The brominated flame retardant, TBCO, impairs oocyte maturation in zebrafish (Danio rerio)

Darren Van Essen; Alper James G Alcaraz; Justin G P Miller; Paul D Jones; Jon A Doering; Steve Wiseman

doi:10.1016/j.aquatox.2021.105929

The brominated flame retardant, TBCO, impairs oocyte maturation in zebrafish (Danio rerio)

Aquat Toxicol. 2021 Aug 3:238:105929. doi: 10.1016/j.aquatox.2021.105929. Online ahead of print.

Authors

Darren Van Essen¹, Alper James G Alcaraz², Justin G P Miller¹, Paul D Jones³, Jon A Doering⁴, Steve Wiseman⁵

Affiliations

¹ Department of Biological Sciences, University of Lethbridge, Lethbridge, Alberta, T1K 3M4, Canada.
² Toxicology Centre, University of Saskatchewan, Saskatoon, SK, S7N 5B3, Canada.
³ Toxicology Centre, University of Saskatchewan, Saskatoon, SK, S7N 5B3, Canada; School of Environment and Sustainability, University of Saskatchewan, Saskatoon, SK, S7N 5B3, Canada.
⁴ Department of Biological Sciences, University of Lethbridge, Lethbridge, Alberta, T1K 3M4, Canada; Intersectoral Centre for Endocrine Disruptor Analysis (ICEDA), Institut National de la Recherche Scientifique (INRS), Centre Eau Terre Environnement, Québec City, QC, G1K 9A9, Canada.
⁵ Department of Biological Sciences, University of Lethbridge, Lethbridge, Alberta, T1K 3M4, Canada; Intersectoral Centre for Endocrine Disruptor Analysis (ICEDA), Institut National de la Recherche Scientifique (INRS), Centre Eau Terre Environnement, Québec City, QC, G1K 9A9, Canada; Water Institute for Sustainable Environments, University of Lethbridge, Lethbridge, AB, T1K 3M4, Canada. Electronic address: steve.wiseman@uleth.ca.

PMID: 34375885
DOI: 10.1016/j.aquatox.2021.105929

Abstract

The brominated flame retardant, 1,2,5,6-tetrabromocyclooctane (TBCO), has been shown to decrease fecundity in Japanese medaka (Oryzias latipes) and there is indirect evidence from analysis of the transcriptome and proteome that this effect might be due to impaired oogenesis. An assay for disruption of oocyte maturation by chemical stressors has not been developed in Japanese medaka. Thus, using zebrafish (Danio rerio) as a model, objectives of the present study were to determine whether exposure to TBCO has effects on maturation of oocytes and to investigate potential mechanisms. Sexually mature female zebrafish were given a diet of 35.3 or 628.8 μg TBCO / g food for 14 days after which, stage IV oocytes were isolated to assess maturation in response to maturation inducing hormone. To explore potential molecular mechanisms, abundances of mRNAs of a suite of genes that regulate oocyte maturation were quantified by use of quantitative real-time PCR, and abundances of microRNAs were determined by use of miRNAseq. Ex vivo maturation of oocytes from fish exposed to TBCO was significantly less than maturation of oocytes from control fish. The percentage of oocytes which matured from control fish and those exposed to low and high TBCO were 89, 71, and 67%, respectively. Among the suite of genes known to regulate oocyte maturation, mRNA abundance of insulin like growth factor-3 was decreased by 1.64- and 3.44-fold in stage IV oocytes from females given the low and high concentrations of TBCO, respectively, compared to the control group. Abundances of microRNAs regulating the expression of proteins that regulate oocyte maturation, including processes related to insulin-like growth factor, were significantly different in stage IV oocytes from fish exposed to TBCO. Overall, results of this study indicated that impaired oocyte maturation might be a mechanism of reduced reproductive performance in TBCO-exposed fish. Results also suggested that effects of TBCO on oocyte maturation might be due to molecular perturbations on insulin-like growth factor signaling and expression of microRNAs.

Keywords: Insulin like growth factor 3; Maturation inducing hormone; Membrane progestin receptor; MicroRNA; Oogenesis; Reproduction.