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Acetochlor affects zebrafish ovarian development by producing estrogen effects and inducing oxidative stress

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Abstract

Acetochlor is one of the most widely used pesticides worldwide and widely distributed in the water environment. However, studies on the reproductive influence of acetochlor are still limited. To investigate the impact and potential mechanism of acetochlor on fish ovarian development, zebrafish were utilized as experiment models. The ovarian histology, ovarian development-related genes, and plasma oxidative stress-related indexes were investigated following acetochlor (at nominal concentration 1, 10, and 100 μg/L) exposure for 7 and 21 days. Results showed that low-dose acetochlor had estrogen effect and induced zebrafish estradiol (E2) and ovarian vitellogenin (Vtg) synthesis and promoted ovarian development, while long-term exposure to higher doses of acetochlor reduced the ability of ovarian resistance to oxidative stress and destroyed the development of the ovary. Moreover, bone morphogenetic protein 15 (bmp15) and growth differentiation factor 9 (gdf9) were also involved in the influence of acetochlor on the ovarian development of zebrafish.

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References

  • Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S (2012) The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol 10:49

    Google Scholar 

  • Chao HT, Lee SY, Lee HM, Liao TL, Weih YH, Kao SH (2005) Repeated ovarian stimulations induce oxidative damage and mitochondrial DNA mutations in mouse ovaries. Ann N Y Acad Sci 1042:148–156

    CAS  Google Scholar 

  • Chen AQ, Liu ZW, Yang ZG, Leng XJ (2012) Characterization of bmp15 and its regulation by human chorionic gonadotropin in the follicle of gibel carp (Carassius auratus gibelio). Comp Biochem Physiol B Biochem Mol Biol 163:121–128

    CAS  Google Scholar 

  • Counihan JL, Duckering M, Dalvie E, Ku WM, Bateman LA, Fisher KJ, Nomura DK (2017) Chemoproteomic profiling of acetanilide herbicides reveals their role in inhibiting fatty acid oxidation. ACS Chem Biol 12:635–642

    CAS  Google Scholar 

  • Craig ZR, Leslie TC, Hatfield KP, Gupta RK, Flaws JA (2010) Mono-hydroxy methoxychlor alters levels of key sex steroids and steroidogenic enzymes in cultured mouse antral follicles. Toxicol Appl Pharmacol 249:107–113

    CAS  Google Scholar 

  • de Castro F, Morón FJ, Montoro L, Montoro L, Real LM, Ruiz A (2005) Pharmacogenetics of controlled ovarian hyperstimulation. Pharmacogenomics 6:629–637

    Google Scholar 

  • Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM (1996) Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383:531–535

    CAS  Google Scholar 

  • Fu L, Lu X, Tan J, Wang L, Chen J (2018) Multiresidue determination and potential risks of emerging pesticides in aquatic products from Northeast China by LC-MS/MS. J Environ Sci 63:116–125

    Google Scholar 

  • Halm S, Ibáñez AJ, Tyler CR, Prat F (2008) Molecular characterisation of growth differentiation factor 9 (gdf9) and bone morphogenetic protein 15 (bmp15) and their patterns of gene expression during the ovarian reproductive cycle in the European Seabass. Mol Cell Endocrinol 291:95–103

    CAS  Google Scholar 

  • Hladik ML, Bouwer EJ, Roberts AL (2008) Neutral chloroacetamide herbicide degradates and related compounds in Midwestern United States drinking water sources. Sci Total Environ 390:155–165

    CAS  Google Scholar 

  • Jones PD, De Coen WM, Tremblay L, Giesy JP (2000) Vitellogenin as a biomarker for environmental estrogens. Water Sci Technol 42:1–14

    CAS  Google Scholar 

  • Li W, Zha J, Li Z, Yang L, Wang Z (2009) Effects of exposure to acetochlor on the expression of thyroid hormone related genes in larval and adult rare minnow (Gobiocypris rarus). Aquat Toxicol 94:87–93

