sRNAs and the virulence of Salmonella enterica serovar Typhimurium

RNA Biology

Volumn 9, Issue 4, 2012, Pages 437-445

  Hébrard, Magali ^a   Kröger, Carsten ^a   Srikumar, Shabarinath ^a   Colgan, Aoife ^a   Händler, Kristian ^a   Hinton, Jay C D ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Post transcriptional regulation; Salmonella typhimurium; sRNA; Virulence

Indexed keywords

COMPLEMENTARY DNA; TRANSFER RNA;

BACTERIAL VIRULENCE; ESCHERICHIA COLI; GENE CONTROL; GENOMICS; HIGH THROUGHPUT SEQUENCING; HUMAN; MAMMAL CELL; NONHUMAN; POSTTRANSCRIPTIONAL GENE SILENCING; REVIEW; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION REGULATION;

MAMMALIA; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM;

EID: 84860774336     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.20480     Document Type: Review

References (117)

1. Frenzen PD, Riggs TL, Buzby JC, Breuer T, Roberts T, Voetsch D, et al. Salmonella cost estimate updated using FoodNet data. Food Review 1999; 22:10-5.
2. Hindley J. Fractionation of 32P-labelled ribonucleic acids on polyacrylamide gels and their characterization by fingerprinting. J Mol Biol 1967; 30:125-36; PMID:4865141; http://dx.doi.org/10.1016/0022-2836(67)90248-3.
3. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, Margalit H, et al. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 2001; 11:941-50; PMID:11448770; http:// dx.doi.org/10.1016/ S0960-9822(01)00270-6.
4. Zhang A, Wassarman KM, Rosenow C, Tjaden BC, Storz G, Gottesman S. Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol 2003; 50:1111-24; PMID:14622403; http://dx.doi. org/10.1046/j.1365-2958.2003.03734.x.
5. Wassarman KM, Repoila F, Rosenow C, Storz G, Gottesman S. Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev 2001; 15:1637-51; PMID:11445539; http://dx.doi. org/10.1101/gad.901001.
6. Rivas E, Klein RJ, Jones TA, Eddy SR. Computational identification of noncoding RNAs in E. coli by comparative genomics. Curr Biol 2001; 11:1369-73; PMID:11553332; http://dx.doi.org/10.1016/S0960- 9822(01)00401-8.
7. Sorek R, Cossart P. Prokaryotic transcriptomics: a new view on regulation, physiology and pathogenicity. Nat Rev Genet 2010; 11:9-16; PMID:19935729; http:// dx.doi.org/10.1038/nrg2695.
8. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, Moghazeh S. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 1993; 12:3967-75; PMID:7691599.
9. Morfeldt E, Taylor D, von Gabain A, Arvidson S. Activation of alpha-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J 1995; 14:4569-77; PMID:7556100.
10. Boisset S, Geissmann T, Huntzinger E, Fechter P, Bendridi N, Possedko M, et al. Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 2007; 21:1353-66; PMID:17545468; http://dx.doi.org/10.1101/gad. 423507.
11. Papenfort K, Vogel J. Regulatory RNA in bacterial pathogens. Cell Host Microbe 2010; 8:116-27; PMID:20638647; http://dx.doi.org/10.1016/j. chom.2010.06.008.
12. Majdalani N, Vanderpool CK, Gottesman S. Bacterial small RNA regulators. Crit Rev Biochem Mol Biol 2005; 40:93-113; PMID:15814430; http://dx.doi. org/10.1080/10409230590918702.
13. Storz G, Vogel J, Wassarman KM. Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 2011; 43:880-91; PMID:21925377; http://dx.doi. org/10.1016/j.molcel.2011.08.022.
14. Pichon C, Felden B. Proteins that interact with bacterial small RNA regulators. FEMS Microbiol Rev 2007; 31:614-25; PMID:17655690; http://dx.doi. org/10.1111/j.1574-6976.2007.00079.x.
15. Vogel J. A rough guide to the non-coding RNA world of Salmonella. Mol Microbiol 2009; 71:1-11; PMID:19007416; http://dx.doi.org/10.1111/j.1365- 2958.2008.06505.x.
16. Georg J, Hess WR. cis-antisense RNA, another level of gene regulation in bacteria. Microbiol Mol Biol Rev 2011; 75:286-300; PMID:21646430; http://dx.doi. org/10.1128/MMBR.00032-10.
