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Bisphenol A in oocytes leads to growth suppression and altered stress performance in juvenile rainbow trout.

ABSTRACT: BACKGROUND: Bisphenol A (BPA), used in the manufacture of plastics, is ubiquitously distributed in the aquatic environment. However, the effect of maternal transfer of these xenobiotics on embryonic development and growth is poorly understood in fish. We tested the hypothesis that BPA in eggs, mimicking maternal transfer, impact development, growth and stress performance in juveniles of rainbow trout (Oncorhynchus mykiss). METHODOLOGY/PRINCIPAL FINDINGS: Trout oocytes were exposed to 0, 30 and 100 microg.mL(-1) BPA for 3 h in ovarian fluid, followed by fertilization. The embryos were maintained in clean water and sampled temporally over 156-days post-fertilization (dpf), and juveniles were sampled at 400-dpf. The egg BPA levels declined steadily after exposure and were undetectable after 21- dpf. Oocyte exposure to BPA led to a delay in hatching and yolk absorption and a consistently lower body mass over 152-dpf. The growth impairment, especially in the high BPA group, correlated with higher growth hormone (GH) content and lower GH receptors gene expression. Also, mRNA abundances of insulin-like growth factors (IGF-1 and IGF-2) and their receptors were suppressed in the BPA treated groups. The juvenile fish grown from the BPA-enriched eggs had lower body mass and showed perturbations in plasma cortisol and glucose response to an acute stressor. CONCLUSION: BPA accumulation in eggs, prior to fertilization, leads to hatching delays, growth suppression and altered stress response in juvenile trout. The somatotropic axis appears to be a key target for BPA impact during early embryogenesis, leading to long term growth and stress performance defects in fish.

SUBMITTER: Aluru N

PROVIDER: S-EPMC2873997 | biostudies-literature | 2010

REPOSITORIES: biostudies-literature

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Bisphenol A in oocytes leads to growth suppression and altered stress performance in juvenile rainbow trout.

Aluru Neelakanteswar N Leatherland John F JF Vijayan Mathilakath M MM

PloS one 20100520 5

<h4>Background</h4>Bisphenol A (BPA), used in the manufacture of plastics, is ubiquitously distributed in the aquatic environment. However, the effect of maternal transfer of these xenobiotics on embryonic development and growth is poorly understood in fish. We tested the hypothesis that BPA in eggs, mimicking maternal transfer, impact development, growth and stress performance in juveniles of rainbow trout (Oncorhynchus mykiss).<h4>Methodology/principal findings</h4>Trout oocytes were exposed t ...[more]

PMID: 20505776

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Project description:We investigated the effects of chronic TCDD exposure on global gene expression in developing rainbow trout (Oncorhynchus mykiss). Juvenile rainbow trout (0.18M-BM-10.01g) were fed Biodiet starter with TCDD added at 0, 0.1, 1, 10 and 100ppb, and ten fish were sampled and pooled from each group for microarray experiments at 28 days after initiation of the exposure. Gene expression analysis was performed using the Genomics Research on All Salmonids Project (cGRASP) 16K cDNA microarrays. TCDD-responsive whole body transcripts identified in the microarray experiments have putative functions involved in various biological processes including cellular process, metabolic process, biological regulation, and response to stimulus. In addition, TCDD caused leisons in multiple organ systems in juvenile rainbow, including skin, oropharynx, liver, gas bladder, intestine, pancreas, nose and kidney. Juvenile rainbow trout (0.18M-BM-10.01g) were fed Biodiet starter (Bio-Oregon) (4% body weight per day) with TCDD added at 0, 0.1, 1, 10 and 100 ppb. Fish were sampled after 28 days. Total RNA from individual fish was isolated using TRIzol reagent (Invitrogen). Total RNA of ten control trout were pooled as a common reference which were labeled with Cy3. Total RNA of ten fish of each treatment were labeled wih Cy5. cDNA were synthesized using SuperScript II Reverse Transcriptase (Invitrogen) (1 M-NM-<g pooled RNA per synthesis). Targets were labeled using the Array 900 Expression Array Detection kit (Genisphere) following the manufacture protocol. 1M-BM-5g RNA of pooled ten control fish were labled with Cy3 and 1M-BM-5g RNA of pooled ten TCDD-treated fish were labled with Cy5, then day-swap was performed. Two arrays were run for each comparison. Microarrays were scanned at 10 M-BM-5m resolution using a ScanArray Express (PerkinElmer Life Sciences, Inc, Boston, MA). The photomultiplier tube settings (PMT) for Cy3 and Cy5 were 70 and 65-66, respectively. TIFF images of arrays were generated with ScanArray Express software (PerkinElmer). Fluorescence intensity data for Cy3 and Cy5 channels were extracted from TIFF images using ImaGene 7.5 software (BioDiscovery Inc., El Segundo, CA). Background correction, data transformation (setting background corrected values < 0.01 to 0.01), Lowess normalization, and analysis (e.g. fold-change calculations) were performed using GeneSpring GX 7.3 (Agilent Technologies, Palo Alto, CA)

Project description:The goal of this project was to use functional genomic methods to identify molecular biomarkers as indicators of the impact of TCDD exposure in rainbow trout. Specifically, we investigated the effects of chronic dietary TCDD exposure on whole juvenile rainbow trout global gene expression associated with histopathological analysis. Juvenile rainbow trout were fed Biodiet starter with TCDD added at 0, 0.1, 1, 10 and 100 ppb (ngTCDD/g food), and fish were sampled from each group at 7, 14, 28 and 42 days after initiation of feeding. 100 ppb TCDD caused 100% mortality at 39 days. Fish fed with 100 ppb TCDD food had TCDD accumulation of 47.37 ppb (ngTCDD/g fish) in whole fish at 28 days. Histological analysis from TCDD-treated trout sampled from 28 and 42 days revealed that obvious lesions were found in skin, oropharynx, liver, gas bladder, intestine, pancreas, nose and kidney. In addition, TCDD caused anemia in peripheral blood, decreases in abdominal fat, increases of remodeling of fin rays, edema in pericardium and retrobulbar hemorrhage in the 100 ppb TCDD-treated rainbow trout compared to the control group at 28 days. Dose- and time-dependent global gene expression analyses were performed using the cGRASP 16,000 (16K) cDNA microarray. TCDD-responsive whole body transcripts identified in the microarray experiments have putative functions involved in various biological processes including growth, cell proliferation, metabolic process, and immune system processes. Nine microarray-identified genes were selected for QPCR validation. CYP1A3 and CYP1A1 were common up-regulated genes and HBB1 was a common down-regulated gene among each group based on microarray data, and their QPCR validations are consistent with microarray data for the 10 and 100 ppb TCDD treatment groups after 28 days exposure (p<0.05). In addition, in the 100 ppb group at 28 days, expression of complement component C3-1 and trypsin-1 precursor have a more than 10-fold induction from the microarray experiments, and their QPCR validations are consistent and showed significant induction in the 100 ppb group at 28 days (p<0.05). Overall, lesion in nasal epithelium is a novel and significant result in this study, and TCDD-responsive rainbow trout transcripts identified in the present study may lead to the development of new molecular biomarkers for assessing the potential impacts of environmental TCDD on rainbow trout populations.

Dataset Information

Bisphenol A in oocytes leads to growth suppression and altered stress performance in juvenile rainbow trout.

Publications

Bisphenol A in oocytes leads to growth suppression and altered stress performance in juvenile rainbow trout.

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