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Article: Gestational exposure to bisphenol A induces region-specific changes in brain metabolomic fingerprints in sheep

Guignard, Davy / Canlet, Cécile / Tremblay-Franco, Marie / Chaillou, Elodie / Gautier, Roselyne / Gayrard, Véronique / Picard-Hagen, Nicole / Schroeder, Henri / Jourdan, Fabien / Zalko, Daniel / Viguié, Catherine / Cabaton, Nicolas J.

Environment international. 2022 July, v. 165

2022

Abstract: Fetal brain development depends on maternofetal thyroid function. In rodents and sheep, perinatal BPA exposure is associated with maternal and/or fetal thyroid disruption and alterations in central nervous system development as demonstrated by metabolic ... ...

Abstract	Fetal brain development depends on maternofetal thyroid function. In rodents and sheep, perinatal BPA exposure is associated with maternal and/or fetal thyroid disruption and alterations in central nervous system development as demonstrated by metabolic modulations in the encephala of mice. We hypothesized that a gestational exposure to a low dose of BPA affects maternofetal thyroid function and fetal brain development in a region-specific manner. Pregnant ewes, a relevant model for human thyroid and brain development, were exposed to BPA (5 µg/kg bw/d, sc). The thyroid status of ewes during gestation and term fetuses at delivery was monitored. Fetal brain development was assessed by metabolic fingerprints at birth in 10 areas followed by metabolic network-based analysis. BPA treatment was associated with a significant time-dependent decrease in maternal TT4 serum concentrations. For 8 fetal brain regions, statistical models allowed discriminating BPA-treated from control lambs. Metabolic network computational analysis revealed that prenatal exposure to BPA modulated several metabolic pathways, in particular excitatory and inhibitory amino-acid, cholinergic, energy and lipid homeostasis pathways. These pathways might contribute to BPA-related neurobehavioral and cognitive disorders. Discrimination was particularly clear for the dorsal hippocampus, the cerebellar vermis, the dorsal hypothalamus, the caudate nucleus and the lateral part of the frontal cortex. Compared with previous results in rodents, the use of a larger animal model allowed to examine specific brain areas, and generate evidence of the distinct region-specific effects of fetal BPA exposure on the brain metabolome. These modifications occur concomitantly to subtle maternal thyroid function alteration. The functional link between such moderate thyroid changes and fetal brain metabolomic fingerprints remains to be determined as well as the potential implication of other modes of action triggered by BPA such as estrogenic ones. Our results pave the ways for new scientific strategies aiming at linking environmental endocrine disruption and altered neurodevelopment.
Keywords	amino acids ; animal models ; biochemical pathways ; bisphenol A ; blood serum ; cerebellum ; cognition ; energy ; environment ; frontal lobe ; hippocampus ; homeostasis ; humans ; hypothalamus ; lipids ; maternal exposure ; metabolome ; metabolomics ; neurodevelopment ; pregnancy ; thyroid function
Language	English
Dates of publication	2022-07
Publishing place	Elsevier Ltd
Document type	Article
ZDB-ID	554791-x
ISSN	1873-6750 ; 0160-4120
ISSN (online)	1873-6750
ISSN	0160-4120
DOI	10.1016/j.envint.2022.107336
Database	NAL-Catalogue (AGRICOLA)

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Article: Biological Role of Pazopanib and Sunitinib Aldehyde Derivatives in Drug-Induced Liver Injury.

Maillard, Maud / Arellano, Cécile / Vachoux, Christelle / Chevreau, Christine / Cabaton, Nicolas J / Pont, Frédéric / Saint-Laurent, Nathalie / Lafont, Thierry / Chatelut, Etienne / Thomas, Fabienne

Metabolites

2022 Volume 12, Issue 9

Abstract: Tyrosine kinase inhibitors pazopanib and sunitinib are both used to treat advanced renal cell carcinoma but expose patients to an increased risk of hepatotoxicity. We have previously identified two aldehyde derivatives for pazopanib and sunitinib (P-CHO ... ...

