Molecular and Epigenetic Impacts of Pesticides on the Female Reproductive System: A Review
DOI:
https://doi.org/10.24233/biov.10.1.2024.434Keywords:
Fungicide , Insecticide , herbicides , Organochlorine , EpigeneticAbstract
Pesticides, primarily originating from agricultural activities, have raised environmental and health concerns due to their suspected effects on the female reproductive system. Despite their widespread application, a significant research void exists concerning their implications for human female reproductive health. This review provides comprehensive information on the adverse effects of pesticides on female reproduction, focusing on their molecular and epigenetic mechanisms. In general, these adverse outcomes include ovarian dysfunction, hormonal irregularities, the onset of endometriosis, and an increased risk of stillbirths. From a mechanistic perspective, pesticides can interfere with the endocrine system, catalyze the formation of reactive oxygen species, and induce oxidative stress. At the molecular level, certain pesticides can act as hormone mimics, disrupting the normal hormonal balance. Moreover, they can trigger epigenetic shifts, leading to alterations in non-coding RNAs, histone configurations, and DNA methylation patterns. These epigenetic alterations not only have an immediate impact but can also be passed on to subsequent generations. Highlighting these concerns, this review underscores the urgent need for stringent regulations and aims to catalyze future in-depth studies on the relationship between pesticides and female reproductive health.
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R. W. Moore, T. A.Rudy, T. M. Lin, K. Ko, and R.E. Peterson, “Abnormalities of sexual development in male rats with in utero and lactational exposure to the antiandrogenic plasticizer Di (2-ethylhexyl) phthalate” Environmental health perspectives, Vol. 109, No 3, PP. 229-237, 2001.
R, Margiana, S.W. Lestari, K. Alawiyah, P. Narulita, A. A. Jusuf, and, K. Ima. “Dietary Soybean (Glycine max (L.) Merr.) Improved the ZP2 Expression in Female Swiss Mice” JBRA Assisted Reproduction, Vol. 27, No. 2, PP. 147, 2023.
D. Meirow, H. Biederman, R.A. Anderson, and, W.H.B. Wallace, “Toxicity of chemotherapy and radiation on female reproduction”. Clinical obstetrics and gynecology, Vol. 53, No. 4, PP. 727-739, 2010.
S. Sifakis, M. Mparmpas, O.P. Soldin, A. Tsatsakis, “Pesticide exposure and health related issues in male and female reproductive system. In: Stoytcheva, M. (Ed.), Pesticides—Formulations, Effects, Fate”. InTech, Rijeka, Croatia, pp. 495–526, 2011.
D.R. Mattison, D. R. Plowchalk, M.J. Meadows, A.Z. Al-Juburi, J. Gandy, and, A. Malek, “Reproductive toxicity: male and female reproductive systems as targets for chemical injury”. Medical Clinics of North America, Vol. 74, No. 2, PP. 391-411, 1990.
M. Ebrahimi, and M. Taherianfard, “The effects of heavy metals exposure on reproductive systems of cyprinid fish from Kor River”. Iranian journal of fisheries science. Vol. 10, No. 1, PP.13-24, 2011.
X. Wang, H. Xie, Z. Wang, and K. He, “Graphene oxide as a pesticide delivery vector for enhancing acaricidal activity against spider mites. Colloids and Surfaces” B: Biointerfaces, Vol. 173, PP. 632-638, 2019.
C. H. King, and D. Bertsch, “Historical perspective: snail control to prevent schistosomiasis”. PLoS neglected tropical diseases, Vol. 9, No. 4, PP. e0003657, 2015.
U. Asghar, M.F. Malik, A. Javed, “Pesticide Exposure and Human Health: A Review.” J. Ecosyst. Ecography , Vol. 01, No. 5, 2016.
R.H. Hall, “A new threat to public health organochlorines and food” Nutr. Health, Vol. 8, PP. 33–43, 1992.
R.C. Gilden, K. Huffling, B. Sattler, “Pesticides and health risks”. J. Obstet.Gynecol. Neonatal Nurs. Vol. 39, PP. 103–110, 2010.
