Transcriptional changes caused by estrogenic endocrine disrupting chemicals in gonad-mesonephros complexes of genetic male Xenopus laevis: Multiple biomarkers for early detection of testis differentiation disruption

Shen, Yanping; Li, Yuanyuan; Zhu, Min; Li, Jinbo; Qin, Zhan-Fen

doi:10.1016/j.scitotenv.2020.138522

Cited by 9 publications

(4 citation statements)

References 43 publications

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“…Testosterone is a steroid hormone and a Cyp17-derivative of pregnenolone or progesterone precursors. Cyp17 expression have recently been found in gonad-mesonephros complex in X. laevis tadpoles, showing that androgen synthesis is possible ( 72 ). Testosterone is the main sex hormone in vertebrate males.…”

Section: Discussionmentioning

confidence: 99%

Relationship between serum thyroid hormones and their associated metabolites, and gene expression bioindicators in the back skin of Rana [Lithobates] catesbeiana tadpoles and frogs during metamorphosis

et al. 2023

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Anuran metamorphosis is characterized by profound morphological changes including remodeling of tissues and organs. This transition is initiated by thyroid hormones (THs). However, the current knowledge of changing levels of THs during metamorphosis relies on pooled samples using methods known for high variability with sparse reporting of measured variation. Moreover, establishing a clear linkage between key gene expression bioindicators and TH levels throughout the metamorphic process is needed. Using state-of-the-art ultra-high performance liquid chromatography isotope-dilution tandem mass spectrometry, we targeted 12 THs and metabolites in the serum of Rana [Lithobates] catesbeiana (n=5-10) across seven distinct postembryonic stages beginning with premetamorphic tadpoles (Gosner stage 31-33) and continuing through metamorphosis to a juvenile frog (Gosner stage 46). TH levels were related to TH-relevant gene transcripts (thra, thrb, and thibz) in back skin of the same individual animals. Significant increases from basal levels were observed for thyroxine (T4) and 3,3’,5-triiodothyronine (T3) at Gosner stage 41, reaching maximal levels at Gosner stage 44 (28 ± 10 and 2.3 ± 0.5 ng/mL, respectively), and decreasing to basal levels in juvenile frogs. In contrast, 3,5-diiodothyronine (T2) increased significantly at Gosner stage 40 and was maintained elevated until stage 44. While thra transcript levels remained constant and then decreased at the end of metamorphic climax, thrb and thibz were induced to maximal levels at Gosner stage 41, followed by a decrease to basal levels in the froglet. This exemplifies the exquisite timing of events during metamorphosis as classic early response genes are transcribed in anticipation of peak TH concentrations. The distinct T2 concentration profile suggests a biological role of this biomolecule in anuran postembryonic development and an additional aspect that may be a target of anthropogenic chemicals that can disrupt anuran metamorphosis and TH signalling. Hence, as a second aim of the study, we set out to find additional bioindicators of metamorphosis, which can aid future investigations of developmental disruption. Using a sensitive nanoLC-Orbitrap system an untargeted analysis workflow was applied. Among 6,062 endogenous metabolites, 421 showed metamorphosis-dependent concentration dynamics. These potential bioindicators included several carnitines, prostaglandins and some steroid hormones.

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Section: Discussionmentioning

confidence: 99%

Relationship between serum thyroid hormones and their associated metabolites, and gene expression bioindicators in the back skin of Rana [Lithobates] catesbeiana tadpoles and frogs during metamorphosis

et al. 2023

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“…crabp2b (cellular retinoic acid binding protein 2b) is involved in the morphogenesis of the hindbrain and the regulation of the retinoic acid receptor signalling pathway during embryonic development and it is thought to stimulate spermatogonial development in zebrafish through an increase in germ cell proliferation activity [ 79 ]. The psmd10 (26S proteasome non-ATPase regulatory subunit 10) gene is supposed to be involved in cell proliferation and testicular differentiation and was proposed as a biomarker to detect the disruption of testis differentiation by oestrogenic endocrine disruptors in Xenopus laevis [ 80 ].…”

Section: Discussionmentioning

confidence: 99%

Effect of high temperatures on sex ratio and differential expression analysis (RNA-seq) of sex-determining genes in Oreochromis niloticus from different river basins in Benin

