Phosphorylation of the transcription factor Atf1 at multiple sites by the MAP kinase Sty1 controls homologous recombination and transcription

Transcription factors are often the downstream effectors of signaling cascades. In fission yeast, the transcription factor Atf1 is phosphorylated by the MAP kinase Sty1 under several environmental stressors to promote transcription initiation of stress genes. However, Sty1 and Atf1 have also been in...

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Autores: Sánchez Mir, Laura, Fraile Beneitez, Rodrigo, Ayté del Olmo, José, Hidalgo Hernando, Elena
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
Fecha de publicación:2020
País:España
Institución:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10230/45910
Acceso en línea:http://hdl.handle.net/10230/45910
http://dx.doi.org/10.1016/j.jmb.2020.08.004
Access Level:acceso abierto
Palabra clave:Atf1
Schizosaccharomyces pombe
Sty1
Homologous recombination
Transcription regulation
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spelling Phosphorylation of the transcription factor Atf1 at multiple sites by the MAP kinase Sty1 controls homologous recombination and transcriptionSánchez Mir, LauraFraile Beneitez, RodrigoAyté del Olmo, JoséHidalgo Hernando, ElenaAtf1Schizosaccharomyces pombeSty1Homologous recombinationTranscription regulationTranscription factors are often the downstream effectors of signaling cascades. In fission yeast, the transcription factor Atf1 is phosphorylated by the MAP kinase Sty1 under several environmental stressors to promote transcription initiation of stress genes. However, Sty1 and Atf1 have also been involved in other cellular processes such as homologous recombination at hotspots, ste11 gene expression during mating and meiosis, or regulation of fbp1 gene transcription under glucose starvation conditions. Using different phospho-mutants of Atf1, we have investigated the role of Atf1 phosphorylation by Sty1 in those biological processes. An Atf1 mutant lacking the canonical MAP kinase phosphorylation sites cannot activate fbp1 transcription when glucose is depleted, but it is still able to induce recombination at ade6.M26 and to induce ste11 after nitrogen depletion; in these last cases, Sty1 is still required, suggesting that additional non-canonical sites are activating the transcription factor. In all cases, an Atf1 phosphomimetic mutant bypasses the requirement of the Sty1 kinase in these diverse biological processes, highlighting the essential role of the DNA binding factor Atf1 on chromatin remodeling and cell adaptation to nutritional changes. We propose that post-translational modifications of Atf1 by Sty1, either at canonical or non-canonical sites, are sufficient to activate some of the functions of Atf1, those involving chromatin remodeling and transcription initiation. However, in the case of fbp1 where Atf1 acts synergistically with other transcription factors, elimination of the canonical sites is sufficient to hamper some of the interactions required in this complex scenario and to impair transcription initiation.We are thankful to Dr. Masayuki Yamamoto for providing strain JX233. This work is supported by the Ministerio de Ciencia, Innovación y Universidades (Spain), PLAN E and FEDER (PGC2018-093920-B-I00 to E.H.). The Oxidative Stress and Cell Cycle group is also supported by Generalitat de Catalunya (Spain) (2017-SGR-539) and by Unidad de Excelencia María de Maeztu from the Ministerio de Ciencia, Innovación y Universidades (CEX2018-000792-M) (Spain).Elsevier20202020info:eu-repo/semantics/articleinfo:eu-repo/semantics/acceptedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/45910http://dx.doi.org/10.1016/j.jmb.2020.08.004reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésJ Mol Biol. 2020; 432(19):5430-46info:eu-repo/grantAgreement/ES/2PE/PGC2018-093920-B-I00© Elsevier http://dx.doi.org/10.1016/j.jmb.2020.08.004info:eu-repo/semantics/openAccessoai:recercat.cat:10230/459102026-05-29T05:05:01Z
dc.title.none.fl_str_mv Phosphorylation of the transcription factor Atf1 at multiple sites by the MAP kinase Sty1 controls homologous recombination and transcription
title Phosphorylation of the transcription factor Atf1 at multiple sites by the MAP kinase Sty1 controls homologous recombination and transcription
