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Oxidative stress induced by methomyl exposure reduces the quality of early embryo development in mice

Published online by Cambridge University Press:  10 May 2021

Daohong He Open the ORCID record for Daohong He [Opens in a new window] ,
Guobo Han ,
Xiaomeng Zhang ,
Jingyu Sun ,
Yongnan Xu ,
Qingguo Jin  and
Qingshan Gao
Daohong He
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000China Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanji133002, China
Guobo Han
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000China Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanji133002, China
Xiaomeng Zhang
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000China Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanji133002, China
Jingyu Sun
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000China Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanji133002, China
Yongnan Xu
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000China Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanji133002, China
Qingguo Jin
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000China Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanji133002, China
Qingshan Gao*
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000China Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanji133002, China
*
Author for correspondence: Qingshan Gao, College of Agriculture, Yanbian University, Yanji, China. E-mail: qsgao@ybu.edu.cn
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Summary

Methomyl is a widely used carbamate insecticide and environmental oestrogen that has adverse effects on the reproductive system. However, there have been no reports on the effect of methomyl on early embryos in mammals. In this study, we explored the effect of methomyl exposure on the quality of early embryonic development in mice and the possible mechanisms. During in vitro culture, different concentrations of methomyl (10, 20, 30 and 35 μM) were added to mouse zygote medium. The results showed that methomyl had an adverse effect on early embryonic development. Compared with the control group, the addition of 30 μM methomyl significantly reduced the rate of early embryo blastocyst formation. Methomyl exposure can increase oxidative stress and impair mitochondrial function, which may be the cause of blastocyst formation. In addition, we found that methomyl exposure promoted apoptosis and autophagy in mouse blastocysts. The toxic effect of methomyl on early embryos may be the result of oxidative stress induction. Taken together, our results indicate that methomyl can cause embryonic development defects in mice, thereby reducing the quality of early embryo development.

Keywords

Embryo developmentMethomylMitochondriaMouseOxidative stress
Type
Research Article
Information
Zygote , Volume 30 , Issue 1 , February 2022 , pp. 57 - 64
Copyright
© The Author(s), (2021). Published by Cambridge University Press

