Disruption of sex steroid hormones biosynthesis by short-term enrofloxacin antibiotic exposure in Carassius auratus var. Pengze

Chemosphere. 2023 Dec:344:140315. doi: 10.1016/j.chemosphere.2023.140315. Epub 2023 Sep 26.

Abstract

Background: It has been reported that antibiotic enrofloxacin can impair reproductive function of mammals, induces multi-generational oscillatory effects on reproduction of Caenorhabditis elegans, and disturbes endocrine system in grass carp.

Objectives: This study aims to explore the effect of short-term enrofloxacin exposure on sex steroid hormones biosynthesis in Carassius auratus var. Pengze through assessing the contents of growth hormone (GH), thyroid hormone 4 (T4), estradiol (E2) and testosterone (T) in plasma, and investigating sex steroid hormones biosynthesis based on targeted metabonomics analysis, and determining expression level of some important genes, gonadotropin-releasing hormone (gnrh), gonadotropin hormone 1-β (gth1-β), gonadotropin hormone 2-β (gth2-β) and cyp19a1a in hypothalamus-pituitary-ovary axis (HPOA).

Results: We found that short-term exposure of enrofloxacin disordered contents of E2 and T in plasma of fish determined by ELISA detection, T content elevation and E2 content decline, which was confirmed by the following data from targeted metabonomics analysis of plasma. The metabonomic results showed that both T and its upstream intermediate products during the process of sex steroid hormones biosynthesis in fish were increased significantly, but E2 content was decreased markedly. At the exposure 24 h of enrofloxacin, expression of gnrh in hypothalamus, gth1-β and gth2-β in pituitary were promoted. Meanwhile GH and T4 contents in plasma, two inducers of sex steroid hormones synthesis, were augmented, which indicated that sex steroid hormones biosynthesis was improved. However cyp19a1a expression in ovary was repressed, and content of estriol (E3) was upregulated. These data suggested that enrofloxacin promoted sex steroid hormones biosynthesis and conversion of E2 to estriol (E3), but inhibited the conversion of T to E2. Finally, content of E2 was declined sharply.

Discussion: Animal specific antibacterial enrofloxacin is widely detectable in aquatic ecosystem, exposure of the agent can induce adverse effects on plants and animals. This study firstly evidenced induction of disruption of sex steroid hormones by enrofloxacin in fish, which indicates enrofloxacin is an endocrine disruption compound that can induce endocrine disruption of animals, including fish.

Keywords: Crucian carp; Enrofloxacin; Sex steroid hormones; Targeted metabonomics analysis.

MeSH terms

  • Animals
  • Anti-Bacterial Agents* / metabolism
  • Anti-Bacterial Agents* / toxicity
  • Ecosystem
  • Enrofloxacin
  • Estradiol / metabolism
  • Estriol
  • Female
  • Goldfish* / metabolism
  • Gonadal Steroid Hormones / metabolism
  • Gonadotropin-Releasing Hormone / metabolism
  • Gonadotropins / metabolism
  • Growth Hormone / genetics
  • Mammals / metabolism

Substances

  • Enrofloxacin
  • Anti-Bacterial Agents
  • Gonadal Steroid Hormones
  • Growth Hormone
  • Estradiol
  • Gonadotropin-Releasing Hormone
  • Gonadotropins
  • Estriol