Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-25T12:58:10.815Z Has data issue: false hasContentIssue false
  • English
  • Français

Toxic effects of methomyl on mouse oocytes and its possible mechanisms

Published online by Cambridge University Press:  22 October 2021

Daohong He Open the ORCID record for Daohong He [Opens in a new window] ,
Yongnan Xu ,
Lina Hou ,
Jing Wang ,
Shaoying Yang ,
Yu Wang ,
Shurui Zhang ,
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
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
Lina Hou
Affiliation:
Yanbian Korean Autonomous Prefecture Animal Husbandry Master Station, Yanji133002, China
Jing Wang
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
Shaoying Yang
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
Yu Wang
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
Shurui 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
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: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Methomyl is a broad-spectrum carbamate insecticide that has a variety of toxic effects on humans and animals. However, there have been no studies on the toxicity of methomyl in female mammalian oocytes. This study investigated the toxic effects of environmental oestrogen methomyl exposure on mouse oocyte maturation and its possible mechanisms. Our results indicated that methomyl exposure inhibited polar body extrusion in mouse oocytes. Compared with that in the control group, in the methomyl treatment group, superoxide anion free radicals in oocytes were significantly increased. In addition, the mitochondrial membrane potential of metaphase II stage oocytes in the methomyl treatment group was significantly decreased, resulting in reduced mouse oocyte quality. After 8.5 h of exposure to methomyl, metaphase I stage mouse oocytes displayed an abnormal spindle morphology. mRNA expression of the pro-apoptotic genes Bax and Caspase-3 in methomyl-treated oocytes increased, which confirmed the apoptosis. Collectively, our results indicated that mouse oocyte maturation is defective after methomyl treatment at least through disruption of spindle morphology, mitochondrial function and by induction of oxidative stress.

