Deep sequencing-based discovery of the Chlamydia trachomatis transcriptome

Albrecht, Marco; Sharma, Cynthia M.; Reinhardt, Richard; Vogel, Jörg; Rudel, Thomas

doi:10.1093/nar/gkp1032

Cited by 190 publications

(203 citation statements)

References 43 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%

“…Many of the pioneering studies were performed using pathogenic bacteria, including S. Typhi (Perkins et al, 2009), Bacillus anthracis (Passalacqua et al, 2009), Burkholderia cenocepacia (Yoder-Himes et al, 2009), Helicobacter pylori or Chlamydia trachomatis (Albrecht et al, 2010), and identified a plethora of novel genes including many new sRNAs (for reviews see (Croucher and Thomson, 2010;Guell et al, 2011;Sorek and Cossart, 2010). The original RNA-seq protocol has since been further modified to increase the informational output: For instance, the usage of a specific exonuclease in a method referred to as differential RNA-seq (dRNA-seq) allowed the selective degradation of processed RNA molecules leaving only primary transcripts, thereby enabling the identification of TSSs on a genome-wide scale .…”

Section: Strand-specificitymentioning

confidence: 99%

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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%

Section: Strand-specificitymentioning

confidence: 99%

Dual RNA-seq of pathogen and host

2012

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“…Analysis of the C. trachomatis transcriptome indicates that several of the BLAST-identified futalosine genes are co-transcribed (32). CT263, a protein of unknown function, is co-transcribed along with the predicted MqnD homolog (CT262).…”

Section: Bioinformatic Support Of Futalosine Pathway In Chlamydiaceae-mentioning

confidence: 99%

Structural and Biochemical Characterization of Chlamydia trachomatis Hypothetical Protein CT263 Supports That Menaquinone Synthesis Occurs through the Futalosine Pathway

Barta

Thomas

Yuan

et al. 2014

Journal of Biological Chemistry

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Background: Specific pathways and components for respiration in Chlamydia are poorly understood. Results: The C. trachomatis hypothetical protein CT263 crystal structure displays strong structural similarity with 5Ј-methylthioadenosine nucleosidase enzymes. Conclusion: Bioinformatic analyses and enzymatic characterization of CT263 suggest menaquinone biosynthesis proceeds through the futalosine pathway in Chlamydiaceae. Significance: Unique structural aspects of the CT263 active site can be leveraged to modify existing transition state inhibitors.

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“…In the past 10 years, the development of new approaches based on high-resolution tiling arrays and RNA deep sequencing (RNA-seq) has uncovered that a significant proportion (depending on the study, varying between 3% and >50%) of protein coding genes are also transcribed from the reverse complementary strand (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17). In most cases, overlapping transcription generates a noncoding antisense transcript whose size can vary between various tens of nucleotides (cisencoded small RNAs) to thousands of nucleotides (antisense RNAs).…”

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confidence: 99%

Genome-wide antisense transcription drives mRNA processing in bacteria

Lasa

Toledo‐Arana

Dobin

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

222

277

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RNA deep sequencing technologies are revealing unexpected levels of complexity in bacterial transcriptomes with the discovery of abundant noncoding RNAs, antisense RNAs, long 5′ and 3′ untranslated regions, and alternative operon structures. Here, by applying deep RNA sequencing to both the long and short RNA fractions (<50 nucleotides) obtained from the major human pathogen Staphylococcus aureus, we have detected a collection of short RNAs that is generated genome-wide through the digestion of overlapping sense/antisense transcripts by RNase III endoribonuclease. At least 75% of sense RNAs from annotated genes are subject to this mechanism of antisense processing. Removal of RNase III activity reduces the amount of short RNAs and is accompanied by the accumulation of discrete antisense transcripts. These results suggest the production of pervasive but hidden antisense transcription used to process sense transcripts by means of creating double-stranded substrates. This process of RNase III-mediated digestion of overlapping transcripts can be observed in several evolutionarily diverse Gram-positive bacteria and is capable of providing a unique genome-wide posttranscriptional mechanism to adjust mRNA levels.antisense RNA | overlapping transcription | RNA processing | posttranscriptional regulation | microRNA F or many years, the catalog of transcripts (transcriptome) produced by bacterial cells was limited to the transcription products of known annotated genes (mRNA), ribosomal RNA (rRNA), and transfer RNA (tRNA). In the past 10 years, the development of new approaches based on high-resolution tiling arrays and RNA deep sequencing (RNA-seq) has uncovered that a significant proportion (depending on the study, varying between 3% and >50%) of protein coding genes are also transcribed from the reverse complementary strand (1-17). In most cases, overlapping transcription generates a noncoding antisense transcript whose size can vary between various tens of nucleotides (cisencoded small RNAs) to thousands of nucleotides (antisense RNAs). The antisense transcript can cover the 5′ end, 3′ end, middle, entire gene, or even various contiguous genes. Alternatively, overlapping transcription can also be due to the overlap between long 5′ or 3′ UTRs of mRNAs transcribed in the opposite direction. Independent of the mechanism by which it is generated, overlapping transcription has been proposed to affect the expression of the target gene at different levels [for review, see Thomason and Storz (18)]. These mechanisms include: (i) the overlapped transcript affects the stability of the target RNA by either promoting (RNA degradation) or blocking (RNA stabilization) cleavage by endoribonucleases or exoribonucleases; (ii) the overlapped transcript induces a change in the structure of the mRNA that affects transcription termination (transcription attenuation); (iii) the overlapped transcript prevents RNA polymerase from binding or extending the transcript encoded in the opposite strand (transcription interference); and (iv) the overl...

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Deep sequencing-based discovery of the Chlamydia trachomatis transcriptome

Cited by 190 publications

References 43 publications

Dual RNA-seq of pathogen and host

Dual RNA-seq of pathogen and host

Structural and Biochemical Characterization of Chlamydia trachomatis Hypothetical Protein CT263 Supports That Menaquinone Synthesis Occurs through the Futalosine Pathway

Genome-wide antisense transcription drives mRNA processing in bacteria

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