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1. Characterization of Novel Ligands of ER alpha, Er beta, and PPAR gamma: The Case of Halogenated Bisphenol A and Their Conjugated Metabolites

Author

Riu, Anne, Le Maire, Albane, Grimaldi, Marina, Audebert, Marc, Hillenweck, Anne, Bourguet, William, Balaguer, Patrick, Zalko, Daniel, ToxAlim (ToxAlim), Institut National de la Recherche Agronomique (INRA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-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-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Ecole d'Ingénieurs de Purpan (INPT - EI Purpan), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Centre de Biochimie Structurale [Montpellier] (CBS), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut National de la Santé et de la Recherche Médicale (INSERM), Institut de recherche en cancérologie de Montpellier (IRCM - U896 Inserm - UM1), CRLCC Val d'Aurelle - Paul Lamarque-Université de Montpellier (UM)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 1 (UM1), Centre régional de lutte contre le cancer, Métabolisme et Xénobiotiques (ToxAlim-MeX), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Recherche Agronomique (INRA)-Université Toulouse III - Paul Sabatier (UT3), Université de Montpellier (UM), European Union network CASCADE (FOOD-CT-2003-506319), Agence Nationale de Securite Sanitaire (RD-2005-02), Programme National de Recherche sur les Perturbateurs Endocriniens, programmes 189, Agence Nationale de la Recherche ANR CES (BISCOT 2010 CESA 004 02 CONTREPERF 2010-CESA-008-03 KISMET 2008-CESA-008-01), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), 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), and Université Montpellier 1 (UM1)-CRLCC Val d'Aurelle - Paul Lamarque-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)

Subjects
obesity, flame retardants, chlorinated derivatives, [SDV]Life Sciences [q-bio], in vitro, halogenated bpa, adipose tissue, endocrine disruptors, estrogen receptor alpha, tandem mass spectrometry, chromatography, nuclear receptor, endocrine disrupter, affinity column, metabolism, tetrachlorobisphenol, tetrabromobisphenol a
Abstract

International audience; The capability of the flame retardants tetrabromobisphenol A (TBBPA) and tetrachlorobisphenol A (TCBPA) to activate peroxysome proliferator-activated receptors (PPARs) alpha, beta, and gamma and estrogen receptors (ERs) alpha and beta has been recently investigated, but the activity of their biotransformation products and of their lower molecular weight analogues formed in the environment remains unexplored. The aim of this study was to investigate the relationship between the degree of halogenation of BPA analogues and their affinity and activity towards human PPAR gamma and ERs and to characterize active metabolites of major marketed halogenated bisphenols. The biological activity of all compounds was studied using reporter cell lines expressing these nuclear receptors (NRs). We used NR-based affinity columns to rapidly evaluate the binding affinity of halogenated bisphenols for PPAR gamma and ERs and to trap active metabolites of TBBPA and TCBPA formed in HepG2 cells. The agonistic potential of BPA analogs highly depends on their halogenation degree: the bulkier halogenated BPA analogs, the greater their capability to activate PPAR gamma. In addition, PPAR gamma-based affinity column, HGELN-PPAR gamma reporter cell line and crystallographic analysis clearly demonstrate that the sulfation pathway, usually considered as a detoxification process, leads for TBBPA and TCBPA, to the formation of sulfate conjugates which possess a residual PPAR gamma-binding activity. Our results highlight the effectiveness NR-based affinity columns to trap and characterize biologically active compounds from complex matrices. Polyhalogenated bisphenols, but also some of their metabolites, are potential disrupters of PPAR gamma activity.

Published
2011

2. Peroxisome Proliferator-Activated Receptor ã Is a Target for Halogenated Analogs of Bisphenol A.

Author

Riu, Anne, Grimaldi, Marina, le Maire, Albane, Bey, Gilbert, Phillips, Kevinps, Boulahtouf, Abdelhay, Perdu, Elisabeth, Zalko, Daniel, Bourguet, William, and Balaguer, Patrick

