RNA-binding proteins involved in post-transcriptional regulation in bacteria

Post-transcriptional regulation is a very important mechanism to control gene expression in changing environments. In the past decade, a lot of interest has been directed toward the role of small RNAs (sRNAs) in bacterial post-transcriptional regulation. However, sRNAs are not the only molecules controlling gene expression at this level, RNA-binding proteins (RBPs) play an important role as well. CsrA and Hfq are the two best studied bacterial proteins of this type, but recently, additional proteins involved in post-transcriptional control have been identified. This review focuses on the general working mechanisms of post-transcriptionally active RBPs, which include (i) adaptation of the susceptibility of mRNAs and sRNAs to RNases, (ii) modulating the accessibility of the ribosome binding site of mRNAs, (iii) recruiting and assisting in the interaction of mRNAs with other molecules and (iv) regulating transcription terminator/antiterminator formation, and gives an overview of both the well-studied and the newly identified proteins that are involved in post-transcriptional regulatory processes. Additionally, the post-transcriptional mechanisms by which the expression or the activity of these proteins is regulated, are described. For many of the newly identified proteins, however, mechanistic questions remain. Most likely, more post-transcriptionally active proteins will be identified in the future.

[1]  É. Massé,et al.  Noncanonical repression of translation initiation through small RNA recruitment of the RNA chaperone Hfq. , 2012, Genes & development.

[2]  J. Belasco,et al.  Lost in translation: the influence of ribosomes on bacterial mRNA decay. , 2005, Genes & development.

[3]  N. Windbichler,et al.  Isolation of small RNA-binding proteins from E. coli: Evidence for frequent interaction of RNAs with RNA polymerase , 2008, RNA biology.

[4]  W. W. Lathem,et al.  Post-Transcriptional Regulation of Gene Expression in Yersinia Species , 2012, Front. Cell. Inf. Microbio..

[5]  A. Camilli,et al.  A broadening world of bacterial small RNAs. , 2010, Current opinion in microbiology.

[6]  Stanley N. Cohen,et al.  Escherichia coli Poly(A)-binding Proteins That Interact with Components of Degradosomes or Impede RNA Decay Mediated by Polynucleotide Phosphorylase and RNase E* , 2001, The Journal of Biological Chemistry.

[7]  V. Stewart,et al.  RNA sequence requirements for NasR-mediated, nitrate-responsive transcription antitermination of the Klebsiella oxytoca M5al nasF operon leader. , 1999, Journal of molecular biology.

[8]  S. Woodson,et al.  Major role for mRNA binding and restructuring in sRNA recruitment by Hfq. , 2011, RNA.

[9]  A. von Haeseler,et al.  Genomic SELEX for Hfq-binding RNAs identifies genomic aptamers predominantly in antisense transcripts , 2010, Nucleic acids research.

[10]  I. Boni,et al.  Multiple activities of RNA-binding proteins S1 and Hfq. , 2012, Biochimie.

[11]  D. B. Kearns,et al.  CsrA–FliW interaction governs flagellin homeostasis and a checkpoint on flagellar morphogenesis in Bacillus subtilis , 2011, Molecular microbiology.

[12]  T. van Biesen,et al.  Degradation of FinP antisense RNA from F-like plasmids: the RNA-binding protein, FinO, protects FinP from ribonuclease E. , 1999, Journal of molecular biology.

[13]  G. Storz,et al.  The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. , 2002, Molecular cell.

[14]  B. Rak,et al.  Regulation of the bgl operon of Escherichia coli by transcriptional antitermination. , 1988, The EMBO journal.

[15]  S. C. Viegas,et al.  The role of RNases in the regulation of small RNAs. , 2014, Current opinion in microbiology.

[16]  J. Vogel,et al.  Targeted decay of a regulatory small RNA by an adaptor protein for RNase E and counteraction by an anti-adaptor RNA. , 2013, Genes & development.

[17]  A. Subramanian Structure and functions of ribosomal protein S1. , 1983, Progress in nucleic acid research and molecular biology.

[18]  S. Porwollik,et al.  Global regulation by CsrA in Salmonella typhimurium , 2003, Molecular microbiology.

[19]  T. Afonyushkin,et al.  Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs. , 2003, RNA.

[20]  Ö. Melefors,et al.  The RNA binding protein CsrA controls cyclic di‐GMP metabolism by directly regulating the expression of GGDEF proteins , 2008, Molecular microbiology.

