Different Regulations of <italic toggle="yes">ROM2</italic> and <italic toggle="yes">LRG1</italic> Expression by Ccr4, Pop2, and Dhh1 in the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Cell Wall Integrity Pathway

ABSTRACT Ccr4, a component of the Ccr4-Not cytoplasmic deadenylase complex, is known to be required for the cell wall integrity (CWI) pathway in the budding yeast Saccharomyces cerevisiae. However, it is not fully understood how Ccr4 and other components of the Ccr4-Not complex regulate the CWI path...

Full description

Bibliographic Details
Main Authors: Xia Li, Tetsuro Ohmori, Kaoru Irie, Yuichi Kimura, Yasuyuki Suda, Tomoaki Mizuno, Kenji Irie
Format: Article
Language:English
Published: American Society for Microbiology 2016-10-01
Series:mSphere
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mSphere.00250-16
_version_ 1818986945140752384
author Xia Li
Tetsuro Ohmori
Kaoru Irie
Yuichi Kimura
Yasuyuki Suda
Tomoaki Mizuno
Kenji Irie
author_facet Xia Li
Tetsuro Ohmori
Kaoru Irie
Yuichi Kimura
Yasuyuki Suda
Tomoaki Mizuno
Kenji Irie
author_sort Xia Li
collection DOAJ
description ABSTRACT Ccr4, a component of the Ccr4-Not cytoplasmic deadenylase complex, is known to be required for the cell wall integrity (CWI) pathway in the budding yeast Saccharomyces cerevisiae. However, it is not fully understood how Ccr4 and other components of the Ccr4-Not complex regulate the CWI pathway. Previously, we showed that Ccr4 functions in the CWI pathway together with Khd1 RNA binding protein. Ccr4 and Khd1 modulate a signal from Rho1 small GTPase in the CWI pathway by regulating the expression of ROM2 mRNA and LRG1 mRNA, encoding a guanine nucleotide exchange factor (GEF) and a GTPase-activating protein (GAP) for Rho1, respectively. Here we examined the possible involvement of the POP2 gene encoding a subunit of the Ccr4-Not complex and the DHH1 gene encoding a DEAD box RNA helicase that associates with the Ccr4-Not complex in the regulation of ROM2 and LRG1 expression. Neither ROM2 mRNA level nor Rom2 function was impaired by pop2Δ or dhh1Δ mutation. The LRG1 mRNA level was increased in pop2Δ and dhh1Δ mutants, as well as the ccr4Δ mutant, and the growth defects caused by pop2Δ and dhh1Δ mutations were suppressed by lrg1Δ mutation. Our results suggest that LRG1 expression is regulated by Ccr4 together with Pop2 and Dhh1 and that ROM2 expression is regulated by Khd1 and Ccr4, but not by Pop2 and Dhh1. Thus, Rho1 activity in the CWI pathway is precisely controlled by modulation of the mRNA levels for Rho1-GEF Rom2 and Rho1-GAP Lrg1. IMPORTANCE We find here that Ccr4, Pop2, and Dhh1 modulate the levels of mRNAs for specific Rho1 regulators, Rom2 and Lrg1. In budding yeast, Rho1 activity is tightly regulated both temporally and spatially. It is anticipated that Ccr4, Pop2, and Dhh1 may contribute to the precise spatiotemporal control of Rho1 activity by regulating expression of its regulators temporally and spatially. Our finding on the roles of the components of the Ccr4-Not complex in yeast would give important information for understanding the roles of the evolutionary conserved Ccr4-Not complex.
