The fetal ovary exhibits temporal sensitivity to a ‘real-life’ mixture of environmental chemicals

Richard G. Lea; Maria R. Amezaga; Benoit Loup; Beatrice Mandon-Pepin; Agnes Stefansdottir; Panagiotis Filis; Carol Kyle; Zulin  Zhang; Ceri  Allen; Laura  Purdie; Luc Jouneau; Corinne Cotinot; Stewart M. Rhind; Kevin D. Sinclair; Paul A. Fowler

doi:10.1038/srep22279

The fetal ovary exhibits temporal sensitivity to a ‘real-life’ mixture of environmental chemicals

Richard G. Lea, Maria R. Amezaga, Benoit Loup, Beatrice Mandon-Pepin, Agnes Stefansdottir, Panagiotis Filis, Carol Kyle, Zulin Zhang, Ceri Allen, Laura Purdie, Luc Jouneau, Corinne Cotinot, Stewart M. Rhind, Kevin D. Sinclair, Paul A. Fowler

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Abstract

The development of fetal ovarian follicles is a critical determinant of adult female reproductive competence. Prolonged exposure to environmental chemicals (ECs) can perturb this process with detrimental consequences for offspring. Here we report on the exposure of pregnant ewes to an environmental mixture of ECs derived from pastures fertilized with sewage sludge (biosolids): a common global agricultural practice. Exposure of pregnant ewes to ECs over 80 day periods during early, mid or late gestation reduced the proportion of healthy early stage fetal follicles comprising the ovarian reserve. Mid and late gestation EC exposures had the most marked effects, disturbing maternal and fetal liver chemical profiles, masculinising fetal anogenital distance and greatly increasing the number of altered fetal ovarian genes and proteins. In conclusion, differential temporal sensitivity of the fetus and its ovaries to EC mixtures has implications for adult ovarian function following adverse exposures during pregnancy.

Original language	English
Article number	22279
Number of pages	13
Journal	Scientific Reports
Volume	6
DOIs	https://doi.org/10.1038/srep22279
Publication status	Published - 2 Mar 2016

Bibliographical note

We thank George Corsar and Jim MacDonald for the management of experimental animals. We thank Ms Evelyn Argo, Mr Ian Davidson (Proteomics Facility), Ms Gillian Milne (Histology & Electron Microscopy Facility) and Mrs Margaret Fraser (Institute of Medical Sciences) at the University of Aberdeen and NHS Grampian for expert technical assistance. We thank Elodie Poumerol (UMR1198 INRA, transcriptome analysis), Christine Kerr and Mark Osprey (James Hutton Institute, chemical analysis) for technical support. This work was funded by the European Commission Framework 7 Programme (Contract No 212885, http://www.abdn.ac.uk/reef/).

Keywords

Developmental biology
Embryology

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10.1038/srep22279Licence: CC BY

The fetal ovary exhibits temporal sensitivity to a ‘real-life’ mixture of environmental chemicals
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Final published version, 2.07 MBLicence: CC BY

Paul Alfred François Fowler
- School of Medicine, Medical Sciences & Nutrition, Molecular and Cellular Function
- School of Medicine, Medical Sciences & Nutrition, Applied Medicine - Chair in Translational Medical Sciences
- School of Medicine, Medical Sciences & Nutrition, Institute of Medical Sciences
Person: Academic

Aberdeen Proteomics
David Stead (Manager)
Medical Sciences
Research Facilities: Facility
Microscopy and Histology
Debbie Wilkinson (Manager) & Gillian Milne (Manager)
Medical Sciences
Research Facilities: Facility

Cite this

Lea, R. G., Amezaga, M. R., Loup, B., Mandon-Pepin, B., Stefansdottir, A., Filis, P., Kyle, C., Zhang, Z., Allen, C., Purdie, L., Jouneau, L., Cotinot, C., Rhind, S. M., Sinclair, K. D., & Fowler, P. A. (2016). The fetal ovary exhibits temporal sensitivity to a ‘real-life’ mixture of environmental chemicals. Scientific Reports, 6, Article 22279. https://doi.org/10.1038/srep22279