    CAS  Google Scholar 

  • Li L, Wang M, Chen S, Zhao W, Zhao Y, Wang X, Zhang Y (2015) A urinary metabonomics analysis of long-term effect of acetochlor exposure on rats by ultra-performance liquid chromatography/mass spectrometry. Pestic Biochem Physiol 128:82–88

    Google Scholar 

  • Li L, Wang M, Chen S, Zhao W, Zhao Y, Wang X, Zhang Y (2016) A urinary metabonomics analysis of long-term effect of acetochlor exposure on rats by ultra-performance liquid chromatography/mass spectrometry. Pestic Biochem Physiol 128:82–88

    CAS  Google Scholar 

  • Liu Y, Zhang Y, Liu J, Huang D (2006) The role of reactive oxygen species in the herbicide acetochlor-induced DNA damage on Bufo raddei tadpole liver. Aquat Toxicol 78:21–26

    CAS  Google Scholar 

  • Liu Z, Chen A, Yang Z, Wei H, Leng X (2012) Molecular characterization of growth differentiation factor 9 and its spatio-temporal expression pattern in gibel carp (Carassius auratus gibelio). Mol Biol Rep 39:3863–3870

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    CAS  Google Scholar 

  • Martin-Romero FJ, Ortiz-de-Galisteo JR, Lara-Laranjeira J, Dominguez-Arroyo JA, Gonzalez-Carrera E, Alvarez IS (2008) Store-operated calcium entry in human oocytes and sensitivity to oxidative stress. Biol Reprod 78:307–315

    CAS  Google Scholar 

  • Nemeth-Konda L, Fuleky G, Morovjan G, Csokan P (2002) Sorption behaviour of acetochlor, atrazine, carbendazim, diazinon, imidacloprid and isoproturon on Hungarian agricultural soil. Chemosphere 48:545–552

    CAS  Google Scholar 

  • Rollerova E, Gasparova Z, Wsolova L, Urbancikova M (2000) Interaction of acetochlor with estrogen receptor in the rat uterus. acetochlor-possible endocrine modulator? Gen Physiol Biophys 19:73–84

    CAS  Google Scholar 

  • Rollerova E, Wsolova L, Urbancikova M (2011) Neonatal exposure to herbicide acetochlor alters pubertal development in female wistar rats. Toxicol Mech Methods 21:406–417

    CAS  Google Scholar 

  • Ruder EH, Hartman TJ, Blumberg J, Goldman MB (2008) Oxidative stress and antioxidants: exposure and impact on female fertility. Hum Reprod Update 14:345–357

    CAS  Google Scholar 

  • Sies H (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82:291–295

    CAS  Google Scholar 

  • Simpson ER, Mahendroo MS, Means GD, Kilgore MW, Hinshelwood MM, Graham-Lorence S, Amarneh B, Ito Y, Fisher CR, Michael MD, Et A (1994) Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev 15:342–355

    CAS  Google Scholar 

  • Song X, Zhang F, Chen D, Bian Q, Zhang H, Liu X, Zhu B (2019) Study on systemic and reproductive toxicity of acetochlor in male mice. Toxicol Res 8:77–89

    CAS  Google Scholar 

  • Sun X, Zhou Q, Ren W, Li X, Ren L (2011) Spatial and temporal distribution of acetochlor in sediments and riparian soils of the Songhua River Basin in northeastern China. J Environ Sci 23:1684–1690

    CAS  Google Scholar 

  • Thomas FH, Vanderhyden BC (2006) Oocyte-granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth. Reprod Biol Endocrinol 4:1–8

    Google Scholar 

  • Van Weerd JH, Richter CJJ (1991) Sex pheromones and ovarian development in teleost fish. Comp Biochem Physiol C 100:517–527

