Knockout of the Glucocorticoid Receptor Impairs Reproduction in Female Zebrafish
The pleiotropic effects of glucocorticoids in metabolic, developmental, immune and stress response processes have been extensively investigated; conversely, their roles in reproduction are still less documented. It is well known that stress or long-lasting therapies can cause a strong increase in th...
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| Format: | Article |
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MDPI AG
2020-11-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/21/23/9073 |
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| author | Francesca Maradonna Giorgia Gioacchini Valentina Notarstefano Camilla Maria Fontana Filippo Citton Luisa Dalla Valle Elisabetta Giorgini Oliana Carnevali |
| author_facet | Francesca Maradonna Giorgia Gioacchini Valentina Notarstefano Camilla Maria Fontana Filippo Citton Luisa Dalla Valle Elisabetta Giorgini Oliana Carnevali |
| author_sort | Francesca Maradonna |
| collection | DOAJ |
| description | The pleiotropic effects of glucocorticoids in metabolic, developmental, immune and stress response processes have been extensively investigated; conversely, their roles in reproduction are still less documented. It is well known that stress or long-lasting therapies can cause a strong increase in these hormones, negatively affecting reproduction. Moreover, the need of glucocorticoid (GC) homeostatic levels is highlighted by the reduced fertility reported in the zebrafish glucocorticoid receptor mutant (<i>nr3c1<sup>ia30/ia30</sup></i>) line (hereafter named <i>gr<sup>−/−</sup>).</i> Starting from such evidence, in this study, we have investigated the role of glucocorticoid receptor (Gr) in the reproduction of female zebrafish. Key signals orchestrating the reproductive process at the brain, liver, and ovarian levels were analyzed using a multidisciplinary approach. An impairment of the kiss-GnRH system was observed at the central level in (<i>gr<sup>−/−</sup></i>) mutants as compared to wild-type (<i>wt</i>) females while, in the liver, vitellogenin <i>(vtg)</i> mRNA transcription was not affected. Changes were instead observed in the ovary, particularly in maturing and fully grown follicles (classes III and IV), as documented by the mRNA levels of signals involved in oocyte maturation and ovulation. Follicles isolated from <i>gr<sup>−/−</sup></i> females displayed a decreased level of signals involved in the acquisition of competence and maturation, causing a reduction in ovulation with respect to <i>wt</i> females. Fourier transform infrared imaging (FTIRI) analysis of <i>gr<sup>−/−</sup></i> follicle cytoplasm showed major changes in macromolecule abundance and distribution with a clear alteration of oocyte composition. Finally, differences in the molecular structure of the zona radiata layer of <i>gr<sup>−/−</sup></i> follicles are likely to contribute to the reduced fertilization rate observed in mutants. |
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| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T14:28:34Z |
| publishDate | 2020-11-01 |
| publisher | MDPI AG |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-d7e481976a3340b49ded9bdc12ab63eb2023-11-20T22:48:20ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-11-012123907310.3390/ijms21239073Knockout of the Glucocorticoid Receptor Impairs Reproduction in Female ZebrafishFrancesca Maradonna0Giorgia Gioacchini1Valentina Notarstefano2Camilla Maria Fontana3Filippo Citton4Luisa Dalla Valle5Elisabetta Giorgini6Oliana Carnevali7Department of Life and Environmental Sciences, Università Politecnica delle Marche, Via Brecce Bianche snc, 60131 Ancona, ItalyDepartment of Life and Environmental Sciences, Università Politecnica delle Marche, Via Brecce Bianche snc, 60131 Ancona, ItalyDepartment of Life and Environmental Sciences, Università Politecnica delle Marche, Via Brecce Bianche snc, 60131 Ancona, ItalyDepartment of Biology, Università di Padova, Via Ugo Bassi 58/B, 35131 Padova, ItalyDepartment of Biology, Università di Padova, Via Ugo Bassi 58/B, 35131 Padova, ItalyDepartment of Biology, Università di Padova, Via Ugo Bassi 58/B, 35131 Padova, ItalyDepartment of Life and Environmental Sciences, Università Politecnica delle Marche, Via Brecce Bianche snc, 60131 Ancona, ItalyDepartment of Life and Environmental Sciences, Università Politecnica delle Marche, Via Brecce Bianche snc, 60131 Ancona, ItalyThe pleiotropic effects of glucocorticoids in metabolic, developmental, immune and stress response processes have been extensively investigated; conversely, their roles in reproduction are still less documented. It is well known that stress or long-lasting therapies can cause a strong increase in these hormones, negatively affecting reproduction. Moreover, the need of glucocorticoid (GC) homeostatic levels is highlighted by the reduced fertility reported in the zebrafish glucocorticoid receptor mutant (<i>nr3c1<sup>ia30/ia30</sup></i>) line (hereafter named <i>gr<sup>−/−</sup>).</i> Starting from such evidence, in this study, we have investigated the role of glucocorticoid receptor (Gr) in the reproduction of female zebrafish. Key signals orchestrating the reproductive process at the brain, liver, and ovarian levels were analyzed using a multidisciplinary approach. An impairment of the kiss-GnRH system was observed at the central level in (<i>gr<sup>−/−</sup></i>) mutants as compared to wild-type (<i>wt</i>) females while, in the liver, vitellogenin <i>(vtg)</i> mRNA transcription was not affected. Changes were instead observed in the ovary, particularly in maturing and fully grown follicles (classes III and IV), as documented by the mRNA levels of signals involved in oocyte maturation and ovulation. Follicles isolated from <i>gr<sup>−/−</sup></i> females displayed a decreased level of signals involved in the acquisition of competence and maturation, causing a reduction in ovulation with respect to <i>wt</i> females. Fourier transform infrared imaging (FTIRI) analysis of <i>gr<sup>−/−</sup></i> follicle cytoplasm showed major changes in macromolecule abundance and distribution with a clear alteration of oocyte composition. Finally, differences in the molecular structure of the zona radiata layer of <i>gr<sup>−/−</sup></i> follicles are likely to contribute to the reduced fertilization rate observed in mutants.https://www.mdpi.com/1422-0067/21/23/9073glucocorticoids<i>gr</i> mutantsoocyte maturationvitellogenesis<i>Danio rerio</i>Fourier transform infrared imaging spectroscopy |
| spellingShingle | Francesca Maradonna Giorgia Gioacchini Valentina Notarstefano Camilla Maria Fontana Filippo Citton Luisa Dalla Valle Elisabetta Giorgini Oliana Carnevali Knockout of the Glucocorticoid Receptor Impairs Reproduction in Female Zebrafish International Journal of Molecular Sciences glucocorticoids <i>gr</i> mutants oocyte maturation vitellogenesis <i>Danio rerio</i> Fourier transform infrared imaging spectroscopy |
| title | Knockout of the Glucocorticoid Receptor Impairs Reproduction in Female Zebrafish |
| title_full | Knockout of the Glucocorticoid Receptor Impairs Reproduction in Female Zebrafish |
| title_fullStr | Knockout of the Glucocorticoid Receptor Impairs Reproduction in Female Zebrafish |
| title_full_unstemmed | Knockout of the Glucocorticoid Receptor Impairs Reproduction in Female Zebrafish |
| title_short | Knockout of the Glucocorticoid Receptor Impairs Reproduction in Female Zebrafish |
| title_sort | knockout of the glucocorticoid receptor impairs reproduction in female zebrafish |
| topic | glucocorticoids <i>gr</i> mutants oocyte maturation vitellogenesis <i>Danio rerio</i> Fourier transform infrared imaging spectroscopy |
| url | https://www.mdpi.com/1422-0067/21/23/9073 |
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