Skip to main content
SpringerLink
Log in

Effects of Broflanilide on Oxidative Stress and Expression of Apoptotic Genes in Zebrafish (Danio rerio) Gill

  • Published:
Bulletin of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Broflanilide exerted negative impacts on the gill of zebrafish. Thus, in this study, zebrafish gill was used to assess the apoptosis toxicity of broflanilide by determining the levels of reactive oxygen species (ROS), superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx), and malondialdehyde (MDA) and apoptosis-related genes. The results found that the minimum threshold for the content and time of broflanilide affecting enzyme content and gene expression was 0.26 mg/L after 24 h exposure. After 96 h exposure, broflanilide could cause apoptosis and exerted significantly increased contents of ROS and MDA, while inhibiting the activities of SOD, CAT, and GPx at 0.26 and 0.57 mg/L. Broflanilide also had adverse effects on apoptosis-related genes, such as tumor protein p53 (p53), associated × (Bax), B-cell lymphama-2 (Bcl-2), caspase-3, caspase-9, and apoptotic protease activating factor-1(apaf-1), at 0.26 mg/L and 0.57 mg/L after 96 h exposure, respectively. These results provide new insight into the potential toxicity mechanisms of broflanilide in zebrafish gills.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Chai T, Cui F, Mu X et al (2016) Stereoselective induction by 2,2,3,4,6-pentachlorobiphenyl in adult zebrafish (Danio rerio): Implication of chirality in oxidative stress and bioaccumulation. Environ Pollut 215:66–76

    Article  CAS  Google Scholar 

  • Chen R, Cui Y, Zhang X et al (2018) Chlorpyrifos induction of testicular-cell apoptosis through generation of reactive oxygen species and phosphorylation of AMP. J Agr Food Chem 66(47):12455–12470. https://doi.org/10.1021/acs.jafc.8b03407

    Article  CAS  Google Scholar 

  • Cheng Z, Wang J, Shuai Z (2017) Acute and subchronic toxicity of pyraclostrobin in zebrafish (Danio rerio). Chemosphere 188:510

    Article  Google Scholar 

  • Chipuk JE, Kuwana T, Bouchier-Hayes L et al (2004) Direct activation of bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303(5660):1010–1014

    Article  CAS  Google Scholar 

  • Danion M, Floch SL, Lamour F (2014) Effects of in vivo chronic exposure to pendimethalin on EROD activity and antioxidant defenses in rainbow trout (Oncorhynchus mykiss). Ecotox Environ Safe 99:21–27

    Article  CAS  Google Scholar 

  • David B, Genan AA, Christopher SR et al (2013) Subtle alterations in swimming speed distributions of rainbow trout exposed to titanium dioxide nanoparticles are associated with gill rather than brain injury. Aquat Toxicol 126(15):116–127

    Google Scholar 

  • Dechao L, Eisaku U, Tsuyoshi K et al (2004) Reactive oxygen species (ROS) control the expression of Bcl-2 family proteins by regulating their phosphorylation and ubiquitination. Cancer Sci 95(8):644–650

    Article  Google Scholar 

  • Dilek E, Ayla Ç et al (2017) Apoptotic gene expression profiles and DNA damage levels in rat liver treated with perfluorooctane sulfonate and protective role of curcumin. Int J Biol Macromol 104:515–520

    Article  Google Scholar 

  • Eze JI, Anene BM, Chukwu CC (2008) Determination of serum and organ malondialdehyde (MDA) concentration, a lipid peroxidation index, in Trypanosoma brucei-infected rats. Comp Clin Path 17(2):67–72

    Article  CAS  Google Scholar 

  • Festilă I, Miresan V, Răducu C et al (2013) Evaluation of oxidative stress in dairy cows through antioxidant enzymes glutathione peroxidase (GPX) and superoxide dismutase (SOD). Bull UASVM Anim Sci Biotech 69:1–2

