LncRNAs of Saccharomyces cerevisiae bypass the cell cycle arrest imposed by ethanol stress

Detalhes bibliográficos
Autor(a) principal: Lázari, Lucas Cardoso [UNESP]
Data de Publicação: 2022
Outros Autores: Wolf, Ivan Rodrigo [UNESP], Schnepper, Amanda Piveta [UNESP], Valente, Guilherme Targino [UNESP]
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1371/journal.pcbi.1010081
http://hdl.handle.net/11449/240146
Resumo: Ethanol alters many subsystems of Saccharomyces cerevisiae, including the cell cycle. Two ethanol-responsive lncRNAs in yeast interact with cell cycle proteins, and here, we investigated the role of these RNAs in cell cycle. Our network dynamic modeling showed that higher and lower ethanol-tolerant strains undergo cell cycle arrest in mitosis and G1 phases, respectively, during ethanol stress. The higher population rebound of the lower ethanol-tolerant phenotype after stress relief responds to the late phase arrest. We found that the lncRNA lnc9136 of SEY6210 (a lower ethanol-tolerant strain) induces cells to skip mitosis arrest. Simulating an overexpression of lnc9136 and analyzing CRISPR–Cas9 mutants lacking this lncRNA suggest that lnc9136 induces a regular cell cycle even under ethanol stress, indirectly regulating Swe1p and Clb1/2 by binding to Gin4p and Hsl1p. Notably, lnc10883 of BY4742 (a higher ethanol-tolerant strain) does not prevent G1 arrest in this strain under ethanol stress. However, lnc19883 circumvents DNA and spindle damage checkpoints, maintaining a functional cell cycle by interacting with Mec1p or Bub1p even in the presence of DNA/spindle damage. Overall, we present the first evidence of direct roles for lncRNAs in regulating yeast cell cycle proteins, the dynamics of this system in different ethanol-tolerant phenotypes, and a new yeast cell cycle model.
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spelling LncRNAs of Saccharomyces cerevisiae bypass the cell cycle arrest imposed by ethanol stressEthanol alters many subsystems of Saccharomyces cerevisiae, including the cell cycle. Two ethanol-responsive lncRNAs in yeast interact with cell cycle proteins, and here, we investigated the role of these RNAs in cell cycle. Our network dynamic modeling showed that higher and lower ethanol-tolerant strains undergo cell cycle arrest in mitosis and G1 phases, respectively, during ethanol stress. The higher population rebound of the lower ethanol-tolerant phenotype after stress relief responds to the late phase arrest. We found that the lncRNA lnc9136 of SEY6210 (a lower ethanol-tolerant strain) induces cells to skip mitosis arrest. Simulating an overexpression of lnc9136 and analyzing CRISPR–Cas9 mutants lacking this lncRNA suggest that lnc9136 induces a regular cell cycle even under ethanol stress, indirectly regulating Swe1p and Clb1/2 by binding to Gin4p and Hsl1p. Notably, lnc10883 of BY4742 (a higher ethanol-tolerant strain) does not prevent G1 arrest in this strain under ethanol stress. However, lnc19883 circumvents DNA and spindle damage checkpoints, maintaining a functional cell cycle by interacting with Mec1p or Bub1p even in the presence of DNA/spindle damage. Overall, we present the first evidence of direct roles for lncRNAs in regulating yeast cell cycle proteins, the dynamics of this system in different ethanol-tolerant phenotypes, and a new yeast cell cycle model.Department of Parasitology Institute of Biomedical Sciences Sāo Paulo University (USP)Department of Bioprocess and Biotechnology School of Agriculture Sao Paulo State University (UNESP)Department of Structural and Functional Biology Institute of Bioscience at Botucatu Sao Paulo State University (UNESP)Max Planck Institute for Heart and Lung ResearchDepartment of Bioprocess and Biotechnology School of Agriculture Sao Paulo State University (UNESP)Department of Structural and Functional Biology Institute of Bioscience at Botucatu Sao Paulo State University (UNESP)Universidade de São Paulo (USP)Universidade Estadual Paulista (UNESP)Max Planck Institute for Heart and Lung ResearchLázari, Lucas Cardoso [UNESP]Wolf, Ivan Rodrigo [UNESP]Schnepper, Amanda Piveta [UNESP]Valente, Guilherme Targino [UNESP]2023-03-01T20:03:26Z2023-03-01T20:03:26Z2022-05-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1371/journal.pcbi.1010081PLoS Computational Biology, v. 18, n. 5, 2022.1553-73581553-734Xhttp://hdl.handle.net/11449/24014610.1371/journal.pcbi.10100812-s2.0-85130851838Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengPLoS Computational Biologyinfo:eu-repo/semantics/openAccess2023-03-01T20:03:26Zoai:repositorio.unesp.br:11449/240146Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T17:01:41.605405Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv LncRNAs of Saccharomyces cerevisiae bypass the cell cycle arrest imposed by ethanol stress