first_indexed 2024-12-20T18:58:51Z
format Article
id doaj.art-33512341f1af40b4b8c7c5cc10f1f547
institution Directory Open Access Journal
issn 2379-5042
language English
last_indexed 2024-12-20T18:58:51Z
publishDate 2016-10-01
publisher American Society for Microbiology
record_format Article
series mSphere
spelling doaj.art-33512341f1af40b4b8c7c5cc10f1f5472022-12-21T19:29:26ZengAmerican Society for MicrobiologymSphere2379-50422016-10-011510.1128/mSphere.00250-16Different Regulations of <italic toggle="yes">ROM2</italic> and <italic toggle="yes">LRG1</italic> Expression by Ccr4, Pop2, and Dhh1 in the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Cell Wall Integrity PathwayXia Li0Tetsuro Ohmori1Kaoru Irie2Yuichi Kimura3Yasuyuki Suda4Tomoaki Mizuno5Kenji Irie6Department of Molecular Cell Biology, Graduate School of Comprehensive Human Sciences and Faculty of Medicine, University of Tsukuba, Tsukuba, JapanDepartment of Molecular Cell Biology, Graduate School of Comprehensive Human Sciences and Faculty of Medicine, University of Tsukuba, Tsukuba, JapanDepartment of Molecular Cell Biology, Graduate School of Comprehensive Human Sciences and Faculty of Medicine, University of Tsukuba, Tsukuba, JapanDepartment of Molecular Cell Biology, Graduate School of Comprehensive Human Sciences and Faculty of Medicine, University of Tsukuba, Tsukuba, JapanDepartment of Molecular Cell Biology, Graduate School of Comprehensive Human Sciences and Faculty of Medicine, University of Tsukuba, Tsukuba, JapanDepartment of Molecular Cell Biology, Graduate School of Comprehensive Human Sciences and Faculty of Medicine, University of Tsukuba, Tsukuba, JapanDepartment of Molecular Cell Biology, Graduate School of Comprehensive Human Sciences and Faculty of Medicine, University of Tsukuba, Tsukuba, JapanABSTRACT Ccr4, a component of the Ccr4-Not cytoplasmic deadenylase complex, is known to be required for the cell wall integrity (CWI) pathway in the budding yeast Saccharomyces cerevisiae. However, it is not fully understood how Ccr4 and other components of the Ccr4-Not complex regulate the CWI pathway. Previously, we showed that Ccr4 functions in the CWI pathway together with Khd1 RNA binding protein. Ccr4 and Khd1 modulate a signal from Rho1 small GTPase in the CWI pathway by regulating the expression of ROM2 mRNA and LRG1 mRNA, encoding a guanine nucleotide exchange factor (GEF) and a GTPase-activating protein (GAP) for Rho1, respectively. Here we examined the possible involvement of the POP2 gene encoding a subunit of the Ccr4-Not complex and the DHH1 gene encoding a DEAD box RNA helicase that associates with the Ccr4-Not complex in the regulation of ROM2 and LRG1 expression. Neither ROM2 mRNA level nor Rom2 function was impaired by pop2Δ or dhh1Δ mutation. The LRG1 mRNA level was increased in pop2Δ and dhh1Δ mutants, as well as the ccr4Δ mutant, and the growth defects caused by pop2Δ and dhh1Δ mutations were suppressed by lrg1Δ mutation. Our results suggest that LRG1 expression is regulated by Ccr4 together with Pop2 and Dhh1 and that ROM2 expression is regulated by Khd1 and Ccr4, but not by Pop2 and Dhh1. Thus, Rho1 activity in the CWI pathway is precisely controlled by modulation of the mRNA levels for Rho1-GEF Rom2 and Rho1-GAP Lrg1. IMPORTANCE We find here that Ccr4, Pop2, and Dhh1 modulate the levels of mRNAs for specific Rho1 regulators, Rom2 and Lrg1. In budding yeast, Rho1 activity is tightly regulated both temporally and spatially. It is anticipated that Ccr4, Pop2, and Dhh1 may contribute to the precise spatiotemporal control of Rho1 activity by regulating expression of its regulators temporally and spatially. Our finding on the roles of the components of the Ccr4-Not complex in yeast would give important information for understanding the roles of the evolutionary conserved Ccr4-Not complex.https://journals.asm.org/doi/10.1128/mSphere.00250-16Ccr4-Not complexRho1cell wallmRNA stabilityyeasts
