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1. Dynamic metabolic disruption in rats perinatally exposed to low doses of bisphenol-A

Author

Ana M. Soto, Fabien Jourdan, Marie Tremblay-Franco, Nicolas J. Cabaton, Daniel Zalko, Florence Vinson, Carlos Sonnenschein, Cécile Canlet, Cheryl M. Schaeberle, Roselyne Gautier, Analyse de Xénobiotiques, Identification, Métabolisme (E20 Metatoul-AXIOM), ToxAlim (ToxAlim), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole d'Ingénieurs de Purpan (INPT - EI Purpan), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Recherche Agronomique (INRA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Recherche Agronomique (INRA)-MetaToul-MetaboHUB, Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Métabolisme et Xénobiotiques (ToxAlim-MeX), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Recherche Agronomique (INRA), Tufts University School of Medicine, National Institute of Environmental Health Sciences [R01ES08314], [RC2ES018822], Zalko, Daniel, Institut National de la Recherche Agronomique (INRA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Ecole d'Ingénieurs de Purpan (INPT - EI Purpan), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-MetaToul-MetaboHUB, Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Tufts University School of Medicine [Boston], Centre Cavaillès, La République des savoirs : Lettres, Sciences, Philosophie, Collège de France (CdF (institution))-Centre National de la Recherche Scientifique (CNRS)-Département de Philosophie - ENS Paris, École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Collège de France (CdF (institution))-Centre National de la Recherche Scientifique (CNRS)-Département de Philosophie - ENS Paris, and Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)

Subjects
Male, medicine.medical_specialty, Proton Magnetic Resonance Spectroscopy, [SDV]Life Sciences [q-bio], lcsh:Medicine, 010501 environmental sciences, Biology, Carbohydrate metabolism, 01 natural sciences, 03 medical and health sciences, chemistry.chemical_compound, Metabolomics, Phenols, Pregnancy, Internal medicine, medicine, Metabolome, Endocrine system, Animals, Benzhydryl compounds, Estrogens, Non-Steroidal, Benzhydryl Compounds, lcsh:Science, Toxicologie, 030304 developmental biology, 0105 earth and related environmental sciences, 0303 health sciences, Chemicals, Multidisciplinary, Perinatal Exposure, lcsh:R, Metabolism, Rats, Xenoestrogen, Endocrinology, chemistry, Liver, lcsh:Q, Female, Energy Metabolism, Research Article
Abstract

International audience; 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. H-1-NMR-based metabolomics was applied to study the effects of bisphenol-A (BPA, 0; 0.25; 2.5, 25 and 250 mu g/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.

Published
2015

2. Perinatal Exposure to Environmentally Relevant Levels of Bisphenol A Decreases Fertility and Fecundity in CD-1 Mice

Author

Ana M. Soto, Michael H. Askenase, Perinaaz R. Wadia, Beverly S. Rubin, Gregory S. Whitt, Nicolas J. Cabaton, Carlos Sonnenschein, Andrew P. Tharp, Jennifer L. Gadbois, Daniel Zalko, Cheryl M. Schaeberle, Métabolisme et Xénobiotiques (ToxAlim-MeX), ToxAlim (ToxAlim), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole d'Ingénieurs de Purpan (INPT - EI Purpan), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Recherche Agronomique (INRA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Recherche Agronomique (INRA), Tufts University School of Medicine, Tufts University, and National Institute of Environmental Health Sciences [ES08314]

Subjects
Health, Toxicology and Mutagenesis, bisphenol A, [SDV]Life Sciences [q-bio], Uterus, 010501 environmental sciences, PROLACTIN-RELEASE, 01 natural sciences, chemistry.chemical_compound, Mice, BINDING, media_common, endocrine disruptor, fertility, 0303 health sciences, Perinatal Exposure, Reproduction, Fecundity, biphasic dose response, medicine.anatomical_structure, Endocrine disruptor, Toxicity, Environmental Pollutants, Female, MOUSE GENITAL-TRACT, hormones, hormone substitutes, and hormone antagonists, MALE REPRODUCTIVE HEALTH, medicine.medical_specialty, endocrine system, media_common.quotation_subject, fecundity, ENDOCRINE-DISRUPTING CHEMICALS, Ovary, Fertility, Biology, perinatal exposure, 03 medical and health sciences, Phenols, DIETHYLSTILBESTROL DES, MAMMARY-GLAND, Internal medicine, fetal origins of adult disease, PRENATAL EXPOSURE, CD1 MICE, CELLS, medicine, Animals, Benzhydryl compounds, Benzhydryl Compounds, 030304 developmental biology, 0105 earth and related environmental sciences, Dose-Response Relationship, Drug, urogenital system, Research, Public Health, Environmental and Occupational Health, Endocrinology, chemistry, Animals, Newborn
Abstract

International audience; BACKGROUND: Perinatal exposure to low-doses of bisphenol A (BPA) results in alterations in the ovary, uterus, and mammary glands and in a sexually dimorphic region of the brain known to be important for estrous cyclicity. OBJECTIVES: We aimed to determine whether perinatal exposure to environmentally relevant doses of BPA alters reproductive capacity. METHODS: Female CD-1 mice that were exposed to BPA at 0, 25 ng, 250 ng, or 25 mu g/kg body weight (BW)/day or diethylstilbestrol (DES) at 10 ng/kg BW/day (positive control) from gestational day 8 through day 16 of lactation were continuously housed with proven breeder males for 32 weeks starting at 2 months of age. At each delivery, pups born to these mating pairs were removed. The cumulative number of pups, number of deliveries, and litter size were recorded. The purity of the BPA used in this and our previous studies was assessed using HPLC, mass spectrometry, and nuclear magnetic resonance. RESULTS: The forced breeding experiment revealed a decrease in the cumulative number of pups, observed as a non-monotonic dose-response effect, and a decline in fertility and fecundity over time in female mice exposed perinatally to BPA. The BPA was 97% pure, with no evidence of contamination by other phenolic compounds. CONCLUSIONS: Perinatal exposure to BPA leads to a dose-dependent decline in the reproductive capacity of female mice. The effects on the cumulative number of pups are comparable to those previously reported in mice developmentally exposed to DES, a compound well known to impair reproduction in women. This association suggests the possibility that early BPA exposure may also affect reproductive capacity in women.

Published
2011

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