Chromatin modifiers: A new class of pollutants with potential epigenetic effects revealed by in vitro assays and transcriptomic analyses

Toxicology - Tập 484 - Trang 153413 - 2023
Chi Tim Leung1,2, Yi Yang1,3, Ting Fung Chan4, Xiao Lin5, Alice Sze Tsai Wong3, Wing Yee Lui3, Karen Wing Yee Yuen3, Richard Yuen Chong Kong1,2,6, Keng Po Lai1,2,6,7, Rudolf Shiu Sun Wu1,8,6
1Southern Marine Science and Engineering Guangdong Laboratory, Guangzhou, PR China
2Department of Chemistry, City University of Hong Kong, Hong Kong SAR, PR China
3School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, PR China
4School of Life Sciences, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Hong Kong SAR, China
5Department of Psychiatry, Icahn School of Medicine at Mount Sinai, USA
6State Key Laboratory of Marine Pollution, City University of Hong Kong, Hong Kong SAR, PR China
7Key Laboratory of Environmental Pollution and Integrative Omics, Guilin Medical University, Education Department of Guangxi Zhuang Autonomous Region, PR China
8Department of Science and Environmental Studies, The Education University of Hong Kong, Hong Kong SAR, PR China

Tài liệu tham khảo

Andrade, 2006, A dose response study following in utero and lactational exposure to di-(2-ethylhexyl) phthalate (DEHP): Reproductive effects on adult male offspring rats, Toxicology, vol. 228, 85, 10.1016/j.tox.2006.08.020 Anway, 2005, Epigenetic transgenerational actions of endocrine disruptors and male fertility, Science, 308, 1466, 10.1126/science.1108190 Armanios, 2012, The telomere syndromes, Nat. Rev. Genet., vol. 13, 693, 10.1038/nrg3246 Aviv, 2002, Telomeres, sex, reactive oxygen species, and human cardiovascular aging, J. Mol. Med., vol. 80, 689, 10.1007/s00109-002-0377-8 Aydos, 2005, Is telomere length one of the determinants of reproductive life span?, Arch. Gynecol. Obstet., vol. 272, 113, 10.1007/s00404-004-0690-2 Barlas, 2020, Influence of in utero di- n -hexyl phthalate and di-cyclohexyl phthalate exposure on the endocrine glands and T3, T4, and TSH hormone levels of male and female rats: Postnatal outcomes, Toxicol. Ind. Health, vol. 36, 399, 10.1177/0748233720931698 Basini, 2021, Evaluation of triclosan effects on cultured swine luteal cells, Animals, vol. 11, 606, 10.3390/ani11030606 Baumstark-Khan, 2010, Cytotoxicity and genotoxicity reporter systems based on the use of mammalian cells, 113 BenMaamar, 2018, Epigenetic transgenerational inheritance of altered sperm histone retention sites, Sci. Rep., vol. 8, 5308, 10.1038/s41598-018-23612-y Buccione, 1990, Interactions between somatic cells and germ cells throughout mammalian Oogenesis1, Biol. Reprod., vol. 43, 543, 10.1095/biolreprod43.4.543 Cao, 2017, Exposure of pregnant mice to triclosan impairs placental development and nutrient transport, Sci. Rep., vol. 7, 44803, 10.1038/srep44803 Cariati, 2020, Bisphenol A-induced epigenetic changes and its effects on the male reproductive system, Front. Endocrinol. (Lausanne), vol. 11, 10.3389/fendo.2020.00453 Carignan, 2018, Paternal urinary concentrations of organophosphate flame retardant metabolites, fertility measures, and pregnancy outcomes among couples undergoing in vitro fertilization, Environ. Int., vol. 111, 232, 10.1016/j.envint.2017.12.005 Carignan, 2017, Urinary concentrations of organophosphate flame retardant metabolites and pregnancy outcomes among women undergoing in vitro fertilization, Environ. Health Perspect., vol. 125, 10.1289/EHP1021 Chen, 2019, The effects