Abstract

Background: The occurrence of halogenated analogs of the xenoestrogen bisphenol A (BPA) has been recently demonstrated both in environmental and human samples. These analogs include brominated [e.g., tetrabromobisphenol A (TBBPA)] and chlorinated [e.g., tetrachlorobisphenol A (TCBPA)] bisphenols, which are both flame retardants. Because of their structural homology with BPA, such chemicals are candidate endocrine disruptors. However, their possible target(s) within the nuclear hormone receptor superfamily has remained unknown. Objectives: We investigated whether BPA and its halogenated analogs could be ligands of estrogen receptors (ERs) and peroxisome proliferator-activated receptors (PPARs) and act as endocrine-disrupting chemicals. Methods: We studied the activity of compounds using reporter cell lines expressing ERs and PPARs. We measured the binding affinities to PPARγ by competitive binding assays with [3H] rosiglitazone and investigated the impact of TBBPA and TCBPA on adipocyte differentiation using NIH3T3-L1 cells. Finally, we determined the binding mode of halogenated BPAs to PPARγ by X-ray crystallography. Results: We observed that TBBPA and TCBPA are human, zebrafish, and Xenopus PPARγ ligands and determined the mechanism by which these chemicals bind to and activate PPARγ. We also found evidence that activation of ERα, ERβ, and PPARγ depends on the degree of halogenation in BPA analogs. We observed that the bulkier brominated BPA analogs, the greater their capability to activate PPARγ and the weaker their estrogenic potential. Conclusions: Our results strongly suggest that polyhalogenated bisphenols could function as obesogens by acting as agonists to disrupt physiological functions regulated by human or animal PPARγ. [ABSTRACT FROM AUTHOR]

Published
2011
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3. Characterization of Novel Ligands of ERα, Erβ, and PPARγ: The Case of Halogenated Bisphenol A and Their Conjugated Metabolites.

Author

Riu, Anne, le Maire, Albane, Grimaldi, Marina, Audebert, Marc, Hillenweck, Anne, Bourguet, William, Balaguer, Patrick, and Zalko, Daniel

Subjects
*LIGANDS (Biochemistry), *FIREPROOFING agents, *ESTROGEN receptors, *BIOTRANSFORMATION (Metabolism), *METABOLITES, *ENDOCRINE system, *OBESITY, *NUCLEAR receptors (Biochemistry)
Abstract

The capability of the flame retardants tetrabromobisphenol A (TBBPA) and tetrachlorobisphenol A (TCBPA) to activate peroxysome proliferator–activated receptors (PPARs) α, β, and γ and estrogen receptors (ERs) α and β has been recently investigated, but the activity of their biotransformation products and of their lower molecular weight analogues formed in the environment remains unexplored. The aim of this study was to investigate the relationship between the degree of halogenation of BPA analogues and their affinity and activity towards human PPARγ and ERs and to characterize active metabolites of major marketed halogenated bisphenols. The biological activity of all compounds was studied using reporter cell lines expressing these nuclear receptors (NRs). We used NR-based affinity columns to rapidly evaluate the binding affinity of halogenated bisphenols for PPARγ and ERs and to trap active metabolites of TBBPA and TCBPA formed in HepG2 cells. The agonistic potential of BPA analogs highly depends on their halogenation degree: the bulkier halogenated BPA analogs, the greater their capability to activate PPARγ. In addition, PPARγ-based affinity column, HGELN-PPARγ reporter cell line and crystallographic analysis clearly demonstrate that the sulfation pathway, usually considered as a detoxification process, leads for TBBPA and TCBPA, to the formation of sulfate conjugates which possess a residual PPARγ-binding activity. Our results highlight the effectiveness NR-based affinity columns to trap and characterize biologically active compounds from complex matrices. Polyhalogenated bisphenols, but also some of their metabolites, are potential disrupters of PPARγ activity. [ABSTRACT FROM AUTHOR]