[21]  M. Liu,et al.  The RNA Chaperone Hfq Is Involved in Stress Tolerance and Virulence in Uropathogenic Proteus mirabilis , 2014, PloS one.

[22]  Christopher A. Vakulskas,et al.  A novel CsrA titration mechanism regulates fimbrial gene expression in Salmonella typhimurium , 2013, The EMBO journal.

[23]  E. Pérez-Rueda,et al.  The Repertoire of DNA-Binding Transcription Factors in Prokaryotes: Functional and Evolutionary Lessons , 2012, Science progress.

[24]  H. Noller,et al.  Footprinting mRNA‐ribosome complexes with chemical probes. , 1994, The EMBO journal.

[25]  E. Sonnleitner,et al.  Distinct and overlapping binding sites of Pseudomonas aeruginosa Hfq and RsmA proteins on the non-coding RNA RsmY. , 2007, Biochemical and biophysical research communications.

[26]  CspC regulates rpoS transcript levels and complements hfq deletions. , 2010, Research in microbiology.

[27]  I. Boni,et al.  Hfq affects mRNA levels independently of degradation , 2010, BMC Molecular Biology.

[28]  Xin Wang,et al.  A novel sRNA component of the carbon storage regulatory system of Escherichia coli , 2003, Molecular microbiology.

[29]  J. Mekalanos,et al.  The Highly Conserved Bacterial RNase YbeY Is Essential in Vibrio cholerae, Playing a Critical Role in Virulence, Stress Regulation, and RNA Processing , 2014, PLoS pathogens.

[30]  I. Artsimovitch,et al.  Termination and antitermination: RNA polymerase runs a stop sign , 2011, Nature Reviews Microbiology.

[31]  P. Babitzke,et al.  RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. , 2005, RNA.

[32]  Li Xu,et al.  The Two-Component GacS-GacA System Activates lipA Translation by RsmE but Not RsmA in Pseudomonas protegens Pf-5 , 2014, Applied and Environmental Microbiology.

[33]  P. Babitzke,et al.  Complex regulation of the global regulatory gene csrA: CsrA‐mediated translational repression, transcription from five promoters by Eσ70 and EσS, and indirect transcriptional activation by CsrA , 2011, Molecular microbiology.

[34]  Lourdes M. Aleman,et al.  Role of Escherichia coli YbeY, a highly conserved protein, in rRNA processing , 2010, Molecular microbiology.

[35]  H. Aiba Mechanism of RNA silencing by Hfq-binding small RNAs. , 2007, Current opinion in microbiology.

[36]  J. Mitobe,et al.  RodZ regulates the post‐transcriptional processing of the Shigella sonnei type III secretion system , 2011, EMBO reports.

[37]  C. Yanofsky,et al.  TRAP, the trp RNA-binding attenuation protein of Bacillus subtilis, is a toroid-shaped molecule that binds transcripts containing GAG or UAG repeats separated by two nucleotides. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[38]  M. Winkler,et al.  Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K‐12 , 1994, Molecular microbiology.

[39]  J. Glover,et al.  ProQ is an RNA chaperone that controls ProP levels in Escherichia coli. , 2011, Biochemistry.

[40]  S. Gottesman,et al.  Bacterial Small RNA-based Negative Regulation: Hfq and Its Accomplices* , 2013, The Journal of Biological Chemistry.

[41]  J. Stülke Control of transcription termination in bacteria by RNA-binding proteins that modulate RNA structures , 2002, Archives of Microbiology.

[42]  C. Oubridge,et al.  RNA-binding proteins: TRAPping RNA bases , 2000, Current Biology.

[43]  E. Hajnsdorf,et al.  The interplay of Hfq, poly(A) polymerase I and exoribonucleases at the 3′ ends of RNAs resulting from Rho-independent termination , 2013, RNA biology.

[44]  A. J. Carpousis The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. , 2007, Annual review of microbiology.

[45]  D. Herschlag RNA Chaperones and the RNA Folding Problem (*) , 1995, The Journal of Biological Chemistry.

[46]  P. Babitzke,et al.  The trp RNA-Binding Attenuation Protein of Bacillus subtilis Regulates Translation of the Tryptophan Transport Gene trpP (yhaG) by Blocking Ribosome Binding , 2004, Journal of bacteriology.

[47]  H. Aiba,et al.  Base‐pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq , 2006, Molecular microbiology.

[48]  G. Storz,et al.  Dual function of the McaS small RNA in controlling biofilm formation. , 2013, Genes & development.

[49]  P. Højrup,et al.  Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction. , 2002, Molecular cell.

