Skip to main content
SpringerLink
Log in

The Primary Transcriptome and Noncoding RNA Repertoire of Helicobacter pylori

  • Chapter
  • First Online:
Helicobacter pylori Research

Abstract

The intense study of Helicobacter pylori, one of the most prevalent human pathogens, has contributed much to understanding of bacterial virulence mechanisms. While genome sequencing revealed a high genetic diversity among Helicobacter strains, its transcriptional organization has been less understood. The H. pylori genome encodes for only a small number of transcriptional regulators, and little is known about the role of posttranscriptional gene regulation and the mechanisms and functions of small regulatory RNAs (sRNAs) in Epsilonproteobacteria. Until recently, Helicobacter was even regarded as a bacterium without RNA-based regulation (riboregulation). However, the development of deep sequencing technology and its application to massively parallel high-throughput cDNA analysis (RNA-seq) has revolutionized transcriptome analysis of pro- and eukaryotes. A differential RNA-seq (dRNA-seq) study of H. pylori strain 26695 selective for primary transcriptome analysis allowed for genome-wide mapping of transcriptional start sites. This study also revealed an unexpectedly complex and compact transcriptional output from the small H. pylori genome. Besides an extensive antisense transcription, more than 60 sRNA candidates were identified, including potential regulators of cis- and trans-encoded target mRNAs. This indicates that posttranscriptional regulation represents an extensive layer of gene expression control in Helicobacter. In this chapter we review how RNA-seq has facilitated transcriptome annotation and identification of novel regulatory features in H. pylori and what is currently known about sRNAs in this widespread gastric pathogen.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Akada JK, Shirai M, Takeuchi H, Tsuda M, Nakazawa T (2000) Identification of the urease operon in Helicobacter pylori and its control by mRNA decay in response to pH. Mol Microbiol 36:1071–1084

    Article  CAS  PubMed  Google Scholar 

  • Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, Margalit H, Altuvia S (2001) Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 11:941–950

    Article  CAS  PubMed  Google Scholar 

  • Austin CM, Maier RJ (2013) Aconitase-mediated posttranscriptional regulation of Helicobacter pylori peptidoglycan deacetylase. J Bacteriol 195:5316–5322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Babitzke P, Romeo T (2007) CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 10:156–163

    Article  CAS  PubMed  Google Scholar 

  • Backofen R, Hess WR (2010) Computational prediction of sRNAs and their targets in bacteria. RNA Biol 7:33–42

    Article  CAS  PubMed  Google Scholar 

  • Baldwin DN, Shepherd B, Kraemer P, Hall MK, Sycuro LK, Pinto-Santini DM, Salama NR (2007) Identification of Helicobacter pylori genes that contribute to stomach colonization. Infect Immun 75:1005–1016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barnard FM, Loughlin MF, Fainberg HP, Messenger MP, Ussery DW, Williams P, Jenks PJ (2004) Global regulation of virulence and the stress response by CsrA in the highly adapted human gastric pathogen Helicobacter pylori. Mol Microbiol 51:15–32

    Article  CAS  PubMed  Google Scholar 

  • Barrick JE, Sudarsan N, Weinberg Z, Ruzzo WL, Breaker RR (2005) 6S RNA is a widespread regulator of eubacterial RNA polymerase that resembles an open promoter. RNA 11:774–784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barquist L, Vogel J (2015) Accelerating discovery and functional analysis of small RNAs with new technologies. Annu Rev Genet 49:367–394

    Article  CAS  PubMed  Google Scholar 

  • Benjamin JA, Masse E (2014) The iron-sensing aconitase B binds its own mRNA to prevent sRNA-induced mRNA cleavage. Nucleic Acids Res 42:10023–10036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bensing BA, Meyer BJ, Dunny GM (1996) Sensitive detection of bacterial transcription initiation sites and differentiation from RNA processing sites in the pheromone-induced plasmid transfer system of Enterococcus faecalis. Proc Natl Acad Sci U S A 93:7794–7799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berk AJ, Sharp PA (1977) Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell 12:721–732

    Article  CAS  PubMed  Google Scholar 

  • Bischler T, Tan HS, Nieselt K, Sharma CM (2015) Differential RNA-seq (dRNA-seq) for annotation of transcriptional start sites and small RNAs in Helicobacter pylori. Methods 86:89–101

