The GNU subunit of PNG kinase, the developmental regulator of mRNA translation, binds BIC-C to localize to RNP granules

  1. Emir E Avilés-Pagán
  2. Masatoshi Hara
  3. Terry L Orr-Weaver  Is a corresponding author
  1. Whitehead Institute/MIT, United States
  2. Osaka University, Japan
  3. Whitehead Institute for Biomedical Research, United States

Abstract

Control of mRNA translation is a key mechanism by which the differentiated oocyte transitions to a totipotent embryo. In Drosophila, the PNG kinase complex regulates maternal mRNA translation at the oocyte-to-embryo transition. We previously showed the GNU activating subunit is crucial in regulating PNG and timing its activity to the window between egg activation and early embryogenesis (Hara et al., 2017). In this study, we find associations between GNU and proteins of RNP granules and demonstrate that GNU localizes to cytoplasmic RNP granules in the mature oocyte, identifying GNU as a new component of a subset of RNP granules. Furthermore, we define roles for the domains of GNU. Interactions between GNU and the granule component BIC-C reveal potential conserved functions for translational regulation in metazoan development. We propose that by binding to BIC-C, upon egg activation GNU brings PNG to its initial targets, translational repressors in RNP granules.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figure 1, Figure 1-Supplement 1, Figure 1-Supplement 2, Figure 1-Supplement 3, Figure 2, Figure 3-Supplement 1, Figure 4, Figure 4-Supplement 1, Figure 5, Figure 5-Supplement 1, Figure 6, Table 1, and Supplementary Table 1.

Article and author information

Author details

  1. Emir E Avilés-Pagán

    Department of Biology, Whitehead Institute/MIT, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1245-0941
  2. Masatoshi Hara

    Frontier Biosciences, Osaka University, Suita, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Terry L Orr-Weaver

    Department of Biology, MIT, Whitehead Institute for Biomedical Research, Cambridge, United States
    For correspondence
    weaver@wi.mit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7934-111X

Funding

National Institutes of Health (GM118090)

  • Terry L Orr-Weaver

JSPS Postdoctoral Fellowship

  • Masatoshi Hara

Uehara Memorial Foundation

  • Masatoshi Hara

JSPS KAKENHI (JP20H05367)

  • Masatoshi Hara

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

Reviewing Editor

  1. Jon Pines, Institute of Cancer Research Research, United Kingdom

Publication history

  1. Received: February 12, 2021
  2. Accepted: July 9, 2021
  3. Accepted Manuscript published: July 12, 2021 (version 1)
  4. Version of Record published: July 26, 2021 (version 2)

Copyright

© 2021, Avilés-Pagán 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. Emir E Avilés-Pagán
  2. Masatoshi Hara
  3. Terry L Orr-Weaver
(2021)
The GNU subunit of PNG kinase, the developmental regulator of mRNA translation, binds BIC-C to localize to RNP granules
eLife 10:e67294.
https://doi.org/10.7554/eLife.67294

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