., and Koji, T. (2016). 5-Aza-2′-deoxycytidine impairs mouse spermatogenesis at multiple stages through different usage of DNA methyltransferases. Toxicology 361–362, 62–72.
| 5-Aza-2′-deoxycytidine impairs mouse spermatogenesis at multiple stages through different usage of DNA methyltransferases.Crossref | GoogleScholarGoogle Scholar | 27396502PubMed |
Spada, F., Haemmer, A., Kuch, D., Rothbauer, U., Schermelleh, L., Kremmer, E., Carell, T., Langst, G., and Leonhardt, H. (2007). DNMT1 but not its interaction with the replication machinery is required for maintenance of DNA methylation in human cells. J. Cell Biol. 176, 565–571.
| DNMT1 but not its interaction with the replication machinery is required for maintenance of DNA methylation in human cells.Crossref | GoogleScholarGoogle Scholar | 17312023PubMed |
Subach, O. M., Maltseva, D. V., Shastry, A., Kolbanovskiy, A., Klimasauskas, S., Geacintov, N. E., and Gromova, E. S. (2007). The stereochemistry of benzo[a]pyrene-2′-deoxyguanosine adducts affects DNA methylation by SssI and HhaI DNA methyltransferases. FEBS J. 274, 2121–2134.
| The stereochemistry of benzo[a]pyrene-2′-deoxyguanosine adducts affects DNA methylation by SssI and HhaI DNA methyltransferases.Crossref | GoogleScholarGoogle Scholar | 17388812PubMed |
Sun, S. J., Kayama, F., Zhao, J.-H., Ge, J., Yang, Y.-X., Fukatsu, H., Iida, T., Terada, M., and Liu, D.-W. (2011). Longitudinal increases in PCDD/F and dl-PCB concentrations in human milk in northern China. Chemosphere 85, 448–453.
| Longitudinal increases in PCDD/F and dl-PCB concentrations in human milk in northern China.Crossref | GoogleScholarGoogle Scholar | 21890171PubMed |
Takemura, N., Miki, K., and Kosuge, T. (2016). New portal-superior mesenteric vein reconstructions using first jejunal vein flap in pancreaticoduodenectomy. World J. Surg. 40, 1462–1466.
| New portal-superior mesenteric vein reconstructions using first jejunal vein flap in pancreaticoduodenectomy.Crossref | GoogleScholarGoogle Scholar | 26801505PubMed |
Tang, J. M., Li, W., Xie, Y.-C., Guo, H.-W., Cheng, P., Chen, H.-H., Zheng, X.-Q., Jiang, L., Cui, D., and Liu, Y. (2013). Morphological and functional deterioration of the rat thyroid following chronic exposure to low-dose PCB118. Exp. Toxicol. Pathol. 65, 989–994.
| Morphological and functional deterioration of the rat thyroid following chronic exposure to low-dose PCB118.Crossref | GoogleScholarGoogle Scholar | 23557935PubMed |
Wang, X., Gong, P., Sheng, J., Joswiak, D. R., and Yao, T. (2015). Long-range atmospheric transport of particulate polycyclic aromatic hydrocarbons and the incursion of aerosols to the southeast Tibetan Plateau. Atmos. Environ. 115, 124–131.
| Long-range atmospheric transport of particulate polycyclic aromatic hydrocarbons and the incursion of aerosols to the southeast Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar |
Xu, C., Chai, J., and Qian, Y. (2013). Effect of in utero and lactational exposure to a binary mixture of 3,3′,4,4′,5-pentachlorobiphenyl (PCB126) and 2,3′,4,4′,5-pentachlorobiphenyl (PCB118) on reproductive function in male rat offsprings. Wei Sheng Yen Chiu 42, 758–763.
| 24218881PubMed |
Zhang, Y., Sun, X., Zhang, L., and Zhang, W. (2017). Testicular Dnmt3 expression and global DNA methylation are down-regulated by gonadotropin releasing hormones in the ricefield eel Monopterus albus. Sci. Rep. 7, 43158.
| Testicular Dnmt3 expression and global DNA methylation are down-regulated by gonadotropin releasing hormones in the ricefield eel Monopterus albus.Crossref | GoogleScholarGoogle Scholar | 28225069PubMed |
Zong, G., Valvi, D., Coull, B., Goen, T., Hu, F. B., Nielsen, F., Grandjean, P., and Sun, Q. (2018). Persistent organic pollutants and risk of type 2 diabetes: a prospective investigation among middle-aged women in Nurses’ Health Study II. Environ. Int. 114, 334–342.
| Persistent organic pollutants and risk of type 2 diabetes: a prospective investigation among middle-aged women in Nurses’ Health Study II.Crossref | GoogleScholarGoogle Scholar | 29477570PubMed |