    Article  CAS  PubMed  Google Scholar 

  • Boisset S, Geissmann T, Huntzinger E, Fechter P, Bendridi N, Possedko M, Chevalier C, Helfer AC, Benito Y, Jacquier A, Gaspin C, Vandenesch F, Romby P (2007) Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 21:1353–1366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borries A, Vogel J, Sharma CM (2010) Differential RNA sequencing (dRNA-seq): deep-sequencing based analysis of primary transcriptomes. In: Harbers M, Kahl G (eds) Tag-based approaches for next-generation sequencing. Wiley-Blackwell-VCH, Hoboken

    Google Scholar 

  • Brantl S (2007) Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr Opin Microbiol 10:102–109

    Article  CAS  PubMed  Google Scholar 

  • Burgess RR, Anthony L (2001) How sigma docks to RNA polymerase and what sigma does. Curr Opin Microbiol 4:126–131

    Article  CAS  PubMed  Google Scholar 

  • Bury-Mone S, Thiberge JM, Contreras M, Maitournam A, Labigne A, De Reuse H (2004) Responsiveness to acidity via metal ion regulators mediates virulence in the gastric pathogen Helicobacter pylori. Mol Microbiol 53:623–638

    Article  CAS  PubMed  Google Scholar 

  • Butcher J, Stintzi A (2013) The transcriptional landscape of Campylobacter jejuni under iron replete and iron limited growth conditions. PLoS One 8:e79475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caron MP, Lafontaine DA, Masse E (2010) Small RNA-mediated regulation at the level of transcript stability. RNA Biol 7:140–144

    Article  CAS  PubMed  Google Scholar 

  • Cavanagh AT, Wassarman KM (2014) 6S RNA, a global regulator of transcription in Escherichia coli, Bacillus subtilis, and beyond. Annu Rev Microbiol 68:45–60

    Article  CAS  PubMed  Google Scholar 

  • Chao Y, Vogel J (2010) The role of Hfq in bacterial pathogens. Curr Opin Microbiol 13:24–33

    Article  CAS  PubMed  Google Scholar 

  • Chaudhuri RR, Yu L, Kanji A, Perkins TT, Gardner PP, Choudhary J, Maskell DJ, Grant AJ (2011) Quantitative RNA-seq analysis of the transcriptome of Campylobacter jejuni. Microbiology 157:2922–2932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chevalier C, Huntzinger E, Fechter P, Boisset S, Vandenesch F, Romby P, Geissmann T (2008) Staphylococcus aureus endoribonuclease III purification and properties. Methods Enzymol 447:309–327

    Article  CAS  PubMed  Google Scholar 

  • Cho BK, Zengler K, Qiu Y, Park YS, Knight EM, Barrett CL, Gao Y, Palsson BO (2009) The transcription unit architecture of the Escherichia coli genome. Nat Biotechnol 27:1043–1049

    Article  CAS  PubMed  Google Scholar 

  • Condon C (2010) What is the role of RNase J in mRNA turnover? RNA Biol 7:316–321

    Article  CAS  PubMed  Google Scholar 

  • Croucher NJ, Thomson NR (2010) Studying bacterial transcriptomes using RNA-seq. Curr Opin Microbiol 13:619–624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Croxen MA, Sisson G, Melano R, Hoffman PS (2006) The Helicobacter pylori chemotaxis receptor TlpB (HP0103) is required for pH taxis and for colonization of the gastric mucosa. J Bacteriol 188:2656–2665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Croxen MA, Ernst PB, Hoffman PS (2007) Antisense RNA modulation of alkyl hydroperoxide reductase levels in Helicobacter pylori correlates with organic peroxide toxicity but not infectivity. J Bacteriol 189:3359–3368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Danielli A, Scarlato V (2010) Regulatory circuits in Helicobacter pylori: network motifs and regulators involved in metal-dependent responses. FEMS Microbiol Rev 34:738–752

    Article  CAS  PubMed  Google Scholar 

  • Danielli A, Amore G, Scarlato V (2010) Built shallow to maintain homeostasis and persistent infection: insight into the transcriptional regulatory network of the gastric human pathogen Helicobacter pylori. PLoS Pathog 6:e1000938