17. Thomason MK, Storz G. Bacterial antisense RNAs: how many are there, and what are they doing? Annu Rev Genet 2010; 44:167-88; PMID:20707673; http:// dx.doi.org/10.1146/annurev-genet-102209-163523.
18. Vogel J, Luisi BF. Hfq and its constellation of RNA. Nat Rev Microbiol 2011; 9:578-89; PMID:21760622; http://dx.doi.org/10.1038/nrmicro2615.
19. Polayes DA, Rice PW, Dahlberg JE. DNA polymerase I activity in Escherichia coli is influenced by spot 42 RNA. J Bacteriol 1988; 170:2083-8; PMID:2452153.
20. Altuvia S, Weinstein-Fischer D, Zhang A, Postow L, Storz G. A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell 1997; 90:43-53; PMID:9230301; http://dx.doi. org/10.1016/S0092-8674(00)80312-8.
21. Massé E, Gottesman S. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci U S A 2002; 99:4620-5; PMID:11917098; http://dx.doi. org/10.1073/pnas.032066599.
22. Boysen A, Møller-Jensen J, Kallipolitis B, Valentin-Hansen P, Overgaard M. Translational regulation of gene expression by an anaerobically induced small noncoding RNA in Escherichia coli. J Biol Chem 2010; 285:10690-702; PMID:20075074; http://dx.doi. org/10.1074/jbc.M109.089755.
23. Durand S, Storz G. Reprogramming of anaerobic metabolism by the FnrS small RNA. Mol Microbiol 2010; 75:1215-31; PMID:20070527; http://dx.doi. org/10.1111/j.1365-2958.2010.07044.x.
24. Sharma CM, Darfeuille F, Plantinga TH, Vogel J. A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites. Genes Dev 2007; 21:2804-17; PMID:17974919; http://dx.doi. org/10.1101/gad.447207.
25. Sharma CM, Papenfort K, Pernitzsch SR, Mollenkopf HJ, Hinton JC, Vogel J. Pervasive post-transcriptional control of genes involved in amino acid metabolism by the Hfq-dependent GcvB small RNA. Mol Microbiol 2011; 81:1144-65; PMID:21696468; http://dx.doi. org/10.1111/j.1365-2958.2011.07751.x.
26. Papenfort K, Bouvier M, Mika F, Sharma CM, Vogel J. Evidence for an autonomous 5′ target recognition domain in an Hfq-associated small RNA. Proc Natl Acad Sci U S A 2010; 107:20435-40; PMID:21059903; http://dx.doi.org/ 10.1073/pnas.1009784107.
27. Guillier M, Gottesman S. The 5′ end of two redundant sRNAs is involved in the regulation of multiple targets, including their own regulator. Nucleic Acids Res 2008; 36:6781-94; PMID:18953042; http://dx.doi. org/10.1093/nar/gkn742.
28. Balbontín R, Fiorini F, Figueroa-Bossi N, Casadesús J, Bossi L. Recognition of heptameric seed sequence underlies multi-target regulation by RybB small RNA in Salmonella enterica. Mol Microbiol 2010; 78:380- 94; PMID:20979336; http://dx.doi.org/10.1111/ j.1365-2958.2010.07342.x.
29. Pfeiffer V, Papenfort K, Lucchini S, Hinton JC, Vogel J. Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation. Nat Struct Mol Biol 2009; 16:840- 6; PMID:19620966; http://dx.doi.org/10.1038/ nsmb.1631.
30. Tjaden B. TargetRNA: a tool for predicting targets of small RNA action in bacteria. Nucleic Acids Res 2008; 36(Web Server issue):W109-13; PMID:18477632; http://dx.doi.org/10.1093/nar/gkn264.
31. Busch A, Richter AS, Backofen R. IntaRNA: efficient prediction of bacterial sRNA targets incorporating target site accessibility and seed regions. Bioinformatics 2008; 24:2849-56; PMID:18940824; http://dx.doi. org/10.1093/bioinformatics/btn544.
32. Padalon-Brauch G, Hershberg R, Elgrably-Weiss M, Baruch K, Rosenshine I, Margalit H, et al. Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res 2008; 36:1913-27; PMID:18267966; http://dx.doi.org/10.1093/nar/ gkn050.
33. Papenfort K, Pfeiffer V, Mika F, Lucchini S, Hinton JC, Vogel J. SigmaE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol Microbiol 2006; 62:1674-88; PMID:17427289; http://dx.doi.org/10.1111/j.1365- 2958.2006.05524.x.
