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Article: The role of RNA‐binding proteins in mediating adaptive responses in Gram‐positive bacteria

Christopoulou, Niki / Granneman, Sander

FEBS journal. 2022 Apr., v. 289, no. 7

2022

Abstract: Bacteria are constantly subjected to stressful conditions, such as antibiotic exposure, nutrient limitation and oxidative stress. For pathogenic bacteria, adapting to the host environment, escaping defence mechanisms and coping with antibiotic stress are ...

Abstract	Bacteria are constantly subjected to stressful conditions, such as antibiotic exposure, nutrient limitation and oxidative stress. For pathogenic bacteria, adapting to the host environment, escaping defence mechanisms and coping with antibiotic stress are crucial for their survival and the establishment of a successful infection. Stress adaptation relies heavily on the rate at which the organism can remodel its gene expression programme to counteract the stress. RNA‐binding proteins mediating co‐ and post‐transcriptional regulation have recently emerged as important players in regulating gene expression during adaptive responses. Most of the research on these layers of gene expression regulation has been done in Gram‐negative model organisms where, thanks to a wide variety of global studies, large post‐transcriptional regulatory networks have been uncovered. Unfortunately, our understanding of post‐transcriptional regulation in Gram‐positive bacteria is lagging behind. One possible explanation for this is that many proteins employed by Gram‐negative bacteria are not well conserved in Gram‐positives. And even if they are conserved, they do not always play similar roles as in Gram‐negative bacteria. This raises the important question whether Gram‐positive bacteria regulate gene expression in a significantly different way. The goal of this review was to discuss this in more detail by reviewing the role of well‐known RNA‐binding proteins in Gram‐positive bacteria and by highlighting their different behaviours with respect to some of their Gram‐negative counterparts. Finally, the second part of this review introduces several unusual RNA‐binding proteins of Gram‐positive species that we believe could also play an important role in adaptive responses.
Keywords	antibiotics ; gene expression ; gene expression regulation ; oxidative stress
Language	English
Dates of publication	2022-04
Size	p. 1746-1764.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	REVIEW
ZDB-ID	2173655-8
ISSN	1742-4658 ; 1742-464X
ISSN (online)	1742-4658
ISSN	1742-464X
DOI	10.1111/febs.15810
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Advantages and limitations of UV cross-linking analysis of protein-RNA interactomes in microbes.

Esteban-Serna, Sofia / McCaughan, Hugh / Granneman, Sander

Molecular microbiology

2023 Volume 120, Issue 4, Page(s) 477–489

Abstract: RNA-binding proteins (RBPs) govern the lifespan of nearly all transcripts and play key roles in adaptive responses in microbes. A robust approach to examine protein-RNA interactions involves irradiating cells with UV light to form covalent adducts ... ...

Abstract	RNA-binding proteins (RBPs) govern the lifespan of nearly all transcripts and play key roles in adaptive responses in microbes. A robust approach to examine protein-RNA interactions involves irradiating cells with UV light to form covalent adducts between RBPs and their cognate RNAs. Combined with RNA or protein purification, these procedures can provide global RBP censuses or transcriptomic maps for all target sequences of a single protein in living cells. The recent development of novel methods has quickly populated the RBP landscape in microorganisms. Here, we provide an overview of prominent UV cross-linking techniques which have been applied to investigate RNA interactomes in microbes. By assessing their advantages and caveats, this technical evaluation intends to guide the selection of appropriate methods and experimental design as well as to encourage the use of complementary UV-dependent techniques to inspect RNA-binding activity.
MeSH term(s)	RNA/metabolism ; Ultraviolet Rays ; RNA-Binding Proteins/genetics ; RNA-Binding Proteins/metabolism ; Gene Expression Profiling/methods ; Transcriptome
Chemical Substances	RNA (63231-63-0) ; RNA-Binding Proteins
Language	English
Publishing date	2023-05-10
Publishing country	England
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	619315-8
ISSN	1365-2958 ; 0950-382X
ISSN (online)	1365-2958
ISSN	0950-382X
DOI	10.1111/mmi.15073
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Article ; Online: The role of RNA-binding proteins in mediating adaptive responses in Gram-positive bacteria.