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abstract = "The development of fetal ovarian follicles is a critical determinant of adult female reproductive competence. Prolonged exposure to environmental chemicals (ECs) can perturb this process with detrimental consequences for offspring. Here we report on the exposure of pregnant ewes to an environmental mixture of ECs derived from pastures fertilized with sewage sludge (biosolids): a common global agricultural practice. Exposure of pregnant ewes to ECs over 80 day periods during early, mid or late gestation reduced the proportion of healthy early stage fetal follicles comprising the ovarian reserve. Mid and late gestation EC exposures had the most marked effects, disturbing maternal and fetal liver chemical profiles, masculinising fetal anogenital distance and greatly increasing the number of altered fetal ovarian genes and proteins. In conclusion, differential temporal sensitivity of the fetus and its ovaries to EC mixtures has implications for adult ovarian function following adverse exposures during pregnancy.",

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AU - Amezaga, Maria R.

AU - Loup, Benoit

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AU - Stefansdottir, Agnes

AU - Filis, Panagiotis

AU - Kyle, Carol

AU - Zhang, Zulin

AU - Allen, Ceri

AU - Purdie, Laura

AU - Jouneau, Luc

AU - Cotinot, Corinne

AU - Rhind, Stewart M.

AU - Sinclair, Kevin D.

AU - Fowler, Paul A.

N1 - We thank George Corsar and Jim MacDonald for the management of experimental animals. We thank Ms Evelyn Argo, Mr Ian Davidson (Proteomics Facility), Ms Gillian Milne (Histology & Electron Microscopy Facility) and Mrs Margaret Fraser (Institute of Medical Sciences) at the University of Aberdeen and NHS Grampian for expert technical assistance. We thank Elodie Poumerol (UMR1198 INRA, transcriptome analysis), Christine Kerr and Mark Osprey (James Hutton Institute, chemical analysis) for technical support. This work was funded by the European Commission Framework 7 Programme (Contract No 212885, http://www.abdn.ac.uk/reef/).

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N2 - The development of fetal ovarian follicles is a critical determinant of adult female reproductive competence. Prolonged exposure to environmental chemicals (ECs) can perturb this process with detrimental consequences for offspring. Here we report on the exposure of pregnant ewes to an environmental mixture of ECs derived from pastures fertilized with sewage sludge (biosolids): a common global agricultural practice. Exposure of pregnant ewes to ECs over 80 day periods during early, mid or late gestation reduced the proportion of healthy early stage fetal follicles comprising the ovarian reserve. Mid and late gestation EC exposures had the most marked effects, disturbing maternal and fetal liver chemical profiles, masculinising fetal anogenital distance and greatly increasing the number of altered fetal ovarian genes and proteins. In conclusion, differential temporal sensitivity of the fetus and its ovaries to EC mixtures has implications for adult ovarian function following adverse exposures during pregnancy.

AB - The development of fetal ovarian follicles is a critical determinant of adult female reproductive competence. Prolonged exposure to environmental chemicals (ECs) can perturb this process with detrimental consequences for offspring. Here we report on the exposure of pregnant ewes to an environmental mixture of ECs derived from pastures fertilized with sewage sludge (biosolids): a common global agricultural practice. Exposure of pregnant ewes to ECs over 80 day periods during early, mid or late gestation reduced the proportion of healthy early stage fetal follicles comprising the ovarian reserve. Mid and late gestation EC exposures had the most marked effects, disturbing maternal and fetal liver chemical profiles, masculinising fetal anogenital distance and greatly increasing the number of altered fetal ovarian genes and proteins. In conclusion, differential temporal sensitivity of the fetus and its ovaries to EC mixtures has implications for adult ovarian function following adverse exposures during pregnancy.

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The fetal ovary exhibits temporal sensitivity to a ‘real-life’ mixture of environmental chemicals

Abstract

Bibliographical note

Keywords

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Paul Alfred François Fowler

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Aberdeen Proteomics

Microscopy and Histology

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