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Nuclear pore complex acetylation regulates mRNA export and cell cycle commitment in budding yeast

Nuclear pore complexes (NPCs) mediate communication between the nucleus and the cytoplasm, and regulate gene expression by interacting with transcription and mRNA export factors. Lysine acetyltransferases (KATs) promote transcription through acetylation of chromatin‐associated proteins. We find that...

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Autores principales: Gomar‐Alba, Mercè, Pozharskaia, Vasilisa, Cichocki, Bogdan, Schaal, Celia, Kumar, Arun, Jacquel, Basile, Charvin, Gilles, Igual, J Carlos, Mendoza, Manuel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9340480/
https://www.ncbi.nlm.nih.gov/pubmed/35735140
http://dx.doi.org/10.15252/embj.2021110271
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author Gomar‐Alba, Mercè
Pozharskaia, Vasilisa
Cichocki, Bogdan
Schaal, Celia
Kumar, Arun
Jacquel, Basile
Charvin, Gilles
Igual, J Carlos
Mendoza, Manuel
author_facet Gomar‐Alba, Mercè
Pozharskaia, Vasilisa
Cichocki, Bogdan
Schaal, Celia
Kumar, Arun
Jacquel, Basile
Charvin, Gilles
Igual, J Carlos
Mendoza, Manuel
author_sort Gomar‐Alba, Mercè
collection PubMed
description Nuclear pore complexes (NPCs) mediate communication between the nucleus and the cytoplasm, and regulate gene expression by interacting with transcription and mRNA export factors. Lysine acetyltransferases (KATs) promote transcription through acetylation of chromatin‐associated proteins. We find that Esa1, the KAT subunit of the yeast NuA4 complex, also acetylates the nuclear pore basket component Nup60 to promote mRNA export. Acetylation of Nup60 recruits the mRNA export factor Sac3, the scaffolding subunit of the Transcription and Export 2 (TREX‐2) complex, to the nuclear basket. The Esa1‐mediated nuclear export of mRNAs in turn promotes entry into S phase, which is inhibited by the Hos3 deacetylase in G1 daughter cells to restrain their premature commitment to a new cell division cycle. This mechanism is not only limited to G1/S‐expressed genes but also inhibits the expression of the nutrient‐regulated GAL1 gene specifically in daughter cells. Overall, these results reveal how acetylation can contribute to the functional plasticity of NPCs in mother and daughter yeast cells. In addition, our work demonstrates dual gene expression regulation by the evolutionarily conserved NuA4 complex, at the level of transcription and at the stage of mRNA export by modifying the nucleoplasmic entrance to nuclear pores.
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spelling pubmed-93404802022-08-09 Nuclear pore complex acetylation regulates mRNA export and cell cycle commitment in budding yeast Gomar‐Alba, Mercè Pozharskaia, Vasilisa Cichocki, Bogdan Schaal, Celia Kumar, Arun Jacquel, Basile Charvin, Gilles Igual, J Carlos Mendoza, Manuel EMBO J Articles Nuclear pore complexes (NPCs) mediate communication between the nucleus and the cytoplasm, and regulate gene expression by interacting with transcription and mRNA export factors. Lysine acetyltransferases (KATs) promote transcription through acetylation of chromatin‐associated proteins. We find that Esa1, the KAT subunit of the yeast NuA4 complex, also acetylates the nuclear pore basket component Nup60 to promote mRNA export. Acetylation of Nup60 recruits the mRNA export factor Sac3, the scaffolding subunit of the Transcription and Export 2 (TREX‐2) complex, to the nuclear basket. The Esa1‐mediated nuclear export of mRNAs in turn promotes entry into S phase, which is inhibited by the Hos3 deacetylase in G1 daughter cells to restrain their premature commitment to a new cell division cycle. This mechanism is not only limited to G1/S‐expressed genes but also inhibits the expression of the nutrient‐regulated GAL1 gene specifically in daughter cells. Overall, these results reveal how acetylation can contribute to the functional plasticity of NPCs in mother and daughter yeast cells. In addition, our work demonstrates dual gene expression regulation by the evolutionarily conserved NuA4 complex, at the level of transcription and at the stage of mRNA export by modifying the nucleoplasmic entrance to nuclear pores. John Wiley and Sons Inc. 2022-06-23 /pmc/articles/PMC9340480/ /pubmed/35735140 http://dx.doi.org/10.15252/embj.2021110271 Text en © 2022 The Authors Open access.
spellingShingle Articles
Gomar‐Alba, Mercè
Pozharskaia, Vasilisa
Cichocki, Bogdan
Schaal, Celia
Kumar, Arun
Jacquel, Basile
Charvin, Gilles
Igual, J Carlos
Mendoza, Manuel
Nuclear pore complex acetylation regulates mRNA export and cell cycle commitment in budding yeast
title Nuclear pore complex acetylation regulates mRNA export and cell cycle commitment in budding yeast
title_full Nuclear pore complex acetylation regulates mRNA export and cell cycle commitment in budding yeast
title_fullStr Nuclear pore complex acetylation regulates mRNA export and cell cycle commitment in budding yeast
title_full_unstemmed Nuclear pore complex acetylation regulates mRNA export and cell cycle commitment in budding yeast
title_short Nuclear pore complex acetylation regulates mRNA export and cell cycle commitment in budding yeast
title_sort nuclear pore complex acetylation regulates mrna export and cell cycle commitment in budding yeast
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9340480/
https://www.ncbi.nlm.nih.gov/pubmed/35735140
http://dx.doi.org/10.15252/embj.2021110271
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