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Davies BW, Kohrer C, Jacob AI, Simmons LA, Zhu J, Aleman LM, Rajbhandary UL, Walker GC (2010) Role of Escherichia coli YbeY, a highly conserved protein, in rRNA processing. Mol Microbiol 78:506–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dorleans A, Li de la Sierra-Gallay I, Piton J, Zig L, Gilet L, Putzer H, Condon C (2011) Molecular basis for the recognition and cleavage of RNA by the bifunctional 5′–3′ exo/endoribonuclease RNase J. Structure 19:1252–1261

    Article  CAS  PubMed  Google Scholar 

  • Douillard FP, Ryan KA, Caly DL, Hinds J, Witney AA, Husain SE, O’Toole PW (2008) Posttranscriptional regulation of flagellin synthesis in Helicobacter pylori by the RpoN chaperone HP0958. J Bacteriol 190:7975–7984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dugar G, Herbig A, Forstner KU, Heidrich N, Reinhardt R, Nieselt K, Sharma CM (2013) High-resolution transcriptome maps reveal strain-specific regulatory features of multiple campylobacter jejuni isolates. PLoS Genet 9:e1003495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faucher SP, Friedlander G, Livny J, Margalit H, Shuman HA (2010) Legionella pneumophila 6S RNA optimizes intracellular multiplication. Proc Natl Acad Sci U S A 107:7533–7538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forsyth MH, Cover TL (1999) Mutational analysis of the vacA promoter provides insight into gene transcription in Helicobacter pylori. J Bacteriol 181:2261–2266

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fozo EM, Hemm MR, Storz G (2008a) Small toxic proteins and the antisense RNAs that repress them. Microbiol Mol Biol Rev 72:579–589, Table of Contents

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fozo EM, Kawano M, Fontaine F, Kaya Y, Mendieta KS, Jones KL, Ocampo A, Rudd KE, Storz G (2008b) Repression of small toxic protein synthesis by the Sib and OhsC small RNAs. Mol Microbiol 70:1076–1093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frohlich KS, Vogel J (2009) Activation of gene expression by small RNA. Curr Opin Microbiol 12:674–682

    Article  PubMed  CAS  Google Scholar 

  • Georg J, Hess WR (2011) cis-antisense RNA, another level of gene regulation in bacteria. Microbiol Mol Biol Rev 75:286–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grinwald M, Ron EZ (2013) The Escherichia coli translation-associated heat shock protein YbeY is involved in rRNA transcription antitermination. PLoS One 8:e62297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guell M, van Noort V, Yus E, Chen WH, Leigh-Bell J, Michalodimitrakis K, Yamada T, Arumugam M, Doerks T, Kuhner S, Rode M, Suyama M, Schmidt S, Gavin AC, Bork P, Serrano L (2009) Transcriptome complexity in a genome-reduced bacterium. Science 326:1268–1271

    Article  PubMed  CAS  Google Scholar 

  • Haddad N, Tresse O, Rivoal K, Chevret D, Nonglaton Q, Burns CM, Prevost H, Cappelier JM (2012) Polynucleotide phosphorylase has an impact on cell biology of Campylobacter jejuni. Front Cell Infect Microbiol 2:30

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hajnsdorf E, Boni IV (2012) Multiple activities of RNA-binding proteins S1 and Hfq. Biochimie 94:1544–1553

    Article  CAS  PubMed  Google Scholar 

  • Heidrich N, Dugar G, Vogel J, Sharma CM (2015) Investigating CRISPR RNA biogenesis and function using RNA-seq. Methods Mol Biol 1311:1–21

    Article  PubMed  Google Scholar 

  • Heroven AK, Bohme K, Dersch P (2012) The Csr/Rsm system of Yersinia and related pathogens: a post-transcriptional strategy for managing virulence. RNA Biol 9:379–391

    Article  CAS  PubMed  Google Scholar 

  • Huntzinger E, Boisset S, Saveanu C, Benito Y, Geissmann T, Namane A, Lina G, Etienne J, Ehresmann B, Ehresmann C, Jacquier A, Vandenesch F, Romby P (2005) Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J 24:824–835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacob AI, Kohrer C, Davies BW, RajBhandary UL, Walker GC (2013) Conserved bacterial RNase YbeY plays key roles in 70S ribosome quality control and 16S rRNA maturation. Mol Cell 49:427–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Josenhans C, Beier D, Linz B, Meyer TF, Suerbaum S (2007) Pathogenomics of helicobacter. Int J Med Microbiol 297:589–600