    Google Scholar 

  • Fulda S, Gorman AM, Hori O et al (2010) Cellular stress responses: cell survival and cell death. Int J Cell Biol 2010:1–23

    Google Scholar 

  • Galluzzi L, López-Soto A, Kumar S et al (2016) Caspases connect cell-death signaling to organismal homeostasis. Immunity 44(2):221–231

    Article  CAS  Google Scholar 

  • Gao X, Zheng Y, Ruan X et al (2018) Salinomycin induces primary chicken cardiomyocytes death via mitochondria mediated apoptosis. Chem-Biol Interact 282:45–54

    Article  CAS  Google Scholar 

  • Gonzalez P, Baudrimont M, Boudou A et al (2006) Comparative effects of direct cadmium contamination on gene expression in gills, liver, skeletal muscles and brain of the zebrafish (Danio rerio). Biometals 19(3):225–235

    Article  CAS  Google Scholar 

  • Heron T, Manoel J, Cauê SL (2022) A canthin-6-one derivative induces cell death by apoptosis/necroptosis-like with DNA damage in acute myeloid cells. Biomed Pharmacother 145:112439

    Article  Google Scholar 

  • Huang Q, Bu S, Yu Y et al (2007) Diazoxide prevents diabetes through inhibiting pancreatic beta-cells from apoptosis via Bcl-2/Bax rate and p38-beta mitogen-activated protein kinase. Endocrinol 148(1):81–91

    Article  CAS  Google Scholar 

  • Jia K, Cheng B, Huang L et al (2020) Thiophanate-methyl induces severe hepatotoxicity in zebrafish. Chemosphere 248:125941

    Article  CAS  Google Scholar 

  • Jiang J, Wu S, Wang Y et al (2015) Carbendazim has the potential to induce oxidative stress, apoptosis, immunotoxicity and endocrine disruption during zebrafish larvae development. Toxicolin Vitro 29(7):1473–1481

    Article  CAS  Google Scholar 

  • Jiao W, Han Q, Xu Y et al (2019) Impaired immune function and structural integrity in the gills of common carp (Cyprinus carpio L.) caused by chlorpyrifos exposure: Through oxidative stress and apoptosis. Fish Shellfish Immun 86:239–245

    Article  CAS  Google Scholar 

  • Jin Y, Zheng S, Pu Y et al (2011) Cypermethrin has the potential to induce hepatic oxidative stress, DNA damage and apoptosis in adult zebrafish (Danio rerio). Chemosphere 82(3):398–404

    Article  CAS  Google Scholar 

  • Li X, Liu H, Li D (2021) Dietary seleno-l-methionine causes alterations in neurotransmitters, ultrastructure of the brain, and behaviors in zebrafish (Danio rerio). Environ Sci Technol 55(17):11894–11905

    Article  CAS  Google Scholar 

  • Lisenn L, Pierre-François C, Philippe J et al (2007) Bax activation and mitochondrial insertion during apoptosis. Apoptosis 12(5):887–896

    Article  Google Scholar 

  • Liu H, Wang F, Yao W (2019) Effection of triclosan on the expressions of apoptosis-related genes in male zebrafish gill tissue. Freshw Fisher 49(3):14–18

    Google Scholar 

  • Ma T, Zhou W, Chen K et al (2017) Toxicity effects of di-(2-ethylhexyl) phthalate to Eisenia fetida at enzyme, cellular and genetic levels. PLoS ONE 12(3):e0173957

    Article  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410

    Article  CAS  Google Scholar 

  • Mu X, Wang K, Chen X et al (2014) Impact of environmental concentrations of betacypermethrin on the antioxidant system in the brain and liver of zebrafish (Danio rerio). Chem Ecol 30:643–652

    Article  CAS  Google Scholar 

  • Peters LD, Livingstone DR (1996) Antioxidant enzyme activities inembryologic and early larval stages of turbot. J Fish Biol 49(5):986–997

