A novel antisense RNA regulates at transcriptional level the virulence gene icsA of Shigella flexneri

Giangrossi, Mara; Prosseda, Gianni; Tran, Chi Nhan; Brandi, Anna; Colonna, Bianca; Falconi, Maurizio

doi:10.1093/nar/gkq025

Cited by 80 publications

(122 citation statements)

References 57 publications

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“…The resulting lncRNA products might simply represent byproducts of transcription and are typically rapidly degraded after synthesis (Clark et al, 2012). (Albrecht et al, 2010(Albrecht et al, , 2011Chabelskaya et al, 2014;Chao et al, 2012;Gong et al, 2011;Grieshaber et al, 2006;Mann et al, 2012;Moon et al, 2013;Ortega et al, 2012;PadalonBrauch et al, 2008;Pfeiffer et al, 2007) crRNA, (Bhaya et al, 2011;Heidrich and Vogel, 2013;Sampson et al, 2013;van der Oost et al, 2014) (Georg and Hess, 2011;Giangrossi et al, 2010;GonzaloAsensio et al, 2013;Gottesman and Storz, 2011;Lasa et al, 2011;Lee and Groisman, 2010;Padalon-Brauch et al, 2008;Sesto et al, 2013) circRNAs rare varies arise from the 3'-5' ligation of both ends of linear RNA molecules n. a. -- (Doose et al, 2013;Vicens and Cech, 2009) - (Conway et al, 2014;Weinberg et al, 2009) Carpenter et al, 2013;Gomez et al, 2013;Iiott et al, 2014;Imamura et al, 2014;Li et al, 2014;Rapicavoli et al, 2013) poly ( …”

Section: Eukaryotic Long Non-coding Rnas (Lncrnas)mentioning

confidence: 99%

Dual RNA-seq of pathogen and host

2012

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SummaryThe infection of a eukaryotic host cell by a bacterial pathogen is one of the most intimate examples of cross-kingdom interactions in biology. Infection processes are highly relevant from both a basic research as well as a clinical point of view. Sophisticated mechanisms have evolved in the pathogen to manipulate the host response and vice versa host cells have developed a wide range of anti-microbial defense strategies to combat bacterial invasion and clear infections.However, it is this diversity and complexity that makes infection research so challenging to technically address as common approaches have either been optimized for bacterial or eukaryotic organisms. Instead, methods are required that are able to deal with the often dramatic discrepancy between host and pathogen with respect to various cellular properties and processes. One class of cellular macromolecules that exemplify this host-pathogen heterogeneity is given by their transcriptomes: Bacterial transcripts differ from their eukaryotic counterparts in many aspects that involve both quantitative and qualitative traits. The entity of RNA transcripts present in a cell is of paramount interest as it reflects the cell's physiological state under the given condition. Genome-wide transcriptomic techniques such as RNA-seq have therefore been used for single-organism analyses for several years, but their applicability has been limited for infection studies.The present work describes the establishment of a novel transcriptomic approach for infection biology which we have termed "Dual RNA-seq". Using this technology, it was intended to shed light particularly on the contribution of non-protein-encoding transcripts to virulence, as these classes have mostly evaded previous infection studies due to the lack of suitable methods. The performance of Dual RNA-seq was evaluated in an in vitro infection model based on the important facultative intracellular pathogen Salmonella enterica serovar Typhimurium and different human cell lines. Dual RNA-seq was found to be capable of capturing all major bacterial and human transcript classes and proved reproducible. During the course of these experiments, a previously largely uncharacterized bacterial small non-coding RNA (sRNA), referred to as STnc440, was identified as one of the most strongly induced genes in intracellular Salmonella.Interestingly, while inhibition of STnc440 expression has been previously shown to cause a virulence defect in different animal models of Salmonellosis, the underlying molecular mechanisms have remained obscure. Here, classical genetics, transcriptomics and biochemical assays proposed a complex model of Salmonella gene expression control that is orchestrated by this sRNA. In particular, STnc440 was found to be involved in the regulation of multiple bacterial target mRNAs by direct base pair interaction with consequences for Salmonella virulence and

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Section: Eukaryotic Long Non-coding Rnas (Lncrnas)mentioning

confidence: 99%

Dual RNA-seq of pathogen and host

2012

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“…Another example is the Shigella flexneri virulence gene icsA (virG), which is controlled by the asRNA RnaG. The asRNA represses the transcription of its target by transcriptional interference (described below) and by transcription attenuation (28). The 5Ј part of the icsA RNA forms two long hairpin motifs that presumably resemble an antiterminator structure.…”

