Cargando…

Yeast mRNA cap-binding protein Cbc1/Sto1 is necessary for the rapid reprogramming of translation after hyperosmotic shock

In response to osmotic stress, global translation is inhibited, but the mRNAs encoding stress-protective proteins are selectively translated to allow cell survival. To date, the mechanisms and factors involved in the specific translation of osmostress-responsive genes in Saccharomyces cerevisiae are...

Descripción completa

Detalles Bibliográficos
Autores principales: Garre, Elena, Romero-Santacreu, Lorena, De Clercq, Nikki, Blasco-Angulo, Nati, Sunnerhagen, Per, Alepuz, Paula
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3248893/
https://www.ncbi.nlm.nih.gov/pubmed/22072789
http://dx.doi.org/10.1091/mbc.E11-05-0419
_version_ 1782220287664717824
author Garre, Elena
Romero-Santacreu, Lorena
De Clercq, Nikki
Blasco-Angulo, Nati
Sunnerhagen, Per
Alepuz, Paula
author_facet Garre, Elena
Romero-Santacreu, Lorena
De Clercq, Nikki
Blasco-Angulo, Nati
Sunnerhagen, Per
Alepuz, Paula
author_sort Garre, Elena
collection PubMed
description In response to osmotic stress, global translation is inhibited, but the mRNAs encoding stress-protective proteins are selectively translated to allow cell survival. To date, the mechanisms and factors involved in the specific translation of osmostress-responsive genes in Saccharomyces cerevisiae are unknown. We find that the mRNA cap-binding protein Cbc1 is important for yeast survival under osmotic stress. Our results provide new evidence supporting a role of Cbc1 in translation initiation. Cbc1 associates with polysomes, while the deletion of the CBC1 gene causes hypersensitivity to the translation inhibitor cycloheximide and yields synthetic “sickness” in cells with limiting amounts of translation initiator factor eIF4E. In cbc1Δ mutants, translation drops sharply under osmotic stress, the subsequent reinitiation of translation is retarded, and “processing bodies” containing untranslating mRNAs remain for long periods. Furthermore, osmostress-responsive mRNAs are transcriptionally induced after osmotic stress in cbc1Δ cells, but their rapid association with polysomes is delayed. However, in cells containing a thermosensitive eIF4E allele, their inability to grow at 37ºC is suppressed by hyperosmosis, and Cbc1 relocalizes from nucleus to cytoplasm. These data support a model in which eIF4E-translation could be stress-sensitive, while Cbc1-mediated translation is necessary for the rapid translation of osmostress-protective proteins under osmotic stress.
format Online
Article
Text
id pubmed-3248893
institution National Center for Biotechnology Information
language English
publishDate 2012
publisher The American Society for Cell Biology
record_format MEDLINE/PubMed
spelling pubmed-32488932012-03-16 Yeast mRNA cap-binding protein Cbc1/Sto1 is necessary for the rapid reprogramming of translation after hyperosmotic shock Garre, Elena Romero-Santacreu, Lorena De Clercq, Nikki Blasco-Angulo, Nati Sunnerhagen, Per Alepuz, Paula Mol Biol Cell Articles In response to osmotic stress, global translation is inhibited, but the mRNAs encoding stress-protective proteins are selectively translated to allow cell survival. To date, the mechanisms and factors involved in the specific translation of osmostress-responsive genes in Saccharomyces cerevisiae are unknown. We find that the mRNA cap-binding protein Cbc1 is important for yeast survival under osmotic stress. Our results provide new evidence supporting a role of Cbc1 in translation initiation. Cbc1 associates with polysomes, while the deletion of the CBC1 gene causes hypersensitivity to the translation inhibitor cycloheximide and yields synthetic “sickness” in cells with limiting amounts of translation initiator factor eIF4E. In cbc1Δ mutants, translation drops sharply under osmotic stress, the subsequent reinitiation of translation is retarded, and “processing bodies” containing untranslating mRNAs remain for long periods. Furthermore, osmostress-responsive mRNAs are transcriptionally induced after osmotic stress in cbc1Δ cells, but their rapid association with polysomes is delayed. However, in cells containing a thermosensitive eIF4E allele, their inability to grow at 37ºC is suppressed by hyperosmosis, and Cbc1 relocalizes from nucleus to cytoplasm. These data support a model in which eIF4E-translation could be stress-sensitive, while Cbc1-mediated translation is necessary for the rapid translation of osmostress-protective proteins under osmotic stress. The American Society for Cell Biology 2012-01-01 /pmc/articles/PMC3248893/ /pubmed/22072789 http://dx.doi.org/10.1091/mbc.E11-05-0419 Text en © 2012 Garre et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society of Cell Biology.
spellingShingle Articles
Garre, Elena
Romero-Santacreu, Lorena
De Clercq, Nikki
Blasco-Angulo, Nati
Sunnerhagen, Per
Alepuz, Paula
Yeast mRNA cap-binding protein Cbc1/Sto1 is necessary for the rapid reprogramming of translation after hyperosmotic shock
title Yeast mRNA cap-binding protein Cbc1/Sto1 is necessary for the rapid reprogramming of translation after hyperosmotic shock
title_full Yeast mRNA cap-binding protein Cbc1/Sto1 is necessary for the rapid reprogramming of translation after hyperosmotic shock
title_fullStr Yeast mRNA cap-binding protein Cbc1/Sto1 is necessary for the rapid reprogramming of translation after hyperosmotic shock
title_full_unstemmed Yeast mRNA cap-binding protein Cbc1/Sto1 is necessary for the rapid reprogramming of translation after hyperosmotic shock
title_short Yeast mRNA cap-binding protein Cbc1/Sto1 is necessary for the rapid reprogramming of translation after hyperosmotic shock
title_sort yeast mrna cap-binding protein cbc1/sto1 is necessary for the rapid reprogramming of translation after hyperosmotic shock
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3248893/
https://www.ncbi.nlm.nih.gov/pubmed/22072789
http://dx.doi.org/10.1091/mbc.E11-05-0419
work_keys_str_mv AT garreelena yeastmrnacapbindingproteincbc1sto1isnecessaryfortherapidreprogrammingoftranslationafterhyperosmoticshock
AT romerosantacreulorena yeastmrnacapbindingproteincbc1sto1isnecessaryfortherapidreprogrammingoftranslationafterhyperosmoticshock
AT declercqnikki yeastmrnacapbindingproteincbc1sto1isnecessaryfortherapidreprogrammingoftranslationafterhyperosmoticshock
AT blascoangulonati yeastmrnacapbindingproteincbc1sto1isnecessaryfortherapidreprogrammingoftranslationafterhyperosmoticshock
AT sunnerhagenper yeastmrnacapbindingproteincbc1sto1isnecessaryfortherapidreprogrammingoftranslationafterhyperosmoticshock
AT alepuzpaula yeastmrnacapbindingproteincbc1sto1isnecessaryfortherapidreprogrammingoftranslationafterhyperosmoticshock