[50]  É. Massé,et al.  Antagonistic functions between the RNA chaperone Hfq and an sRNA regulate sensitivity to the antibiotic colicin , 2013, The EMBO journal.

[51]  H. Yang,et al.  The product of the pleiotropic Escherichia coli gene csrA modulates glycogen biosynthesis via effects on mRNA stability , 1995, Journal of bacteriology.

[52]  M. Malecki,et al.  Bacterial adaptation to cold. , 2013, Microbiology.

[53]  F. Briani,et al.  Hfq affects the length and the frequency of short oligo(A) tails at the 3' end of Escherichia coli rpsO mRNAs. , 2003, Nucleic acids research.

[54]  R. Brennan,et al.  Recognition of U-rich RNA by Hfq from the Gram-positive pathogen Listeria monocytogenes , 2014, RNA.

[55]  Tony Romeo,et al.  Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems. , 2013, Environmental microbiology.

[56]  J. Glover,et al.  FinO is an RNA chaperone that facilitates sense–antisense RNA interactions , 2003, The EMBO journal.

[57]  J. Mackay,et al.  The prospects for designer single-stranded RNA-binding proteins , 2011, Nature Structural &Molecular Biology.

[58]  Andrew Wright,et al.  A bacterial gene involved in transcription antitermination: Regulation at a rho-independent terminator in the bgl operon of E. coli , 1987, Cell.

[59]  G. Walker,et al.  A highly conserved protein of unknown function in Sinorhizobium meliloti affects sRNA regulation similar to Hfq , 2011, Nucleic acids research.

[60]  P. Gollnick,et al.  Translation of trpG in Bacillus subtilis is regulated by the trp RNA-binding attenuation protein (TRAP) , 1995, Journal of bacteriology.

[61]  M. Parsek,et al.  Pseudomonas aeruginosa biofilm matrix polysaccharide Psl is regulated transcriptionally by RpoS and post-transcriptionally by RsmA , 2010, Molecular microbiology.

[62]  C. Bond,et al.  RNA binding protein , 2015 .

[63]  E. Birney,et al.  Pfam: the protein families database , 2013, Nucleic Acids Res..

[64]  T. Link,et al.  Structure of Escherichia coli Hfq bound to polyriboadenylate RNA , 2009, Proceedings of the National Academy of Sciences.

[65]  F. O'Gara,et al.  Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. , 2006, Microbiology.

[66]  K. Djinović-Carugo,et al.  The Pseudomonas aeruginosa Catabolite Repression Control Protein Crc Is Devoid of RNA Binding Activity , 2013, PloS one.

[67]  B. Večerek,et al.  Translational autocontrol of the Escherichia coli hfq RNA chaperone gene. , 2005, RNA.

[68]  M. Inouye,et al.  Escherichia coli CspA-family RNA chaperones are transcription antiterminators. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[69]  B. Stevenson,et al.  Bpur, the Lyme Disease Spirochete's PUR Domain Protein , 2013, The Journal of Biological Chemistry.

[70]  B. Henderson Post-Transcriptional Regulation , 2002 .

[71]  Paul Gollnick,et al.  Complexity in regulation of tryptophan biosynthesis in Bacillus subtilis. , 2005, Annual review of genetics.

[72]  L. Betts,et al.  An unusual CsrA family member operates in series with RsmA to amplify posttranscriptional responses in Pseudomonas aeruginosa , 2013, Proceedings of the National Academy of Sciences.

[73]  A. Joachimiak,et al.  N. meningitidis 1681 is a member of the FinO family of RNA chaperones , 2010, RNA biology.

[74]  Y. Lu,et al.  Function of RNA secondary structures in transcriptional attenuation of the Bacillus subtilis pyr operon. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[75]  P. Valentin‐Hansen,et al.  Structures of the pleiotropic translational regulator Hfq and an Hfq–RNA complex: a bacterial Sm‐like protein , 2002, The EMBO journal.

[76]  Clémentine Dressaire,et al.  Examination of post-transcriptional regulations in prokaryotes by integrative biology. , 2009, Comptes rendus biologies.

[77]  Diogo M. Camacho,et al.  Central role for RNase YbeY in Hfq-dependent and Hfq-independent small-RNA regulation in bacteria , 2014, BMC Genomics.

[78]  J. Stülke,et al.  Regulation of the Bacillus subtilis GlcT Antiterminator Protein by Components of the Phosphotransferase System , 1998, Journal of bacteriology.

[79]  Rapid binding and release of Hfq from ternary complexes during RNA annealing , 2011, Nucleic acids research.