and possible mechanisms of triclosan on steroidogenesis in primary rat granulosa cells, Reprod. Toxicol., vol. 83, 28, 10.1016/j.reprotox.2018.11.001 Crawford, 2012, Disruption of blastocyst implantation by triclosan in mice: Impacts of repeated and acute doses and combination with bisphenol-A, Reprod. Toxicol., vol. 34, 607, 10.1016/j.reprotox.2012.09.008 Delclos, 2009, Overlapping but distinct effects of genistein and ethinyl estradiol (EE2) in female Sprague–Dawley rats in multigenerational reproductive and chronic toxicity studies, Reprod. Toxicol., vol. 27, 117, 10.1016/j.reprotox.2008.12.005 Derouiche, 2015, Developmental exposure to Ethinylestradiol affects transgenerationally sexual behavior and neuroendocrine networks in male mice, Sci. Rep., vol. 5, 17457, 10.1038/srep17457 Derouiche, 2015, Developmental exposure to ethinylestradiol affects reproductive physiology, the GnRH neuroendocrine network and behaviors in female mouse, Front. Neurosci., vol. 9, 10.3389/fnins.2015.00463 Di, 2018, Chronic low-dose exposure of nonylphenol alters energy homeostasis in the reproductive system of female rats, Toxicol. Appl. Pharmacol., vol. 348, 67, 10.1016/j.taap.2018.04.007 Dobrzyńska, 2014, DNA damage in organs of female and male mice exposed to nonylphenol, as a single agent or in combination with ionizing irradiation: a comet assay study, Mutat. Res. Toxicol. Environ. Mutagen., vol. 772, 14, 10.1016/j.mrgentox.2014.07.003 Dobrzyńska, 2012, DNA damage to somatic cells of mice exposed to nonylphenol and to a combination of ionizing radiation and nonylphenol, Rocz. Panstw. Zakl. Hig., vol. 63, 417 Durlinger, 2002, Anti-Müllerian hormone inhibits initiation of primordial follicle growth in the mouse ovary, Endocrinology, vol. 143, 1076, 10.1210/endo.143.3.8691 Findlay, 2010, Estrogen signaling in the regulation of female reproductive functions, Handb. Exp. Pharmacol., 29, 10.1007/978-3-642-02062-9_2 Fitzgerald, 2008, Trophoblast invasion: the role of intracellular cytokine signalling via signal transducer and activator of transcription 3 (STAT3), Hum. Reprod. Update, vol. 14, 335, 10.1093/humupd/dmn010 De La Fuente, 2001, Transcriptional activity of the mouse oocyte genome: companion granulosa cells modulate transcription and chromatin remodeling, Dev. Biol., vol. 229, 224, 10.1006/dbio.2000.9947 Gunjan, 2006, The emergence of regulated histone proteolysis, Curr. Opin. Genet. Dev., vol. 16, 112, 10.1016/j.gde.2006.02.010 Guo, 2019, Role of mTOR Signaling in Female Reproduction, Front. Endocrinol. (Lausanne), vol. 10, 10.3389/fendo.2019.00692 Haggerty, 2021, Reproductive toxicology: pregnancy exposure to endocrine disrupting chemicals: implications for women’s health, Reproduction, vol. 162, F169, 10.1530/REP-21-0051 Hanna, 2009, Telomere length and reproductive aging, Hum. Reprod., vol. 24, 1206, 10.1093/humrep/dep007 Hauer, 2017, Histone degradation in response to DNA damage enhances chromatin dynamics and recombination rates, Nat. Struct. Mol. Biol., vol. 24, 99, 10.1038/nsmb.3347 Hwang, 2011, Gene alterations of ovarian cancer cells expressing estrogen receptors by Estrogen and Bisphenol A using microarray analysis, Lab. Anim. Res., vol. 27, 99, 10.5625/lar.2011.27.2.99 Karpeta, 2016, Different mechanisms of action of 2, 2′, 4, 4′-tetrabromodiphenyl ether (BDE-47) and its metabolites (5-OH-BDE-47 and 6-OH-BDE-47) on cell proliferation in OVCAR-3 ovarian cancer cells and MCF-7 breast cancer cells, J. Appl. Toxicol., vol. 36, 1558, 