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References

Agarwal, A, Durairajanayagam, D and du Plessis, SS (2014). Utility of antioxidants during assisted reproductive techniques: an evidence based review. Reprod Biol Endocrinol 12, 112.CrossRefGoogle Scholar
Alm, H, Greising, T, Brüssow, KP, Torner, H and Tiemann, U (2002). The influence of the mycotoxins deoxynivalenol and zearalenol on in vitro maturation of pig oocytes and in vitro culture of pig zygotes. Toxicol In Vitro 16, 643–8.CrossRefGoogle ScholarPubMed
An, Q, Peng, W, Cheng, Y, Lu, Z, Zhou, C, Zhang, Y and Su, J (2019). Melatonin supplementation during in vitro maturation of oocyte enhances subsequent development of bovine cloned embryos. J Cell Physiol 234, 17370–81.CrossRefGoogle ScholarPubMed
Babayev, E and Seli, E (2015). Oocyte mitochondrial function and reproduction. Curr Opin Obstet Gynecol 27, 175–81.CrossRefGoogle ScholarPubMed
Badawy, ME and El-Aswad, AF (2014). Bioactive paper sensor based on the acetylcholinesterase for the rapid detection of organophosphate and carbamate pesticides. Int J Anal Chem 2014, 536823.CrossRefGoogle ScholarPubMed
Calix, RX, Ornaghi, S, Wilson, JH, Fernandez, N, Vialard, F, Barnea, ER and Paidas, MJ (2017). Preimplantation factor and endocrinology of implantation and establishment of early pregnancy: a contemporary view. Pediatr Endocrinol Rev 15, 147–58.Google ScholarPubMed
Chowdhury, MA, Banik, S, Uddin, B, Moniruzzaman, M, Karim, N and Gan, SH (2012). Organophosphorus and carbamate pesticide residues detected in water samples collected from paddy and vegetable fields of the Savar and Dhamrai Upazilas in Bangladesh. Int J Environ Res Public Health 9, 3318–29.CrossRefGoogle ScholarPubMed
Dennery, PA (2007). Effects of oxidative stress on embryonic development. Birth Defects Res C Embryo Today 81, 155–62.CrossRefGoogle ScholarPubMed
Derbalah, A, Sunday, M, Kato, R, Takeda, K and Sakugawa, H (2020). Photoformation of reactive oxygen species and their potential to degrade highly toxic carbaryl and methomyl in river water. Chemosphere 244, 125464.CrossRefGoogle ScholarPubMed
Dumollard, R, Duchen, M and Carroll, J (2007). The role of mitochondrial function in the oocyte and embryo. Curr Topic Dev Biol 77, 21–49.CrossRefGoogle ScholarPubMed
El-Demerdash, F, Attia, AA and Elmazoudy, RH (2012). Biochemical and histopathological changes induced by different time intervals of methomyl treatment in mice liver. J Environ Sci Health A Tox Hazard Subst Environ Eng 47, 1948–54.CrossRefGoogle ScholarPubMed
Farag, AT, Eweidah, MH and El-Okazy, AM (2000). Reproductive toxicology of acephate in male mice. Reprod Toxicol 14, 457–62.CrossRefGoogle ScholarPubMed
Goodale, LF, Hayrabedyan, S, Todorova, K, Roussev, R, Ramu, S, Stamatkin, C, Coulam, CB, Barnea, ER and Gilbert, RO (2017). PreImplantation Factor (PIF) protects cultured embryos against oxidative stress: relevance for recurrent pregnancy loss (RPL) therapy. Oncotarget 8, 32419–32.CrossRefGoogle ScholarPubMed
Guo, J, Zhao, MH, Shin, KT, Niu, YJ, Ahn, YD, Kim, NH and Cui, XS (2017). The possible molecular mechanisms of bisphenol A action on porcine early embryonic development. Sci Rep 7, 8632.CrossRefGoogle ScholarPubMed
Harvey, AJ (2019). Mitochondria in early development: linking the microenvironment, metabolism and the epigenome. Reproduction 157, R159–79.CrossRefGoogle Scholar
Hoizey, G, Canas, F, Binet, L, Kaltenbach, ML, Jeunehomme, G, Bernard, MH and Lamiable, D (2008). Thiodicarb and methomyl tissue distribution in a fatal multiple compounds poisoning. J Forensic Sci 53, 499–502.CrossRefGoogle Scholar
Kauppila, TES, Kauppila, JHK and Larsson, NG (2017). Mammalian mitochondria and aging: an update. Cell Metab 25, 57–71.CrossRefGoogle ScholarPubMed
Kyle, ME, Miccadei, S, Nakae, D and Farber, JL (1987). Superoxide dismutase and catalase protect cultured hepatocytes from the cytotoxicity of acetaminophen. Biochem Biophys Res Commun 149, 889–96.CrossRefGoogle ScholarPubMed
Lee, SJ, Cho, KS and Koh, JY (2009). Oxidative injury triggers autophagy in astrocytes: the role of endogenous zinc. Glia 57, 1351–61.CrossRefGoogle ScholarPubMed
Levine, B and Kroemer, G (2008). Autophagy in the pathogenesis of disease. Cell 132, 27–42.CrossRefGoogle ScholarPubMed
Liu, L, Trimarchi, JR and Keefe, DL (2000). Involvement of mitochondria in oxidative stress-induced cell death in mouse zygotes. Biol Reprod 62, 1745–53.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–8.CrossRefGoogle Scholar
Mahgoub, AA and El-Medany, AH (2001). Evaluation of chronic exposure of the male rat reproductive system to the insecticide methomyl. Pharm Res 44, 73–80.CrossRefGoogle Scholar
Mansour, SA, Mossa, AT and Heikal, TM (2009). Effects of methomyl on lipid peroxidation and antioxidant enzymes in rat erythrocytes: in vitro studies. Toxicol Ind Health 25, 557–63.CrossRefGoogle ScholarPubMed
