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Article ; Online: A posttranscriptional pathway regulates cell wall mRNA expression in budding yeast.

Bresson, Stefan / Shchepachev, Vadim / Tollervey, David

2023 Volume 42, Issue 3, Page(s) 112184

Abstract: The fungal cell wall provides protection and structure and is an important target for antifungal compounds. A mitogen-activated protein (MAP) kinase cascade termed the cell wall integrity (CWI) pathway regulates transcriptional responses to cell wall ... ...

Abstract	The fungal cell wall provides protection and structure and is an important target for antifungal compounds. A mitogen-activated protein (MAP) kinase cascade termed the cell wall integrity (CWI) pathway regulates transcriptional responses to cell wall damage. Here, we describe a posttranscriptional pathway that plays an important complementary role. We report that the RNA-binding proteins (RBPs) Mrn1 and Nab6 specifically target the 3' UTRs of a largely overlapping set of cell wall-related mRNAs. These mRNAs are downregulated in the absence of Nab6, indicating a function in target mRNA stabilization. Nab6 acts in parallel to CWI signaling to maintain appropriate expression of cell wall genes during stress. Cells lacking both pathways are hypersensitive to antifungal compounds targeting the cell wall. Deletion of MRN1 partially alleviates growth defects associated with Δnab6, and Mrn1 has an opposing function in mRNA destabilization. Our results uncover a posttranscriptional pathway that mediates cellular resistance to antifungal compounds.
MeSH term(s)	Antifungal Agents/pharmacology ; Antifungal Agents/metabolism ; Saccharomyces cerevisiae/metabolism ; Saccharomycetales/genetics ; Cell Wall/metabolism ; RNA, Messenger/genetics ; RNA, Messenger/metabolism ; Saccharomyces cerevisiae Proteins/genetics ; Saccharomyces cerevisiae Proteins/metabolism ; Gene Expression Regulation, Fungal
Chemical Substances	Antifungal Agents ; RNA, Messenger ; Saccharomyces cerevisiae Proteins
Language	English
Publishing date	2023-02-28
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2023.112184
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: A posttranscriptional pathway regulates cell wall mRNA expression in budding yeast

Stefan Bresson / Vadim Shchepachev / David Tollervey

Cell Reports, Vol 42, Iss 3, Pp 112184- (2023)

2023

Abstract: Summary: The fungal cell wall provides protection and structure and is an important target for antifungal compounds. A mitogen-activated protein (MAP) kinase cascade termed the cell wall integrity (CWI) pathway regulates transcriptional responses to cell ...

Abstract	Summary: The fungal cell wall provides protection and structure and is an important target for antifungal compounds. A mitogen-activated protein (MAP) kinase cascade termed the cell wall integrity (CWI) pathway regulates transcriptional responses to cell wall damage. Here, we describe a posttranscriptional pathway that plays an important complementary role. We report that the RNA-binding proteins (RBPs) Mrn1 and Nab6 specifically target the 3′ UTRs of a largely overlapping set of cell wall-related mRNAs. These mRNAs are downregulated in the absence of Nab6, indicating a function in target mRNA stabilization. Nab6 acts in parallel to CWI signaling to maintain appropriate expression of cell wall genes during stress. Cells lacking both pathways are hypersensitive to antifungal compounds targeting the cell wall. Deletion of MRN1 partially alleviates growth defects associated with Δnab6, and Mrn1 has an opposing function in mRNA destabilization. Our results uncover a posttranscriptional pathway that mediates cellular resistance to antifungal compounds.
Keywords	CP: Molecular biology ; CP: Cell biology ; Biology (General) ; QH301-705.5
Subject code	571
Language	English
Publishing date	2023-03-01T00:00:00Z
Publisher	Elsevier
Document type	Article ; Online
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Article ; Online: Tailing Off: PABP and CNOT Generate Cycles of mRNA Deadenylation.