Christopoulou, Niki / Granneman, Sander

The FEBS journal

2021 Volume 289, Issue 7, Page(s) 1746–1764

Abstract	Bacteria are constantly subjected to stressful conditions, such as antibiotic exposure, nutrient limitation and oxidative stress. For pathogenic bacteria, adapting to the host environment, escaping defence mechanisms and coping with antibiotic stress are crucial for their survival and the establishment of a successful infection. Stress adaptation relies heavily on the rate at which the organism can remodel its gene expression programme to counteract the stress. RNA-binding proteins mediating co- and post-transcriptional regulation have recently emerged as important players in regulating gene expression during adaptive responses. Most of the research on these layers of gene expression regulation has been done in Gram-negative model organisms where, thanks to a wide variety of global studies, large post-transcriptional regulatory networks have been uncovered. Unfortunately, our understanding of post-transcriptional regulation in Gram-positive bacteria is lagging behind. One possible explanation for this is that many proteins employed by Gram-negative bacteria are not well conserved in Gram-positives. And even if they are conserved, they do not always play similar roles as in Gram-negative bacteria. This raises the important question whether Gram-positive bacteria regulate gene expression in a significantly different way. The goal of this review was to discuss this in more detail by reviewing the role of well-known RNA-binding proteins in Gram-positive bacteria and by highlighting their different behaviours with respect to some of their Gram-negative counterparts. Finally, the second part of this review introduces several unusual RNA-binding proteins of Gram-positive species that we believe could also play an important role in adaptive responses.
MeSH term(s)	Anti-Bacterial Agents/metabolism ; Gene Expression Regulation, Bacterial ; Gram-Negative Bacteria/genetics ; Gram-Negative Bacteria/metabolism ; Gram-Positive Bacteria/genetics ; Gram-Positive Bacteria/metabolism ; RNA-Binding Proteins/genetics ; RNA-Binding Proteins/metabolism
Chemical Substances	Anti-Bacterial Agents ; RNA-Binding Proteins
Language	English
Publishing date	2021-03-25
Publishing country	England
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	2173655-8
ISSN	1742-4658 ; 1742-464X
ISSN (online)	1742-4658
ISSN	1742-464X
DOI	10.1111/febs.15810
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Defining Bacterial RNA-RNA Interactomes Using CLASH.

Esteban-Serna, Sofia / Chu, Liang-Cui / Chauhan, Mehak / Raja, Pujitha / Granneman, Sander

Methods in molecular biology (Clifton, N.J.)

2024 Volume 2741, Page(s) 307–345

Abstract: Methicillin-resistant Staphylococcus aureus (MRSA) is a bacterial pathogen accounting for high mortality rates among infected patients. Transcriptomic regulation by small RNAs (sRNAs) has been shown to regulate networks promoting antibiotic resistance ... ...

Abstract	Methicillin-resistant Staphylococcus aureus (MRSA) is a bacterial pathogen accounting for high mortality rates among infected patients. Transcriptomic regulation by small RNAs (sRNAs) has been shown to regulate networks promoting antibiotic resistance and virulence in S. aureus. Yet, the biological role of most sRNAs during MRSA host infection remains unknown. To fill this gap, in collaboration with the lab of Jai Tree, we performed comprehensive RNA-RNA interactome analyses in MRSA using CLASH under conditions that mimic the host environment. Here we present a detailed version of this optimized CLASH (cross-linking, ligation, and sequencing of hybrids) protocol we recently developed, which has been tailored to explore the RNA interactome in S. aureus as well as other Gram-positive bacteria. Alongside, we introduce a compilation of helpful Python functions for analyzing folding energies of putative RNA-RNA interactions and streamlining sRNA and mRNA seed discovery in CLASH data. In the accompanying computational demonstration, we aim to establish a standardized strategy to evaluate the likelihood that observed chimeras arise from true RNA-RNA interactions.
MeSH term(s)	Humans ; RNA, Bacterial/genetics ; Staphylococcus aureus/genetics ; Methicillin-Resistant Staphylococcus aureus/genetics ; Computational Biology/methods ; RNA, Messenger/genetics ; Gene Expression Regulation, Bacterial ; RNA, Small Untranslated/genetics
Chemical Substances	RNA, Bacterial ; RNA, Messenger ; RNA, Small Untranslated
Language	English
Publishing date	2024-01-13
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-3565-0_17
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Structural basis of ribosomal 30S subunit degradation by RNase R.

Dimitrova-Paternoga, Lyudmila / Kasvandik, Sergo / Beckert, Bertrand / Granneman, Sander / Tenson, Tanel / Wilson, Daniel N / Paternoga, Helge

Nature

2024 Volume 626, Issue 8001, Page(s) 1133–1140

Abstract: Protein synthesis is a major energy-consuming process of the cell that requires the controlled ... ...