V.I. Lushchak, T.M. Matviishyn, V.V. Husak, J.M. Storey, K.B. Storey, “Pesticide toxicity: A mechanistic approach”, EXCLI J, Vol. 17, PP. 1101–1136, 2018.
M. Ando, H. Saito, and I. Wakisaka, “Gas chromatographic and mass spectrometric analysis of polychlorinated biphenyls in human placenta and cord blood”, Env. Rer., Vol. 41, PP. 14–22,1986.
M.S. Wolff, S. Engel, G.S. Berkowitz, S. Teitelbaum, J. Siskind, D.B. Barr, et al., “Prenatal pesticide and PCB exposures and birth outcomes”. Pediat Res, Vol. 61, No. 2, PP. 243–250, 2007.
O.J. Rando, “Daddy Issues: Paternal Effects on Phenotype”, Cell, Vol. 151, PP. 702–708, 2012.
Q. Chen, Q.C.W. Yan, and, E. Duan, “Epigenetic inheritance of acquired traits through sperm RNAs and sperm RNA modifications”. Nat. Rev. Genet. Vol. 17, PP. 733–743, 2016.
E.C. Oerke, “Crop losses to pests”. J. Agric. Sci. Vol. 144, PP.31–43, 2006.
M.M. Akashe, A.V. Nikam, and U.V. Pawade, “Classification of Pesticides : A Review”. International Journal of Research in Ayurveda and Pharmacy. Vol. 9, No. 4, 2018.
A. El Nemr, A.A. Moneer, A. El-Sikaily, A. Khaled, “PCBs and pesticides in the soft tissue of bivalves along the coast of north Egypt”. Blue Biotechnology Journal, Vol. 1, No.2, PP, 301–313, 2012.
Hassaan and Nemr, “Pesticides pollution: Classifications, human health impact, extraction and treatment techniques”, Egyptian journal of aquatic research, Vol. 46, No. 3, PP. 207-220, 2020.
Y. Abubakar, H. Tijjani, C. Egbuna, C.O. Adetunji, S. Kala, T.L. Kryeziu, J.C. Ifemeje, Iwuanyunwu, C.P. Kingsley. 2020. Pesticides, History, and Classification. Natural remedies for pest, disease and weed control, PP. 29–42, 2020.
Z.J. Tano, “Identity physical and chemical properties of pesticides, in: Pesticides in the Modern World: Trends in Pesticides Analysis”, InTechopen, pp. 1e18, 2011.
I.C. Yadav, N.L. Devi, J.H. Syed, Z. Cheng, J. Li, G. Zhang, K.C. Jones, “Current status of persistent organic pesticides residues in air, water, and soil, and their possible effect on neighboring countries: a comprehensive review of India”, Sci. Total Environ, Vol. 511, PP. 123-137, 2015.
A.R. Baerwald, “Human antral folliculogenesis: what we have learned from the bovine and equine models”, Anim. Reprod., Vol. 6, No.1,PP. 20-29, 2009.
M. Puttabyatappa and V. Padmanabhan, “Developmental Programming of Ovarian Functions and Dysfunctions”, Vitam Horm. Vol. 107, PP. 377-422, 2018.
B.E. Rani, M.K. Krishnakumari, “Prenatal toxicity of heptachlor in albino rats”, Pharmacol Toxicol, Vol. 76, PP, 112-114, 1995.
J.A. Oduma, E.O. Wango, D. Oduor-Okelo, et al., “In vivo and in vitro effects of graded doses of the pesticide heptachlor on female sex steroid hormone production in rats. Comp. Biochem. Phyriol”, C. Pharmacol. Toxicol. Endocrinol, Vol. 111, PP. 191–196, 1993.
J. Boberg, H.K. Johansson, D. Franssen, M.K. Draskau, S. Christiansen, J. Cramer, and T. Svingen, Exposure to the pesticides linuron, dimethomorph and imazalil alters steroid hormone profiles and gene expression in developing rat ovaries. Toxicology Letters, Vol. 373, PP. 114-122, 2023.