Abstract	Tyrosine kinase inhibitors pazopanib and sunitinib are both used to treat advanced renal cell carcinoma but expose patients to an increased risk of hepatotoxicity. We have previously identified two aldehyde derivatives for pazopanib and sunitinib (P-CHO and S-CHO, respectively) in liver microsomes. In this study, we aimed to decipher their role in hepatotoxicity by treating HepG2 and HepaRG hepatic cell lines with these derivatives and evaluating cell viability, mitochondrial dysfunction, and oxidative stress accumulation. Additionally, plasma concentrations of P-CHO were assessed in a cohort of patients treated with pazopanib. Results showed that S-CHO slightly decreased the viability of HepG2, but to a lesser extent than sunitinib, and affected the maximal respiratory capacity of the mitochondrial chain. P-CHO decreased viability and ATP production in HepG2. Traces of P-CHO were detected in the plasma of patients treated with pazopanib. Overall, these results showed that P-CHO and S-CHO affect hepatocyte integrity and could be involved in the pazopanib and sunitinib hepatotoxicity.
Language	English
Publishing date	2022-09-11
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2662251-8
ISSN	2218-1989
ISSN	2218-1989
DOI	10.3390/metabo12090852
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Article ; Online: Gestational exposure to bisphenol A induces region-specific changes in brain metabolomic fingerprints in sheep.

Environment international

2022 Volume 165, Page(s) 107336

Abstract	Fetal brain development depends on maternofetal thyroid function. In rodents and sheep, perinatal BPA exposure is associated with maternal and/or fetal thyroid disruption and alterations in central nervous system development as demonstrated by metabolic modulations in the encephala of mice. We hypothesized that a gestational exposure to a low dose of BPA affects maternofetal thyroid function and fetal brain development in a region-specific manner. Pregnant ewes, a relevant model for human thyroid and brain development, were exposed to BPA (5 µg/kg bw/d, sc). The thyroid status of ewes during gestation and term fetuses at delivery was monitored. Fetal brain development was assessed by metabolic fingerprints at birth in 10 areas followed by metabolic network-based analysis. BPA treatment was associated with a significant time-dependent decrease in maternal TT4 serum concentrations. For 8 fetal brain regions, statistical models allowed discriminating BPA-treated from control lambs. Metabolic network computational analysis revealed that prenatal exposure to BPA modulated several metabolic pathways, in particular excitatory and inhibitory amino-acid, cholinergic, energy and lipid homeostasis pathways. These pathways might contribute to BPA-related neurobehavioral and cognitive disorders. Discrimination was particularly clear for the dorsal hippocampus, the cerebellar vermis, the dorsal hypothalamus, the caudate nucleus and the lateral part of the frontal cortex. Compared with previous results in rodents, the use of a larger animal model allowed to examine specific brain areas, and generate evidence of the distinct region-specific effects of fetal BPA exposure on the brain metabolome. These modifications occur concomitantly to subtle maternal thyroid function alteration. The functional link between such moderate thyroid changes and fetal brain metabolomic fingerprints remains to be determined as well as the potential implication of other modes of action triggered by BPA such as estrogenic ones. Our results pave the ways for new scientific strategies aiming at linking environmental endocrine disruption and altered neurodevelopment.
MeSH term(s)	Animals ; Benzhydryl Compounds/toxicity ; Brain ; Endocrine Disruptors/toxicity ; Female ; Humans ; Maternal Exposure/adverse effects ; Mice ; Phenols/toxicity ; Pregnancy ; Prenatal Exposure Delayed Effects ; Sheep
Chemical Substances	Benzhydryl Compounds ; Endocrine Disruptors ; Phenols ; bisphenol A (MLT3645I99)
Language	English
Publishing date	2022-06-06
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	554791-x
ISSN	1873-6750 ; 0160-4120
ISSN (online)	1873-6750
ISSN	0160-4120
DOI	10.1016/j.envint.2022.107336
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Article: Important Considerations for Sample Collection in Metabolomics Studies with a Special Focus on Applications to Liver Functions.