[80]  E. Sonnleitner,et al.  Regulation of Hfq by the RNA CrcZ in Pseudomonas aeruginosa Carbon Catabolite Repression , 2014, PLoS genetics.

[81]  M. Saier,et al.  Multiple Phosphorylation of SacY, a Bacillus subtilisTranscriptional Antiterminator Negatively Controlled by the Phosphotransferase System* , 1997, The Journal of Biological Chemistry.

[82]  C. Yanofsky,et al.  trp RNA-binding attenuation protein (TRAP)-trp leader RNA interactions mediate translational as well as transcriptional regulation of the Bacillus subtilis trp operon , 1995, Journal of bacteriology.

[83]  D. Giedroc,et al.  The RNA Molecule CsrB Binds to the Global Regulatory Protein CsrA and Antagonizes Its Activity in Escherichia coli * , 1997, The Journal of Biological Chemistry.

[84]  W. Winkler,et al.  The Mechanism for RNA Recognition by ANTAR Regulators of Gene Expression , 2012, PLoS genetics.

[85]  P. Babitzke,et al.  CsrA post‐transcriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli , 2005, Molecular microbiology.

[86]  R. Hengge-aronis,et al.  The RNA-binding protein HF-I, known as a host factor for phage Qbeta RNA replication, is essential for rpoS translation in Escherichia coli. , 1996, Genes & development.

[87]  J. Lemaire,et al.  Role of FlbT in flagellin production in Brucella melitensis. , 2011, Microbiology.

[88]  E. Hajnsdorf,et al.  Host factor Hfq of Escherichia coli stimulates elongation of poly(A) tails by poly(A) polymerase I. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[89]  D. Green Major Role for β , 2007 .

[90]  P. Babitzke,et al.  CsrA Inhibits Translation Initiation of Escherichia coli hfq by Binding to a Single Site Overlapping the Shine-Dalgarno Sequence , 2007, Journal of bacteriology.

[91]  S. R. Kushner,et al.  Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. , 2006, Genes & development.

[92]  C. Reimmann,et al.  Posttranscriptional Repression of GacS/GacA-Controlled Genes by the RNA-Binding Protein RsmE Acting Together with RsmA in the Biocontrol Strain Pseudomonas fluorescens CHA0 , 2005, Journal of bacteriology.

[93]  L. Bossi,et al.  RNA remodeling by bacterial global regulator CsrA promotes Rho-dependent transcription termination , 2014, Genes & development.

[94]  Lan Huang,et al.  Quantitative Profiling of In Vivo-assembled RNA-Protein Complexes Using a Novel Integrated Proteomic Approach* , 2011, Molecular & Cellular Proteomics.

[95]  H. Putzer,et al.  RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis , 2009, The EMBO journal.

[96]  R. Kulkarni,et al.  Prediction of CsrA-regulating small RNAs in bacteria and their experimental verification in Vibrio fischeri , 2006, Nucleic acids research.

[97]  É. Massé,et al.  New insights into small RNA-dependent translational regulation in prokaryotes. , 2013, Trends in genetics : TIG.

[98]  S. Aymerich,et al.  Specificity determinants and structural features in the RNA target of the bacterial antiterminator proteins of the BglG/SacY family. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[99]  H. Aiba,et al.  Hfq binding at RhlB‐recognition region of RNase E is crucial for the rapid degradation of target mRNAs mediated by sRNAs in Escherichia coli , 2011, Molecular microbiology.

[100]  S. Jourdan,et al.  Rapid cleavage of RNA by RNase E in the absence of 5′ monophosphate stimulation , 2009, Molecular microbiology.

[101]  C. Yanofsky,et al.  TRAP, the trp RNA-binding attenuation protein of Bacillus subtilis, is a multisubunit complex that appears to recognize G/UAG repeats in the trpEDCFBA and trpG transcripts. , 1994, The Journal of biological chemistry.

[102]  A. Feig,et al.  Escherichia coli Hfq has distinct interaction surfaces for DsrA, rpoS and poly(A) RNAs , 2004, Nature Structural &Molecular Biology.

[103]  B. Kallipolitis,et al.  The RNA-Binding Protein Hfq of Listeria monocytogenes: Role in Stress Tolerance and Virulence , 2004, Journal of bacteriology.

[104]  Christopher A. Vakulskas,et al.  Circuitry linking the Csr and stringent response global regulatory systems , 2011, Molecular Microbiology.