    Article  CAS  PubMed  Google Scholar 

  • Jousselin A, Metzinger L, Felden B (2009) On the facultative requirement of the bacterial RNA chaperone, Hfq. Trends Microbiol 17:399–405

    Article  CAS  PubMed  Google Scholar 

  • Kao CY, Sheu BS, Wu JJ (2014) CsrA regulates helicobacter pylori J99 motility and adhesion by controlling flagella formation. Helicobacter 19:443–454

    Article  CAS  PubMed  Google Scholar 

  • König J, Zarnack K, Luscombe NM, Ule J (2012) Protein-RNA interactions: new genomic technologies and perspectives. Nat Rev Genet 13:77–83

    Article  PubMed  CAS  Google Scholar 

  • Kortmann J, Narberhaus F (2012) Bacterial RNA thermometers: molecular zippers and switches. Nat Rev Microbiol 10:255–265

    Article  CAS  PubMed  Google Scholar 

  • Lee KY, Lee KY, Kim JH, Lee IG, Lee SH, Sim DW, Won HS, Lee BJ (2015) Structure-based functional identification of Helicobacter pylori HP0268 as a nuclease with both DNA nicking and RNase activities. Nucleic Acids Res 43:5194–5207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lertsethtakarn P, Ottemann KM, Hendrixson DR (2011) Motility and chemotaxis in Campylobacter and Helicobacter. Annu Rev Microbiol 65:389–410

    Article  CAS  PubMed  Google Scholar 

  • Lin YF, A DR, Guan S, Mamanova L, McDowall KJ (2013) A combination of improved differential and global RNA-seq reveals pervasive transcription initiation and events in all stages of the life-cycle of functional RNAs in Propionibacterium acnes, a major contributor to wide-spread human disease. BMC Genomics 14:620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lioliou E, Sharma CM, Caldelari I, Helfer AC, Fechter P, Vandenesch F, Vogel J, Romby P (2012) Global regulatory functions of the Staphylococcus aureus endoribonuclease III in gene expression. PLoS Genet 8:e1002782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livny J, Brencic A, Lory S, Waldor MK (2006) Identification of 17 Pseudomonas aeruginosa sRNAs and prediction of sRNA-encoding genes in 10 diverse pathogens using the bioinformatic tool sRNAPredict2. Nucleic Acids Res 34:3484–3493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lundin A, Nilsson C, Gerhard M, Andersson DI, Krabbe M, Engstrand L (2003) The NudA protein in the gastric pathogen Helicobacter pylori is an ubiquitous and constitutively expressed dinucleoside polyphosphate hydrolase. J Biol Chem 278:12574–12578

    Article  CAS  PubMed  Google Scholar 

  • Mao F, Dam P, Chou J, Olman V, Xu Y (2009) DOOR: a database for prokaryotic operons. Nucleic Acids Res 37:D459–D463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mathy N, Hebert A, Mervelet P, Benard L, Dorleans A, Li de la Sierra-Gallay I, Noirot P, Putzer H, Condon C (2010) Bacillus subtilis ribonucleases J1 and J2 form a complex with altered enzyme behaviour. Mol Microbiol 75:489–498

    Article  CAS  PubMed  Google Scholar 

  • McGee DJ, Langford ML, Watson EL, Carter JE, Chen YT, Ottemann KM (2005) Colonization and inflammation deficiencies in Mongolian gerbils infected by Helicobacter pylori chemotaxis mutants. Infect Immun 73:1820–1827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendoza-Vargas A, Olvera L, Olvera M, Grande R, Vega-Alvarado L, Taboada B, Jimenez-Jacinto V, Salgado H, Juarez K, Contreras-Moreira B, Huerta AM, Collado-Vides J, Morett E (2009) Genome-wide identification of transcription start sites, promoters and transcription factor binding sites in E. coli. PLoS One 4:e7526

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Merrell DS, Goodrich ML, Otto G, Tompkins LS, Falkow S (2003) pH-regulated gene expression of the gastric pathogen Helicobacter pylori. Infect Immun 71:3529–3539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitarai N, Andersson AM, Krishna S, Semsey S, Sneppen K (2007) Efficient degradation and expression prioritization with small RNAs. Phys Biol 4:164–171