Abstract	Protein synthesis is a major energy-consuming process of the cell that requires the controlled production
MeSH term(s)	Exoribonucleases/metabolism ; Ribosomal Proteins/metabolism ; Ribosomes/chemistry ; Ribosomes/metabolism ; Kinetics ; Binding Sites
Chemical Substances	Exoribonucleases (EC 3.1.-) ; ribonuclease R (EC 3.1.27.-) ; Ribosomal Proteins
Language	English
Publishing date	2024-02-07
Publishing country	England
Document type	Journal Article
ZDB-ID	120714-3
ISSN	1476-4687 ; 0028-0836
ISSN (online)	1476-4687
ISSN	0028-0836
DOI	10.1038/s41586-024-07027-6
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Article ; Online: Probing the RNA-Binding Proteome from Yeast to Man: Major Advances and Challenges.

Beckmann, Benedikt M / Granneman, Sander

Methods in molecular biology (Clifton, N.J.)

2019 Volume 2049, Page(s) 213–231

Abstract: RNA-binding proteins are important for core cellular processes such as mRNA transcription, splicing, transport, translation, and degradation. Recently, hundreds of novel RNA-binders have been identified in vivo in various organisms and cell types. We ... ...

Abstract	RNA-binding proteins are important for core cellular processes such as mRNA transcription, splicing, transport, translation, and degradation. Recently, hundreds of novel RNA-binders have been identified in vivo in various organisms and cell types. We discuss the RNA interactome capture technique which enabled this boost in identifying new RNA-binding proteins in eukaryotes. A focus of this chapter, however, is the presentation of different challenges and problems that need to be addressed to be able to understand the conserved mRNA-bound proteomes from yeast to man.
MeSH term(s)	Animals ; Mice ; Models, Biological ; Proteome/analysis ; Proteome/metabolism ; RNA, Messenger/metabolism ; RNA-Binding Proteins/genetics ; RNA-Binding Proteins/metabolism ; Saccharomyces cerevisiae/metabolism
Chemical Substances	Proteome ; RNA, Messenger ; RNA-Binding Proteins
Language	English
Publishing date	2019-10-10
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-9736-7_13
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Temporal-iCLIP captures co-transcriptional RNA-protein interactions.

Cordiner, Ross A / Dou, Yuhui / Thomsen, Rune / Bugai, Andrii / Granneman, Sander / Heick Jensen, Torben

Nature communications

2023 Volume 14, Issue 1, Page(s) 696

Abstract: Dynamic RNA-protein interactions govern the co-transcriptional packaging of RNA polymerase II (RNAPII)-derived transcripts. Yet, our current understanding of this process in vivo primarily stems from steady state analysis. To remedy this, we here conduct ...

Abstract	Dynamic RNA-protein interactions govern the co-transcriptional packaging of RNA polymerase II (RNAPII)-derived transcripts. Yet, our current understanding of this process in vivo primarily stems from steady state analysis. To remedy this, we here conduct temporal-iCLIP (tiCLIP), combining RNAPII transcriptional synchronisation with UV cross-linking of RNA-protein complexes at serial timepoints. We apply tiCLIP to the RNA export adaptor, ALYREF; a component of the Nuclear Exosome Targeting (NEXT) complex, RBM7; and the nuclear cap binding complex (CBC). Regardless of function, all tested factors interact with nascent RNA as it exits RNAPII. Moreover, we demonstrate that the two transesterification steps of pre-mRNA splicing temporally separate ALYREF and RBM7 binding to splicing intermediates, and that exon-exon junction density drives RNA 5'end binding of ALYREF. Finally, we identify underappreciated steps in snoRNA 3'end processing performed by RBM7. Altogether, our data provide a temporal view of RNA-protein interactions during the early phases of transcription.
MeSH term(s)	RNA-Binding Proteins/metabolism ; Cell Nucleus/metabolism ; RNA Precursors/metabolism ; RNA Splicing ; RNA Polymerase II/metabolism ; RNA, Small Nucleolar/metabolism
Chemical Substances	RNA-Binding Proteins ; RNA Precursors ; RNA Polymerase II (EC 2.7.7.-) ; RNA, Small Nucleolar
Language	English
Publishing date	2023-02-08
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-36345-y
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: diffBUM-HMM: a robust statistical modeling approach for detecting RNA flexibility changes in high-throughput structure probing data.

Marangio, Paolo / Law, Ka Ying Toby / Sanguinetti, Guido / Granneman, Sander

Genome biology

2021 Volume 22, Issue 1, Page(s) 165

Abstract: Advancing RNA structural probing techniques with next-generation sequencing has generated demands for complementary computational tools to robustly extract RNA structural information amidst sampling noise and variability. We present diffBUM-HMM, a noise- ... ...

