1. Chromosomes and Gene Expression
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Phosphorylation of luminal region of the SUN-domain protein Mps3 promotes nuclear envelope localization during meiosis

  1. Hanumanthu BD Prasada Rao
  2. Takeshi Sato
  3. Kiran Challa
  4. Yurika Fujita
  5. Miki Shinohara
  6. Akira Shinohara  Is a corresponding author
  1. National Institute for Animal Biotechnology, India
  2. Kyoto Pharmaceutical University, Japan
  3. Osaka University, Japan
Research Article
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Cite this article as: eLife 2021;10:e63119 doi: 10.7554/eLife.63119

Abstract

During meiosis, protein ensembles in the nuclear envelope (NE) containing SUN- and KASH-domain proteins, called linker nucleocytoskeleton and cytoskeleton (LINC) complex, promote the chromosome motion. Yeast SUN-domain protein, Mps3, forms multiple meiosis-specific ensembles on NE, which show dynamic localisation for chromosome motion; however, the mechanism by which these Mps3 ensembles are formed during meiosis remains largely unknown. Here, we showed that the cyclin-dependent protein kinase (CDK) and Dbf4-dependent Cdc7 protein kinase (DDK) regulate meiosis-specific dynamics of Mps3 on NE, particularly by mediating the resolution of Mps3 clusters and telomere clustering. We also found that the luminal region of Mps3 juxtaposed to the inner nuclear membrane is required for meiosis-specific localisation of Mps3 on NE. Negative charges introduced by meiosis-specific phosphorylation in the luminal region of Mps3 alter its interaction with negatively charged lipids by electric repulsion in reconstituted liposomes. Phospho-mimetic substitution in the luminal region suppresses the localisation of Mps3 via the inactivation of CDK or DDK. Our study revealed multi-layered phosphorylation-dependent regulation of the localisation of Mps3 on NE for meiotic chromosome motion and NE remodelling.

Data availability

The numerical data in all Figures (graphs) are provided in Source data. Original blots and gels are provided in Source data.

Article and author information

Author details

  1. Hanumanthu BD Prasada Rao

    National Institute for Animal Biotechnology, Hyderabad, India
    Competing interests
    The authors declare that no competing interests exist.
  2. Takeshi Sato

    Pharmaceutical education, Kyoto Pharmaceutical University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Kiran Challa

    Osaka University, Suita/Osaka, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Yurika Fujita

    Osaka University, Suita/Osaka, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Miki Shinohara

    Integrated protein functions, Osaka University, Suita, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Akira Shinohara

    Osaka University, Suita/Osaka, Japan
    For correspondence
    ashino@protein.osaka-u.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4207-8247

Funding

Japan Society for the Promotion of Science (2212500,22125002,15H05973,16H04742,19H00981)

  • Akira Shinohara

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

Reviewing Editor

  1. Adèle L Marston, University of Edinburgh, United Kingdom

Publication history

  1. Received: September 15, 2020
  2. Accepted: September 26, 2021
  3. Accepted Manuscript published: September 29, 2021 (version 1)

Copyright

© 2021, Prasada Rao 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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