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Glyphosate decreases bovine oocyte quality by inducing oxidative stress and apoptosis

Published online by Cambridge University Press:  09 June 2022

Zhiqiang E
Affiliation:
Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University, Yanji, 133002, China College of Agriculture, Yanbian University, China Jilin Engineering Research Center of Yanbian Yellow Cattle Resources Reservation, China
Yuhan Zhao
Affiliation:
Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University, Yanji, 133002, China College of Agriculture, Yanbian University, China Jilin Engineering Research Center of Yanbian Yellow Cattle Resources Reservation, China
Jingyu Sun
Affiliation:
Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University, Yanji, 133002, China College of Agriculture, Yanbian University, China Jilin Engineering Research Center of Yanbian Yellow Cattle Resources Reservation, China
Xiaomeng Zhang
Affiliation:
Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University, Yanji, 133002, China College of Agriculture, Yanbian University, China Jilin Engineering Research Center of Yanbian Yellow Cattle Resources Reservation, China
Qingguo Jin
Affiliation:
Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University, Yanji, 133002, China College of Agriculture, Yanbian University, China Jilin Engineering Research Center of Yanbian Yellow Cattle Resources Reservation, China
Qingshan Gao*
Affiliation:
Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University, Yanji, 133002, China College of Agriculture, Yanbian University, China Jilin Engineering Research Center of Yanbian Yellow Cattle Resources Reservation, China
*
Author for correspondence: Qingshan Gao. Departamento College of Agriculture, Yanbian University. Tel: +86 433 243 6435. E-mail: qsgao@ybu.edu.cn

Summary

Glyphosate is a universal herbicide with genital toxicity, but the effect of glyphosate on oocytes has not been reported. This study aimed to evaluate the effect of glyphosate (0, 10, 20, 50 and 100 mM) on bovine oocyte in vitro maturation. We showed that 50 mM glyphosate adversely affects the development of bovine oocytes. Exposure of oocytes to 50 mM glyphosate caused an abnormal reduction in oxidative (redox) levels compared with that in the control group, with a significantly higher reactive oxide species level (P < 0.05) and significantly lower glutathione (GSH) expression (P < 0.05). Additionally, the mRNA levels of antioxidant genes (SOD1, SOD2, SIRT2, SIRT3) and the mitochondrial membrane potential (MMP) were significantly reduced (P < 0.05). Furthermore, treatment with 50 mM glyphosate-induced apoptosis, and the mRNA levels of the apoptotic genes Caspase-3 and Caspase-4 were significantly higher than those in the control group (P < 0.05); however, the mRNA level of BAX was significantly higher than that in the control group (P < 0.01). Additionally, the mRNA levels of the anti-apoptotic genes Survivin and BCL-XL were significantly lower than those in the control group (P < 0.05), and oocyte quality was adversely affected. Together, our results confirmed that glyphosate impairs the quality of oocytes by promoting abnormal oocyte redox levels and apoptosis.

Type
Research Article
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Al-Zubaidi, U., Liu, J., Cinar, O., Robker, R. L., Adhikari, D. and Carroll, J. (2019). The spatio-temporal dynamics of mitochondrial membrane potential during oocyte maturation. Molecular Human Reproduction, 25(11), 695705. doi: 10.1093/molehr/gaz055 CrossRefGoogle ScholarPubMed
Alarcón, R., Rivera, O. E., Ingaramo, P. I., Tschopp, M. V., Dioguardi, G. H., Milesi, M. M., Muñoz-de-Toro, M. and Luque, E. H. (2020). Neonatal exposure to a glyphosate-based herbicide alters the uterine differentiation of prepubertal ewe lambs. Environmental Pollution. Barking, Essex, UK, 265(B), 114874. doi: 10.1016/j.envpol.2020.114874 CrossRefGoogle ScholarPubMed