    Article  CAS  PubMed  Google Scholar 

  • Mitobe J, Yanagihara I, Ohnishi K, Yamamoto S, Ohnishi M, Ishihama A, Watanabe H (2011) RodZ regulates the post-transcriptional processing of the Shigella sonnei type III secretion system. EMBO Rep 12:911–916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moll I, Grill S, Gualerzi CO, Blasi U (2002) Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Mol Microbiol 43:239–246

    Article  CAS  PubMed  Google Scholar 

  • Moll I, Hirokawa G, Kiel MC, Kaji A, Blasi U (2004) Translation initiation with 70S ribosomes: an alternative pathway for leaderless mRNAs. Nucleic Acids Res 32:3354–3363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morita T, Maki K, Aiba H (2005) RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev 19:2176–2186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moxon R, Bayliss C, Hood D (2006) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu Rev Genet 40:307–333

    Article  CAS  PubMed  Google Scholar 

  • Pandey SP, Minesinger BK, Kumar J, Walker GC (2011) A highly conserved protein of unknown function in Sinorhizobium meliloti affects sRNA regulation similar to Hfq. Nucleic Acids Res 39:4691–4708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pandey SP, Winkler JA, Li H, Camacho DM, Collins JJ, Walker GC (2014) Central role for RNase YbeY in Hfq-dependent and Hfq-independent small-RNA regulation in bacteria. BMC Genomics 15:121

    Article  PubMed  PubMed Central  Google Scholar 

  • Papenfort K, Vogel J (2010) Regulatory RNA in bacterial pathogens. Cell Host Microbe 8:116–127

    Article  CAS  PubMed  Google Scholar 

  • Passalacqua KD, Varadarajan A, Weist C, Ondov BD, Byrd B, Read TD, Bergman NH (2012) Strand-specific RNA-seq reveals ordered patterns of sense and antisense transcription in Bacillus anthracis. PLoS One 7:e43350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira L, Hoover TR (2005) Stable accumulation of sigma54 in Helicobacter pylori requires the novel protein HP0958. J Bacteriol 187:4463–4469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira LE, Tsang J, Mrazek J, Hoover TR (2011) The zinc-ribbon domain of Helicobacter pylori HP0958: requirement for RpoN accumulation and possible roles of homologs in other bacteria. Microb Inform Exp 1:1–10

    Article  PubMed  CAS  Google Scholar 

  • Pernitzsch SR, Tirier SM, Beier D, Sharma CM (2014) A variable homopolymeric G-repeat defines small RNA-mediated posttranscriptional regulation of a chemotaxis receptor in Helicobacter pylori. Proc Natl Acad Sci U S A 111:E501–E510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petersen L, Larsen TS, Ussery DW, On SL, Krogh A (2003) RpoD promoters in Campylobacter jejuni exhibit a strong periodic signal instead of a -35 box. J Mol Biol 326:1361–1372

    Article  CAS  PubMed  Google Scholar 

  • Porcelli I, Reuter M, Pearson BM, Wilhelm T, van Vliet AH (2013) Parallel evolution of genome structure and transcriptional landscape in the Epsilonproteobacteria. BMC Genomics 14:616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rader BA, Wreden C, Hicks KG, Sweeney EG, Ottemann KM, Guillemin K (2011) Helicobacter pylori perceives the quorum-sensing molecule AI-2 as a chemorepellent via the chemoreceptor TlpB. Microbiology 157:2445–2455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramakrishnan V (2002) Ribosome structure and the mechanism of translation. Cell 108:557–572

    Article  CAS  PubMed  Google Scholar 

  • Rasouly A, Schonbrun M, Shenhar Y, Ron EZ (2009) YbeY, a heat shock protein involved in translation in Escherichia coli. J Bacteriol 191:2649–2655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rasouly A, Davidovich C, Ron EZ (2010) The heat shock protein YbeY is required for optimal activity of the 30S ribosomal subunit. J Bacteriol 192:4592–4596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Redko Y, Aubert S, Stachowicz A, Lenormand P, Namane A, Darfeuille F, Thibonnier M, De Reuse H (2013) A minimal bacterial RNase J-based degradosome is associated with translating ribosomes. Nucleic Acids Res 41:288–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richards J, Liu Q, Pellegrini O, Celesnik H, Yao S, Bechhofer DH, Condon C, Belasco JG (2011) An RNA pyrophosphohydrolase triggers 5′-exonucleolytic degradation of mRNA in Bacillus subtilis. Mol Cell 43:940–949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rieder R, Reinhardt R, Sharma CM, Vogel J (2012) Experimental tools to identify RNA-protein interactions in Helicobacter pylori. RNA Biol 9:520–531