spellingShingle Xia Li
Tetsuro Ohmori
Kaoru Irie
Yuichi Kimura
Yasuyuki Suda
Tomoaki Mizuno
Kenji Irie
Different Regulations of <italic toggle="yes">ROM2</italic> and <italic toggle="yes">LRG1</italic> Expression by Ccr4, Pop2, and Dhh1 in the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Cell Wall Integrity Pathway
mSphere
Ccr4-Not complex
Rho1
cell wall
mRNA stability
yeasts
title Different Regulations of <italic toggle="yes">ROM2</italic> and <italic toggle="yes">LRG1</italic> Expression by Ccr4, Pop2, and Dhh1 in the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Cell Wall Integrity Pathway
title_full Different Regulations of <italic toggle="yes">ROM2</italic> and <italic toggle="yes">LRG1</italic> Expression by Ccr4, Pop2, and Dhh1 in the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Cell Wall Integrity Pathway
title_fullStr Different Regulations of <italic toggle="yes">ROM2</italic> and <italic toggle="yes">LRG1</italic> Expression by Ccr4, Pop2, and Dhh1 in the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Cell Wall Integrity Pathway
title_full_unstemmed Different Regulations of <italic toggle="yes">ROM2</italic> and <italic toggle="yes">LRG1</italic> Expression by Ccr4, Pop2, and Dhh1 in the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Cell Wall Integrity Pathway
title_short Different Regulations of <italic toggle="yes">ROM2</italic> and <italic toggle="yes">LRG1</italic> Expression by Ccr4, Pop2, and Dhh1 in the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Cell Wall Integrity Pathway
title_sort different regulations of italic toggle yes rom2 italic and italic toggle yes lrg1 italic expression by ccr4 pop2 and dhh1 in the named content content type genus species saccharomyces cerevisiae named content cell wall integrity pathway
topic Ccr4-Not complex
Rho1
cell wall
mRNA stability
yeasts
url https://journals.asm.org/doi/10.1128/mSphere.00250-16
work_keys_str_mv AT xiali differentregulationsofitalictoggleyesrom2italicanditalictoggleyeslrg1italicexpressionbyccr4pop2anddhh1inthenamedcontentcontenttypegenusspeciessaccharomycescerevisiaenamedcontentcellwallintegritypathway
AT tetsuroohmori differentregulationsofitalictoggleyesrom2italicanditalictoggleyeslrg1italicexpressionbyccr4pop2anddhh1inthenamedcontentcontenttypegenusspeciessaccharomycescerevisiaenamedcontentcellwallintegritypathway
AT kaoruirie differentregulationsofitalictoggleyesrom2italicanditalictoggleyeslrg1italicexpressionbyccr4pop2anddhh1inthenamedcontentcontenttypegenusspeciessaccharomycescerevisiaenamedcontentcellwallintegritypathway
AT yuichikimura differentregulationsofitalictoggleyesrom2italicanditalictoggleyeslrg1italicexpressionbyccr4pop2anddhh1inthenamedcontentcontenttypegenusspeciessaccharomycescerevisiaenamedcontentcellwallintegritypathway
AT yasuyukisuda differentregulationsofitalictoggleyesrom2italicanditalictoggleyeslrg1italicexpressionbyccr4pop2anddhh1inthenamedcontentcontenttypegenusspeciessaccharomycescerevisiaenamedcontentcellwallintegritypathway
AT tomoakimizuno differentregulationsofitalictoggleyesrom2italicanditalictoggleyeslrg1italicexpressionbyccr4pop2anddhh1inthenamedcontentcontenttypegenusspeciessaccharomycescerevisiaenamedcontentcellwallintegritypathway
AT kenjiirie differentregulationsofitalictoggleyesrom2italicanditalictoggleyeslrg1italicexpressionbyccr4pop2anddhh1inthenamedcontentcontenttypegenusspeciessaccharomycescerevisiaenamedcontentcellwallintegritypathway