Estrogenic Exposure Alters the Spermatogonial Stem Cells in the Developing Testis, Permanently Reducing Crossover Levels in the Adult
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{"title"=>"Estrogenic Exposure Alters the Spermatogonial Stem Cells in the Developing Testis, Permanently Reducing Crossover Levels in the Adult", "type"=>"journal", "authors"=>[{"first_name"=>"Lisa A.", "last_name"=>"Vrooman", "scopus_author_id"=>"36242600400"}, {"first_name"=>"Jon M.", "last_name"=>"Oatley", "scopus_author_id"=>"6602612889"}, {"first_name"=>"Jodi E.", "last_name"=>"Griswold", "scopus_author_id"=>"26632893000"}, {"first_name"=>"Terry J.", "last_name"=>"Hassold", "scopus_author_id"=>"7005809089"}, {"first_name"=>"Patricia A.", "last_name"=>"Hunt", "scopus_author_id"=>"7202324453"}], "year"=>2015, "source"=>"PLoS Genetics", "identifiers"=>{"pmid"=>"25615633", "sgr"=>"84924405570", "scopus"=>"2-s2.0-84924405570", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "doi"=>"10.1371/journal.pgen.1004949", "pui"=>"602890973", "issn"=>"15537404"}, "id"=>"7cf7707e-df6f-3448-8dde-e34f7386a5ad", "abstract"=>"Bisphenol A (BPA) and other endocrine disrupting chemicals have been reported to induce negative effects on a wide range of physiological processes, including reproduction. In the female, BPA exposure increases meiotic errors, resulting in the production of chromosomally abnormal eggs. Although numerous studies have reported that estrogenic exposures negatively impact spermatogenesis, a direct link between exposures and meiotic errors in males has not been evaluated. To test the effect of estrogenic chemicals on meiotic chromosome dynamics, we exposed male mice to either BPA or to the strong synthetic estrogen, ethinyl estradiol during neonatal development when the first cells initiate meiosis. Although chromosome pairing and synapsis were unperturbed, exposed outbred CD-1 and inbred C3H/HeJ males had significantly reduced levels of crossovers, or meiotic recombination (as defined by the number of MLH1 foci in pachytene cells) by comparison with placebo. Unexpectedly, the effect was not limited to cells exposed at the time of meiotic entry but was evident in all subsequent waves of meiosis. To determine if the meiotic effects induced by estrogen result from changes to the soma or germline of the testis, we transplanted spermatogonial stem cells from exposed males into the testes of unexposed males. Reduced recombination was evident in meiocytes derived from colonies of transplanted cells. Taken together, our results suggest that brief exogenous estrogenic exposure causes subtle changes to the stem cell pool that result in permanent alterations in spermatogenesis (i.e., reduced recombination in descendent meiocytes) in the adult male.", "link"=>"http://www.mendeley.com/research/estrogenic-exposure-alters-spermatogonial-stem-cells-developing-testis-permanently-reducing-crossove", "reader_count"=>41, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>5, "Researcher"=>10, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>2, "Other"=>1, "Student > Bachelor"=>6, "Student > Master"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>5, "Researcher"=>10, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>2, "Other"=>1, "Student > Bachelor"=>6, "Student > Master"=>1}, "reader_count_by_subject_area"=>{"Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>11, "Agricultural and Biological Sciences"=>22, "Medicine and Dentistry"=>1, "Psychology"=>1, "Chemistry"=>1, "Computer Science"=>1, "Veterinary Science and Veterinary Medicine"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Psychology"=>{"Psychology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>22}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>11}, "Environmental Science"=>{"Environmental Science"=>3}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United States"=>2, "United Kingdom"=>1, "France"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1871616"], "description"=>"<p>A) Normal MI spermatocyte from a placebo male. B) MI spermatocyte with small autosomal univalents (arrows) and sex chromosome univalents (X and Y) from an EE-exposed male. C) Normal MII spermatocyte from a placebo male. D) MII spermatocyte with an extra chromatid (arrow) from an EE-exposed male. Scale bars represent 10 μm.