10.1002/jat.3316 Karpeta, 2014, Different action of 2,2′,4,4′-tetrabromodiphenyl ether (BDE-47) and its hydroxylated metabolites on ERα and ERβ gene and protein expression, Toxicol. Lett., vol. 229, 250, 10.1016/j.toxlet.2014.05.022 Karuputhula, 2013, Oxidative status in granulosa cells of infertile women undergoing IVF, Syst. Biol. Reprod. Med., vol. 59, 91, 10.3109/19396368.2012.743197 Kim, 2020, Histological analysis of reproductive system in low-dose Nonylphenol-treated F1 female mice, Dev. Reprod., vol. 24, 159, 10.12717/DR.2020.24.3.159 Kirigaya, 2015, Developmental effects of ethinylestradiol on reproductive organs of female mice, Vivo, vol. 20, 867 Kojima, 2013, In vitro endocrine disruption potential of organophosphate flame retardants via human nuclear receptors, Toxicology, vol. 314, 76, 10.1016/j.tox.2013.09.004 Kyo, 1999, Estrogen activates telomerase, Cancer Res, vol. 59, 5917 Lai, 2019, Hypoxia causes transgenerational impairment of ovarian development and hatching success in fish, Environ. Sci. Technol., vol. 53, 3917, 10.1021/acs.est.8b07250 Lai, 2016, Hypoxia alters steroidogenesis in female marine medaka through miRNAs regulation, Aquat. Toxicol., vol. 172, 1, 10.1016/j.aquatox.2015.12.012 Leduc, 2012, Leukemia inhibitory factor regulates differentiation of Trophoblastlike BeWo cells through the activation of JAK/STAT and MAPK3/1 MAP kinase-signaling pathways1, Biol. Reprod., vol. 86, 2, 10.1095/biolreprod.111.094334 Lee, 2005, Effect of long-term hormone therapy on telomere length in postmenopausal women, Yonsei Med. J., vol. 46, 471, 10.3349/ymj.2005.46.4.471 Lefèvre, 2021, Polybrominated diphenyl ethers in human follicular fluid dysregulate mural and cumulus granulosa cell gene expression, Endocrinology, vol. 162, 10.1210/endocr/bqab003 Lempradl, 2020, Germ cell-mediated mechanisms of epigenetic inheritance, Semin. Cell Dev. Biol., vol. 97, 116, 10.1016/j.semcdb.2019.07.012 Li, 2021, The use of glutathione to reduce oxidative stress status and its potential for modifying the extracellular matrix organization in cleft lip, Free Radic. Biol. Med., vol. 164, 130, 10.1016/j.freeradbiomed.2020.12.455 Li, 2012, Effects of DEHP on endometrial receptivity and embryo implantation in pregnant mice, J. Hazard. Mater., vol. 241–242, 231, 10.1016/j.jhazmat.2012.09.038 Lister-Shimauchi, 2021, Gametes deficient for Pot1 telomere binding proteins alter levels of telomeric foci for multiple generations, Commun. Biol., vol. 4, 158, 10.1038/s42003-020-01624-7 Liu, 2017, Di (2-ethylhexyl) phthalate exposure impairs meiotic progression and DNA damage repair in fetal mouse oocytes in vitro, Cell Death Dis., vol. 8, 10.1038/cddis.2017.350 Liu, 2021, DEHP exposure to lactating mice affects ovarian hormone production and antral follicle development of offspring, J. Hazard. Mater., vol. 416, 10.1016/j.jhazmat.2021.125862 Li, 2020, Regulation of DNA damage-induced ATM activation by histone modifications, Genome Instab. Dis., vol. 1, 20, 10.1007/s42764-019-00004-8 Mansur, 2018, Corrigendum: Bisphenol-A exposure and gene expression in human luteinized membrana granulosa cells in vitro, Hum. Reprod., vol. 33, 10.1093/humrep/dey068 Matthews, 2012, Transgenerational inheritance of stress pathology, Exp. Neurol., vol. 233, 95, 10.1016/j.expneurol.2011.01.009 Meyer, 2019, Exposure to 17α-ethinyl estradiol during early pregnancy affects fetal growth and survival in mice, Environ. Pollut., vol. 251, 493, 10.1016/j.envpol.2019.04.144 Mukherjee, 2018, Telomere