Arroyo, A., Kim, B. and Yeh, J. (2020). Luteinizing hormone action in human oocyte maturation and quality: Signaling pathways, regulation, and clinical impact. Reproductive Sciences, 27(6), 12231252. doi: 10.1007/s43032-019-00137-x CrossRefGoogle ScholarPubMed
Barros, F. D. A., Adona, P. R., Guemra, S. and Damião, B. C. M. (2019). Oxidative homeostasis in oocyte competence for in vitro embryo development. Animal Science Journal = Nihon Chikusan Gakkaiho, 90(10), 13431349. doi: 10.1111/asj.13256 Google ScholarPubMed
Beckie, H. J., Flower, K. C. and Ashworth, M. B. (2020). Farming without glyphosate? Plants, 9(1), 96. doi: 10.3390/plants9010096 CrossRefGoogle ScholarPubMed
Caiati, C., Pollice, P., Favale, S. and Lepera, M. E. (2020). The herbicide glyphosate and its apparently controversial effect on human health: An updated clinical perspective. Endocrine, Metabolic and Immune Disorders Drug Targets, 20(4), 489505. doi: 10.2174/1871530319666191015191614 CrossRefGoogle ScholarPubMed
Cao, M., Wang, Y., Yang, F., Li, J. and Qin, X. (2021). Melatonin rescues the reproductive toxicity of low-dose glyphosate-based herbicide during mouse oocyte maturation via the GPER signaling pathway. Journal of Pineal Research, 70(3), e12718. doi: 10.1111/jpi.12718 CrossRefGoogle ScholarPubMed
Chen, L., Yin, T., Nie, Z. W., Wang, T., Gao, Y. Y., Yin, S. Y., Huo, L. J., Zhang, X., Yang, J. and Miao, Y. L. (2018). Survivin regulates chromosome segregation by modulating the phosphorylation of Aurora B during porcine oocyte meiosis. Cell Cycle, 17(21–22), 24362446. doi: 10.1080/15384101.2018.1542894 CrossRefGoogle ScholarPubMed
Chen, X., Xuan, B., Xu, D., Wang, Q., Cheng, M. and Jin, Y. (2019). Crocin supplementation during oocyte maturation enhances antioxidant defence and subsequent cleavage rate. Zuchthygiene, 54(2), 300308. doi: 10.1111/rda.13361 Google ScholarPubMed
Duan, X. and Sun, S. C. (2019). Actin cytoskeleton dynamics in mammalian oocyte meiosis. Biology of Reproduction, 100(1), 1524. doi: 10.1093/biolre/ioy163 CrossRefGoogle ScholarPubMed
Escobar, M. L., Echeverria, O. M., Palacios-Martínez, S., Juárez-Chavero, S., Sánchez-Sánchez, L. and Vázquez-Nin, G. H. (2019). Beclin 1 interacts with active caspase-3 and Bax in oocytes from atretic follicles in the rat ovary. Journal of Histochemistry and Cytochemistry: Official Journal of the Histochemistry Society, 67(12), 873889. doi: 10.1369/0022155419881127 CrossRefGoogle ScholarPubMed
Fuchs, B., Saikkonen, K. and Helander, M. (2021). Glyphosate-modulated biosynthesis driving plant defense and species interactions. Trends in Plant Science, 26(4), 312323. doi: 10.1016/j.tplants.2020.11.004 CrossRefGoogle ScholarPubMed
Gao, J., Zhang, Y., He, Y. and Ding, D. (2019). [Effects of cigarette smoke on the oxidative damage of mice oocytes and developmental potential]. Wei Sheng Yan Jiu = Journal of Hygiene Research, 48(1), 109113.Google ScholarPubMed
Gillezeau, C., van Gerwen, M., Shaffer, R. M., Rana, I., Zhang, L., Sheppard, L. and Taioli, E. (2019). The evidence of human exposure to glyphosate: A review. Environmental Health: A Global Access Science Source, 18(1), 2. doi: 10.1186/s12940-018-0435-5 CrossRefGoogle ScholarPubMed
Helander, M., Pauna, A., Saikkonen, K. and Saloniemi, I. (2019). Glyphosate residues in soil affect crop plant germination and growth. Scientific Reports, 9(1), 19653. doi: 10.1038/s41598-019-56195-3 CrossRefGoogle ScholarPubMed
Iljas, J. D., Wei, Z. and Homer, H. A. (2020). Sirt1 sustains female fertility by slowing age-related decline in oocyte quality required for post-fertilization embryo development. Aging Cell, 19(9), e13204. doi: 10.1111/acel.13204 CrossRefGoogle ScholarPubMed
Khan, S., Zhou, J. L., Ren, L. and Mojiri, A. (2020). Effects of glyphosate on germination, photosynthesis and chloroplast morphology in tomato. Chemosphere, 258, 127350. doi: 10.1016/j.chemosphere.2020.127350 CrossRefGoogle ScholarPubMed