Keywords

MethomylMitochondriaMouseOocyteOxidative stress
Type
Research Article
Information
Zygote , Volume 30 , Issue 3 , June 2022 , pp. 358 - 364
Copyright
© The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Balboula, AZ, Yamanaka, K, Sakatani, M, Kawahara, M, Hegab, AO, Zaabel, SM and Takahashi, M (2013) Cathepsin B activity has a crucial role in the developmental competence of bovine cumulus–oocyte complexes exposed to heat shock during in vitro maturation. Reproduction 146, 407–17.CrossRefGoogle Scholar
Bernardi, P, Di Lisa, F, Fogolari, F and Lippe, G (2015). From ATP to PTP and back: A dual function for the mitochondrial ATP synthase. Circ Res 116, 1850–62.CrossRefGoogle ScholarPubMed
Chen, Y, Azad, MB and Gibson, SB (2009). Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ 16, 1040–52.CrossRefGoogle ScholarPubMed
Cui, XS, Jeong, YJ, Lee, HY, Cheon, SH and Kim, NH (2004). Fetal bovine serum influences apoptosis and apoptosis-related gene expression in porcine parthenotes developing in vitro. Reproduction 127, 125–30.CrossRefGoogle ScholarPubMed
Djeffal, A, Messarah, M, Boumendjel, A, Kadeche, L and Feki, AE (2015). Protective effects of vitamin C and selenium supplementation on methomyl-induced tissue oxidative stress in adult rats. Toxicol Ind Health 31, 31–43.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
Gely-Pernot, A, Saci, S, Kernanec, PY, Hao, C, Giton, F, Kervarrec, C, Tevosian, S, Mazaud-Guittot, S and Smagulova, F (2017). Embryonic exposure to the widely-used herbicide atrazine disrupts meiosis and normal follicle formation in female mice. Sci Rep 7, 3526.CrossRefGoogle Scholar
Holmström, KM and Finkel, T (2014). Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat Rev Mol Cell Biol 15, 411–21.CrossRefGoogle ScholarPubMed
Hou, YJ, Zhu, CC, Xu, YX, Cui, XS, Kim, NH and Sun, SC (2015). Zearalenone exposure affects mouse oocyte meiotic maturation and granulosa cell proliferation. Environ Toxicol 30, 1226–33.CrossRefGoogle ScholarPubMed
Jia, ZZ, Zhang, JW, Zhou, D, Xu, DQ and Feng, XZ (2019). Deltamethrin exposure induces oxidative stress and affects meiotic maturation in mouse oocyte. Chemosphere 223, 704–13.CrossRefGoogle ScholarPubMed
Jiang, WJ, Yao, XR, Zhao, YH, Gao, QS, Jin, QG, Li, YH, Yan, AG and Xu, YN (2019). L-Carnitine prevents bovine oocyte aging and promotes subsequent embryonic development. J Reprod Dev 65, 499–506.CrossRefGoogle ScholarPubMed
Luddi, A, Capaldo, A, Focarelli, R, Gori, M, Morgante, G, Piomboni, P and De Leo, V (2016). Antioxidants reduce oxidative stress in follicular fluid of aged women undergoing IVF. Reprod Biol Endocrinol 14, 57.CrossRefGoogle ScholarPubMed
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
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
Nicholas, B, Alberio, R, Fouladi-Nashta, AA and Webb, R (2005). Relationship between low-molecular-weight insulin-like growth factor-binding proteins, caspase-3 activity, and oocyte quality. Biol Reprod 72, 796–804.CrossRefGoogle ScholarPubMed
Park, HJ, Park, SY, Kim, JW, Yang, SG, Kim, MJ, Jegal, HG, Kim, IS, Choo, YK and Koo, DB (2018). Melatonin improves oocyte maturation and mitochondrial functions by reducing bisphenol A-derived superoxide in porcine oocytes in vitro. Int J Mol Sci 19, 3422.CrossRefGoogle ScholarPubMed
Perkins, AT, Das, TM, Panzera, LC and Bickel, SE (2016). Oxidative stress in oocytes during midprophase induces premature loss of cohesion and chromosome segregation errors. Proc Natl Acad Sci USA 113, E6823–30.CrossRefGoogle ScholarPubMed
Porter, AG and Jänicke, RU (1999). Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6, 99–104.CrossRefGoogle ScholarPubMed
Rao, X, Huang, X, Zhou, Z and Lin, X (2013). An improvement of the 2(–DDCt) method for quantitative real-time polymerase chain reaction data analysis. Biostat Bioinforma Biomath 3, 71–85.Google Scholar
Roth, Z (2018). Symposium review: Reduction in oocyte developmental competence by stress is associated with alterations in mitochondrial function. J Dairy Sci 101, 3642–54.CrossRefGoogle ScholarPubMed
Sambuu, R, Takagi, M, Namula, Z, Otoi, T, Shiga, S, Rodrigues dos Santos, R and Fink-Gremmels, J (2011). Effects of exposure to zearalenone on porcine oocytes and sperm during maturation and fertilization in vitro. J Reprod Dev 57, 547–50.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
Shen, J, Wang, Z, Shen, X, Zheng, Z, Zhang, Q, Feng, X, Hu, L and Lei, L (2015). Abnormal dynamic changes in β-tubulin in somatic nuclear transfer cloned mouse embryos. Zygote 23, 76–82.CrossRefGoogle ScholarPubMed
Tsutsumi, O (2005). Assessment of human contamination of estrogenic endocrine-disrupting chemicals and their risk for human reproduction. J Steroid Biochem Mol Biol 93(2–5), 325–30.CrossRefGoogle ScholarPubMed
Ureshino, RP, Rocha, KK, Lopes, GS, Bincoletto, C and Smaili, SS (2014). Calcium signaling alterations, oxidative stress, and autophagy in aging. Antioxid Redox Signal 21, 123–37.CrossRefGoogle Scholar
Van Blerkom, J and Davis, P (2007). Mitochondrial signaling and fertilization. Mol Hum Reprod 13, 759–70.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
Yang, SE, Hsieh, MT, Tsai, TH and Hsu, SL (2002). Down-modulation of Bcl-XL, release of cytochrome c and sequential activation of caspases during honokiol-induced apoptosis in human squamous lung cancer CH27 cells. Biochem Pharmacol 63, 1641–51.CrossRefGoogle ScholarPubMed
Yao, X, Jiang, H, Liang, S, Shen, X, Gao, Q, Xu, YN and Kim, NH (2018). Laminarin enhances the quality of aged pig oocytes by reducing oxidative stress. J Reprod Dev 64, 489–94.CrossRefGoogle ScholarPubMed
Yu, M, Qiu, ZL, Li, H, Zeng, WS, Chen, LN, Li, QH and Quan, S (2011). [Association between cell apoptosis and the quality of early mouse embryos]. Nan Fang Yi Ke Da Xue Xue Bao = J South Med Univ 31, 409–13.Google Scholar
Yu, X, Huang, B, Zhou, Z, Tang, J and Yu, Y (2017). Involvement of caspase3 in the acute stress response to high temperature and elevated ammonium in stony coral Pocillopora damicornis. Gene 637, 108–14.CrossRefGoogle ScholarPubMed
Yuan, B, Liang, S, Jin, YX, Zhang, MJ, Zhang, JB and Kim, NH (2017). Toxic effects of atrazine on porcine oocytes and possible mechanisms of action. PLoS One 12, e0179861.CrossRefGoogle ScholarPubMed
Žalmanová, T, Hošková, K, Nevoral, J, Adámková, K, Kott, T, Šulc, M, Kotíková, Z, Prokešová, Š, Jílek, F, Králíčková, M and Petr, J (2017). Bisphenol S negatively affects the meiotic maturation of pig oocytes. Sci Rep 7, 485.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
Zhang, M, Miao, Y, Chen, Q, Cai, M, Dong, W, Dai, X, Lu, Y, Zhou, C, Cui, Z and Xiong, B (2018). BaP exposure causes oocyte meiotic arrest and fertilization failure to weaken female fertility. FASEB J 32, 342–52.CrossRefGoogle ScholarPubMed
Zhang, Y, Han, J, Zhu, CC, Tang, F, Cui, XS, Kim, NH and Sun, SC (2016). Exposure to HT-2 toxin causes oxidative stress induced apoptosis/autophagy in porcine oocytes. Sci Rep 6, 33904.CrossRefGoogle ScholarPubMed
Zhu, JQ, Liu, Y, Zhang, JH, Liu, YF, Cao, JQ, Huang, ZT, Yuan, Y, Bian, JC and Liu, ZP (2018). Cadmium exposure of female mice impairs the meiotic maturation of oocytes and subsequent embryonic development. Toxicol Sci 164, 289–99.CrossRefGoogle ScholarPubMed