Smith, Lorraine / Villaret-Cazadamont, Joran / Claus, Sandrine P / Canlet, Cécile / Guillou, Hervé / Cabaton, Nicolas J / Ellero-Simatos, Sandrine

Metabolites

2020 Volume 10, Issue 3

Abstract: Metabolomics has found numerous applications in the study of liver metabolism in health and disease. Metabolomics studies can be conducted in a variety of biological matrices ranging from easily accessible biofluids such as urine, blood or feces, to ... ...

Abstract	Metabolomics has found numerous applications in the study of liver metabolism in health and disease. Metabolomics studies can be conducted in a variety of biological matrices ranging from easily accessible biofluids such as urine, blood or feces, to organs, tissues or even cells. Sample collection and storage are critical steps for which standard operating procedures must be followed. Inappropriate sample collection or storage can indeed result in high variability, interferences with instrumentation or degradation of metabolites. In this review, we will first highlight important general factors that should be considered when planning sample collection in the study design of metabolomic studies, such as nutritional status and circadian rhythm. Then, we will discuss in more detail the specific procedures that have been described for optimal pre-analytical handling of the most commonly used matrices (urine, blood, feces, tissues and cells).
Language	English
Publishing date	2020-03-12
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2662251-8
ISSN	2218-1989
ISSN	2218-1989
DOI	10.3390/metabo10030104
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Article ; Online: Bisphenol A Exposure Disrupts Neurotransmitters Through Modulation of Transaminase Activity in the Brain of Rodents.

Zalko, Daniel / Soto, Ana M / Canlet, Cecile / Tremblay-Franco, Marie / Jourdan, Fabien / Cabaton, Nicolas J

Endocrinology

2016 Volume 157, Issue 5, Page(s) 1736–1739

Language	English
Publishing date	2016-05
Publishing country	United States
Document type	Journal Article
ZDB-ID	427856-2
ISSN	1945-7170 ; 0013-7227
ISSN (online)	1945-7170
ISSN	0013-7227
DOI	10.1210/en.2016-1207
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Article: An Untargeted Metabolomics Approach to Investigate the Metabolic Modulations of HepG2 Cells Exposed to Low Doses of Bisphenol A and 17β-Estradiol.

Cabaton, Nicolas J / Poupin, Nathalie / Canlet, Cécile / Tremblay-Franco, Marie / Audebert, Marc / Cravedi, Jean-Pierre / Riu, Anne / Jourdan, Fabien / Zalko, Daniel

Frontiers in endocrinology

2018 Volume 9, Page(s) 571

Abstract: The model xeno-estrogen bisphenol A (BPA) has been extensively studied over the past two decades, contributing to major advances in the field of endocrine disrupting chemicals research. Besides its well documented adverse effects on reproduction and ... ...

Abstract	The model xeno-estrogen bisphenol A (BPA) has been extensively studied over the past two decades, contributing to major advances in the field of endocrine disrupting chemicals research. Besides its well documented adverse effects on reproduction and development observed in rodents, latest studies strongly suggest that BPA disrupts several endogenous metabolic pathways, with suspected steatogenic and obesogenic effects. BPA's adverse effects on reproduction are attributed to its ability to activate estrogen receptors (ERs), but its effects on metabolism and its mechanism(s) of action at low doses are so far only marginally understood. Metabolomics based approaches are increasingly used in toxicology to investigate the biological changes induced by model toxicants and chemical mixtures, to identify markers of toxicity and biological effects. In this study, we used proton nuclear magnetic resonance (
Language	English
Publishing date	2018-09-25
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2592084-4
ISSN	1664-2392
ISSN	1664-2392
DOI	10.3389/fendo.2018.00571
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Article: An Optimized Dual Extraction Method for the Simultaneous and Accurate Analysis of Polar Metabolites and Lipids Carried out on Single Biological Samples.