Malvezzi, H., Da Broi, M. G., Meola, J., Rosa-E-Silva, J. C., Ferriani, R. A. and Navarro, P. A. (2018). Peritoneal fluid of women with endometriosis reduces SOD1 in bovine oocytes in vitro maturation. Cell and Tissue Research, 372(3), 621628. doi: 10.1007/s00441-018-2805-2 CrossRefGoogle ScholarPubMed
Martínez, M. A., Rodríguez, J. L., Lopez-Torres, B., Martínez, M., Martínez-Larrañaga, M. R., Maximiliano, J. E., Anadón, A. and Ares, I. (2020). Use of human neuroblastoma SH-SY5Y cells to evaluate glyphosate-induced effects on oxidative stress, neuronal development and cell death signaling pathways. Environment International, 135, 105414. doi: 10.1016/j.envint.2019.105414 CrossRefGoogle ScholarPubMed
Maskey, E., Crotty, H., Wooten, T. and Khan, I. A. (2019). Disruption of oocyte maturation by selected environmental chemicals in zebrafish. Toxicology in Vitro, 54, 123129. doi: 10.1016/j.tiv.2018.09.017 CrossRefGoogle ScholarPubMed
Meftaul, I. M., Venkateswarlu, K., Dharmarajan, R., Annamalai, P., Asaduzzaman, M., Parven, A. and Megharaj, M. (2020). Controversies over human health and ecological impacts of glyphosate: Is it to be banned in modern agriculture? Environmental Pollution, 263(A), 114372. doi: 10.1016/j.envpol.2020.114372 CrossRefGoogle ScholarPubMed
Mukherjee, S., Forde, R., Belton, A. and Duttaroy, A. (2011). SOD2, the principal scavenger of mitochondrial superoxide, is dispensable for embryogenesis and imaginal tissue development but essential for adult survival. Fly, 5(1), 3946. doi: 10.4161/fly.5.1.14007 CrossRefGoogle ScholarPubMed
Nagy, K., Tessema, R. A., Budnik, L. T. and Ádám, B. (2019). Comparative cyto- and genotoxicity assessment of glyphosate and glyphosate-based herbicides in human peripheral white blood cells. Environmental Research, 179 (B), 108851. doi: 10.1016/j.envres.2019.108851 CrossRefGoogle ScholarPubMed
Nie, X., Dai, Y., Zheng, Y., Bao, D., Chen, Q., Yin, Y., Fu, H. and Hou, D. (2018). Establishment of a mouse model of premature ovarian failure using consecutive superovulation. Cellular Physiology and Biochemistry: International Journal of Experimental Cellular Physiology, Biochemistry, and Pharmacology, 51(5), 23412358. doi: 10.1159/000495895 CrossRefGoogle ScholarPubMed
Nie, J., Yan, K., Sui, L., Zhang, H., Zhang, H., Yang, X., Lu, S., Lu, K. and Liang, X. (2020). Mogroside V improves porcine oocyte in vitro maturation and subsequent embryonic development. Theriogenology, 141, 3540. doi: 10.1016/j.theriogenology.2019.09.010 CrossRefGoogle ScholarPubMed
Pan, B. and Li, J. (2019). The art of oocyte meiotic arrest regulation. Reproductive Biology and Endocrinology: RB&E, 17(1), 8. doi: 10.1186/s12958-018-0445-8 CrossRefGoogle ScholarPubMed
Sasaki, H., Hamatani, T., Kamijo, S., Iwai, M., Kobanawa, M., Ogawa, S., Miyado, K. and Tanaka, M. (2019). Impact of oxidative stress on age-associated decline in oocyte developmental competence. Frontiers in Endocrinology, 10, 811. doi: 10.3389/fendo.2019.00811 CrossRefGoogle ScholarPubMed
Schnabel, K., Schmitz, R., Frahm, J., Meyer, U., Breves, G. and Dänicke, S. (2020). Functionality and DNA-damage properties of blood cells in lactating cows exposed to glyphosate contaminated feed at different feed energy levels. Archives of Animal Nutrition, 74(2), 87106. doi: 10.1080/1745039X.2020.1718474 CrossRefGoogle ScholarPubMed
Somfai, T., Nguyen, H. T., Nguyen, M. T., Dang-Nguyen, T. Q., Kaneko, H., Noguchi, J. and Kikuchi, K. (2020). Vitrification of porcine cumulus–oocyte complexes at the germinal vesicle stage does not trigger apoptosis in oocytes and early embryos, but activates anti-apoptotic Bcl-XL gene expression beyond the 4-cell stage. Journal of Reproduction and Development, 66(2), 115123. doi: 10.1262/jrd.2019-094 CrossRefGoogle Scholar
Tatsuta, T., Hosono, M., Miura, Y., Sugawara, S., Kariya, Y., Hakomori, S. and Nitta, K. (2013). Involvement of ER stress in apoptosis induced by sialic acid-binding lectin (leczyme) from bullfrog eggs. International Journal of Oncology, 43(6), 17991808. doi: 10.3892/ijo.2013.2128 CrossRefGoogle ScholarPubMed