Bresson, Stefan / Tollervey, David

Molecular cell

2018 Volume 70, Issue 6, Page(s) 987–988

Abstract: In this issue of Molecular Cell, Webster et al. (2018) and Yi et al. (2018) dissect the mechanisms underlying cytoplasmic mRNA deadenylation by the Ccr4-Not (CNOT) complex. Crucial to this process is the poly(A) binding protein Pab1/PABPC1, which both ... ...

Abstract	In this issue of Molecular Cell, Webster et al. (2018) and Yi et al. (2018) dissect the mechanisms underlying cytoplasmic mRNA deadenylation by the Ccr4-Not (CNOT) complex. Crucial to this process is the poly(A) binding protein Pab1/PABPC1, which both stimulates and suppresses the activity of different deadenylases.
MeSH term(s)	Poly(A)-Binding Proteins ; RNA, Messenger ; RNA-Binding Proteins
Chemical Substances	Poly(A)-Binding Proteins ; RNA, Messenger ; RNA-Binding Proteins
Language	English
Publishing date	2018-06-19
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Comment
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2018.06.009
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Article ; Online: Surveillance-ready transcription: nuclear RNA decay as a default fate.

Bresson, Stefan / Tollervey, David

Open biology

2018 Volume 8, Issue 3

Abstract: Eukaryotic cells synthesize enormous quantities of RNA from diverse classes, most of which are subject to extensive processing. These processes are inherently error-prone, and cells have evolved robust quality control mechanisms to selectively remove ... ...

Abstract	Eukaryotic cells synthesize enormous quantities of RNA from diverse classes, most of which are subject to extensive processing. These processes are inherently error-prone, and cells have evolved robust quality control mechanisms to selectively remove aberrant transcripts. These surveillance pathways monitor all aspects of nuclear RNA biogenesis, and in addition remove nonfunctional transcripts arising from spurious transcription and a host of non-protein-coding RNAs (ncRNAs). Surprisingly, this is largely accomplished with only a handful of RNA decay enzymes. It has, therefore, been unclear how these factors efficiently distinguish between functional RNAs and huge numbers of diverse transcripts that must be degraded. Here we describe how bona fide transcripts are specifically protected, particularly by 5' and 3' modifications. Conversely, a plethora of factors associated with the nascent transcripts all act to recruit the RNA quality control, surveillance and degradation machinery. We conclude that initiating RNAPII is 'surveillance ready', with degradation being a default fate for all transcripts that lack specific protective features. We further postulate that this promiscuity is a key feature that allowed the proliferation of vast numbers of ncRNAs in eukaryotes, including humans.
MeSH term(s)	Animals ; Eukaryota/genetics ; Eukaryota/metabolism ; Humans ; RNA Polymerase II/metabolism ; RNA Processing, Post-Transcriptional ; RNA Stability ; RNA, Messenger/chemistry ; RNA, Untranslated/chemistry ; Transcription, Genetic
Chemical Substances	RNA, Messenger ; RNA, Untranslated ; RNA Polymerase II (EC 2.7.7.-)
Language	English
Publishing date	2018-03-21
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2630944-0
ISSN	2046-2441 ; 2046-2441
ISSN (online)	2046-2441
ISSN	2046-2441
DOI	10.1098/rsob.170270
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Article ; Online: Surveillance-ready transcription