</p>", "links"=>[], "tags"=>["exogenous estrogenic exposure causes", "meiotic entry", "meiotic errors", "pachytene cells", "inbred C 3H males", "unexposed males", "meiotic effects", "BPA exposure increases meiotic errors", "meiotic chromosome dynamics", "ethinyl estradiol", "Crossover Levels", "descendent meiocytes", "impact spermatogenesis", "outbred CD", "chromosome pairing", "Reduced recombination", "estrogen result", "cell pool", "estrogenic chemicals", "estrogenic exposures", "meiotic recombination", "Estrogenic Exposure Alters", "Adult Bisphenol", "MLH 1 foci", "Spermatogonial Stem Cells"], "article_id"=>1293900, "categories"=>["Uncategorised"], "users"=>["Lisa A. Vrooman", "Jon M. Oatley", "Jodi E. Griswold", "Terry J. Hassold", "Patricia A. Hunt"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004949.g002", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_metaphase_I_MI_and_metaphase_II_MII_cells_in_C3H_spermatocytes_from_placebo_and_exposed_males_/1293900", "title"=>"Analysis of metaphase I (MI) and metaphase II (MII) cells in C3H spermatocytes from placebo and exposed males.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-23 03:03:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1871624"], "description"=>"<p><sup>1</sup>Recipients with different letters were transplanted on different days.</p><p><sup>2</sup>Germ cells from placebo-exposed donors in one testis.</p><p><sup>3</sup>Germ cells from EE-exposed males in the contralateral testis.</p><p>Values represent mean MLH1 ± SEM.</p><p>n = number of cells analyzed.</p><p>*indicates significant difference between exposed and placebo cells in one-tailed t-test (p<0.05)</p><p>Recombination in transplanted males.</p>", "links"=>[], "tags"=>["exogenous estrogenic exposure causes", "meiotic entry", "meiotic errors", "pachytene cells", "inbred C 3H males", "unexposed males", "meiotic effects", "BPA exposure increases meiotic errors", "meiotic chromosome dynamics", "ethinyl estradiol", "Crossover Levels", "descendent meiocytes", "impact spermatogenesis", "outbred CD", "chromosome pairing", "Reduced recombination", "estrogen result", "cell pool", "estrogenic chemicals", "estrogenic exposures", "meiotic recombination", "Estrogenic Exposure Alters", "Adult Bisphenol", "MLH 1 foci", "Spermatogonial Stem Cells"], "article_id"=>1293908, "categories"=>["Uncategorised"], "users"=>["Lisa A. Vrooman", "Jon M. Oatley", "Jodi E. Griswold", "Terry J. Hassold", "Patricia A. Hunt"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004949.t004", "stats"=>{"downloads"=>4, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Recombination_in_transplanted_males_/1293908", "title"=>"Recombination in transplanted males.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-01-23 03:03:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1871619"], "description"=>"<p>A) RAD51 foci in zygotene cell from 20 dpp CD-1 male exposed to 0.25 ng/g/day EE. RAD51 = green, SYCP3 = red, scale bar = 10 μm. B, C) Mean RAD51 counts in placebo and EE-exposed CD-1 males at 20 dpp (B) and 12 weeks of age (C). Data points represent RAD51 foci values from 20–25 zygotene cells from 3–4 males from <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004949#pgen.1004949.t001\" target=\"_blank\">Table 1</a>. D-F) Total autosomal SC length (μm) in pachytene cells from placebo and exposed CD-1 males at 20 dpp (D), 12 weeks (E) and 1 year of age (F). Data points represent total SC length from 25–30 pachytene cells from 3–5 CD-1 males. Black bars denote group mean. Placebo and exposure groups were compared by a one-tailed t-test; red asterisk denotes significant difference (p<0.05).