length-dependent transcription and epigenetic modifications in promoters remote from telomere ends, PLoS Genet., vol. 14, 10.1371/journal.pgen.1007782 Mullen, 2008, Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5′ to 3′ and 3′ to 5′, Genes Dev., vol. 22, 50, 10.1101/gad.1622708 Nagao, 2001, Reproductive effects of nonylphenol in rats after gavage administration: a two-generation study, Reprod. Toxicol., vol. 15, 293, 10.1016/S0890-6238(01)00123-X Nakamura, 2015, Effects of maternal and lactational exposure to 2-Hydroxy-4-Methoxybenzone on development and reproductive organs in male and female rat offspring, Birth Defects Res. Part B Dev. Reprod. Toxicol., vol. 104, 35, 10.1002/bdrb.21137 Nilsson, 2015, Environmentally induced epigenetic transgenerational inheritance of reproductive disease1, Biol. Reprod., vol. 93, 6, 10.1095/biolreprod.115.134817 Pastuschek, 2015, Stimulation of the JAK/STAT pathway by LIF and OSM in the human granulosa cell line COV434, J. Reprod. Immunol., vol. 108, 48, 10.1016/j.jri.2015.03.002 Philippat, 2012, Exposure to phthalates and phenols during pregnancy and offspring size at birth, Environ. Health Perspect., vol. 120, 464, 10.1289/ehp.1103634 Philippat, 2011, Maternal exposure to phthalates and phenols and fetal growth among male newborns, Epidemiology, vol. 22, S127, 10.1097/01.ede.0000392058.70591.a3 Pocar, 2017, Maternal exposure to di(2-ethylhexyl)phthalate (DEHP) promotes the transgenerational inheritance of adult-onset reproductive dysfunctions through the female germline in mice, Toxicol. Appl. Pharmacol., vol. 322, 113, 10.1016/j.taap.2017.03.008 Poehlmann, 2005, “rophoblast invasion: tuning through LIF, signalling via Stat3, Placenta, vol. 26, S37, 10.1016/j.placenta.2005.01.007 Rahman, 2020, Multigenerational and transgenerational impact of paternal bisphenol A exposure on male fertility in a mouse model, Hum. Reprod., vol. 35, 1740, 10.1093/humrep/deaa139 Rathore, 2012, Green tea catechin extract in intervention of chronic breast cell carcinogenesis induced by environmental carcinogens, Mol. Carcinog., vol. 51, 280, 10.1002/mc.20844 Rattan, 2018, Di(2-Ethylhexyl) phthalate exposure during prenatal development causes adverse transgenerational effects on female fertility in mice, Toxicol. Sci., vol. 163, 420, 10.1093/toxsci/kfy042 Rattan, 2018, Prenatal exposure to di(2-ethylhexyl) phthalate disrupts ovarian function in a transgenerational manner in female mice, Biol. Reprod., vol. 98, 130, 10.1093/biolre/iox154 Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, vol. 26, 139, 10.1093/bioinformatics/btp616 Santamaria, 2020, Dermal exposure to the UV filter benzophenone-3 during early pregnancy affects fetal growth and sex ratio of the progeny in mice, Arch. Toxicol., vol. 94, 2847, 10.1007/s00204-020-02776-5 Santangeli, 2017, Effects of BPA on female reproductive function: the involvement of epigenetic mechanism, Gen. Comp. Endocrinol., vol. 245, 122, 10.1016/j.ygcen.2016.08.010 Seidel, 2020, Reproductive toxicity of benzophenone-3, Arch. Toxicol., vol. 94, 3593, 10.1007/s00204-020-02865-5 Shi, 2019, Prenatal exposure to Bisphenol A, E, and S induces transgenerational effects on female reproductive functions in mice, Toxicol. Sci., vol. 172, 320, 10.1093/toxsci/kfz124 Shi, 2021, The interference effects of bisphenol A on the synthesis of steroid hormones in human ovarian granulosa cells, Environ. Toxicol., vol. 36, 665, 10.1002/tox.23070 Singh, 2010, Excess histone levels mediate