Stefan Bresson / David Tollervey

Open Biology, Vol 8, Iss

nuclear RNA decay as a default fate

2018 Volume 3

Abstract	Eukaryotic cells synthesize enormous quantities of RNA from diverse classes, most of which are subject to extensive processing. These processes are inherently error-prone, and cells have evolved robust quality control mechanisms to selectively remove aberrant transcripts. These surveillance pathways monitor all aspects of nuclear RNA biogenesis, and in addition remove nonfunctional transcripts arising from spurious transcription and a host of non-protein-coding RNAs (ncRNAs). Surprisingly, this is largely accomplished with only a handful of RNA decay enzymes. It has, therefore, been unclear how these factors efficiently distinguish between functional RNAs and huge numbers of diverse transcripts that must be degraded. Here we describe how bona fide transcripts are specifically protected, particularly by 5′ and 3′ modifications. Conversely, a plethora of factors associated with the nascent transcripts all act to recruit the RNA quality control, surveillance and degradation machinery. We conclude that initiating RNAPII is ‘surveillance ready’, with degradation being a default fate for all transcripts that lack specific protective features. We further postulate that this promiscuity is a key feature that allowed the proliferation of vast numbers of ncRNAs in eukaryotes, including humans.
Keywords	rna surveillance ; gene expression ; quality control ; rna processing ; Biology (General) ; QH301-705.5
Subject code	572
Language	English
Publishing date	2018-03-01T00:00:00Z
Publisher	The Royal Society
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: The SPARC complex defines RNAPII promoters in

Staneva, Desislava P / Bresson, Stefan / Auchynnikava, Tatsiana / Spanos, Christos / Rappsilber, Juri / Jeyaprakash, A Arockia / Tollervey, David / Matthews, Keith R / Allshire, Robin C

eLife

2022 Volume 11

Abstract: Kinetoplastids are a highly divergent lineage of eukaryotes with unusual mechanisms for regulating gene expression. We previously surveyed 65 putative chromatin factors in the ... ...

Abstract	Kinetoplastids are a highly divergent lineage of eukaryotes with unusual mechanisms for regulating gene expression. We previously surveyed 65 putative chromatin factors in the kinetoplastid
MeSH term(s)	Chromatin/metabolism ; Heterochromatin/metabolism ; Histone Methyltransferases/genetics ; RNA Polymerase II/metabolism ; RNA, Messenger/metabolism ; Transcription, Genetic ; Trypanosoma brucei brucei/genetics ; Trypanosoma brucei brucei/metabolism ; Variant Surface Glycoproteins, Trypanosoma/genetics
Chemical Substances	Chromatin ; Heterochromatin ; RNA, Messenger ; Variant Surface Glycoproteins, Trypanosoma ; Histone Methyltransferases (EC 2.1.1.-) ; RNA Polymerase II (EC 2.7.7.-)
Language	English
Publishing date	2022-09-28
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.83135
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Article: Stress-Induced Translation Inhibition through Rapid Displacement of Scanning Initiation Factors

Bresson, Stefan / Shchepachev, Vadim / Spanos, Christos / Turowski, Tomasz W / Rappsilber, Juri / Tollervey, David

Molecular cell. 2020 Nov. 05, v. 80, no. 3

2020

Abstract: Cellular responses to environmental stress are frequently mediated by RNA-binding proteins (RBPs). Here, we examined global RBP dynamics in Saccharomyces cerevisiae in response to glucose starvation and heat shock. Each stress induced rapid remodeling of ...

Abstract	Cellular responses to environmental stress are frequently mediated by RNA-binding proteins (RBPs). Here, we examined global RBP dynamics in Saccharomyces cerevisiae in response to glucose starvation and heat shock. Each stress induced rapid remodeling of the RNA-protein interactome without corresponding changes in RBP abundance. Consistent with general translation shutdown, ribosomal proteins contacting the mRNA showed decreased RNA association. Among translation components, RNA association was most reduced for initiation factors involved in 40S scanning (eukaryotic initiation factor 4A [eIF4A], eIF4B, and Ded1), indicating a common mechanism of translational repression. In unstressed cells, eIF4A, eIF4B, and Ded1 primarily targeted the 5′ ends of mRNAs. Following glucose withdrawal, 5′ binding was abolished within 30 s, explaining the rapid translation shutdown, but mRNAs remained stable. Heat shock induced progressive loss of 5′ RNA binding by initiation factors over ∼16 min and provoked mRNA degradation, particularly for translation-related factors, mediated by Xrn1. Taken together, these results reveal mechanisms underlying translational control of gene expression during stress.
Keywords	Saccharomyces cerevisiae ; gene expression ; glucose ; heat stress ; starvation
Language	English
Dates of publication	2020-1105
Size	p. 470-484.e8.
Publishing place	Elsevier Inc.
Document type	Article
Note	NAL-AP-2-clean
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2020.09.021
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Article ; Online: Stress-Induced Translation Inhibition through Rapid Displacement of Scanning Initiation Factors.