Villaret-Cazadamont, Joran / Poupin, Nathalie / Tournadre, Anthony / Batut, Aurélie / Gales, Lara / Zalko, Daniel / Cabaton, Nicolas J / Bellvert, Floriant / Bertrand-Michel, Justine

Metabolites

2020 Volume 10, Issue 9

Abstract: The functional understanding of metabolic changes requires both a significant investigation into metabolic pathways, as enabled by global metabolomics and lipidomics approaches, and the comprehensive and accurate exploration of specific key pathways. To ... ...

Abstract	The functional understanding of metabolic changes requires both a significant investigation into metabolic pathways, as enabled by global metabolomics and lipidomics approaches, and the comprehensive and accurate exploration of specific key pathways. To answer this pivotal challenge, we propose an optimized approach, which combines an efficient sample preparation, aiming to reduce the variability, with a biphasic extraction method, where both the aqueous and organic phases of the same sample are used for mass spectrometry analyses. We demonstrated that this double extraction protocol allows working with one single sample without decreasing the metabolome and lipidome coverage. It enables the targeted analysis of 40 polar metabolites and 82 lipids, together with the absolute quantification of 32 polar metabolites, providing comprehensive coverage and quantitative measurement of the metabolites involved in central carbon energy pathways. With this method, we evidenced modulations of several lipids, amino acids, and energy metabolites in HepaRG cells exposed to fenofibrate, a model hepatic toxicant, and metabolic modulator. This new protocol is particularly relevant for experiments involving limited amounts of biological material and for functional metabolic explorations and is thus of particular interest for studies aiming to decipher the effects and modes of action of metabolic disrupting compounds.
Language	English
Publishing date	2020-08-19
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2662251-8
ISSN	2218-1989
ISSN	2218-1989
DOI	10.3390/metabo10090338
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Article ; Online: Large-Scale Modeling Approach Reveals Functional Metabolic Shifts during Hepatic Differentiation.

Poupin, Nathalie / Corlu, Anne / Cabaton, Nicolas J / Dubois-Pot-Schneider, Hélène / Canlet, Cécile / Person, Elodie / Bruel, Sandrine / Frainay, Clément / Vinson, Florence / Maurier, Florence / Morel, Fabrice / Robin, Marie-Anne / Fromenty, Bernard / Zalko, Daniel / Jourdan, Fabien

Journal of proteome research

2018 Volume 18, Issue 1, Page(s) 204–216

Abstract: Being able to explore the metabolism of broad metabolizing cells is of critical importance in many research fields. This article presents an original modeling solution combining metabolic network and omics data to identify modulated metabolic pathways ... ...

Abstract	Being able to explore the metabolism of broad metabolizing cells is of critical importance in many research fields. This article presents an original modeling solution combining metabolic network and omics data to identify modulated metabolic pathways and changes in metabolic functions occurring during differentiation of a human hepatic cell line (HepaRG). Our results confirm the activation of hepato-specific functionalities and newly evidence modulation of other metabolic pathways, which could not be evidenced from transcriptomic data alone. Our method takes advantage of the network structure to detect changes in metabolic pathways that do not have gene annotations and exploits flux analyses techniques to identify activated metabolic functions. Compared to the usual cell-specific metabolic network reconstruction approaches, it limits false predictions by considering several possible network configurations to represent one phenotype rather than one arbitrarily selected network. Our approach significantly enhances the comprehensive and functional assessment of cell metabolism, opening further perspectives to investigate metabolic shifts occurring within various biological contexts.
MeSH term(s)	Cell Differentiation ; Cell Line ; Humans ; Liver/cytology ; Liver/metabolism ; Metabolic Networks and Pathways ; Metabolomics/methods ; Models, Biological
Language	English
Publishing date	2018-11-19
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2078618-9
ISSN	1535-3907 ; 1535-3893
ISSN (online)	1535-3907
ISSN	1535-3893
DOI	10.1021/acs.jproteome.8b00524
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Article ; Online: Low-dose BPA exposure alters the mesenchymal and epithelial transcriptomes of the mouse fetal mammary gland.

