Prolonged ovarian storage of mature Drosophila oocytes dramatically increases meiotic spindle instability

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Abstract

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^oC. 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.

Data availability

Data has been uploaded to BioProjects at NCBI under PRJNA573922.

The following data sets were generated

(2019) Ribosome profiling and mRNA sequencing of aging oocytes in Drosophila.
NCBI Bioprojects, PRJNA57392.

https://www.ncbi.nlm.nih.gov/sra/PRJNA573922

Article and author information

Author details

Ethan Joseph Greenblatt

Department of Embryology, Howard Hughes Medical Institute, Carnegie Institution for Science, Baltimore, United States

Competing interests
No competing interests declared.
Rebecca Obniski

Department of Embryology, Howard Hughes Medical Institute, Carnegie Institution for Science, Baltimore, United States

Competing interests
No competing interests declared.
Claire Mical

Department of Embryology, Howard Hughes Medical Institute, Carnegie Institution for Science, Baltimore, United States

Competing interests
No competing interests declared.
Allan C Spradling

Department of Embryology, Howard Hughes Medical Institute, Carnegie Institution for Science, Baltimore, United States

For correspondence
spradling@ciwemb.edu

Competing interests
Allan C Spradling, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0002-5251-1801

Funding

Howard Hughes Medical Institute

Allan C Spradling

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.