1. Chromosomes and Gene Expression
  2. Developmental Biology
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The E2 Marie Kondo and the CTLH E3 ligase clear deposited RNA binding proteins during the maternal-to-zygotic transition

  1. Michael Zavortink
  2. Lauren N Rutt
  3. Svetlana Dzitoyeva
  4. Jesslyn C Henriksen
  5. Chloe Barrington
  6. Danielle Y Bilodeau
  7. Miranda Wang
  8. Lily Xiao Xiao Chen
  9. Olivia S Rissland  Is a corresponding author
  1. University of Colorado School of Medicine, United States
  2. The Hospital for Sick Children, Canada
Research Article
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Cite this article as: eLife 2020;9:e53889 doi: 10.7554/eLife.53889

Abstract

The maternal-to-zygotic transition (MZT) is a conserved step in animal development, where control is passed from the maternal to the zygotic genome. Although the MZT is typically considered from its impact on the transcriptome, we previously found that three maternally deposited Drosophila RNA binding proteins (ME31B, Trailer Hitch [TRAL], and Cup) are also cleared during the MZT by unknown mechanisms. Here, we show that these proteins are degraded by the ubiquitin-proteasome system. Marie Kondo, an E2 conjugating enzyme, and the E3 CTLH ligase are required for the destruction of ME31B, TRAL, and Cup. Structure modeling of the Drosophila CTLH complex suggests that substrate recognition is different than orthologous complexes. Despite occurring hours earlier, egg activation mediates clearance of these proteins through the Pan Gu kinase, which stimulates translation of Kondo mRNA. Clearance of the maternal protein dowry thus appears to be a coordinated, but as-yet underappreciated, aspect of the MZT.

Data availability

Sequencing data have been deposited in GEO under accession code GSE140436. All data generated during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 2 and 4.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Michael Zavortink

    Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Lauren N Rutt

    Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Svetlana Dzitoyeva

    Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jesslyn C Henriksen

    Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Chloe Barrington

    Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Danielle Y Bilodeau

    Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8086-4233
  7. Miranda Wang

    Molecular Medicine Program, The Hospital for Sick Children, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  8. Lily Xiao Xiao Chen

    Molecular Medicine Program, The Hospital for Sick Children, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  9. Olivia S Rissland

    Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, United States
    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

National Institute of General Medical Sciences (R35GM128680)

  • Olivia S Rissland

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, University of California, Berkeley, United States

Publication history

  1. Received: November 23, 2019
  2. Accepted: June 23, 2020
  3. Accepted Manuscript published: June 23, 2020 (version 1)
  4. Version of Record published: July 27, 2020 (version 2)

Copyright

© 2020, Zavortink 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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