J.K. Bhardwaj, and P. Saraf, “Malathion-induced granulosa cell apoptosis in caprine antral follicles: an ultrastructural and flow cytometric analysis”. Microscopy and microanalysis, Vol. 20, No.6, PP. 1861-1868, 2014.
Y. T. He, L. L. Yang, Y. Zhao, W. Shen, S. Yin, and Q. Y. Sun, “Fenoxaprop-ethyl affects mouse oocyte quality and the underlying mechanisms,” Pest Manag Sci, vol. 75, no. 3, pp. 844–851, Mar. 2019, doi: 10.1002/ps.5190.
W.G. Foster, A. McMahon, E.V. Younglai, et al., “Alterations in circulating ovarian steroids in hexachlorobenzene-exposed monkeys”, Reprod. Toxicol., Vol. 9, PP. 341–348, 1993.
W.G. Foster, J.A. Pentick, A. McMahon, et al., “Ovarian toxicity of hexachlorobenzene (HCB) in the superovulated female rat”. J. Biochem. Toxicol, Vol. 7, No. 1–4, 1992.
J.A. Oduma, E.O. Wango, D. Oduor-Okelo, et al., “In vivo and in vitro effects of graded doses of the pesticide heptachlor on female sex steroid hormone production in rats”, Comp. Biochem. Phyriol. C. Pharmacol. Toxicol. Endocrinol, Vol. 111, PP. 191–196, 1993.
A. Lindenau, B. Fischer B, P. Seiler, H.M. Beier, “Effects of persistent chlorinated hydrocarbons on reproductive tissues in female rabbits”. Hum Reprod, Vol. 9, No. 772-80, 1994.
L.J. Guillete, T.S. Gross, G.R. Masson, et al., “Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida”, Environ. Health Perrp., Vol. 102, PP. 608–613, 1994.
Y. Guo, A.G. Hendrickx, and J.W. Overstreet, “Endocrine biomarkers of early fetal loss in cynomolgus macaques (Macaca farcicularir) following exposure to dioxin”. Biol. Reprod., Vol. 60, PP. 707–713, 1999.
A.P. van Birgelen, C.D. Hebert, M.L. Wenk, et al., “Toxicity of 3,3’,4,4’-tetrachloroazoxybenzene in rats and mice”. Toxicol. Appl. Pharmacol., 156, 206–221, 1999.
J.Z. Yang and W.G. Foster, “Continuous Exposure to 2,3,7,8-Tetrachlorodibenzo-P-Dioxin Inhibits the Growth of Surgically Induced Endometriosis in the Ovariectomized Mouse Treated with high Dose Estradiol”, Toxicology and Industrial Health, Vol. 13, No. 1, PP. 15–25, 1997.
R.K. Gupta, R.A. Schuh, G. Fiskum, J.A. Flaws, “Methoxychlor causes mitochondrial dysfunction and oxidative damage in themouse ovary”. Toxicol Appl Pharmacol. Vol. 216, PP. 436–45, 2006.
D. Tomic, M.S. Frech, K. Janice, J.K. Babus, R.K. Gupta, P.A. Furth, et al., “Methoxychlor induces atresia of antral follicles in ER-overexpressing mice”. Toxicol Sci, Vol. 93, PP.196–204, 2006.
H. Tatemoto, N. Sakurai, and N. Muto. “Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells”, Biol Reprod Vol. 63, PP. 805–10, 2000.
A.N. Fatehi, E.C. Zeinstra, R.V. Kooij RV, B. Colenbrander, M.M. Bevers, “Effect of cumulus cell removal of in vitro matured bovine oocytes prior to in vitro fertilization on subsequent cleavage rate”. Theriogenology, Vol. 57, No. 1347–55, 2002.
A.M. Cummings, “Methoxychlor as a model for environmental estrogens”, Crit Rev Toxicol, Vol. 27, PP. 367-379, 1997.