spellingShingle Phosphorylation of the transcription factor Atf1 at multiple sites by the MAP kinase Sty1 controls homologous recombination and transcription
Sánchez Mir, Laura
Atf1
Schizosaccharomyces pombe
Sty1
Homologous recombination
Transcription regulation
title_short Phosphorylation of the transcription factor Atf1 at multiple sites by the MAP kinase Sty1 controls homologous recombination and transcription
title_full Phosphorylation of the transcription factor Atf1 at multiple sites by the MAP kinase Sty1 controls homologous recombination and transcription
title_fullStr Phosphorylation of the transcription factor Atf1 at multiple sites by the MAP kinase Sty1 controls homologous recombination and transcription
title_full_unstemmed Phosphorylation of the transcription factor Atf1 at multiple sites by the MAP kinase Sty1 controls homologous recombination and transcription
title_sort Phosphorylation of the transcription factor Atf1 at multiple sites by the MAP kinase Sty1 controls homologous recombination and transcription
dc.creator.none.fl_str_mv Sánchez Mir, Laura
Fraile Beneitez, Rodrigo
Ayté del Olmo, José
Hidalgo Hernando, Elena
author Sánchez Mir, Laura
author_facet Sánchez Mir, Laura
Fraile Beneitez, Rodrigo
Ayté del Olmo, José
Hidalgo Hernando, Elena
author_role author
author2 Fraile Beneitez, Rodrigo
Ayté del Olmo, José
Hidalgo Hernando, Elena
author2_role author
author
author
dc.subject.none.fl_str_mv Atf1
Schizosaccharomyces pombe
Sty1
Homologous recombination
Transcription regulation
topic Atf1
Schizosaccharomyces pombe
Sty1
Homologous recombination
Transcription regulation
description Transcription factors are often the downstream effectors of signaling cascades. In fission yeast, the transcription factor Atf1 is phosphorylated by the MAP kinase Sty1 under several environmental stressors to promote transcription initiation of stress genes. However, Sty1 and Atf1 have also been involved in other cellular processes such as homologous recombination at hotspots, ste11 gene expression during mating and meiosis, or regulation of fbp1 gene transcription under glucose starvation conditions. Using different phospho-mutants of Atf1, we have investigated the role of Atf1 phosphorylation by Sty1 in those biological processes. An Atf1 mutant lacking the canonical MAP kinase phosphorylation sites cannot activate fbp1 transcription when glucose is depleted, but it is still able to induce recombination at ade6.M26 and to induce ste11 after nitrogen depletion; in these last cases, Sty1 is still required, suggesting that additional non-canonical sites are activating the transcription factor. In all cases, an Atf1 phosphomimetic mutant bypasses the requirement of the Sty1 kinase in these diverse biological processes, highlighting the essential role of the DNA binding factor Atf1 on chromatin remodeling and cell adaptation to nutritional changes. We propose that post-translational modifications of Atf1 by Sty1, either at canonical or non-canonical sites, are sufficient to activate some of the functions of Atf1, those involving chromatin remodeling and transcription initiation. However, in the case of fbp1 where Atf1 acts synergistically with other transcription factors, elimination of the canonical sites is sufficient to hamper some of the interactions required in this complex scenario and to impair transcription initiation.
publishDate 2020
dc.date.none.fl_str_mv 2020
2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/acceptedVersion
format article
status_str acceptedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/45910
http://dx.doi.org/10.1016/j.jmb.2020.08.004
url http://hdl.handle.net/10230/45910
http://dx.doi.org/10.1016/j.jmb.2020.08.004
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv J Mol Biol. 2020; 432(19):5430-46
info:eu-repo/grantAgreement/ES/2PE/PGC2018-093920-B-I00
dc.rights.none.fl_str_mv © Elsevier http://dx.doi.org/10.1016/j.jmb.2020.08.004
info:eu-repo/semantics/openAccess
rights_invalid_str_mv © Elsevier http://dx.doi.org/10.1016/j.jmb.2020.08.004
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
repository.mail.fl_str_mv
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