ME31B globally represses maternal mRNAs by two distinct mechanisms during the Drosophila maternal-to-zygotic transition

  1. Miranda Wang
  2. Michael Ly
  3. Andrew Lugowski
  4. John D Laver
  5. Howard D Lipshitz
  6. Craig A Smibert
  7. Olivia S Rissland  Is a corresponding author
  1. The Hospital for Sick Children, Canada
  2. University of Toronto, Canada

Abstract

In animal embryos, control of development is passed from exclusively maternal gene products to those encoded by the embryonic genome in a process referred to as the maternal-to-zygotic transition (MZT). We show that the RNA-binding protein, ME31B, binds to and represses the expression of thousands of maternal mRNAs during the Drosophila MZT. However, ME31B carries out repression in different ways during different phases of the MZT. Early, it represses translation while, later, its binding leads to mRNA destruction, most likely as a consequence of translational repression in the context of robust mRNA decay. In a process dependent on the PNG kinase, levels of ME31B and its partners, Cup and Trailer Hitch (TRAL), decrease by over 10-fold during the MZT, leading to a change in the composition of mRNA-protein complexes. We propose that ME31B is a global repressor whose regulatory impact changes based on its biological context.

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The following previously published data sets were used

Article and author information

Author details

  1. Miranda Wang

    Molecular Medicine Program, The Hospital for Sick Children, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. Michael Ly

    Molecular Medicine Program, The Hospital for Sick Children, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Andrew Lugowski

    Molecular Medicine Program, The Hospital for Sick Children, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. John D Laver

    Department of Molecular Genetics, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Howard D Lipshitz

    Department of Molecular Genetics, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Craig A Smibert

    Department of Molecular Genetics, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  7. Olivia S Rissland

    Molecular Medicine Program, The Hospital for Sick Children, Toronto, Canada
    For correspondence
    olivia.rissland@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2619-6019

Funding

Natural Sciences and Engineering Research Council of Canada

  • Craig A Smibert
  • Olivia S Rissland

Canadian Institutes of Health Research

  • Howard D Lipshitz

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

Reviewing Editor

  1. Rachel Green, Johns Hopkins School of Medicine, United States

Version history

  1. Received: April 18, 2017
  2. Accepted: September 4, 2017
  3. Accepted Manuscript published: September 6, 2017 (version 1)
  4. Version of Record published: September 19, 2017 (version 2)

Copyright

© 2017, Wang 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. Miranda Wang
  2. Michael Ly
  3. Andrew Lugowski
  4. John D Laver
  5. Howard D Lipshitz
  6. Craig A Smibert
  7. Olivia S Rissland
(2017)
ME31B globally represses maternal mRNAs by two distinct mechanisms during the Drosophila maternal-to-zygotic transition
eLife 6:e27891.
https://doi.org/10.7554/eLife.27891

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https://doi.org/10.7554/eLife.27891

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