Zearalenone interferes with the sperm-triggered inflammation in the bovine uterus in vitro: Negative impact on sperm motility and survival

Reprod Toxicol. 2022 Jan:107:81-89. doi: 10.1016/j.reprotox.2021.12.001. Epub 2021 Dec 3.

Abstract

Zearalenone (ZEN)-contaminated diets induce detrimental effects on the bovine reproduction. Recently, we reported that active sperm induce pro-inflammatory responses in bovine endometrial epithelial cells (BEECs) in vitro. This study aimed to investigate the impact of presence of ZEN on the sperm-uterine crosstalk in vitro. BEECs monolayers were stimulated by ZEN (10, 100, and 1000 ng/mL) for 0, 3, 6, 12, or 24 h and gene expressions were analyzed by real-time PCR. Moreover, BEECs were pre-exposed to ZEN (10, 100, and 1000 ng/mL) for 24 h then, co-incubated with sperm for 6 h. Conditioned media (CM) from a sperm-BEECs co-culture, after pre-exposure to ZEN, were harvested and exploited to challenge either polymorphonuclear cells (PMNs) or sperm. Both PMNs phagocytic activity toward sperm and sperm motility parameters were then assessed. Results showed that ZEN alone induced pro-inflammatory responses in BEECs through the induction of mRNA expressions of pro-inflammatory cytokines (TNFA and IL1B) and PGES1 at different time points. Pre-exposure of BEECs to ZEN, amplified the sperm-triggered upregulation of pro-inflammatory cytokines (TNFA and IL1B) and chemokine IL8 mRNA abundance in BEECs. Sperm-BEECs conditioned media, primed by ZEN, stimulated the PMNs phagocytosis for sperm whereas suppressed sperm motility parameters. Taken together, these findings indicate that the presence of ZEN augments the pro-inflammatory cascade triggered by sperm in BEECs, provokes PMNs phagocytosis for sperm, and reduces sperm motility parameters. Such immunological reactions may create a hostile environment for sperm competence and survival in the bovine uterus, thus impair fertility.

Keywords: Bovine; Immunity; Inflammation; Sperm; Uterus; Zearalenone.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cattle
  • Cells, Cultured
  • Coculture Techniques
  • Cytokines / genetics
  • Epithelial Cells / drug effects
  • Estrogens, Non-Steroidal / toxicity*
  • Female
  • Inflammation* / genetics
  • Male
  • Neutrophils / physiology
  • Phagocytosis
  • Sperm Motility / drug effects*
  • Spermatozoa / drug effects*
  • Spermatozoa / physiology
  • Uterus* / cytology
  • Zearalenone / toxicity*

Substances

  • Cytokines
  • Estrogens, Non-Steroidal
  • Zearalenone