[105]  J. Vogel,et al.  In vivo expression and purification of aptamer-tagged small RNA regulators , 2009, Nucleic acids research.

[106]  D. Touati,et al.  Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator , 2004, The EMBO journal.

[107]  H. Aiba,et al.  RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. , 2005, Genes & development.

[108]  P. Valentin‐Hansen,et al.  Regulation of ompA mRNA stability: the role of a small regulatory RNA in growth phase‐dependent control , 2005, Molecular microbiology.

[109]  R. Zielke,et al.  Analysis and Expansion of the Role of the Escherichia coli Protein ProQ , 2013, PloS one.

[110]  V. Kaberdin,et al.  Composition and conservation of the mRNA-degrading machinery in bacteria , 2011, Journal of Biomedical Science.

[111]  E. Sonnleitner,et al.  Small RNA as global regulator of carbon catabolite repression in Pseudomonas aeruginosa , 2009, Proceedings of the National Academy of Sciences.

[112]  G. Mackie Ribonuclease E is a 5′-end-dependent endonuclease , 1998, Nature.

[113]  M. Inouye,et al.  The Nucleic Acid Melting Activity of Escherichia coliCspE Is Critical for Transcription Antitermination and Cold Acclimation of Cells* , 2002, The Journal of Biological Chemistry.

[114]  A. D. Jones,et al.  CsrA Regulates Translation of the Escherichia coli Carbon Starvation Gene, cstA, by Blocking Ribosome Access to the cstA Transcript , 2003, Journal of bacteriology.

[115]  P. Cary,et al.  Hfq binding changes the structure of Escherichia coli small noncoding RNAs OxyS and RprA, which are involved in the riboregulation of rpoS , 2013, RNA.

[116]  P. Babitzke,et al.  CsrA Represses Translation of sdiA, Which Encodes the N-Acylhomoserine-l-Lactone Receptor of Escherichia coli, by Binding Exclusively within the Coding Region of sdiA mRNA , 2011, Journal of bacteriology.

[117]  P. Babitzke,et al.  CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli , 2002, Molecular microbiology.

[118]  C. Yanofsky,et al.  A Bacillus subtilis Gene of Previously Unknown Function, yhaG, Is Translationally Regulated by Tryptophan-Activated TRAP and Appears To Be Involved in Tryptophan Transport , 2000, Journal of bacteriology.

[119]  Amanda G. Oglesby-Sherrouse,et al.  A method for in vivo identification of bacterial small RNA-binding proteins , 2014, MicrobiologyOpen.

[120]  S. Gottesman,et al.  Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. , 2003, Genes & development.

[121]  G. Mackie RNase E: at the interface of bacterial RNA processing and decay , 2012, Nature Reviews Microbiology.

[122]  I. Hofacker,et al.  Impact of Hfq on the Bacillus subtilis Transcriptome , 2014, PloS one.

[123]  Rutberg Antitermination of transcription of catabolic operons , 1997, Molecular microbiology.

[124]  P. Schlax,et al.  Interactions of ribosomal protein S1 with DsrA and rpoS mRNA. , 2006, Biochemical and biophysical research communications.

[125]  C. Clayton Post-transcriptional regulation , 2003 .

[126]  V. Arluison,et al.  The Sm‐like RNA chaperone Hfq mediates transcription antitermination at Rho‐dependent terminators , 2011, The EMBO journal.

[127]  O. Pellegrini,et al.  Ribonucleases J1 and J2: two novel endoribonucleases in B.subtilis with functional homology to E.coli RNase E , 2005, Nucleic acids research.

[128]  S. Lory,et al.  Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA , 2009, Molecular microbiology.

[129]  S. Marzi,et al.  The Crc global regulator binds to an unpaired A-rich motif at the Pseudomonas putida alkS mRNA coding sequence and inhibits translation initiation , 2009, Nucleic acids research.

[130]  Marc Dreyfus,et al.  AU-Rich Sequences within 5′ Untranslated Leaders Enhance Translation and Stabilize mRNA in Escherichia coli , 2005, Journal of bacteriology.

[131]  F. O'Gara,et al.  Computational prediction of the Crc regulon identifies genus-wide and species-specific targets of catabolite repression control in Pseudomonas bacteria , 2010, BMC Microbiology.

[132]  P. Babitzke,et al.  trp RNA-binding Attenuation Protein-mediated Long Distance RNA Refolding Regulates Translation of trpE inBacillus subtilis * , 1998, The Journal of Biological Chemistry.