title LncRNAs of Saccharomyces cerevisiae bypass the cell cycle arrest imposed by ethanol stress
spellingShingle LncRNAs of Saccharomyces cerevisiae bypass the cell cycle arrest imposed by ethanol stress
Lázari, Lucas Cardoso [UNESP]
title_short LncRNAs of Saccharomyces cerevisiae bypass the cell cycle arrest imposed by ethanol stress
title_full LncRNAs of Saccharomyces cerevisiae bypass the cell cycle arrest imposed by ethanol stress
title_fullStr LncRNAs of Saccharomyces cerevisiae bypass the cell cycle arrest imposed by ethanol stress
title_full_unstemmed LncRNAs of Saccharomyces cerevisiae bypass the cell cycle arrest imposed by ethanol stress
title_sort LncRNAs of Saccharomyces cerevisiae bypass the cell cycle arrest imposed by ethanol stress
author Lázari, Lucas Cardoso [UNESP]
author_facet Lázari, Lucas Cardoso [UNESP]
Wolf, Ivan Rodrigo [UNESP]
Schnepper, Amanda Piveta [UNESP]
Valente, Guilherme Targino [UNESP]
author_role author
author2 Wolf, Ivan Rodrigo [UNESP]
Schnepper, Amanda Piveta [UNESP]
Valente, Guilherme Targino [UNESP]
author2_role author
author
author
dc.contributor.none.fl_str_mv Universidade de São Paulo (USP)
Universidade Estadual Paulista (UNESP)
Max Planck Institute for Heart and Lung Research
dc.contributor.author.fl_str_mv Lázari, Lucas Cardoso [UNESP]
Wolf, Ivan Rodrigo [UNESP]
Schnepper, Amanda Piveta [UNESP]
Valente, Guilherme Targino [UNESP]
description Ethanol alters many subsystems of Saccharomyces cerevisiae, including the cell cycle. Two ethanol-responsive lncRNAs in yeast interact with cell cycle proteins, and here, we investigated the role of these RNAs in cell cycle. Our network dynamic modeling showed that higher and lower ethanol-tolerant strains undergo cell cycle arrest in mitosis and G1 phases, respectively, during ethanol stress. The higher population rebound of the lower ethanol-tolerant phenotype after stress relief responds to the late phase arrest. We found that the lncRNA lnc9136 of SEY6210 (a lower ethanol-tolerant strain) induces cells to skip mitosis arrest. Simulating an overexpression of lnc9136 and analyzing CRISPR–Cas9 mutants lacking this lncRNA suggest that lnc9136 induces a regular cell cycle even under ethanol stress, indirectly regulating Swe1p and Clb1/2 by binding to Gin4p and Hsl1p. Notably, lnc10883 of BY4742 (a higher ethanol-tolerant strain) does not prevent G1 arrest in this strain under ethanol stress. However, lnc19883 circumvents DNA and spindle damage checkpoints, maintaining a functional cell cycle by interacting with Mec1p or Bub1p even in the presence of DNA/spindle damage. Overall, we present the first evidence of direct roles for lncRNAs in regulating yeast cell cycle proteins, the dynamics of this system in different ethanol-tolerant phenotypes, and a new yeast cell cycle model.
publishDate 2022
dc.date.none.fl_str_mv 2022-05-01
2023-03-01T20:03:26Z
2023-03-01T20:03:26Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1371/journal.pcbi.1010081
PLoS Computational Biology, v. 18, n. 5, 2022.
1553-7358
1553-734X
http://hdl.handle.net/11449/240146
10.1371/journal.pcbi.1010081
2-s2.0-85130851838
url http://dx.doi.org/10.1371/journal.pcbi.1010081
http://hdl.handle.net/11449/240146
identifier_str_mv PLoS Computational Biology, v. 18, n. 5, 2022.
1553-7358
1553-734X
10.1371/journal.pcbi.1010081
2-s2.0-85130851838
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv PLoS Computational Biology
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.source.none.fl_str_mv Scopus
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
repository.mail.fl_str_mv
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