Resveratrol Protects against Zearalenone-Induced Mitochondrial Defects during Porcine Oocyte Maturation via PINK1/Parkin-Mediated Mitophagy

Toxins (Basel). 2022 Sep 16;14(9):641. doi: 10.3390/toxins14090641.

Abstract

Mitochondria hold redox homeostasis and energy metabolism as a crucial factor during oocyte maturation, while the exposure of estrogenic mycotoxin zearalenone causes developmental incapacity in porcine oocyte. This study aimed to reveal a potential resistance of phytoalexin resveratrol against zearalenone during porcine oocyte maturation and whether its mechanism was related with PTEN-induced kinase 1 (PINK1)/Parkin-mediated mitophagy. Porcine oocytes were exposed to 20 μM zearalenone with or without 2 μM resveratrol during in vitro maturation. As for the results, zearalenone impaired ultrastructure of mitochondria, causing mitochondrial depolarization, oxidative stress, apoptosis and embryonic developmental incapacity, in which mitophagy was induced in response to mitochondrial dysfunction. Phytoalexin resveratrol enhanced mitophagy through PINK1/Parkin in zearalenone-exposed oocytes, manifesting as enhanced mitophagy flux, upregulated PINK1, Parkin, microtubule-associated protein light-chain 3 beta-II (LC3B-II) and downregulated substrates mitofusin 2 (MFN2), voltage-dependent anion channels 1 (VDAC1) and p62 expressions. Resveratrol redressed zearalenone-induced mitochondrial depolarization, oxidative stress and apoptosis, and accelerated mitochondrial DNA copy during maturation, which improved embryonic development. This study offered an antitoxin solution during porcine oocyte maturation and revealed the involvement of PINK1/Parkin-mediated mitophagy, in which resveratrol mitigated zearalenone-induced embryonic developmental incapacity.

Keywords: PINK1/Parkin; mitophagy; porcine oocyte; resveratrol; zearalenone.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antitoxins* / metabolism
  • DNA, Mitochondrial
  • Microtubule-Associated Proteins / metabolism
  • Mitochondria / metabolism
  • Mitophagy / genetics
  • Oocytes / metabolism
  • Phytoalexins
  • Protein Kinases
  • Resveratrol / pharmacology
  • Sesquiterpenes
  • Swine
  • Ubiquitin-Protein Ligases / genetics
  • Zearalenone* / metabolism
  • Zearalenone* / toxicity

Substances

  • Antitoxins
  • DNA, Mitochondrial
  • Microtubule-Associated Proteins
  • Sesquiterpenes
  • Zearalenone
  • Ubiquitin-Protein Ligases
  • Protein Kinases
  • Resveratrol
  • Phytoalexins

Grants and funding

This research was funded by the National Key Research and Development Plan, grant number 2021YFD1200301; Chongqing Technology Innovation and Application Development Project, grant number CSTC2021-JSCX-DXWTBX0004; and Ningbo Science and Technology Innovation 2025 Major Project, grant number 2019B10023.