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Research Article

Bisphenol A alters early oogenesis and follicle formation in the fetal ovary of the rhesus monkey

Patricia A. Hunt, Crystal Lawson, Mary Gieske, Brenda Murdoch, Helen Smith, Alyssa Marre, Terry Hassold, and Catherine A. VandeVoort
PNAS first published September 24, 2012; https://doi.org/10.1073/pnas.1207854109
Patricia A. Hunt
aSchool of Molecular Biosciences and Center for Reproductive Biology, Washington State University, Pullman, WA 99164; and
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  • For correspondence: pathunt@vetmed.wsu.edu
Crystal Lawson
aSchool of Molecular Biosciences and Center for Reproductive Biology, Washington State University, Pullman, WA 99164; and
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Mary Gieske
aSchool of Molecular Biosciences and Center for Reproductive Biology, Washington State University, Pullman, WA 99164; and
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Brenda Murdoch
aSchool of Molecular Biosciences and Center for Reproductive Biology, Washington State University, Pullman, WA 99164; and
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Helen Smith
aSchool of Molecular Biosciences and Center for Reproductive Biology, Washington State University, Pullman, WA 99164; and
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Alyssa Marre
aSchool of Molecular Biosciences and Center for Reproductive Biology, Washington State University, Pullman, WA 99164; and
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Terry Hassold
aSchool of Molecular Biosciences and Center for Reproductive Biology, Washington State University, Pullman, WA 99164; and
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Catherine A. VandeVoort
bDepartment of Obstetrics and Gynecology and California National Primate Research Center, University of California, Davis, CA 95616
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  1. Edited* by Joan V. Ruderman, Harvard Medical School, Boston, MA, and approved August 24, 2012 (received for review May 9, 2012)

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Abstract

Widespread use of the endocrine disrupting chemical bisphenol A (BPA) in consumer products has resulted in nearly continuous human exposure. In rodents, low-dose exposures have been reported to adversely affect two distinct stages of oogenesis in the developing ovary: the events of prophase at the onset of meiosis in the fetal ovary and the formation of follicles in the perinatal ovary. Because these effects could influence the reproductive longevity and success of the exposed individual, we conducted studies in the rhesus monkey to determine whether BPA induces similar disturbances in the developing primate ovary. The routes and levels of human exposure are unclear; hence, two different exposure protocols were used: single daily oral doses and continuous exposure via subdermal implant. Our analyses of second trimester fetuses exposed at the time of meiotic onset suggest that, as in mice, BPA induces subtle disturbances in the prophase events that set the stage for chromosome segregation at the first meiotic division. Our analyses of third-trimester fetuses exposed to single daily oral doses during the time of follicle formation revealed an increase in multioocyte follicles analogous to that reported in rodents. However, two unique phenotypes were evident in continuously exposed animals: persistent unenclosed oocytes in the medullary region and small, nongrowing oocytes in secondary and antral follicles. Because effects on both stages of oogenesis were elicited using doses that yield circulating levels of BPA analogous to those reported in humans, these findings raise concerns for human reproductive health.

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: pathunt{at}vetmed.wsu.edu.
  • Author contributions: P.A.H. and C.A.V. designed research; P.A.H., C.L., M.G., B.M., H.S., A.M., and C.A.V. performed research; P.A.H., C.L., T.H., and C.A.V. analyzed data; and P.A.H., T.H., and C.A.V. wrote the paper.

  • The authors declare no conflict of interest.

  • ↵*This Direct Submission article had a prearranged editor.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1207854109/-/DCSupplemental.

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BPA alters early oogenesis
Patricia A. Hunt, Crystal Lawson, Mary Gieske, Brenda Murdoch, Helen Smith, Alyssa Marre, Terry Hassold, Catherine A. VandeVoort
Proceedings of the National Academy of Sciences Sep 2012, 201207854; DOI: 10.1073/pnas.1207854109

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BPA alters early oogenesis
Patricia A. Hunt, Crystal Lawson, Mary Gieske, Brenda Murdoch, Helen Smith, Alyssa Marre, Terry Hassold, Catherine A. VandeVoort
Proceedings of the National Academy of Sciences Sep 2012, 201207854; DOI: 10.1073/pnas.1207854109
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