Mansour, SA, Abbassy, MA and Shaldam, HA (2017). Zinc ameliorate oxidative stress and hormonal disturbance induced by methomyl, abamectin, and their mixture in male rats. Toxics 5, 37.CrossRefGoogle ScholarPubMed
Mastrorocco, A, Martino, NA, Marzano, G, Lacalandra, GM, Ciani, E, Roelen, BAJ, Dell’Aquila, ME and Minervini, F (2019). The mycotoxin beauvericin induces oocyte mitochondrial dysfunction and affects embryo development in the juvenile sheep. Mol Reprod Dev 86, 1430–43.CrossRefGoogle ScholarPubMed
Meng, S, Qiu, L, Hu, G, Fan, L, Song, C, Zheng, Y, Wu, W, Qu, J, Li, D, Chen, J and Xu, P (2016). Effects of methomyl on steroidogenic gene transcription of the hypothalamic–pituitary–gonad–liver axis in male tilapia. Chemosphere 165, 152–62.CrossRefGoogle ScholarPubMed
Rodríguez-Fuentes, G, Rubio-Escalante, FJ, Noreña-Barroso, E, Escalante-Herrera, KS and Schlenk, D (2015). Impacts of oxidative stress on acetylcholinesterase transcription, and activity in embryos of zebrafish (Danio rerio) following Chlorpyrifos exposure. Comp Biochem Physiol C Toxicol Pharmacol 172–3, 19–25.CrossRefGoogle Scholar
Sakr, S, Hassanien, H, Bester, MJ, Arbi, S, Sobhy, A, El Negris, H and Steenkamp, V (2018). Beneficial effects of folic acid on the kidneys and testes of adult albino rats after exposure to methomyl. Toxicol Res 7, 480–91.CrossRefGoogle ScholarPubMed
Seleem, AA (2019). Teratogenicity and neurotoxicity effects induced by methomyl insecticide on the developmental stages of Bufo arabicus. Neurotoxicol Teratol 72, 1–9.CrossRefGoogle ScholarPubMed
Shalaby, MA, El Zorba, HY and Ziada, RM (2010). Reproductive toxicity of methomyl insecticide in male rats and protective effect of folic acid. Food Chem Toxicol 48, 3221–6.CrossRefGoogle ScholarPubMed
Shanthalatha, A, Madhuranath, BN and Yajurvedi, HN (2012). Effect of methomyl formulation, a carbamate pesticide on ovarian follicular development and fertility in albino mice. J Environ Biol 33, 33–7.Google ScholarPubMed
Terao, H, Wada-Hiraike, O, Nagumo, A, Kunitomi, C, Azhary, JMK, Harada, M, Hirata, T, Hirota, Y, Koga, K, Fujii, T and Osuga, Y (2019). Role of oxidative stress in follicular fluid on embryos of patients undergoing assisted reproductive technology treatment. J Obstet Gynaecol Res 45, 1884–91.CrossRefGoogle ScholarPubMed
Tsujimoto, Y and Shimizu, S (2005). Another way to die: autophagic programmed cell death. Cell Death Diff 12(Suppl 2), 1528–34.CrossRefGoogle ScholarPubMed
Valko, M, Leibfritz, D, Moncol, J, Cronin, MT, Mazur, M and Telser, J (2007). Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39, 44–84.CrossRefGoogle ScholarPubMed
Van Blerkom, J (2011). Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 11, 797–813.CrossRefGoogle ScholarPubMed
Van Scoy, AR, Yue, M, Deng, X and Tjeerdema, RS (2013). Environmental fate and toxicology of methomyl. Rev Environ Contam Toxicol 222, 93–109.Google ScholarPubMed
Wang, LY, Wang, DH, Zou, XY and Xu, CM (2009). Mitochondrial functions on oocytes and preimplantation embryos. J Zhejiang Univ Sci B 10, 483–92.CrossRefGoogle ScholarPubMed
Wilding, M, Dale, B, Marino, M, di Matteo, L, Alviggi, C, Pisaturo, ML, Lombardi, L and De Placido, G (2001). Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum Reprod 16, 909–17.CrossRefGoogle ScholarPubMed
Wu, M, Xu, H, Shen, Y, Qiu, W and Yang, M (2011). Oxidative stress in zebrafish embryos induced by short-term exposure to bisphenol A, nonylphenol, and their mixture. Environ Toxicol Chem 30, 2335–41.CrossRefGoogle ScholarPubMed
Xu, YN, Cui, XS, Sun, SC, Lee, SE, Li, YH, Kwon, JS, Lee, SH, Hwang, KC and Kim, NH (2011). Mitochondrial dysfunction influences apoptosis and autophagy in porcine parthenotes developing in vitro . J Reprod Dev 57, 143–50.CrossRefGoogle ScholarPubMed
Xu, Y, Zhang, KH, Sun, MH, Lan, M, Wan, X, Zhang, Y and Sun, SC (2019). Protective effects of melatonin against zearalenone toxicity on porcine embryos in vitro . Front Pharmacol 10, 327.CrossRefGoogle ScholarPubMed
Ying, C, Hsu, WL, Hong, W F, Cheng, WT and Yang, Y (2000). Estrogen receptor is expressed in pig embryos during preimplantation development. Mol Reprod Dev 55, 83–8.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Yuan, B, Liang, S, Jin, Y X, Zhang, M J, Zhang, JB and Kim, NH (2017). Toxic effects of atrazine on porcine oocytes and possible mechanisms of action. PLoS One 12, e0179861.CrossRefGoogle ScholarPubMed
Zhang, H, Kong, X, Kang, J, Su, J, Li, Y, Zhong, J and Sun, L (2009). Oxidative stress induces parallel autophagy and mitochondria dysfunction in human glioma U251 cells. Toxicol Sci 110, 376–88.CrossRefGoogle ScholarPubMed
Zhao, Y, Xu, Y, Li, Y, Jin, Q, Sun, JEZ and Gao, Q (2020). Supplementation of kaempferol to in vitro maturation medium regulates oxidative stress and enhances subsequent embryonic development in vitro . Zygote 28, 59–64.CrossRefGoogle ScholarPubMed