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

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 dynami...

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Autores principales:	Hanumanthu BD Prasada Rao, Takeshi Sato, Kiran Challa, Yurika Fujita, Miki Shinohara, Akira Shinohara
Formato:	article
Lenguaje:	EN
Publicado:	eLife Sciences Publications Ltd 2021
Materias:	meiosis chromosome motion nuclear envelope sun domain Mps3 phosphorylation Medicine R Science Q Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/dadae1455c794b3c91bfee5485642f01
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spelling	oai:doaj.org-article:dadae1455c794b3c91bfee5485642f012021-11-05T16:22:24ZPhosphorylation of luminal region of the SUN-domain protein Mps3 promotes nuclear envelope localization during meiosis10.7554/eLife.631192050-084Xe63119https://doaj.org/article/dadae1455c794b3c91bfee5485642f012021-09-01T00:00:00Zhttps://elifesciences.org/articles/63119https://doaj.org/toc/2050-084XDuring 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.Hanumanthu BD Prasada RaoTakeshi SatoKiran ChallaYurika FujitaMiki ShinoharaAkira ShinoharaeLife Sciences Publications Ltdarticlemeiosischromosome motionnuclear envelopesun domainMps3phosphorylationMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	meiosis chromosome motion nuclear envelope sun domain Mps3 phosphorylation Medicine R Science Q Biology (General) QH301-705.5
spellingShingle	meiosis chromosome motion nuclear envelope sun domain Mps3 phosphorylation Medicine R Science Q Biology (General) QH301-705.5 Hanumanthu BD Prasada Rao Takeshi Sato Kiran Challa Yurika Fujita Miki Shinohara Akira Shinohara Phosphorylation of luminal region of the SUN-domain protein Mps3 promotes nuclear envelope localization during meiosis
description	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.
format	article
author	Hanumanthu BD Prasada Rao Takeshi Sato Kiran Challa Yurika Fujita Miki Shinohara Akira Shinohara
author_facet	Hanumanthu BD Prasada Rao Takeshi Sato Kiran Challa Yurika Fujita Miki Shinohara Akira Shinohara
author_sort	Hanumanthu BD Prasada Rao
title	Phosphorylation of luminal region of the SUN-domain protein Mps3 promotes nuclear envelope localization during meiosis
title_short	Phosphorylation of luminal region of the SUN-domain protein Mps3 promotes nuclear envelope localization during meiosis
title_full	Phosphorylation of luminal region of the SUN-domain protein Mps3 promotes nuclear envelope localization during meiosis
title_fullStr	Phosphorylation of luminal region of the SUN-domain protein Mps3 promotes nuclear envelope localization during meiosis
title_full_unstemmed	Phosphorylation of luminal region of the SUN-domain protein Mps3 promotes nuclear envelope localization during meiosis
title_sort	phosphorylation of luminal region of the sun-domain protein mps3 promotes nuclear envelope localization during meiosis
publisher	eLife Sciences Publications Ltd
publishDate	2021
url	https://doaj.org/article/dadae1455c794b3c91bfee5485642f01
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Phosphorylation of luminal region of the SUN-domain protein Mps3 promotes nuclear envelope localization during meiosis

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