Prolonged ovarian storage of mature Drosophila oocytes dramatically increases meiotic spindle instability
Human oocytes frequently generate aneuploid embryos that subsequently miscarry. In contrast, Drosophila oocytes from outbred laboratory stocks develop fully regardless of maternal age. Since mature Drosophila oocytes are not extensively stored in the ovary under laboratory conditions like they are i...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2019-11-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/49455 |
| _version_ | 1811201364837007360 |
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| author | Ethan J Greenblatt Rebecca Obniski Claire Mical Allan C Spradling |
| author_facet | Ethan J Greenblatt Rebecca Obniski Claire Mical Allan C Spradling |
| author_sort | Ethan J Greenblatt |
| collection | DOAJ |
| description | Human oocytes frequently generate aneuploid embryos that subsequently miscarry. In contrast, Drosophila oocytes from outbred laboratory stocks develop fully regardless of maternal age. Since mature Drosophila oocytes are not extensively stored in the ovary under laboratory conditions like they are in the wild, we developed a system to investigate how storage affects oocyte quality. The developmental capacity of stored mature Drosophila oocytes decays in a precise manner over 14 days at 25°C. These oocytes are transcriptionally inactive and persist using ongoing translation of stored mRNAs. Ribosome profiling revealed a progressive 2.3-fold decline in average translational efficiency during storage that correlates with oocyte functional decay. Although normal bipolar meiotic spindles predominate during the first week, oocytes stored for longer periods increasingly show tripolar, monopolar and other spindle defects, and give rise to embryos that fail to develop due to aneuploidy. Thus, meiotic chromosome segregation in mature Drosophila oocytes is uniquely sensitive to prolonged storage. Our work suggests the chromosome instability of human embryos could be mitigated by reducing the period of time mature human oocytes are stored in the ovary prior to ovulation. |
| first_indexed | 2024-04-12T02:20:39Z |
| format | Article |
| id | doaj.art-ff381f4e727040ad8bf44c4b17538dbb |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:20:39Z |
| publishDate | 2019-11-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-ff381f4e727040ad8bf44c4b17538dbb2022-12-22T03:52:08ZengeLife Sciences Publications LtdeLife2050-084X2019-11-01810.7554/eLife.49455Prolonged ovarian storage of mature Drosophila oocytes dramatically increases meiotic spindle instabilityEthan J Greenblatt0https://orcid.org/0000-0002-3805-0113Rebecca Obniski1Claire Mical2Allan C Spradling3https://orcid.org/0000-0002-5251-1801Department of Embryology, Howard Hughes Medical Institute Research Laboratories, Carnegie Institution for Science, Baltimore, United StatesDepartment of Embryology, Howard Hughes Medical Institute Research Laboratories, Carnegie Institution for Science, Baltimore, United StatesDepartment of Embryology, Howard Hughes Medical Institute Research Laboratories, Carnegie Institution for Science, Baltimore, United StatesDepartment of Embryology, Howard Hughes Medical Institute Research Laboratories, Carnegie Institution for Science, Baltimore, United StatesHuman oocytes frequently generate aneuploid embryos that subsequently miscarry. In contrast, Drosophila oocytes from outbred laboratory stocks develop fully regardless of maternal age. Since mature Drosophila oocytes are not extensively stored in the ovary under laboratory conditions like they are in the wild, we developed a system to investigate how storage affects oocyte quality. The developmental capacity of stored mature Drosophila oocytes decays in a precise manner over 14 days at 25°C. These oocytes are transcriptionally inactive and persist using ongoing translation of stored mRNAs. Ribosome profiling revealed a progressive 2.3-fold decline in average translational efficiency during storage that correlates with oocyte functional decay. Although normal bipolar meiotic spindles predominate during the first week, oocytes stored for longer periods increasingly show tripolar, monopolar and other spindle defects, and give rise to embryos that fail to develop due to aneuploidy. Thus, meiotic chromosome segregation in mature Drosophila oocytes is uniquely sensitive to prolonged storage. Our work suggests the chromosome instability of human embryos could be mitigated by reducing the period of time mature human oocytes are stored in the ovary prior to ovulation.https://elifesciences.org/articles/49455oocytefertilitymRNA translationagingmeiotic spindleaneuploidy |
| spellingShingle | Ethan J Greenblatt Rebecca Obniski Claire Mical Allan C Spradling Prolonged ovarian storage of mature Drosophila oocytes dramatically increases meiotic spindle instability eLife oocyte fertility mRNA translation aging meiotic spindle aneuploidy |
| title | Prolonged ovarian storage of mature Drosophila oocytes dramatically increases meiotic spindle instability |
| title_full | Prolonged ovarian storage of mature Drosophila oocytes dramatically increases meiotic spindle instability |
| title_fullStr | Prolonged ovarian storage of mature Drosophila oocytes dramatically increases meiotic spindle instability |
| title_full_unstemmed | Prolonged ovarian storage of mature Drosophila oocytes dramatically increases meiotic spindle instability |
| title_short | Prolonged ovarian storage of mature Drosophila oocytes dramatically increases meiotic spindle instability |
| title_sort | prolonged ovarian storage of mature drosophila oocytes dramatically increases meiotic spindle instability |
| topic | oocyte fertility mRNA translation aging meiotic spindle aneuploidy |
| url | https://elifesciences.org/articles/49455 |
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