I. Gerhard, B. Monga, J. Krähe, B. Runnebaum, “Chlorinated hydrocarbons in infertile women”, Environ Res, Vol. 80, PP. 299-310,1999.
K.L. Bruner-Tran, et al., “Dioxin may promote inflammation-related development of endometriosis”, Fertility and sterility, Vol. 89, PP. 1287–1298, 2008.
A.C. Holloway, J.J. Petrik, E.V. Younglai, “Influence of dichlorodiphenylchloroethylene on vascular endothelial growth factor and insulin-like growth factor in human and rat ovarian cells”, Reprod Toxicol, Vol. 24, PP. 359–64, 2007.
B. Simic, J. Kniewald, Z. Kniewald, “Effects of atrazine on reproductive performance in the rat”, J Appl Toxicol, Vol. 14, PP. 401–4, 1994.
T. Gojmerac, M. Uremovic, Z. Uremovic, et al., “Reproductive disturbance caused by an S-triazine herbicide in pigs”, Acta Vet Hung, Vol. 47, PP. 129–35, 1999.
L.T. Wetzel, L.G. Luempert, C.B. Breckenridge, et al., “Chronic effects of atrazine on estrus and mammary tumor formation in female Sprague-Dawley and Fischer 344 rats”, J Toxicol Environ Health.Vol. 43, PP. 69–82, 1994.
P.N. Baligar, B.B. Kaliwal, “Induction of gonadal toxicity to female rats after chronic exposure to mancozeb”, Ind Health. Vol. 39, PP. 235–43, 2001.
J.K. Bhardwaj, and P. Saraf, “Malathion-induced granulosa cell apoptosis in caprine antral follicles: an ultrastructural and flow cytometric analysis”. Microscopy and microanalysis, Vol. 20, No.6, PP. 1861-1868, 2014.
K. Nishi, and S.S. Hundal, “Chlorpyrifos induced toxicity in reproductive organs of female Wistar rats”, Food and Chemical Toxicology, Vol. 622013, PP. 732–738.
M.H.M. Azarnia, M. Koochesfahani, Y. Rajabi, A. Tahamtani, A. Tamadon, “Histological examination of endosulfan effects on follicular development of BALB/c mice”, Bulg. J. Vet. Med., Vol.12, No. 1, PP.33−41, 2009
N.D. Koc,et al., “Dose-dependent effect of endosulfan and malathion on adult wistar albino rat ovaries”. Pakistan journal of biological sciences, Vol. 12, No. 6, PP. 498–503, 2009.
M. Guney, et al., “a. Ovarian toxicity in rats caused by methidathion and ameliorating effect of vitamins E and C”. Human & experimental toxicology, Vol. 26, PP. 491–498, 2007.
S. Medithi, Y.D. Kasa, B. Jee, K. Venkaiah, and, P.R. Jonnalagadda,”Alterations in reproductive hormone levels among farm women and their children occupationally exposed to organophosphate pesticides”. Women & Health, Vol. 62, No. 5, PP. 454-464, 2022.
P. Sood, “Imidacloprid Induced Reproductive Toxicity in Female Albino Rats”. Indian Journal of Entomology, PP. 1-5, 2022.
X. Wang, A. Anadón, Q. Wu, F. Qiao, I. Ares, Martínez-Larrañaga, M.R. Yuan, and, Z. M.A. Martínez. “Mechanism of Neonicotinoid Toxicity: Impact on Oxidative Stress and Metabolism”. Annu. Rev. Pharmacol. Toxicol. Vol. 58, PP. 471–507, 2018.
J. U. I. Iheanacho, P. I. K. Onyeka, H. I. Udujih, O. G. Udujih, & C. C. Iwuala, “Effects of sub-lethal exposure of lambda-cyhalothrin on birth outcome of female wistar rats”. World journal of pharmaceutical and medical research. Vol. 6, No. 3, PP. 41-44, 2020.
P. Wang, Y. Tian, X. J. Wang, Y. Gao, R. Shi, G. Q. Wang, and X. M. Shen, “Organophosphate pesticide exposure and perinatal outcomes in Shanghai, China” . Environment international, Vol. 42, PP. 100-104, 2012.
