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

  1. Ethan Joseph Greenblatt
  2. Rebecca Obniski
  3. Claire Mical
  4. Allan C Spradling  Is a corresponding author
  1. Howard Hughes Medical Institute, Carnegie Institution for Science, United States

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 25oC. 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

Article and author information

Author details

  1. Ethan Joseph Greenblatt

    Department of Embryology, Howard Hughes Medical Institute, Carnegie Institution for Science, Baltimore, United States
    Competing interests
    No competing interests declared.
  2. Rebecca Obniski

    Department of Embryology, Howard Hughes Medical Institute, Carnegie Institution for Science, Baltimore, United States
    Competing interests
    No competing interests declared.
  3. Claire Mical

    Department of Embryology, Howard Hughes Medical Institute, Carnegie Institution for Science, Baltimore, United States
    Competing interests
    No competing interests declared.
  4. 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.
    ORCID icon "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.

Reviewing Editor

  1. Michael B Eisen, HHMI, University of California, Berkeley, United States

Publication history

  1. Received: June 18, 2019
  2. Accepted: November 17, 2019
  3. Accepted Manuscript published: November 22, 2019 (version 1)
  4. Version of Record published: December 11, 2019 (version 2)

Copyright

© 2019, Greenblatt et al.

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.

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  1. Ethan Joseph Greenblatt
  2. Rebecca Obniski
  3. Claire Mical
  4. Allan C Spradling
(2019)
Prolonged ovarian storage of mature Drosophila oocytes dramatically increases meiotic spindle instability
eLife 8:e49455.
https://doi.org/10.7554/eLife.49455

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