Bresson, Stefan / Shchepachev, Vadim / Spanos, Christos / Turowski, Tomasz W / Rappsilber, Juri / Tollervey, David

Molecular cell

2020 Volume 80, Issue 3, Page(s) 470–484.e8

Abstract	Cellular responses to environmental stress are frequently mediated by RNA-binding proteins (RBPs). Here, we examined global RBP dynamics in Saccharomyces cerevisiae in response to glucose starvation and heat shock. Each stress induced rapid remodeling of the RNA-protein interactome without corresponding changes in RBP abundance. Consistent with general translation shutdown, ribosomal proteins contacting the mRNA showed decreased RNA association. Among translation components, RNA association was most reduced for initiation factors involved in 40S scanning (eukaryotic initiation factor 4A [eIF4A], eIF4B, and Ded1), indicating a common mechanism of translational repression. In unstressed cells, eIF4A, eIF4B, and Ded1 primarily targeted the 5' ends of mRNAs. Following glucose withdrawal, 5' binding was abolished within 30 s, explaining the rapid translation shutdown, but mRNAs remained stable. Heat shock induced progressive loss of 5' RNA binding by initiation factors over ∼16 min and provoked mRNA degradation, particularly for translation-related factors, mediated by Xrn1. Taken together, these results reveal mechanisms underlying translational control of gene expression during stress.
MeSH term(s)	5' Untranslated Regions ; DEAD-box RNA Helicases/metabolism ; Eukaryotic Initiation Factor-4A/metabolism ; Eukaryotic Initiation Factor-4G/metabolism ; Eukaryotic Initiation Factors/metabolism ; Glucose/metabolism ; Heat-Shock Response/physiology ; Peptide Initiation Factors/metabolism ; Peptide Initiation Factors/physiology ; Protein Biosynthesis/physiology ; RNA, Messenger/genetics ; RNA-Binding Proteins/metabolism ; Ribosomal Proteins/metabolism ; Ribosomal Proteins/physiology ; Saccharomyces cerevisiae/metabolism ; Saccharomyces cerevisiae Proteins/metabolism ; Stress, Physiological/physiology
Chemical Substances	5' Untranslated Regions ; Eukaryotic Initiation Factor-4G ; Eukaryotic Initiation Factors ; Peptide Initiation Factors ; RNA, Messenger ; RNA-Binding Proteins ; Ribosomal Proteins ; Saccharomyces cerevisiae Proteins ; eIF-4B ; Eukaryotic Initiation Factor-4A (EC 2.7.7.-) ; DEAD-box RNA Helicases (EC 3.6.4.13) ; Glucose (IY9XDZ35W2)
Language	English
Publishing date	2020-10-13
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2020.09.021
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Article ; Online: Nuclear RNA Decay Pathways Aid Rapid Remodeling of Gene Expression in Yeast.

Bresson, Stefan / Tuck, Alex / Staneva, Desislava / Tollervey, David

Molecular cell

2017 Volume 65, Issue 5, Page(s) 787–800.e5

Abstract: In budding yeast, the nuclear RNA surveillance system is active on all pre-mRNA transcripts and modulated by nutrient availability. To test the role of nuclear surveillance in reprogramming gene expression, we identified transcriptome-wide binding sites ... ...