    Google Scholar 

  • Vitt UA, McGee EA, Hayashi M, Hsueh AJ (2000) In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. Endocrinology 141:3814–3820

    CAS  Google Scholar 

  • Wang Z, Lu Y, Wang Y, Ma M (2002) Assessing the ecological risk of substituted benzenes in Huaihe River, China. Acta Sci Circumst 22:300–303

    CAS  Google Scholar 

  • Wang H, Meng Z, Zhou L, Cao Z, Liao X, Ye R, Lu H (2019) Effects of acetochlor on neurogenesis and behaviour in zebrafish at early developmental stages. Chemosphere 220:954–964

    CAS  Google Scholar 

  • Xu C, Tu W, Deng M, Jin Y, Lu B, Zhang C, Lin C, Wu Y, Liu W (2016) Stereoselective induction of developmental toxicity and immunotoxicity by acetochlor in the early life stage of zebrafish. Chemosphere 164:618–626

    CAS  Google Scholar 

  • Yan C, Wang P, DeMayo J, DeMayo FJ, Elvin JA, Carino C, Prasad SV, Skinner SS, Dunbar BS, Dube JL (2001) Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol 15:854–866

    CAS  Google Scholar 

  • Yang M, Hu J, Li S, Ma Y, Gui W, Zhu G (2016) Thyroid endocrine disruption of acetochlor on zebrafish (Danio rerio) larvae. J Appl Toxicol 36:844–852

    CAS  Google Scholar 

  • Yin XH, Li SN, Zhang L, Zhu GN, Zhuang HS (2008) Evaluation of DNA damage in Chinese toad (Bufo bufo gargarizans) after in vivo exposure to sublethal concentrations of four herbicides using the comet assay. Ecotoxicology 17:280–286

    CAS  Google Scholar 

  • Yu Z, Jin F, Li H, An W, Yang M (2014) Residual levels of acetochlor in source water and drinking water of China's major cities. Environ Sci 35:1694–1697

    Google Scholar 

  • Zerin T, Song H, Kim Y (2015) Extracellular signal-regulated kinase pathway play distinct role in acetochlor-mediated toxicity and intrinsic apoptosis in A549 cells. Toxicol In Vitro 29:85–92

    CAS  Google Scholar 

  • Zhang X, Gao L, Yang K, Tian H, Wang W, Ru S (2013a) Monocrotophos pesticide modulates the expression of sexual differentiation genes and causes phenotypic feminization in zebrafish (Danio rerio). Comp Biochem Physiol C Toxicol Pharmacol 157:33–40

    CAS  Google Scholar 

  • Zhang J, Liang W, Wu X, Jiang S, Li Q (2013b) Toxic effects of acetochlor on mortality, reproduction and growth of Caenorhabditis elegans and Pristionchus pacificus. Bull Environ Contam Toxicol 90:364–368

    CAS  Google Scholar 

  • Zhang Y, Yuan C, Qin F, Hu G, Wang Z (2014) Molecular characterization of gdf9 and bmp15 genes in rare minnow Gobiocypris rarus and their expression upon bisphenol A exposure in adult females. Gene 546:214–221

    CAS  Google Scholar 

  • Zhang Y, Wu L, Zhang G, Guan Y, Wang Z (2016) Effect of low-dose malathion on the gonadal development of adult rare minnow Gobiocypris rarus. Ecotoxicol Environ Saf 125:135–140

    CAS  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (31800435).

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Correspondence to Wenzhi Wei.

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The authors declare that they have no conflict of interest.

All experimental procedures were approved by the animal ethics committee of Yangzhou University. Fish were humanely treated during the whole experiment.

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Responsible Editor: Cinta Porte

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Zhang, Y., Xue, W., Long, R. et al. Acetochlor affects zebrafish ovarian development by producing estrogen effects and inducing oxidative stress. Environ Sci Pollut Res 27, 27688–27696 (2020). https://doi.org/10.1007/s11356-020-09050-2

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