Abstract	Advancing RNA structural probing techniques with next-generation sequencing has generated demands for complementary computational tools to robustly extract RNA structural information amidst sampling noise and variability. We present diffBUM-HMM, a noise-aware model that enables accurate detection of RNA flexibility and conformational changes from high-throughput RNA structure-probing data. diffBUM-HMM is widely compatible, accounting for sampling variation and sequence coverage biases, and displays higher sensitivity than existing methods while robust against false positives. Our analyses of datasets generated with a variety of RNA probing chemistries demonstrate the value of diffBUM-HMM for quantitatively detecting RNA structural changes and RNA-binding protein binding sites.
MeSH term(s)	Algorithms ; Base Sequence ; Binding Sites ; Databases, Genetic ; High-Throughput Nucleotide Sequencing ; Markov Chains ; Models, Statistical ; Models, Theoretical ; Mutation/genetics ; Nucleotides/genetics ; Protein Binding ; RNA/chemistry ; RNA/genetics ; RNA Precursors/genetics ; RNA, Long Noncoding/genetics ; Ribosomes/metabolism
Chemical Substances	Nucleotides ; RNA Precursors ; RNA, Long Noncoding ; XIST non-coding RNA ; RNA (63231-63-0)
Language	English
Publishing date	2021-05-27
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2040529-7
ISSN	1474-760X ; 1474-760X
ISSN (online)	1474-760X
ISSN	1474-760X
DOI	10.1186/s13059-021-02379-y
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: diffBUM-HMM: a robust statistical modeling approach for detecting RNA flexibility changes in high-throughput structure probing data

Marangio, Paolo / Law, Ka Ying Toby / Sanguinetti, Guido / Granneman, Sander

Genome biology. 2021 Dec., v. 22, no. 1

2021

Abstract	Advancing RNA structural probing techniques with next-generation sequencing has generated demands for complementary computational tools to robustly extract RNA structural information amidst sampling noise and variability. We present diffBUM-HMM, a noise-aware model that enables accurate detection of RNA flexibility and conformational changes from high-throughput RNA structure-probing data. diffBUM-HMM is widely compatible, accounting for sampling variation and sequence coverage biases, and displays higher sensitivity than existing methods while robust against false positives. Our analyses of datasets generated with a variety of RNA probing chemistries demonstrate the value of diffBUM-HMM for quantitatively detecting RNA structural changes and RNA-binding protein binding sites.
Keywords	RNA ; RNA-binding proteins ; data collection ; genome
Language	English
Dates of publication	2021-12
Size	p. 165.
Publishing place	BioMed Central
Document type	Article
ZDB-ID	2040529-7
ISSN	1474-760X
ISSN	1474-760X
DOI	10.1186/s13059-021-02379-y
Database	NAL-Catalogue (AGRICOLA)

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Article: The mRNA derived MalH sRNA contributes to alternative carbon source utilization by tuning maltoporin expression in E. coli

Iosub, Ira A / Marchioretto, Marta / van Nues, Rob W / McKellar, Stuart / Viero, Gabriella / Granneman, Sander

RNA biology. 2021 June 03, v. 18, no. 6

2021

Abstract: Previous high-throughput studies in Gram-negative bacteria identified a large number of 3ʹUTR fragments that potentially function as sRNAs. Here we extensively characterize the MalH sRNA. We show that MalH is a stable degradation intermediate derived ... ...

Abstract	Previous high-throughput studies in Gram-negative bacteria identified a large number of 3ʹUTR fragments that potentially function as sRNAs. Here we extensively characterize the MalH sRNA. We show that MalH is a stable degradation intermediate derived from the 3ʹ end of malG, which is part of the maltose uptake operon transcript malEFG. Unlike the majority of bacterial sRNAs, MalH is transiently expressed during the transition from the exponential to the stationary growth phase, suggesting that it contributes to adaptation to changes in nutrient availability. Over-expression of MalH reduces expression of general outer membrane porins and MicA, a repressor of the high-affinity maltose/maltodextrin transporter LamB. Disrupting MalH production and function significantly reduces lamB accumulation when maltose is the only available carbon source, presumably due to the accumulation of the MicA repressor. We propose that MalH is part of a regulatory network that, during the transition phase, directly or indirectly promotes accumulation of high-affinity maltose transporters in the outer membrane by dampening competing pathways.
Keywords	Escherichia coli ; carbon ; maltodextrins ; maltose ; nutrient availability ; operon ; porins
Language	English
Dates of publication	2021-0603
Size	p. 914-931.
Publishing place	Taylor & Francis
Document type	Article
Note	NAL-AP-2-clean
ISSN	1555-8584
DOI	10.1080/15476286.2020.1827784
Database	NAL-Catalogue (AGRICOLA)

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