Abstract	In budding yeast, the nuclear RNA surveillance system is active on all pre-mRNA transcripts and modulated by nutrient availability. To test the role of nuclear surveillance in reprogramming gene expression, we identified transcriptome-wide binding sites for RNA polymerase II and the exosome cofactors Mtr4 (TRAMP complex) and Nab3 (NNS complex) by UV crosslinking immediately following glucose withdrawal (0, 4, and 8 min). In glucose, mRNA binding by Nab3 and Mtr4 was mainly restricted to promoter-proximal sites, reflecting early transcription termination. Following glucose withdrawal, many growth-related mRNAs showed reduced transcription but increased Nab3 binding, accompanied by downstream recruitment of Mtr4, and oligo(A) tailing. We conclude that transcription termination is followed by TRAMP-mediated RNA decay. Upregulated transcripts evaded increased surveillance factor binding following glucose withdrawal. Some upregulated genes showed use of alternative transcription starts to bypass strong NNS binding sites. We conclude that nuclear surveillance pathways regulate both positive and negative responses to glucose availability.
MeSH term(s)	Adaptation, Physiological ; Binding Sites ; Cell Nucleus/metabolism ; DEAD-box RNA Helicases/genetics ; DEAD-box RNA Helicases/metabolism ; Gene Expression Regulation, Fungal ; Glucose/deficiency ; Glucose/metabolism ; Nuclear Proteins/genetics ; Nuclear Proteins/metabolism ; Protein Binding ; RNA Polymerase II/genetics ; RNA Polymerase II/metabolism ; RNA Processing, Post-Transcriptional ; RNA Stability ; RNA, Fungal/genetics ; RNA, Fungal/metabolism ; RNA, Messenger/genetics ; RNA, Messenger/metabolism ; RNA, Nuclear/genetics ; RNA, Nuclear/metabolism ; RNA-Binding Proteins/genetics ; RNA-Binding Proteins/metabolism ; Saccharomyces cerevisiae/genetics ; Saccharomyces cerevisiae/metabolism ; Saccharomyces cerevisiae Proteins/genetics ; Saccharomyces cerevisiae Proteins/metabolism ; Time Factors ; Transcription, Genetic
Chemical Substances	NAB3 protein, S cerevisiae ; Nuclear Proteins ; RNA, Fungal ; RNA, Messenger ; RNA, Nuclear ; RNA-Binding Proteins ; Saccharomyces cerevisiae Proteins ; RNA Polymerase II (EC 2.7.7.-) ; MTR4 protein, S cerevisiae (EC 3.6.1.-) ; DEAD-box RNA Helicases (EC 3.6.4.13) ; Glucose (IY9XDZ35W2)
Language	English
Publishing date	2017-02-09
Publishing country	United States
Document type	Journal Article
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2017.01.005
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Article: Nuclear RNA Decay Pathways Aid Rapid Remodeling of Gene Expression in Yeast

Bresson, Stefan / Tuck, Alex / Staneva, Desislava / Tollervey, David

Molecular cell. 2017 Mar. 02, v. 65, no. 5

2017

Abstract	In budding yeast, the nuclear RNA surveillance system is active on all pre-mRNA transcripts and modulated by nutrient availability. To test the role of nuclear surveillance in reprogramming gene expression, we identified transcriptome-wide binding sites for RNA polymerase II and the exosome cofactors Mtr4 (TRAMP complex) and Nab3 (NNS complex) by UV crosslinking immediately following glucose withdrawal (0, 4, and 8 min). In glucose, mRNA binding by Nab3 and Mtr4 was mainly restricted to promoter-proximal sites, reflecting early transcription termination. Following glucose withdrawal, many growth-related mRNAs showed reduced transcription but increased Nab3 binding, accompanied by downstream recruitment of Mtr4, and oligo(A) tailing. We conclude that transcription termination is followed by TRAMP-mediated RNA decay. Upregulated transcripts evaded increased surveillance factor binding following glucose withdrawal. Some upregulated genes showed use of alternative transcription starts to bypass strong NNS binding sites. We conclude that nuclear surveillance pathways regulate both positive and negative responses to glucose availability.
Keywords	DNA-directed RNA polymerase ; binding sites ; crosslinking ; exosomes ; gene expression ; gene expression regulation ; genes ; glucose ; messenger RNA ; monitoring ; nutrient availability ; transcription termination ; yeasts
Language	English
Dates of publication	2017-0302
Size	p. 787-800.e5.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2017.01.005
Database	NAL-Catalogue (AGRICOLA)

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