Teleken, J. L., Gomes, E. C. Z., Marmentini, C., Moi, M. B., Ribeiro, R. A., Balbo, S. L., Amorim, E. M. P. and Bonfleur, M. L. (2020). Glyphosate-based herbicide exposure during pregnancy and lactation malprograms the male reproductive morphofunction in F1 offspring. Journal of Developmental Origins of Health and Disease, 11(2), 146153. doi: 10.1017/S2040174419000382 CrossRefGoogle ScholarPubMed
Van Bruggen, A. H. C., He, M. M., Shin, K., Mai, V., Jeong, K. C., Finckh, M. R. and Morris, J. G., Jr. (2018). Environmental and health effects of the herbicide glyphosate. Science of the Total Environment, 616–617, 255268. doi: 10.1016/j.scitotenv.2017.10.309 CrossRefGoogle ScholarPubMed
Wang, L., Deng, Q., Hu, H., Liu, M., Gong, Z., Zhang, S., Xu-Monette, Z. Y., Lu, Z., Young, K. H., Ma, X. and Li, Y. (2019). Glyphosate induces benign monoclonal gammopathy and promotes multiple myeloma progression in mice. Journal of Hematology and Oncology, 12(1), 70. doi: 10.1186/s13045-019-0767-9 CrossRefGoogle ScholarPubMed
Wang, Y., Li, L., Fan, L. H., Jing, Y., Li, J., Ouyang, Y. C., Wang, Z. B., Hou, Y. and Sun, Q. Y. (2019). N-Acetyl-L-cysteine (NAC) delays post-ovulatory oocyte aging in mouse. Aging, 11(7), 20202030. doi: 10.18632/aging.101898 CrossRefGoogle Scholar
Wang, Y., Huang, H., Zeng, M., Quan, R. P., Yang, J. T., Guo, D., Sun, Y., Deng, H. and Xiao, H. (2020). Mutation of rat Zp2 causes ROS-mediated oocyte apoptosis. Reproduction (Cambridge, England), 160(3), 353365. doi: 10.1530/REP-20-0037 CrossRefGoogle ScholarPubMed
Weeks Santos, S., Gonzalez, P., Cormier, B., Mazzella, N., Bonnaud, B., Morin, S., Clérandeau, C., Morin, B. and Cachot, J. (2019). A glyphosate-based herbicide induces sub-lethal effects in early life stages and liver cell line of rainbow trout, Oncorhynchus mykiss. Aquatic Toxicology, 216, 105291. doi: 10.1016/j.aquatox.2019.105291 CrossRefGoogle ScholarPubMed
Wrobel, M. H. (2018). Glyphosate affects the secretion of regulators of uterine contractions in cows while it does not directly impair the motoric function of myometrium in vitro . Toxicology and Applied Pharmacology, 349, 5561. doi: 10.1016/j.taap.2018.04.031 CrossRefGoogle Scholar
Xu, D., Wu, L., Jiang, X., Yang, L., Cheng, J., Chen, H., Hua, R., Geng, G., Yang, L. and Li, Q. (2019). SIRT2 inhibition results in meiotic arrest, mitochondrial dysfunction, and disturbance of redox homeostasis during bovine oocyte maturation. International Journal of Molecular Sciences, 20(6), 1365. doi: 10.3390/ijms20061365 CrossRefGoogle ScholarPubMed
Yang, Q., Dai, S., Luo, X., Zhu, J., Li, F., Liu, J., Yao, G. and Sun, Y. (2018). Melatonin attenuates postovulatory oocyte dysfunction by regulating SIRT1 expression. Reproduction (Cambridge, England), 156(1), 8192. doi: 10.1530/REP-18-0211 CrossRefGoogle ScholarPubMed
Zanardi, M. V., Schimpf, M. G., Gastiazoro, M. P., Milesi, M. M., Muñoz-de-Toro, M., Varayoud, J. and Durando, M. (2020). Glyphosate-based herbicide induces hyperplastic ducts in the mammary gland of aging Wistar rats. Molecular and Cellular Endocrinology, 501, 110658. doi: 10.1016/j.mce.2019.110658 CrossRefGoogle ScholarPubMed
Zhang, J. W., Xu, D. Q. and Feng, X. Z. (2019). The toxic effects and possible mechanisms of glyphosate on mouse oocytes. Chemosphere, 237, 124435. doi: 10.1016/j.chemosphere.2019.124435 CrossRefGoogle ScholarPubMed
Zhang, J., Zhao, C., Shi, F., Zhang, S., Wang, S. and Feng, X. (2021). Melatonin alleviates the deterioration of oocytes and hormonal disorders from mice subjected to glyphosate. Molecular and Cellular Endocrinology, 520, 111073. doi: 10.1016/j.mce.2020.111073 CrossRefGoogle ScholarPubMed
Zhou, C., Zhang, X., Chen, Y., Liu, X., Sun, Y. and Xiong, B. (2019). Glutathione alleviates the cadmium exposure-caused porcine oocyte meiotic defects via eliminating the excessive ROS. Environmental Pollution, 255(1), 113194. doi: 10.1016/j.envpol.2019.113194 CrossRefGoogle ScholarPubMed
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