Wadia, Perinaaz R / Cabaton, Nicolas J / Borrero, Michael D / Rubin, Beverly S / Sonnenschein, Carlos / Shioda, Toshi / Soto, Ana M

PloS one

2013 Volume 8, Issue 5, Page(s) e63902

Abstract: Exposure of rodent fetuses to low doses of the endocrine disruptor bisphenol A (BPA) causes subtle morphological changes in the prenatal mammary gland and results in pre-cancerous and cancerous lesions during adulthood. To examine whether the BPA-induced ...

Abstract	Exposure of rodent fetuses to low doses of the endocrine disruptor bisphenol A (BPA) causes subtle morphological changes in the prenatal mammary gland and results in pre-cancerous and cancerous lesions during adulthood. To examine whether the BPA-induced morphological alterations of the fetal mouse mammary glands are a) associated with changes in mRNA expression reflecting estrogenic actions and/or b) dependent on the estrogen receptor α (ERα), we compared the transcriptomal effects of BPA and the steroidal estrogen ethinylestradiol (EE2) on fetal mammary tissues of wild type and ERα knock-out mice. Mammary glands from fetuses of dams exposed to vehicle, 250 ng BPA/kg BW/d or 10 ng EE2/kg BW/d from embryonic day (E) 8 were harvested at E19. Transcriptomal analyses on the ductal epithelium and periductal stroma revealed altered expression of genes involved in the focal adhesion and adipogenesis pathways in the BPA-exposed stroma while genes regulating the apoptosis pathway changed their expression in the BPA-exposed epithelium. These changes in gene expression correlated with previously reported histological changes in matrix organization, adipogenesis, and lumen formation resulting in enhanced maturation of the fat-pad and delayed lumen formation in the epithelium of BPA-exposed fetal mammary glands. Overall similarities in the transcriptomal effects of BPA and EE2 were more pronounced in the epithelium, than in the stroma. In addition, the effects of BPA and EE2 on the expression of various genes involved in mammary stromal-epithelial interactions were suppressed in the absence of ERα. These observations support a model whereby BPA and EE2 act directly on the stroma, which expresses ERα, ERβ and GPR30 in fetal mammary glands, and that the stroma, in turn, affects gene expression in the epithelium, where ERα and ERβ are below the level of detection at this stage of development.
MeSH term(s)	Animals ; Apoptosis/drug effects ; Apoptosis/genetics ; Benzhydryl Compounds/toxicity ; Cluster Analysis ; Epithelium/drug effects ; Epithelium/metabolism ; Estrogen Receptor alpha/metabolism ; Ethinyl Estradiol/pharmacology ; Female ; Fetus/drug effects ; Fetus/metabolism ; Focal Adhesions/drug effects ; Focal Adhesions/metabolism ; Gene Expression Profiling ; Gene Expression Regulation, Developmental/drug effects ; Mammary Glands, Animal/drug effects ; Mammary Glands, Animal/embryology ; Mammary Glands, Animal/metabolism ; Mammary Glands, Animal/pathology ; Mesoderm/drug effects ; Mesoderm/metabolism ; Mice ; Mice, Inbred C57BL ; Phenols/toxicity ; Pregnancy ; Prenatal Exposure Delayed Effects/genetics ; Prenatal Exposure Delayed Effects/pathology ; Principal Component Analysis ; RNA, Messenger/genetics ; RNA, Messenger/metabolism ; Signal Transduction/drug effects ; Signal Transduction/genetics ; Stromal Cells/drug effects ; Stromal Cells/metabolism ; Transcription, Genetic/drug effects ; Transcriptome/genetics ; Troponin C/metabolism
Chemical Substances	Benzhydryl Compounds ; Estrogen Receptor alpha ; Phenols ; RNA, Messenger ; Troponin C ; Ethinyl Estradiol (423D2T571U) ; bisphenol A (MLT3645I99)
Language	English
Publishing date	2013-05-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0063902
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Article ; Online: Dynamic Metabolic Disruption in Rats Perinatally Exposed to Low Doses of Bisphenol-A.

