Spatial control of translation repression and polarized growth by conserved NDR kinase Orb6 and RNA-binding protein Sts5

  1. Illyce Nuñez
  2. Marbelys Rodriguez Pino
  3. David J Wiley
  4. Maitreyi E Das
  5. Chuan Chen
  6. Tetsuya Goshima
  7. Kazunori Kume
  8. Dai Hirata
  9. Takashi Toda
  10. Fulvia Verde  Is a corresponding author
  1. University of Miami School of Medicine, United States
  2. The University of Tennessee, United States
  3. National Research Institute of Brewing, Japan
  4. Hiroshima University, Japan
  5. The Francis Crick Institute, United Kingdom

Abstract

RNA-binding proteins contribute to the formation of ribonucleoprotein (RNP) granules by phase transition, but regulatory mechanisms are not fully understood. Conserved fission yeast NDR (Nuclear Dbf2-Related) kinase Orb6 governs cell morphogenesis in part by spatially controlling Cdc42 GTPase. Here we describe a novel, independent function for Orb6 kinase in negatively regulating the recruitment of RNA-binding protein Sts5 into RNPs to promote polarized cell growth. We find that Orb6 kinase inhibits Sts5 recruitment into granules, its association with processing (P) bodies, and degradation of Sts5-bound mRNAs by promoting Sts5 interaction with 14-3-3 protein Rad24. Many Sts5-bound mRNAs encode essential factors for polarized cell growth, and Orb6 kinase spatially and temporally controls the extent of Sts5 granule formation. Disruption of this control system affects cell morphology and alters the pattern of polarized cell growth, revealing a role for Orb6 kinase in the spatial control of translational repression that enables normal cell morphogenesis.

Article and author information

Author details

  1. Illyce Nuñez

    Molecular and Cellular Pharmacology, University of Miami School of Medicine, Miami, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Marbelys Rodriguez Pino

    Molecular and Cellular Pharmacology, University of Miami School of Medicine, Miami, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. David J Wiley

    Molecular and Cellular Pharmacology, University of Miami School of Medicine, Miami, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Maitreyi E Das

    Department of Biochemistry and Cellular and Molecular Biology, The University of Tennessee, Knoxville, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Chuan Chen

    Molecular and Cellular Pharmacology, University of Miami School of Medicine, Miami, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Tetsuya Goshima

    National Research Institute of Brewing, Higashi-Hiroshima, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Kazunori Kume

    Department of Molecular Biotechnology, Hiroshima University, Higashi-Hiroshima, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. Dai Hirata

    Department of Molecular Biotechnology, Hiroshima University, Higashi-Hiroshima, Japan
    Competing interests
    The authors declare that no competing interests exist.
  9. Takashi Toda

    The Francis Crick Institute, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. Fulvia Verde

    Molecular and Cellular Pharmacology, University of Miami School of Medicine, Miami, United States
    For correspondence
    fverde@miami.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2575-0823

Funding

National Institutes of Health (GM095867)

  • Marbelys Rodriguez Pino
  • David J Wiley
  • Maitreyi E Das
  • Chuan Chen
  • Fulvia Verde

National Science Foundation (745129)

  • Maitreyi E Das
  • Fulvia Verde

Cancer Research UK

  • Takashi Toda

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

Reviewing Editor

  1. J Paul Taylor, St Jude Children's Research Hospital, United States

Version history

  1. Received: January 8, 2016
  2. Accepted: July 28, 2016
  3. Accepted Manuscript published: July 30, 2016 (version 1)
  4. Version of Record published: September 5, 2016 (version 2)

Copyright

© 2016, Nuñez 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. Illyce Nuñez
  2. Marbelys Rodriguez Pino
  3. David J Wiley
  4. Maitreyi E Das
  5. Chuan Chen
  6. Tetsuya Goshima
  7. Kazunori Kume
  8. Dai Hirata
  9. Takashi Toda
  10. Fulvia Verde
(2016)
Spatial control of translation repression and polarized growth by conserved NDR kinase Orb6 and RNA-binding protein Sts5
eLife 5:e14216.
https://doi.org/10.7554/eLife.14216

Share this article

https://doi.org/10.7554/eLife.14216

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