    Article  CAS  PubMed  Google Scholar 

  • Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS (2002) Comparative genomics of thiamin biosynthesis in procaryotes. New genes and regulatory mechanisms. J Biol Chem 277:48949–48959

    Article  CAS  PubMed  Google Scholar 

  • Romeo T, Vakulskas CA, Babitzke P (2013) Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems. Environ Microbiol 15:313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenzweig JA, Chopra AK (2013) The exoribonuclease polynucleotide phosphorylase influences the virulence and stress responses of yersiniae and many other pathogens. Front Cell Infect Microbiol 3:81

    PubMed  PubMed Central  Google Scholar 

  • Roux CM, DeMuth JP, Dunman PM (2011) Characterization of components of the Staphylococcus aureus mRNA degradosome holoenzyme-like complex. J Bacteriol 193:5520–5526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryan KA, Karim N, Worku M, Moore SA, Penn CW, O’Toole PW (2005) HP0958 is an essential motility gene in Helicobacter pylori. FEMS Microbiol Lett 248:47–55

    Article  CAS  PubMed  Google Scholar 

  • Sachs G, Weeks DL, Melchers K, Scott DR (2003) The gastric biology of Helicobacter pylori. Annu Rev Physiol 65:349–369

    Article  CAS  PubMed  Google Scholar 

  • Said N, Rieder R, Hurwitz R, Deckert J, Urlaub H, Vogel J (2009) In vivo expression and purification of aptamer-tagged small RNA regulators. Nucleic Acids Res 37:e133

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Salama NR, Hartung ML, Muller A (2013) Life in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori. Nat Rev Microbiol 11:385–399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salgado H, Peralta-Gil M, Gama-Castro S, Santos-Zavaleta A, Muniz-Rascado L, Garcia-Sotelo JS, Weiss V, Solano-Lira H, Martinez-Flores I, Medina-Rivera A, Salgado-Osorio G, Alquicira-Hernandez S, Alquicira-Hernandez K, Lopez-Fuentes A, Porron-Sotelo L, Huerta AM, Bonavides-Martinez C, Balderas-Martinez YI, Pannier L, Olvera M, Labastida A, Jimenez-Jacinto V, Vega-Alvarado L, Del Moral-Chavez V, Hernandez-Alvarez A, Morett E, Collado-Vides J (2013) RegulonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more. Nucleic Acids Res 41:D203–D213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saliba AE, Westermann AJ, Gorski SA, Vogel J (2014) Single-cell RNA-seq: advances and future challenges. Nucleic Acids Res 42:8845–8860

    Article  PubMed  PubMed Central  Google Scholar 

  • Serganov A, Nudler E (2013) A decade of riboswitches. Cell 152:17–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sesto N, Wurtzel O, Archambaud C, Sorek R, Cossart P (2013) The excludon: a new concept in bacterial antisense RNA-mediated gene regulation. Nat Rev Microbiol 11:75–82

    Article  CAS  PubMed  Google Scholar 

  • Seyll E, Van Melderen L (2013) The ribonucleoprotein Csr network. Int J Mol Sci 14:22117–22131

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sharma CM, Vogel J (2009) Experimental approaches for the discovery and characterization of regulatory small RNA. Curr Opin Microbiol 12:536–546

    Article  CAS  PubMed  Google Scholar 

  • Sharma CM, Vogel J (2014) Differential RNA-seq: the approach behind and the biological insight gained. Curr Opin Microbiol 19C:97–105

    Article  CAS  Google Scholar 

  • Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, Sittka A, Chabas S, Reiche K, Hackermuller J, Reinhardt R, Stadler PF, Vogel J (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464:250–255