Section: Transcription Terminationmentioning

confidence: 99%

“…This proposed mechanism is supported by structural probing experiments. (28). The 5Ј region of the newly transcribed icsA message forms the stem-loop structure AH1 (1), and, without binding to RnaG, another stem-loop (AH2) is formed.…”

Section: Transcription Terminationmentioning

confidence: 99%

cis-Antisense RNA, Another Level of Gene Regulation in Bacteria

Georg

Hess

2011

Microbiol Mol Biol Rev

361

348

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SUMMARY A substantial amount of antisense transcription is a hallmark of gene expression in eukaryotes. However, antisense transcription was first demonstrated in bacteria almost 50 years ago. The transcriptomes of bacteria as different as Helicobacter pylori , Bacillus subtilis , Escherichia coli , Synechocystis sp. strain PCC6803, Mycoplasma pneumoniae , Sinorhizobium meliloti , Geobacter sulfurreducens , Vibrio cholerae , Chlamydia trachomatis , Pseudomonas syringae , and Staphylococcus aureus have now been reported to contain antisense RNA (asRNA) transcripts for a high percentage of genes. Bacterial asRNAs share functional similarities with trans -acting regulatory RNAs, but in addition, they use their own distinct mechanisms. Among their confirmed functional roles are transcription termination, codegradation, control of translation, transcriptional interference, and enhanced stability of their respective target transcripts. Here, we review recent publications indicating that asRNAs occur as frequently in simple unicellular bacteria as they do in higher organisms, and we provide a comprehensive overview of the experimentally confirmed characteristics of asRNA actions and intimately linked quantitative aspects. Emerging functional data suggest that asRNAs in bacteria mediate a plethora of effects and are involved in far more processes than were previously anticipated. Thus, the functional impact of asRNAs should be considered when developing new strategies against pathogenic bacteria and when optimizing bacterial strains for biotechnology.

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“…On the other hand, under conditions of high levels of cysteine, transcription from the downstream S-box promoter tends to reduce the expression of ubiG mRNA. Similarly, antisense transcription from the icsA/ RnaG locus of virulence plasmid pINV of Shigella flexneri, allows controlling the expression of icsA mRNA, which encodes an invasion protein required for colonization of host by the bacterial pathogen [81]. This locus encodes a non-coding antisense RnaG RNA, which overlaps with icsA mRNA at the 5' end, and has been shown to cause premature termination of icsA mRNA following a transcriptional attenuation mechanism [81].…”

Section: Coupled Effect Of Transcriptional Interference and Antisensementioning

confidence: 99%

“…Similarly, antisense transcription from the icsA/ RnaG locus of virulence plasmid pINV of Shigella flexneri, allows controlling the expression of icsA mRNA, which encodes an invasion protein required for colonization of host by the bacterial pathogen [81]. This locus encodes a non-coding antisense RnaG RNA, which overlaps with icsA mRNA at the 5' end, and has been shown to cause premature termination of icsA mRNA following a transcriptional attenuation mechanism [81]. In addition to antisense RNA interaction mediated regulation, the stronger RnaG promoter exerts transcriptional interference on the weaker icsA promoter icsA, further reducing activity of the latter.…”

Section: Coupled Effect Of Transcriptional Interference and Antisensementioning

confidence: 99%

cis-Antisense RNA and Transcriptional Interference: Coupled Layers of Gene Regulation

2013

J Gene Ther

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Antisense transcription is omnipresent occurring broadly in most living organisms. Growing evidence suggests the presence of noncoding cis-antisense RNA's that can silence gene expression. Recent studies also indicate the role of transcriptional interference in regulating expression of neighboring genes arranged in convergent orientation. A combination of transcriptional interference and cis-antisense RNA interaction has the potential to add multiple-levels of regulation which can allow such a system to have a tunable and complex higher-order system response to environmental stimuli. This presents an important insight into the functional role of antisense transcription.

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A novel antisense RNA regulates at transcriptional level the virulence gene icsA of Shigella flexneri

Cited by 80 publications

References 57 publications

Dual RNA-seq of pathogen and host

Dual RNA-seq of pathogen and host

cis-Antisense RNA, Another Level of Gene Regulation in Bacteria

cis-Antisense RNA and Transcriptional Interference: Coupled Layers of Gene Regulation

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