Phosphorylation of luminal region of the SUN-domain protein Mps3 promotes nuclear envelope localization during meiosis

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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.

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

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Hanumanthu BD Prasada Rao

National Institute for Animal Biotechnology, Hyderabad, India

Competing interests
The authors declare that no competing interests exist.
Takeshi Sato

Pharmaceutical education, Kyoto Pharmaceutical University, Kyoto, Japan

Competing interests
The authors declare that no competing interests exist.
Kiran Challa

Osaka University, Suita/Osaka, Japan

Competing interests
The authors declare that no competing interests exist.
Yurika Fujita

Osaka University, Suita/Osaka, Japan

Competing interests
The authors declare that no competing interests exist.
Miki Shinohara

Integrated protein functions, Osaka University, Suita, Japan

Competing interests
The authors declare that no competing interests exist.
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.

"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.

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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.