</p>", "links"=>[], "tags"=>["exogenous estrogenic exposure causes", "meiotic entry", "meiotic errors", "pachytene cells", "inbred C 3H males", "unexposed males", "meiotic effects", "BPA exposure increases meiotic errors", "meiotic chromosome dynamics", "ethinyl estradiol", "Crossover Levels", "descendent meiocytes", "impact spermatogenesis", "outbred CD", "chromosome pairing", "Reduced recombination", "estrogen result", "cell pool", "estrogenic chemicals", "estrogenic exposures", "meiotic recombination", "Estrogenic Exposure Alters", "Adult Bisphenol", "MLH 1 foci", "Spermatogonial Stem Cells"], "article_id"=>1293903, "categories"=>["Uncategorised"], "users"=>["Lisa A. Vrooman", "Jon M. Oatley", "Jodi E. Griswold", "Terry J. Hassold", "Patricia A. Hunt"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004949.g004", "stats"=>{"downloads"=>1, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RAD51_foci_counts_and_SC_length_measurements_in_placebo_and_exposed_CD_1_males_/1293903", "title"=>"RAD51 foci counts and SC length measurements in placebo and exposed CD-1 males.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-23 03:03:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1871620"], "description"=>"<p>*Mean MLH1 ± SEM for 25–30 pachytene cells per male, with 5–12 males/group.</p><p><sup>a-d</sup> Exposure within a strain and age were compared by one-way ANOVA (CD-1, C57BL/6J) or one-tail t-test (C3H/HeJ, C3H/B6 F1). Superscript letters denote significant differences as determined by a Newman-Keuls post hoc test (p<0.05); like letters indicate no difference.</p><p>— Denotes experimental group was not performed.</p><p>Recombination rates<sup><a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004949#t001fn001\" target=\"_blank\">*</a></sup> in placebo and exposed males.</p>", "links"=>[], "tags"=>["exogenous estrogenic exposure causes", "meiotic entry", "meiotic errors", "pachytene cells", "inbred C 3H males", "unexposed males", "meiotic effects", "BPA exposure increases meiotic errors", "meiotic chromosome dynamics", "ethinyl estradiol", "Crossover Levels", "descendent meiocytes", "impact spermatogenesis", "outbred CD", "chromosome pairing", "Reduced recombination", "estrogen result", "cell pool", "estrogenic chemicals", "estrogenic exposures", "meiotic recombination", "Estrogenic Exposure Alters", "Adult Bisphenol", "MLH 1 foci", "Spermatogonial Stem Cells"], "article_id"=>1293904, "categories"=>["Uncategorised"], "users"=>["Lisa A. Vrooman", "Jon M. Oatley", "Jodi E. Griswold", "Terry J. Hassold", "Patricia A. Hunt"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004949.t001", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Recombination_rates_in_placebo_and_exposed_males_/1293904", "title"=>"Recombination rates<sup>*</sup> in placebo and exposed males.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-01-23 03:03:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1871618"], "description"=>"<p>C3H male pups from timed-pregnant C3H females were orally exposed to placebo or 0.25 ng/g/day EE from 1–12 dpp. At 13 dpp, testes were pooled per exposure group, germ cells were isolated, and transplanted into W/W<sup>v</sup> adult males. Placebo cells were injected into one testis, and EE-exposed cells into the contralateral testis. Different letters and numbers represent different transplantation days and individuals, respectively. Meiotic analyses occurred 8 weeks post-transplantation.</p>", "links"=>[], "tags"=>["exogenous estrogenic exposure causes", "meiotic entry", "meiotic errors", "pachytene cells", "inbred C 3H males", "unexposed males", "meiotic effects", "BPA exposure increases meiotic errors", "meiotic chromosome dynamics", "ethinyl estradiol", "Crossover Levels", "descendent meiocytes", "impact spermatogenesis", "outbred CD", "chromosome pairing", "Reduced recombination", "estrogen result", "cell pool", "estrogenic chemicals", "estrogenic exposures", "meiotic recombination", "Estrogenic Exposure Alters", "Adult Bisphenol", "MLH 1 foci", "Spermatogonial Stem Cells"], "article_id"=>1293902, "categories"=>["Uncategorised"], "users"=>["Lisa A. Vrooman", "Jon M. Oatley", "Jodi E. Griswold", "Terry J. Hassold", "Patricia A. Hunt"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004949.g003", "stats"=>{"downloads"=>5, "page_views"=>88, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Germ_cell_transplantation_experimental_design_/1293902", "title"=>"Germ cell transplantation experimental design.