Tremblay-Franco, Marie / Cabaton, Nicolas J / Canlet, Cécile / Gautier, Roselyne / Schaeberle, Cheryl M / Jourdan, Fabien / Sonnenschein, Carlos / Vinson, Florence / Soto, Ana M / Zalko, Daniel

PloS one

2015 Volume 10, Issue 10, Page(s) e0141698

Abstract: Along with the well-established effects on fertility and fecundity, perinatal exposure to endocrine disrupting chemicals, and notably to xeno-estrogens, is strongly suspected of modulating general metabolism. The metabolism of a perinatally exposed ... ...

Abstract	Along with the well-established effects on fertility and fecundity, perinatal exposure to endocrine disrupting chemicals, and notably to xeno-estrogens, is strongly suspected of modulating general metabolism. The metabolism of a perinatally exposed individual may be durably altered leading to a higher susceptibility of developing metabolic disorders such as obesity and diabetes; however, experimental designs involving the long term study of these dynamic changes in the metabolome raise novel challenges. 1H-NMR-based metabolomics was applied to study the effects of bisphenol-A (BPA, 0; 0.25; 2.5, 25 and 250 μg/kg BW/day) in rats exposed perinatally. Serum and liver samples of exposed animals were analyzed on days 21, 50, 90, 140 and 200 in order to explore whether maternal exposure to BPA alters metabolism. Partial Least Squares-Discriminant Analysis (PLS-DA) was independently applied to each time point, demonstrating a significant pair-wise discrimination for liver as well as serum samples at all time-points, and highlighting unequivocal metabolic shifts in rats perinatally exposed to BPA, including those exposed to lower doses. In BPA exposed animals, metabolism of glucose, lactate and fatty acids was modified over time. To further explore dynamic variation, ANOVA-Simultaneous Component Analysis (A-SCA) was used to separate data into blocks corresponding to the different sources of variation (Time, Dose and Time*Dose interaction). A-SCA enabled the demonstration of a dynamic, time/age dependent shift of serum metabolome throughout the rats' lifetimes. Variables responsible for the discrimination between groups clearly indicate that BPA modulates energy metabolism, and suggest alterations of neurotransmitter signaling, the latter finding being compatible with the neurodevelopmental effect of this xenoestrogen. In conclusion, long lasting metabolic effects of BPA could be characterized over 200 days, despite physiological (and thus metabolic) changes connected with sexual maturation and aging.
MeSH term(s)	Animals ; Benzhydryl Compounds/administration & dosage ; Benzhydryl Compounds/pharmacology ; Energy Metabolism/drug effects ; Estrogens, Non-Steroidal/administration & dosage ; Estrogens, Non-Steroidal/pharmacology ; Female ; Liver/drug effects ; Liver/metabolism ; Male ; Metabolome/drug effects ; Phenols/administration & dosage ; Phenols/pharmacology ; Pregnancy ; Proton Magnetic Resonance Spectroscopy/methods ; Rats
Chemical Substances	Benzhydryl Compounds ; Estrogens, Non-Steroidal ; Phenols ; bisphenol A (MLT3645I99)
Language	English
Publishing date	2015-10-30
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0141698
Database	MEDical Literature Analysis and Retrieval System OnLINE

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