Fagbémi,

Nivelle,

Muller

et al. 2023

Environmental Epigenetics

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The high temperature sex reversal process leading to functional phenotypic masculinization during development has been widely described in Nile tilapia (Oreochromis niloticus) under laboratory or aquaculture conditions and in the wild. In this study, we selected five wild populations of O. niloticus from different river basins in Benin and produced twenty full-sib families of mixed-sex (XY and XX) by natural reproduction. Progenies were exposed to room temperature or high (36.5°C) temperatures between 10 and 30 days post-fertilization (dpf). In control groups, we observed sex ratios from 40 to 60% males as expected, except for 3 families from the Gobé region which showed a bias towards males. High temperature treatment significantly increased male rates in each family up to 88%. Transcriptome analysis was performed by RNA-sequencing (RNA-seq) on brains and gonads from control and treated batches of six families at 15 dpf and 40 dpf. Analysis of differentially expressed genes, differentially spliced genes, and correlations with sex reversal was performed. In 40 dpf gonads, genes involved in sex determination such as dmrt1, cyp11c1, amh, cyp19a1b, ara, and dax1 were upregulated. In 15 dpf brains, a negative correlation was found between the expression of cyp19a1b and the reversal rate, while at 40 dpf a negative correlation was found between the expression of foxl2, cyp11c1, and sf1 and positive correlation was found between dmrt1 expression and reversal rate. Ontology analysis of the genes affected by high temperatures revealed that male sex differentiation processes, primary male sexual characteristics, autophagy, and cilium organization were affected. Based on these results, we conclude that sex reversal by high temperature treatment leads to similar modifications of the transcriptomes in the gonads and brains in offspring of different natural populations of Nile tilapia, which thus may activate a common cascade of reactions inducing sex reversal in progenies.

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“…Some studies [12][13][14][15] found that DES had a damaging impact on male Sprague-Dawley rattos' reproductive systems through decreasing the numbers of spermatogonia, Sertoli cells, and Leydig cells, which affect steroidogenesis and spermatogenesis. Estrogenic endocrinedisrupting chemical (EDC) exposure, including to E2, DES, mestranol, and 4-n-nonyphenol, disrupts testis differentiation and causes xenopus laevis feminization to different degrees [16].…”

Section: Introductionmentioning

confidence: 99%

Effects of Diethylstilbestrol on Zebrafish Gonad Development and Endocrine Disruption Mechanism

Xie

Liu

2021

Biomolecules

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Environmental estrogen is a substance that functions as an endocrine hormone in organisms and can cause endocrine system disruption. A typical environmental estrogen, diethylstilbestrol (DES), can affect normal sexual function and organism development. However, even though the effects of different exposure stages of DES on the endocrine system and gonadal development of zebrafish juveniles are unknown, sex determination is strongly influenced by endocrine-disrupting chemicals (EDCs). From 10–90 days post fertilization (dpf), juvenile zebrafish were exposed to DES (100 and 1000 ng/L) in three different stages (initial development stage (IDS), 10–25 dpf; gonadal differentiation stage (GDS), 25–45 dpf and gonadal maturity stage (GMS), 45–60 dpf). Compared with that of IDS and GMS, the growth indicators (body length, body weight, and others) decreased significantly at GDS, and the proportion of zebrafish females exposed to 100 ng/L DES was significantly higher (by 59.65%) than that of the control; in addition, the zebrafish were biased towards female differentiation. The GDS is a critical period for sex differentiation. Our results show that exposure to environmental estrogen during the critical gonadal differentiation period not only affects the development of zebrafish, but also affects the population development.

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Transcriptional changes caused by estrogenic endocrine disrupting chemicals in gonad-mesonephros complexes of genetic male Xenopus laevis: Multiple biomarkers for early detection of testis differentiation disruption

Cited by 9 publications

References 43 publications

Relationship between serum thyroid hormones and their associated metabolites, and gene expression bioindicators in the back skin of Rana [Lithobates] catesbeiana tadpoles and frogs during metamorphosis

Relationship between serum thyroid hormones and their associated metabolites, and gene expression bioindicators in the back skin of Rana [Lithobates] catesbeiana tadpoles and frogs during metamorphosis

Effect of high temperatures on sex ratio and differential expression analysis (RNA-seq) of sex-determining genes in Oreochromis niloticus from different river basins in Benin

Effects of Diethylstilbestrol on Zebrafish Gonad Development and Endocrine Disruption Mechanism

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