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-23 03:03:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1871615"], "description"=>"<p>A) Representative spermatocyte with an SC lacking an MLH1 focus (white arrow) from an adult C3H male orally exposed to 0.25 ng EE from 1–12 dpp. MLH1 = green, SYCP3 = red. B, C) The frequency of cells with an SC lacking MLH1 in placebo and exposed males analyzed at 20 dpp, 12 week-old, and 1 year-old CD-1 males (B) and 20 dpp and 12 week-old C3H males (C). Differences were tested by Chi-square analysis. For CD-1, X<sup>2</sup> = 51.70 (p<0.0001) at 20 dpp, X<sup>2</sup> = 3.57 (p>0.05) at 12 weeks, and X<sup>2</sup> = 1.56 (p>0.05) at 1 year-old. For C3H, X<sup>2</sup> = 32.87 (p<0.0001) at 20 dpp, and X<sup>2</sup> = 13.95 (p<0.001) at 12 weeks.</p>", "links"=>[], "tags"=>["exogenous estrogenic exposure causes", "meiotic entry", "meiotic errors", "pachytene cells", "inbred C 3H males", "unexposed males", "meiotic effects", "BPA exposure increases meiotic errors", "meiotic chromosome dynamics", "ethinyl estradiol", "Crossover Levels", "descendent meiocytes", "impact spermatogenesis", "outbred CD", "chromosome pairing", "Reduced recombination", "estrogen result", "cell pool", "estrogenic chemicals", "estrogenic exposures", "meiotic recombination", "Estrogenic Exposure Alters", "Adult Bisphenol", "MLH 1 foci", "Spermatogonial Stem Cells"], "article_id"=>1293899, "categories"=>["Uncategorised"], "users"=>["Lisa A. Vrooman", "Jon M. Oatley", "Jodi E. Griswold", "Terry J. Hassold", "Patricia A. Hunt"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004949.g001", "stats"=>{"downloads"=>1, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_pachytene_cells_from_CD_1_and_C3H_males_/1293899", "title"=>"Analysis of pachytene cells from CD-1 and C3H males.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-23 03:03:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1871626", "https://ndownloader.figshare.com/files/1871627", "https://ndownloader.figshare.com/files/1871628", "https://ndownloader.figshare.com/files/1871629", "https://ndownloader.figshare.com/files/1871630"], "description"=>"<div><p>Bisphenol A (BPA) and other endocrine disrupting chemicals have been reported to induce negative effects on a wide range of physiological processes, including reproduction. In the female, BPA exposure increases meiotic errors, resulting in the production of chromosomally abnormal eggs. Although numerous studies have reported that estrogenic exposures negatively impact spermatogenesis, a direct link between exposures and meiotic errors in males has not been evaluated. To test the effect of estrogenic chemicals on meiotic chromosome dynamics, we exposed male mice to either BPA or to the strong synthetic estrogen, ethinyl estradiol during neonatal development when the first cells initiate meiosis. Although chromosome pairing and synapsis were unperturbed, exposed outbred CD-1 and inbred C3H/HeJ males had significantly reduced levels of crossovers, or meiotic recombination (as defined by the number of MLH1 foci in pachytene cells) by comparison with placebo. Unexpectedly, the effect was not limited to cells exposed at the time of meiotic entry but was evident in all subsequent waves of meiosis. To determine if the meiotic effects induced by estrogen result from changes to the soma or germline of the testis, we transplanted spermatogonial stem cells from exposed males into the testes of unexposed males. Reduced recombination was evident in meiocytes derived from colonies of transplanted cells. Taken together, our results suggest that brief exogenous estrogenic exposure causes subtle changes to the stem cell pool that result in permanent alterations in spermatogenesis (i.e., reduced recombination in descendent meiocytes) in the adult male.