Y. J. Zhou, Q. F. Qiao, L. Q. Wang, T. Y. Sheng, M. X. Cui, Q. D. Chen, and, Y. X. Zhang, “Toxicity mechanism of peri-implantation pesticide beta-cypermethrin exposure on endometrial remodeling in early pregnant mice”. Toxicology, Vol. 489, PP. 153497, 2023.
S. E. Rier, D. C. Martin, R. E. Bowman, et al. “Endometriosis in rhesus monkeys (Macaca mulatta) following chronic exposure to 2,3,7,8- tetrachlorodibenzo-p-dioxin. Fundam. Appl”. Toxicol, Vol. 21, PP. 433–441, 1993.
L. M. Pastore, I. Hertz-Picciotto , J.J. Beaumont, “Risk of stillbirth from occupational and residential exposures”. Occup Environ Med, Vol. 54, PP. 511-518, 1997.
T. E. Arbuckle, Z. Lin , L. S. Mery , “An exploratory analysis of the effect of pesticide exposure on the risk of spontaneous abortion in an Ontario farm population”. Environ Health Perspect, Vol. 109, PP. 851-857, 2001.
J. U. I. Iheanacho, P. I. K. Onyeka, H. I. Udujih, O. G. Udujih, and C. C. Iwuala, “Effects of sub-lethal exposure of lambda-cyhalothrin on birth outcome of female wistar rats” . World journal of pharmaceutical and medical research.VOL. 6. No. 3, PP. 41-44, 2020.
Y. Shukla, and, P. Taneja, “Mutagenic potential of cypermethrin in mouse dominant lethal assay”. Journal of environmental pathology, toxicology and oncology, Vol. 21, No. 3, 2002.
M. S. Ullah, M. Ahmad, N. Ahmad, M. Z. Khan, , and , I. Ahmad, “Toxic effects of cypermethrin in female rabbits” . Pakistan Vet. J, Vol. 26, No. 4, PP. 193-196, 2006.
A. Abell , S. Juul , J. P. Bonde, “Time to pregnancy among female greenhouse workers”. Scand J Work Environ Health, Vol. 26, PP. 131-136, 2000.
A. J. Idrovo ,L. H. Sanin , D. Cole , J. Chavarro , H. Caceres , J. Narvaez , “Restrepo M: Time to first pregnancy among women working in agricultural production” . Int Arch Occup Environ Health, Vol. 78, PP.493-500, 2005.
J. Varayoud, L. Monje, T. Bernhardt, M. Muñoz-de-Toro, E. H. Luque, and J. G. Ramos, “Endosulfan modulates estrogen-dependent genes like a non-uterotrophic dose of 17β-estradiol,” Reproductive Toxicology, Vol. 26, no. 2, PP. 138–145, 2008.
G. Rasier et al., “Mechanisms of interaction of endocrine-disrupting chemicals with glutamate-evoked secretion of gonadotropin-releasing hormone,” Toxicological Sciences, Vol. 102, No. 1, PP. 33–41, Mar. 2008.
G. Rasier, A. S. Parent, A. Gérard, M. C. Lebrethon, and J. P. Bourguignon, “Early maturation of gonadotropin-releasing hormone secretion and sexual precocity after exposure of infant female rats to estradiol or dichlorodiphenyltrichloroethane” , Biol Reprod, Vol. 77, No. 4, PP. 734–742, Oct. 2007.
A. L. Strong et al., “Effects of the endocrine-disrupting chemical DDT on self-renewal and differentiation of human Mesenchymal stem cells”, Environ Health Perspect, Vol. 123, No. 1, PP. 42–48, 2015.
M. R. Bratton et al., “The organochlorine o,p’-DDT plays a role in coactivator-mediated MAPK crosstalk in MCF-7 breast cancer cells” , Environ Health Perspect, Vol. 120, No. 9, PP. 1291–1296, 2012.
