eIF2A represses cell wall biogenesis gene expression in Saccharomyces cerevisiae.

Translation initiation is a complex and highly regulated process that represents an important mechanism, controlling gene expression. eIF2A was proposed as an alternative initiation factor, however, its role and biological targets remain to be discovered. To further gain insight into the function of...

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Main Authors: Laura Meyer, Baptiste Courtin, Maïté Gomard, Abdelkader Namane, Emmanuelle Permal, Gwenael Badis, Alain Jacquier, Micheline Fromont-Racine
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0293228&type=printable
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author Laura Meyer
Baptiste Courtin
Maïté Gomard
Abdelkader Namane
Emmanuelle Permal
Gwenael Badis
Alain Jacquier
Micheline Fromont-Racine
author_facet Laura Meyer
Baptiste Courtin
Maïté Gomard
Abdelkader Namane
Emmanuelle Permal
Gwenael Badis
Alain Jacquier
Micheline Fromont-Racine
author_sort Laura Meyer
collection DOAJ
description Translation initiation is a complex and highly regulated process that represents an important mechanism, controlling gene expression. eIF2A was proposed as an alternative initiation factor, however, its role and biological targets remain to be discovered. To further gain insight into the function of eIF2A in Saccharomyces cerevisiae, we identified mRNAs associated with the eIF2A complex and showed that 24% of the most enriched mRNAs encode proteins related to cell wall biogenesis and maintenance. In agreement with this result, we showed that an eIF2A deletion sensitized cells to cell wall damage induced by calcofluor white. eIF2A overexpression led to a growth defect, correlated with decreased synthesis of several cell wall proteins. In contrast, no changes were observed in the transcriptome, suggesting that eIF2A controls the expression of cell wall-related proteins at a translational level. The biochemical characterization of the eIF2A complex revealed that it strongly interacts with the RNA binding protein, Ssd1, which is a negative translational regulator, controlling the expression of cell wall-related genes. Interestingly, eIF2A and Ssd1 bind several common mRNA targets and we found that the binding of eIF2A to some targets was mediated by Ssd1. Surprisingly, we further showed that eIF2A is physically and functionally associated with the exonuclease Xrn1 and other mRNA degradation factors, suggesting an additional level of regulation. Altogether, our results highlight new aspects of this complex and redundant fine-tuned regulation of proteins expression related to the cell wall, a structure required to maintain cell shape and rigidity, providing protection against harmful environmental stress.
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spelling doaj.art-d6ae11a88d104476b0f3b374692de1dc2023-12-12T05:33:28ZengPublic Library of Science (PLoS)PLoS ONE1932-62032023-01-011811e029322810.1371/journal.pone.0293228eIF2A represses cell wall biogenesis gene expression in Saccharomyces cerevisiae.Laura MeyerBaptiste CourtinMaïté GomardAbdelkader NamaneEmmanuelle PermalGwenael BadisAlain JacquierMicheline Fromont-RacineTranslation initiation is a complex and highly regulated process that represents an important mechanism, controlling gene expression. eIF2A was proposed as an alternative initiation factor, however, its role and biological targets remain to be discovered. To further gain insight into the function of eIF2A in Saccharomyces cerevisiae, we identified mRNAs associated with the eIF2A complex and showed that 24% of the most enriched mRNAs encode proteins related to cell wall biogenesis and maintenance. In agreement with this result, we showed that an eIF2A deletion sensitized cells to cell wall damage induced by calcofluor white. eIF2A overexpression led to a growth defect, correlated with decreased synthesis of several cell wall proteins. In contrast, no changes were observed in the transcriptome, suggesting that eIF2A controls the expression of cell wall-related proteins at a translational level. The biochemical characterization of the eIF2A complex revealed that it strongly interacts with the RNA binding protein, Ssd1, which is a negative translational regulator, controlling the expression of cell wall-related genes. Interestingly, eIF2A and Ssd1 bind several common mRNA targets and we found that the binding of eIF2A to some targets was mediated by Ssd1. Surprisingly, we further showed that eIF2A is physically and functionally associated with the exonuclease Xrn1 and other mRNA degradation factors, suggesting an additional level of regulation. Altogether, our results highlight new aspects of this complex and redundant fine-tuned regulation of proteins expression related to the cell wall, a structure required to maintain cell shape and rigidity, providing protection against harmful environmental stress.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0293228&type=printable
spellingShingle Laura Meyer
Baptiste Courtin
Maïté Gomard
Abdelkader Namane
Emmanuelle Permal
Gwenael Badis
Alain Jacquier
Micheline Fromont-Racine
eIF2A represses cell wall biogenesis gene expression in Saccharomyces cerevisiae.
PLoS ONE
title eIF2A represses cell wall biogenesis gene expression in Saccharomyces cerevisiae.
title_full eIF2A represses cell wall biogenesis gene expression in Saccharomyces cerevisiae.
title_fullStr eIF2A represses cell wall biogenesis gene expression in Saccharomyces cerevisiae.
title_full_unstemmed eIF2A represses cell wall biogenesis gene expression in Saccharomyces cerevisiae.
title_short eIF2A represses cell wall biogenesis gene expression in Saccharomyces cerevisiae.
title_sort eif2a represses cell wall biogenesis gene expression in saccharomyces cerevisiae
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0293228&type=printable
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