[133]  Steffen Schmidt,et al.  Small RNA binding to the lateral surface of Hfq hexamers and structural rearrangements upon mRNA target recognition , 2012, Proceedings of the National Academy of Sciences.

[134]  Chan Li,et al.  Structural Rearrangement in an RsmA/CsrA Ortholog of Pseudomonas aeruginosa Creates a Dimeric RNA-Binding Protein, RsmN , 2013, Structure.

[135]  W. Scott,et al.  Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover , 2005, Nature.

[136]  Yuqing Chen,et al.  Expression hierarchy in the Yersinia type III secretion system established through YopD recognition of RNA , 2011, Molecular microbiology.

[137]  F. Rojo,et al.  The Crc and Hfq proteins of Pseudomonas putida cooperate in catabolite repression and formation of ribonucleic acid complexes with specific target motifs. , 2015, Environmental microbiology.

[138]  J. Vogel,et al.  Hfq and its constellation of RNA , 2011, Nature Reviews Microbiology.

[139]  P. Babitzke,et al.  The trp RNA-binding attenuation protein regulates TrpG synthesis by binding to the trpG ribosome binding site of Bacillus subtilis , 1997, Journal of bacteriology.

[140]  K. Nierhaus,et al.  How the ribosome moves along the mRNA during protein synthesis. , 1994, The Journal of biological chemistry.

[141]  J. Helmann,et al.  The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins , 2008, Proceedings of the National Academy of Sciences.

[142]  H. Vaucheret,et al.  Form, Function, and Regulation of ARGONAUTE Proteins , 2010, Plant Cell.

[143]  J. Helmann,et al.  The FsrA sRNA and FbpB Protein Mediate the Iron-Dependent Induction of the Bacillus subtilis LutABC Iron-Sulfur-Containing Oxidases , 2012, Journal of bacteriology.

[144]  J. Shine,et al.  The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[145]  Christopher A. Vakulskas,et al.  Dual posttranscriptional regulation via a cofactor-responsive mRNA leader. , 2013, Journal of molecular biology.

[146]  J. Gober,et al.  FlbT, the post‐transcriptional regulator of flagellin synthesis in Caulobacter crescentus, interacts with the 5′ untranslated region of flagellin mRNA , 2000, Molecular microbiology.

[147]  G. Storz,et al.  Regulation by small RNAs in bacteria: expanding frontiers. , 2011, Molecular cell.

[148]  O. Schneewind,et al.  Translational Regulation of Yersinia enterocolitica mRNA Encoding a Type III Secretion Substrate* , 2013, The Journal of Biological Chemistry.

[149]  P. Gollnick,et al.  Interaction of the trp RNA-binding attenuation protein (TRAP) with anti-TRAP. , 2004, Journal of molecular biology.

[150]  I. Moll,et al.  Hfq (HF1) stimulates ompA mRNA decay by interfering with ribosome binding. , 2000, Genes & development.

[151]  P. Babitzke Regulation of transcription attenuation and translation initiation by allosteric control of an RNA-binding protein: the Bacillus subtilis TRAP protein. , 2004, Current opinion in microbiology.

[152]  Jie Dong,et al.  Hfq Is a Global Regulator That Controls the Pathogenicity of Staphylococcus aureus , 2010, PloS one.

[153]  J. Vogel,et al.  Experimental tools to identify RNA-protein interactions in Helicobacter pylori , 2012, RNA biology.

[154]  C. Valverde,et al.  The bacterial protein Hfq: much more than a mere RNA-binding factor , 2012, Critical reviews in microbiology.

[155]  S. R. Kushner,et al.  The Sm‐like protein Hfq regulates polyadenylation dependent mRNA decay in Escherichia coli , 2004, Molecular microbiology.

[156]  G. Walker,et al.  Conserved bacterial RNase YbeY plays key roles in 70S ribosome quality control and 16S rRNA maturation. , 2013, Molecular cell.

[157]  O. Pellegrini,et al.  The poly(A) binding protein Hfq protects RNA from RNase E and exoribonucleolytic degradation. , 2003, Nucleic acids research.

[158]  Grant S. Jones,et al.  Posttranscriptional Self-Regulation by the Lyme Disease Bacterium's BpuR DNA/RNA-Binding Protein , 2013, Journal of bacteriology.

[159]  E. Sauer Structure and RNA-binding properties of the bacterial LSm protein Hfq , 2013, RNA biology.

[160]  Christopher A. Vakulskas,et al.  CsrA activates flhDC expression by protecting flhDC mRNA from RNase E‐mediated cleavage , 2013, Molecular microbiology.