M. R. Bratton et al., “Organochlorine-mediated potentiation of the general coactivator p300 through p38 mitogen-activated protein kinase” , Carcinogenesis, Vol. 30, No. 1, PP. 106–113, 2009.
D. E. Frigo et al., “Mechanism of Ap-1-mediated gene expression by select organochlorines through the p38 MAPK pathway”, Carcinogenesis, Vol. 25, No. 2 , PP. 249–261, Feb. 2004.
C. D. Foradori, A. D. Zimmerman, L. R. Hinds, K. L. Zuloaga, C. B. Breckenridge, and R. J. Handa, “Atrazine inhibits pulsatile gonadotropin-releasing hormone (GnRH) release without altering GnRH messenger RNA or protein levels in the female rat,” Biol Reprod, vol. 88, no. 1, Jan. 2013, doi: 10.1095/biolreprod.112.102277.
G. P. Dooley, R. B. Tjalkens, and W. H. Hanneman, “The atrazine metabolite diaminochlorotriazine suppresses LH release from murine LβT2 cells by suppressing GnRH-induced intracellular calcium transients,” Toxicol Res (Camb), vol. 2, no. 3, pp. 180–186, 2013, doi: 10.1039/c3tx20088d.
M. V. Hofmeister and E. C. Bonefeld-Jørgensen, “Effects of the pesticides prochloraz and methiocarb on human estrogen receptor α and β mRNA levels analyzed by on-line RT-PCR,” Toxicology in Vitro, vol. 18, no. 4, pp. 427–433, Aug. 2004, doi: 10.1016/j.tiv.2003.12.008.
R. Kamata, F. Sfflraishi, S. Takahashi, A. Shimizu, and H. Shiraishi, “Reproductive and developmental effects of transovarian exposure to o,p’-DDT in japanese quails,” Environ Toxicol Chem, vol. 28, no. 4, pp. 782–790, Apr. 2009, doi: 10.1897/08-218R.1.
R. Kamata, F. Shiraishi, and K. Nakamura, “Avian eggshell thinning caused by transovarian exposure to o,p′-DDT: changes in histology and calcium-binding protein production in the oviduct uterus,” 2020. doi: 10.2131/jts.45.131.
L. Holm, A. Blomqvist, I. Brandt, B. Brunström, Y. Ridderstråle, and C. Berg, “Embryonic exposure to o,p′-DDT causes eggshell thinning and altered shell gland carbonic anhydrase expression in the domestic hen,” Environ Toxicol Chem, vol. 25, no. 10, pp. 2787–2793, Oct. 2006, doi: 10.1897/05-619R.1.
Z. Wang et al., “The fungicide Mancozeb reduces spheroid attachment onto endometrial epithelial cells through downregulation of estrogen receptor β and integrin β3 in Ishikawa cells,” Ecotoxicol Environ Saf, vol. 208, Jan. 2021, doi: 10.1016/j.ecoenv.2020.111606.
T. E. Arbuckle, Z. Lin, and L. S. Mery, “An Exploratory Analysis of the Effect of Pesticide Exposure on the Risk of Spontaneous Abortion in an Ontario Farm Population,” Environmental Health Perspectives , vol. 109, no. 8, pp. 851–857, 2001, doi: 10.1289/ehp.01109851.
S. L. Farr, G. S. Cooper, J. Cai, D. A. Savitz, and D. P. Sandler, “Pesticide use and menstrual cycle characteristics among premenopausal women in the Agricultural Health Study,” Am J Epidemiol, vol. 160, no. 12, pp. 1194–1204, Dec. 2004, doi: 10.1093/aje/kwi006.
V. F. Garry, M. Harkins, A. Lyubimov, L. Erickson, and L. Long, “Reproductive Outcomes In The Women Of The Red River Valley Of The North. I. The Spouses Of Pesticide Applicators: Pregnancy Loss, Age At Menarche, And Exposures To Pesticides,” J Toxicol Environ Health A, vol. 65, no. 11, pp. 769–786, 2002, doi: 10.1080/00984100290071333.