cytotoxicity via multiple mechanisms, Cell Cycle, vol. 9, 4236, 10.4161/cc.9.20.13636 Skinner, 2011, Epigenetic transgenerational actions of endocrine disruptors, Reprod. Toxicol., vol. 31, 337, 10.1016/j.reprotox.2010.10.012 Skvortsova, 2018, Functions and mechanisms of epigenetic inheritance in animals, Nat. Rev. Mol. Cell Biol., vol. 19, 774, 10.1038/s41580-018-0074-2 Song, 2021, Combining metabolomics with bioanalysis methods to investigate the potential toxicity of dihexyl phthalate, Environ. Toxicol., vol. 36, 213, 10.1002/tox.23027 Sun, 2016, Persistent halogenated compounds in fish from rivers in the Pearl River Delta, South China: geographical pattern and implications for anthropogenic effects on the environment, Environ. Res., vol. 146, 371, 10.1016/j.envres.2016.01.021 Sun, 2018, Hexabromocyclododecanes (HBCDs) in fish: Evidence of recent HBCD input into the coastal environment, Mar. Pollut. Bull., vol. 126, 357, 10.1016/j.marpolbul.2017.11.040 Titus, 2013, Impairment of BRCA1-related DNA double-strand break repair leads to ovarian aging in mice and humans, Sci. Transl. Med., vol. 5, 172, 10.1126/scitranslmed.3004925 Toyooka, 2012, Nonylphenol polyethoxylates induce phosphorylation of histone H2AX, Mutat. Res. Toxicol. Environ. Mutagen., vol. 741, 57, 10.1016/j.mrgentox.2011.10.006 Tse, 2016, Hypoxia alters testicular functions of marine medaka through microRNAs regulation, Aquat. Toxicol., vol. 180, 266, 10.1016/j.aquatox.2016.10.007 VonZglinicki, 2003, Replicative senescence and the art of counting, Exp. Gerontol., vol. 38, 1259, 10.1016/j.exger.2003.09.015 Wang, 2016, Hypoxia causes transgenerational impairments in reproduction of fish, Nat. Commun., vol. 7, 12114, 10.1038/ncomms12114 Waring, 2011, Endocrine disrupters—a threat to women’s health?, Maturitas, vol. 68, 111, 10.1016/j.maturitas.2010.10.008 Wasson, 2013, Restoring totipotency through epigenetic reprogramming, Brief. Funct. Genom., vol. 12, 118, 10.1093/bfgp/els042 Wei, 2021, Parabens as chemicals of emerging concern in the environment and humans: a review, Sci. Total Environ., vol. 778, 10.1016/j.scitotenv.2021.146150 Wolff, 2008, Prenatal phenol and phthalate exposures and birth outcomes, Environ. Health Perspect., vol. 116, 1092, 10.1289/ehp.11007 Ye, 2014, Exposure to DEHP and MEHP from hatching to adulthood causes reproductive dysfunction and endocrine disruption in marine medaka (Oryzias melastigma), Aquat. Toxicol., vol. 146, 115, 10.1016/j.aquatox.2013.10.025 Yin, 2019, Tris(1,3–dichloro‐2–propyl) phosphate disturbs mouse embryonic development by inducing apoptosis and abnormal DNA methylation, Environ. Mol. Mutagen., vol. 60, 807, 10.1002/em.22322 Zacharewski, 1998, Examination of thein Vitroandin VivoEstrogenic activities of eight commercial phthalate esters, Toxicol. Sci., vol. 46, 282 Zhang, 2013, A review of environmental and human exposure to persistent organic pollutants in the Pearl River Delta, South China, Sci. Total Environ., vol. 463–464, 1093, 10.1016/j.scitotenv.2012.10.104 Zhang, 2013, Effects of diethylhexyl phthalate (DEHP) given neonatally on spermatogenesis of mice, Mol. Biol. Rep., vol. 40, 6509, 10.1007/s11033-013-2769-y Zhang, 2013, Cytochrome P450 3A1 mediates 2,2′,4,4′-tetrabromodiphenyl ether-induced reduction of spermatogenesis in adult rats, PLoS One, vol. 8 Zheng, 2012, Functional roles of the phosphatidylinositol 3-kinases (PI3Ks) signaling in the mammalian ovary, Mol. Cell. Endocrinol., vol. 356, 24, 10.1016/j.mce.2011.05.027