    Article  CAS  PubMed  Google Scholar 

  • Sharwood RE, Hotto AM, Bollenbach TJ, Stern DB (2011) Overaccumulation of the chloroplast antisense RNA AS5 is correlated with decreased abundance of 5S rRNA in vivo and inefficient 5S rRNA maturation in vitro. RNA 17:230–243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shirai M, Fujinaga R, Akada JK, Nakazawa T (1999) Activation of Helicobacter pylori ureA promoter by a hybrid Escherichia coli-H. pylori rpoD gene in E. coli. Gene 239:351–359

    Article  CAS  PubMed  Google Scholar 

  • Singh N, Wade JT (2014) Identification of regulatory RNA in bacterial genomes by genome-scale mapping of transcription start sites. Methods Mol Biol 1103:1–10

    Article  CAS  PubMed  Google Scholar 

  • Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, Binnewies TT, Hinton JC, Vogel J (2008) Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 4:e1000163

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sorek R, Cossart P (2010) Prokaryotic transcriptomics: a new view on regulation, physiology and pathogenicity. Nat Rev Genet 11:9–16

    Article  CAS  PubMed  Google Scholar 

  • Spohn G, Scarlato V (1999) Motility of Helicobacter pylori is coordinately regulated by the transcriptional activator FlgR, an NtrC homolog. J Bacteriol 181:593–599

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spohn G, Beier D, Rappuoli R, Scarlato V (1997) Transcriptional analysis of the divergent cagAB genes encoded by the pathogenicity island of Helicobacter pylori. Mol Microbiol 26:361–372

    Article  CAS  PubMed  Google Scholar 

  • Storz G, Vogel J, Wassarman KM (2011) Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 43:880–891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suerbaum S, Josenhans C (2007) Helicobacter pylori evolution and phenotypic diversification in a changing host. Nat Rev Microbiol 5:441–452

    Article  CAS  PubMed  Google Scholar 

  • Tang Y, Guest JR (1999) Direct evidence for mRNA binding and post-transcriptional regulation by Escherichia coli aconitases. Microbiology 145(Pt 11):3069–3079

    Article  CAS  PubMed  Google Scholar 

  • Taveirne ME, Theriot CM, Livny J, DiRita VJ (2013) The complete Campylobacter jejuni transcriptome during colonization of a natural host determined by RNAseq. PLoS One 8:e73586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thibonnier M, Thiberge JM, De Reuse H (2008) Trans-translation in Helicobacter pylori: essentiality of ribosome rescue and requirement of protein tagging for stress resistance and competence. PLoS One 3:e3810

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thibonnier M, Aubert S, Ecobichon C, De Reuse H (2010) Study of the functionality of the Helicobacter pylori trans-translation components SmpB and SsrA in an heterologous system. BMC Microbiol 10:91

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thomason MK, Storz G (2010) Bacterial antisense RNAs: how many are there, and what are they doing? Annu Rev Genet 44:167–188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JA, Radonovich MF, Salzman NP (1979) Characterization of the 5′-terminal structure of simian virus 40 early mRNA’s. J Virol 31:437–446

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson LJ, Merrell DS, Neilan BA, Mitchell H, Lee A, Falkow S (2003) Gene expression profiling of Helicobacter pylori reveals a growth-phase-dependent switch in virulence gene expression. Infect Immun 71:2643–2655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD, Ketchum KA, Klenk HP, Gill S, Dougherty BA, Nelson K, Quackenbush J, Zhou L, Kirkness EF, Peterson S, Loftus B, Richardson D, Dodson R, Khalak HG, Glodek A, McKenney K, Fitzegerald LM, Lee N, Adams MD, Hickey EK, Berg DE, Gocayne JD, Utterback TR, Peterson JD, Kelley JM, Cotton MD, Weidman JM, Fujii C, Bowman C, Watthey L, Wallin E, Hayes WS, Borodovsky M, Karp PD, Smith HO, Fraser CM, Venter JC (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539–547

    Article  CAS  PubMed  Google Scholar 

  • Tsao MY, Lin TL, Hsieh PF, Wang JT (2009) The 3′-to-5′ exoribonuclease (encoded by HP1248) of Helicobacter pylori regulates motility and apoptosis-inducing genes. J Bacteriol 191:2691–2702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogel J, Luisi BF (2011) Hfq and its constellation of RNA. Nat Rev Microbiol 9:578–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jager JG, Huttenhofer A, Wagner EG (2003) RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res 31:6435–6443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wade JT, Grainger DC (2014) Pervasive transcription: illuminating the dark matter of bacterial transcriptomes. Nat Rev Microbiol 12:647–653