B. B. Bindali and B. B. Kaliwal, “Anti-implantation Effect of a Carbamate Fungicide Mancozeb in Albino Mice,” Ind Health, vol. 40, pp. 191–197, 2002, doi: 10.2486/indhealth.40.191.
L. Legoff et al., “Ovarian dysfunction following prenatal exposure to an insecticide, chlordecone, associates with altered epigenetic features,” Epigenetics Chromatin, vol. 12, no. 1, May 2019, doi: 10.1186/s13072-019-0276-7.
M. Manikkam, M. M. Haque, C. Guerrero-Bosagna, E. E. Nilsson, and M. K. Skinner, “Pesticide methoxychlor promotes the epigenetic transgenerational inheritance of adult-onset disease through the female germline,” PLoS One, vol. 9, no. 7, Jul. 2014, doi: 10.1371/journal.pone.0102091.
M. M. Milesi, J. Varayoud, J. G. Ramos, and E. H. Luque, “Uterine ERα epigenetic modifications are induced by the endocrine disruptor endosulfan in female rats with impaired fertility,” Mol Cell Endocrinol, vol. 454, pp. 1–11, Oct. 2017, doi: 10.1016/j.mce.2017.05.028.
J. A. Cleary, D. E. Tillitt, F. S. vom Saal, D. K. Nicks, R. A. Claunch, and R. K. Bhandari, “Atrazine induced transgenerational reproductive effects in medaka (Oryzias latipes),” Environmental Pollution, vol. 251, pp. 639–650, Aug. 2019, doi: 10.1016/j.envpol.2019.05.013.
V. Lorenz, M. M. Milesi, M. G. Schimpf, E. H. Luque, and J. Varayoud, “Epigenetic disruption of estrogen receptor alpha is induced by a glyphosate-based herbicide in the preimplantation uterus of rats,” Mol Cell Endocrinol, vol. 480, pp. 133–141, Jan. 2019, doi: 10.1016/j.mce.2018.10.022.
Y. Liu et al., “Protective effects of resveratrol against mancozeb induced apoptosis damage in mouse oocytes,” Oncotarget, vol. 8, no. 4, pp. 6233–6245, 2017.
E. Nilsson, G. Larsen, M. Manikkam, C. Guerrero-Bosagna, M. I. Savenkova, and M. K. Skinner, “Environmentally induced epigenetic transgenerational inheritance of ovarian disease,” PLoS One, vol. 7, no. 5, May 2012, doi: 10.1371/journal.pone.0036129.
Z. Liang, A. Riaz, S. Chachar, Y. Ding, H. Du, and X. Gu, “Epigenetic Modifications of mRNA and DNA in Plants,” Molecular Plant, vol. 13, no. 1. Cell Press, pp. 14–30, Jan. 06, 2020. doi: 10.1016/j.molp.2019.12.007.
D. J. Patel and Z. Wang, “Readout of epigenetic modifications,” Annual Review of Biochemistry, vol. 82. pp. 81–118, Jun. 2013. doi: 10.1146/annurev-biochem-072711-165700.
A. M. Zama and M. Uzumcu, “Fetal and neonatal exposure to the endocrine disruptor methoxychlor causes epigenetic alterations in adult ovarian genes”, Endocrinology, vol. 150, no. 10, pp. 4681–4691, Oct. 2009, doi: 10.1210/en.2009-0499.
E. Nilsson et al., “Environmental toxicant induced epigenetic transgenerational inheritance of ovarian pathology and granulosa cell epigenome and transcriptome alterations: ancestral origins of polycystic ovarian syndrome and primary ovarian insufiency”, Epigenetics, vol. 13, no. 8, pp. 875–895, Aug. 2018, doi: 10.1080/15592294.2018.1521223.
M. Manikkam, M. M. Haque, C. Guerrero-Bosagna, E. E. Nilsson, and M. K. Skinner, “Pesticide methoxychlor promotes the epigenetic transgenerational inheritance of adult-onset disease through the female germline” , PLoS One, Vol. 9, No. 7, Jul. 2014.
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