Published
2011
Full Text
View/download PDF

4. Warm Reception? Halogenated BPA Flame Retardants and PPARγ Activation

Author

Kevin J. Phillips, Abdelhay Boulahtouf, William Bourguet, Elisabeth Perdu, Anne Riu, Gilbert Bey, Marina Grimaldi, Daniel Zalko, Patrick Balaguer, Albane le Maire, ToxAlim (ToxAlim), Institut National de la Recherche Agronomique (INRA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-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-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Ecole d'Ingénieurs de Purpan (INPT - EI Purpan), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Institut de Recherche en Cancérologie de Montpellier (IRCM - U1194 Inserm - UM), CRLCC Val d'Aurelle - Paul Lamarque-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM), Institut de recherche en cancérologie de Montpellier (IRCM - U896 Inserm - UM1), CRLCC Val d'Aurelle - Paul Lamarque-Université de Montpellier (UM)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 1 (UM1), NovAliX, Métabolisme et Xénobiotiques (ToxAlim-MeX), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Recherche Agronomique (INRA)-Université Toulouse III - Paul Sabatier (UT3), Centre de Biochimie Structurale [Montpellier] (CBS), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut National de la Santé et de la Recherche Médicale (INSERM), European Union FOOD-CT-2003-506319, Agence Nationale de Securite Sanitaire RD-2005-02, Programme National de Recherche sur les Perturbateurs Endocriniens, ECOPI 189, Agence Nationale de la Recherche, Contaminants, Ecosystemes, Sante BISCOT 2010 CESA 004 02, CONTREPERF 2010 CESA 008 03, KISMET 2008 CESA 008 01, Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), 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 Montpellier 1 (UM1)-CRLCC Val d'Aurelle - Paul Lamarque-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM), Riu, Anne, Grimaldi, Marina, le Maire, Albane, Bey, Gilbert, Boulahtouf, Abdelhay, Perdu, Elisabeth, Zalko, Daniel, Bourguet, William, and Balaguer, Patrick

Subjects
obesity, PPARγ, Health, Toxicology and Mutagenesis, Xenopus, [SDV]Life Sciences [q-bio], Peroxisome proliferator-activated receptor, BPA, endocrine disruptor, obesity, PPARγ, TBBPA, TCBPA, 010501 environmental sciences, Endocrine Disruptors, Crystallography, X-Ray, Ligands, 01 natural sciences, chemistry.chemical_compound, TCBPA, PPAR delta, Receptor, News | Science Selections, Zebrafish, Flame Retardants, chemistry.chemical_classification, endocrine disruptor, 0303 health sciences, BPA, TBBPA, Xenoestrogen, Reproductive Health, Endocrine disruptor, Biochemistry, Tetrabromobisphenol A, Peroxisome proliferator-activated receptor delta, Bisphenol A (BPA), hormones, hormone substitutes, and hormone antagonists, Chlorophenols, medicine.medical_specialty, endocrine system, Polybrominated Biphenyls, Binding, Competitive, Cell Line, 03 medical and health sciences, Internal medicine, medicine, Animals, Estrogen Receptor beta, Humans, PPAR alpha, Estrogens, Non-Steroidal, 030304 developmental biology, 0105 earth and related environmental sciences, Endocrine Health, urogenital system, Research, Public Health, Environmental and Occupational Health, Estrogen Receptor alpha, PPAR gamma, Endocrinology, Metabolism, chemistry, Nuclear receptor, Estrogen receptor alpha
Abstract

International audience; Background: The occurrence of halogenated analogs of the xenoestrogen bisphenol A (BPA) has been recently demonstrated both in environmental and human samples. These analogs include brominated [e.g., tetrabromobisphenol A (TBBPA)] and chlorinated [e.g., tetrachlorobisphenol A (TCBPA)] bisphenols, which are both flame retardants. Because of their structural homology with BPA, such chemicals are candidate endocrine disruptors. However, their possible target(s) within the nuclear hormone receptor superfamily has remained unknown.Objectives: We investigated whether BPA and its halogenated analogs could be ligands of estrogen receptors (ERs) and peroxisome proliferator–activated receptors (PPARs) and act as endocrine-disrupting chemicals.Methods: We studied the activity of compounds using reporter cell lines expressing ERs and PPARs. We measured the binding affinities to PPARγ by competitive binding assays with [3H]‑rosiglitazone and investigated the impact of TBBPA and TCBPA on adipocyte differentiation using NIH3T3-L1 cells. Finally, we determined the binding mode of halogenated BPAs to PPARγ by X‑ray crystallography.Results: We observed that TBBPA and TCBPA are human, zebrafish, and Xenopus PPARγ ligands and determined the mechanism by which these chemicals bind to and activate PPARγ. We also found evidence that activation of ERα, ERβ, and PPARγ depends on the degree of halogenation in BPA analogs. We observed that the bulkier brominated BPA analogs, the greater their capability to activate PPARγ and the weaker their estrogenic potential.Conclusions: Our results strongly suggest that polyhalogenated bisphenols could function as obesogens by acting as agonists to disrupt physiological functions regulated by human or animal PPARγ.

Published
2011

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