    Article  CAS  PubMed  Google Scholar 

  • Wagner EG, Unoson C (2012) The toxin-antitoxin system tisB-istR1: expression, regulation, and biological role in persister phenotypes. RNA Biol 9:1513–1519

    Article  CAS  PubMed  Google Scholar 

  • Wagner EG, Altuvia S, Romby P (2002) Antisense RNAs in bacteria and their genetic elements. Adv Genet 46:361–398

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wassarman KM, Saecker RM (2006) Synthesis-mediated release of a small RNA inhibitor of RNA polymerase. Science 314:1601–1603

    Article  CAS  PubMed  Google Scholar 

  • Waters LS, Storz G (2009) Regulatory RNAs in bacteria. Cell 136:615–628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen Y, Marcus EA, Matrubutham U, Gleeson MA, Scott DR, Sachs G (2003) Acid-adaptive genes of Helicobacter pylori. Infect Immun 71:5921–5939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen Y, Feng J, Scott DR, Marcus EA, Sachs G (2011) A cis-encoded antisense small RNA regulated by the HP0165-HP0166 two-component system controls expression of ureB in Helicobacter pylori. J Bacteriol 193:40–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen Y, Feng J, Sachs G (2013) Helicobacter pylori 5′ureB-sRNA, a cis-encoded antisense small RNA, negatively regulates ureAB expression by transcription termination. J Bacteriol 195:444–452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westermann AJ, Gorski SA, Vogel J (2012) Dual RNA-seq of pathogen and host. Nat Rev Microbiol 10:618–630

    Article  CAS  PubMed  Google Scholar 

  • Williams SM, Chen YT, Andermann TM, Carter JE, McGee DJ, Ottemann KM (2007) Helicobacter pylori chemotaxis modulates inflammation and bacterium-gastric epithelium interactions in infected mice. Infect Immun 75:3747–3757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Windbichler N, Schroeder R (2006) Isolation of specific RNA-binding proteins using the streptomycin-binding RNA aptamer. Nat Protoc 1:637–640

    Article  CAS  PubMed  Google Scholar 

  • Wosten MM, Boeve M, Koot MG, van Nuenen AC, van der Zeijst BA (1998) Identification of Campylobacter jejuni promoter sequences. J Bacteriol 180:594–599

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wurtzel O, Sapra R, Chen F, Zhu Y, Simmons BA, Sorek R (2010) A single-base resolution map of an archaeal transcriptome. Genome Res 20:133–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao B, Li W, Guo G, Li B, Liu Z, Jia K, Guo Y, Mao X, Zou Q (2009a) Identification of small noncoding RNAs in Helicobacter pylori by a bioinformatics-based approach. Curr Microbiol 58:258–263

    Article  CAS  PubMed  Google Scholar 

  • Xiao B, Li W, Guo G, Li BS, Liu Z, Tang B, Mao XH, Zou QM (2009b) Screening and identification of natural antisense transcripts in Helicobacter pylori by a novel approach based on RNase I protection assay. Mol Biol Rep 36:1853–1858

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Research Center for Infectious Diseases (ZINF), University of Würzburg, Josef-Schneider-Straße 2/D15, 97080, Würzburg, Germany

    Sandy R. Pernitzsch & Cynthia M. Sharma

  2. INSERM U869, University of Bordeaux, 146 rue Léo Saignat, 33076, Bordeaux, France

    Fabien Darfeuille

Authors
  1. Sandy R. Pernitzsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fabien Darfeuille
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cynthia M. Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cynthia M. Sharma .

Editor information

Editors and Affiliations

  1. Division of Microbiology;Dept of Biology, Friedrich Alexander Univ;Erlangen-Nuremb, Erlangen, Bayern, Germany

    Steffen Backert

  2. Dept of Medicine-Gastroenteology, Baylor College of Medicine, Houston, USA

    Yoshio Yamaoka

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Japan

About this chapter

Cite this chapter

Pernitzsch, S.R., Darfeuille, F., Sharma, C.M. (2016). The Primary Transcriptome and Noncoding RNA Repertoire of Helicobacter pylori . In: Backert, S., Yamaoka, Y. (eds) Helicobacter pylori Research. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55936-8_8

Download citation

Publish with us

Policies and ethics

Search

Navigation