Maternal Zearalenone Exposure Affects Gut Microbiota and Follicular Development in Suckled Offspring

J Agric Food Chem. 2022 Dec 14;70(49):15570-15582. doi: 10.1021/acs.jafc.2c06457. Epub 2022 Dec 1.

Abstract

Zearalenone (ZEN) is a mycotoxin that is widely present in feed and agricultural products. Studies have demonstrated that ZEN, as a type of estrogen analogue, can significantly affect the female reproductive system. Breast milk is the best nutrient for infant growth and development, but it is still unknown whether ZEN influences the fertility of offspring through suckling. In this study, we collected fecal and ovarian tissue from neonatal female offspring, whose mothers were exposed to ZEN for 21 days, and explored the effects of maternal ZEN exposure on intestinal microecology and follicular development in the mouse using 16S rRNA amplicon sequencing technology. Our findings suggested that maternal ZEN exposure significantly diminished ovarian reserve, increased apoptosis of ovarian granulosa cell (GC), and impacted the developmental competence of oocytes in lactating offspring. In addition, the results of 16S rRNA sequencing showed that the abundance of gut microbiota in offspring was significantly changed, including Bacteroidetes, Proteobacteria, and Firmicutes. This leads to alterations of glutathione metabolism and the expression of antioxidant enzymes in ovaries. In summary, our findings supported a potential relationship between gut microbiota and abnormal ovarian development caused by ZEN, which offers novel insights for therapeutic strategies for reproductive disorders induced by ZEN exposure.

Keywords: follicle development; glutathione metabolism; gut microbiota; mouse; oocyte; zearalenone.

MeSH terms

  • Animals
  • Female
  • Gastrointestinal Microbiome*
  • Humans
  • Lactation
  • Maternal Exposure / adverse effects
  • Mice
  • RNA, Ribosomal, 16S / genetics
  • Zearalenone* / toxicity

Substances

  • Zearalenone
  • RNA, Ribosomal, 16S