</p></div>", "links"=>[], "tags"=>["exogenous estrogenic exposure causes", "meiotic entry", "meiotic errors", "pachytene cells", "inbred C 3H males", "unexposed males", "meiotic effects", "BPA exposure increases meiotic errors", "meiotic chromosome dynamics", "ethinyl estradiol", "Crossover Levels", "descendent meiocytes", "impact spermatogenesis", "outbred CD", "chromosome pairing", "Reduced recombination", "estrogen result", "cell pool", "estrogenic chemicals", "estrogenic exposures", "meiotic recombination", "Estrogenic Exposure Alters", "Adult Bisphenol", "MLH 1 foci", "Spermatogonial Stem Cells"], "article_id"=>1293910, "categories"=>["Uncategorised"], "users"=>["Lisa A. Vrooman", "Jon M. Oatley", "Jodi E. Griswold", "Terry J. Hassold", "Patricia A. Hunt"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004949.s001", "https://dx.doi.org/10.1371/journal.pgen.1004949.s002", "https://dx.doi.org/10.1371/journal.pgen.1004949.s003", "https://dx.doi.org/10.1371/journal.pgen.1004949.s004", "https://dx.doi.org/10.1371/journal.pgen.1004949.s005"], "stats"=>{"downloads"=>8, "page_views"=>46, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Estrogenic_Exposure_Alters_the_Spermatogonial_Stem_Cells_in_the_Developing_Testis_Permanently_Reducing_Crossover_Levels_in_the_Adult_/1293910", "title"=>"Estrogenic Exposure Alters the Spermatogonial Stem Cells in the Developing Testis, Permanently Reducing Crossover Levels in the Adult", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-01-23 03:03:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1871623"], "description"=>"<p>*Data represent number of cells and percentage in parentheses from 20–25 MII cells per animal from 3 placebo and 5 EE-exposed C3H males.</p><p>Analysis of metaphase II in placebo and exposed males.</p>", "links"=>[], "tags"=>["exogenous estrogenic exposure causes", "meiotic entry", "meiotic errors", "pachytene cells", "inbred C 3H males", "unexposed males", "meiotic effects", "BPA exposure increases meiotic errors", "meiotic chromosome dynamics", "ethinyl estradiol", "Crossover Levels", "descendent meiocytes", "impact spermatogenesis", "outbred CD", "chromosome pairing", "Reduced recombination", "estrogen result", "cell pool", "estrogenic chemicals", "estrogenic exposures", "meiotic recombination", "Estrogenic Exposure Alters", "Adult Bisphenol", "MLH 1 foci", "Spermatogonial Stem Cells"], "article_id"=>1293907, "categories"=>["Uncategorised"], "users"=>["Lisa A. Vrooman", "Jon M. Oatley", "Jodi E. Griswold", "Terry J. Hassold", "Patricia A. Hunt"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004949.t003", "stats"=>{"downloads"=>2, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_metaphase_II_in_placebo_and_exposed_males_/1293907", "title"=>"Analysis of metaphase II in placebo and exposed males.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-01-23 03:03:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1871622"], "description"=>"<p>*Data represent number of cells and percentage in parentheses from 20–27 MI cells per animal from 3 placebo and 5 EE-exposed C3H males; X<sup>2</sup> = 8.65, p<0.005 for comparison of normal and abnormal cells.</p><p>Analysis of metaphase I in placebo and exposed C3H males.</p>", "links"=>[], "tags"=>["exogenous estrogenic exposure causes", "meiotic entry", "meiotic errors", "pachytene cells", "inbred C 3H males", "unexposed males", "meiotic effects", "BPA exposure increases meiotic errors", "meiotic chromosome dynamics", "ethinyl estradiol", "Crossover Levels", "descendent meiocytes", "impact spermatogenesis", "outbred CD", "chromosome pairing", "Reduced recombination", "estrogen result", "cell pool", "estrogenic chemicals", "estrogenic exposures", "meiotic recombination", "Estrogenic Exposure Alters", "Adult Bisphenol", "MLH 1 foci", "Spermatogonial Stem Cells"], "article_id"=>1293906, "categories"=>["Uncategorised"], "users"=>["Lisa A. Vrooman", "Jon M. Oatley", "Jodi E. Griswold", "Terry J. Hassold", "Patricia A. Hunt"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004949.t002", "stats"=>{"downloads"=>1, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_metaphase_I_in_placebo_and_exposed_C3H_males_/1293906", "title"=>"Analysis of metaphase I in placebo and exposed C3H males.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-01-23 03:03:59"}

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{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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