    Article  CAS  Google Scholar 

  • Piret H, Žuravskaja M, Kärner M et al (2013) Apoptosis regulator BCL-2. Papers Anthropol 22:63–67

    Article  Google Scholar 

  • Shen N, Li Y, Leviticus K (2021) Effect of broflanilide on the phytophagous mite Tetranychus urticae and the predatory mite Typhlodromips swirskii. Pest Manage Sci 77(6):2964–2970

    Article  CAS  Google Scholar 

  • Song PP, Ping LW, Gao JP (2018) Ecotoxicological effects of fertilizers made from pulping waste liquor on earthworm Eisenia fetida. Ecotox Environ Saf 166:237–241

    Article  CAS  Google Scholar 

  • Srikanth K, Pereira E, Duarte AC (2013) Glutathione and its dependent enzymes’ modulatory responses to toxic metals and metalloids in fish-a review. Environ Sci Pollut Res 20:2133–2149

    Article  CAS  Google Scholar 

  • Vanessa SM, Liam C, Lorraine R et al (2002) Apoptosis initiated by Bcl-2-regulated caspase activation independently of the cytochrome c/Apaf-1/caspase-9 apoptosome. Nature 419(6907):634–637

    Article  Google Scholar 

  • Wang K, Wang C, Wang J (2022) Acute toxicity of broflanilide on neurosecretory system and locomotory behavior of zebrafish (Danio rerio). Chemosphere 305:135426

    Article  CAS  Google Scholar 

  • Winston GW, Moore MN, Kirchin MA (1996) Production of reactive oxygen species by hemocytes from the marine mussel, Mytilus edulis: lysosomal localization and effect of xenobiotics. Comp Biochem Phys C 113(2):221–229

    CAS  Google Scholar 

  • Wu S, Liu J, Shu L et al (2015) Anti-oxidative responses of zebrafish (danio rerio) gill, liver and brain tissues upon acute cold shock. Comp Biochem Physiol a: Mol Integr Physiol 187:202–213

    Article  CAS  Google Scholar 

  • Xu B, Zang S, Lang L et al (2020) Down-regulation of miR-383-5p suppresses apoptosis in oxidative stress rat hepatocytes by targeting Bcl2. J Anim Physiol an N 104(6):1948–1959

    Article  CAS  Google Scholar 

  • Yamashita M (2003) Apoptosis in zebrafish development. Comp Biochem Phys B 136(4):731–742

    Article  Google Scholar 

  • Yan S, Wang J, Zhu L (2015) Toxic effects of nitenpyram on antioxidant enzyme system and DN in zebrafish (Danio rerio) livers. Ecotox Environ Saf 122:54–60

    Article  CAS  Google Scholar 

  • Zhong Q, Elz A, Su G (2022) Sublethal doses of broflanilide prevents molting in the fall armyworm, Spodoptera frugiperda via altering molting hormone biosynthesis. Pestic Biochem Phys 181:105017

    Article  Google Scholar 

Download references

Acknowledgements

This work was funded by the Department of Science and Technology Liaoning Province (grant code: 2021JH2/10200016).

Author information

Author notes

  1. Kai Wang and Wunan Che contributed equally to this work.

Authors and Affiliations

  1. Plant Protection College, Shenyang Agricultural University, Shenyang, China

    Kai Wang, Wunan Che, Xiuwei Li & Lu He

  2. College of Science, China Agricultural University, Beijing, China

    Manman Duan & Chengju Wang

Authors
  1. Kai Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wunan Che
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Manman Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chengju Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiuwei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lu He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Kai Wang or Lu He.

Ethics declarations

Conflict of interest

No potential conflict of interest was reported by the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 15 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, K., Che, W., Duan, M. et al. Effects of Broflanilide on Oxidative Stress and Expression of Apoptotic Genes in Zebrafish (Danio rerio) Gill. Bull Environ Contam Toxicol 110, 91 (2023). https://doi.org/10.1007/s00128-023-03733-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00128-023-03733-5

Keywords

Search

Navigation