34. Massé E, Vanderpool CK, Gottesman S. Effect of RyhB small RNA on global iron use in Escherichia coli. J Bacteriol 2005; 187:6962-71; PMID:16199566; http:// dx.doi.org/10.1128/JB.187.20.6962-6971.2005.
35. Urban JH, Vogel J. Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res 2007; 35:1018-37; PMID:17264113; http:// dx.doi.org/10.1093/nar/gkl1040.
36. Frohlich KS, Papenfort K, Berger AA, Vogel J. A conserved RpoS-dependent small RNA controls the synthesis of major porin OmpD. Nucleic Acids Res 2011; PMID:22180532.
37. Pfeiffer V, Sittka A, Tomer R, Tedin K, Brinkmann V, Vogel J. A small non-coding RNA of the invasion gene island (SPI-1) represses outer membrane protein synthesis from the Salmonella core genome. Mol Microbiol 2007; 66:1174-91; PMID:17971080; http://dx.doi.org/10.1111/j.1365-2958.2007.05991.x.
38. Martínez LC, Yakhnin H, Camacho MI, Georgellis D, Babitzke P, Puente JL, et al. Integration of a complex regulatory cascade involving the SirA/BarA and Csr global regulatory systems that controls expression of the Salmonella SPI-1 and SPI-2 virulence regulons through HilD. Mol Microbiol 2011; 80:1637-56; PMID:21518393; http://dx.doi.org/10.1111/j.1365- 2958.2011.07674.x.
39. Timmermans J, Van Melderen L. Post-transcriptional global regulation by CsrA in bacteria. Cell Mol Life Sci 2010; 67:2897-908; PMID:20446015; http://dx.doi. org/10.1007/s00018-010-0381-z.
40. Fortune DR, Suyemoto M, Altier C. Identification of CsrC and characterization of its role in epithelial cell invasion in Salmonella enterica serovar Typhimurium. Infect Immun 2006; 74:331-9; PMID:16368988; http://dx.doi.org/10.1128/IAI.74.1.331-339.2006.
41. Hershberg R, Altuvia S, Margalit H. A survey of small RNA-encoding genes in Escherichia coli. Nucleic Acids Res 2003; 31:1813-20; PMID:12654996; http:// dx.doi.org/10.1093/nar/gkg297.
42. Huang HY, Chang HY, Chou CH, Tseng CP, Ho SY, Yang CD, et al. sRNAMap: genomic maps for small non-coding RNAs, their regulators and their targets in microbial genomes. Nucleic Acids Res 2009; 37(Database issue):D150-4; PMID:19015153; http:// dx.doi.org/10.1093/nar/gkn852.
43. Chinni SV, Raabe CA, Zakaria R, Randau G, Hoe CH, Zemann A, et al. Experimental identification and characterization of 97 novel npcRNA candidates in Salmonella enterica serovar Typhi. Nucleic Acids Res 2010; 38:5893-908; PMID:20460466; http://dx.doi. org/10.1093/nar/gkq281.
44. Kröger C, Dillon SC, Cameron AD, Papenfort K, Sivasankaran SK, Hokamp K, et al. The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc Natl Acad Sci USA 2012; In press.
45. Papenfort K, Podkaminski D, Hinton JC, Vogel J. The ancestral SgrS RNA discriminates horizontally acquired Salmonella mRNAs through a single G-U wobble pair. Proc Natl Acad Sci U S A 2012; 109:E757-64; PMID:22383560; http://dx.doi.org/10.1073/ pnas.1119414109.
46. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, et al. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 2001; 413:852-6; PMID:11677609; http://dx.doi.org/10.1038/35101614.
47. Doolittle RF, Feng DF, Tsang S, Cho G, Little E. Determining divergence times of the major kingdoms of living organisms with a protein clock. Science 1996; 271:470-7.
48. Achtman M. Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu Rev Microbiol 2008; 62:53-70; PMID:18785837; http://dx.doi.org/10.1146/annurev. micro.62.081307.162832.
49. Alvarez-Ordóñez A, Begley M, Prieto M, Messens W, López M, Bernardo A, et al. Salmonella spp. survival strategies within the host gastrointestinal tract. Microbiology 2011; 157:3268-81; PMID:22016569; http://dx.doi.org/10.1099/mic.0.050351-0.
50. Shimoni Y, Friedlander G, Hetzroni G, Niv G, Altuvia S, Biham O, et al. Regulation of gene expression by small non-coding RNAs: a quantitative view. Mol Syst Biol 2007; 3:138; PMID:17893699; http://dx.doi. org/10.1038/msb4100181.
51. Julio SM, Heithoff DM, Mahan MJ. ssrA (tmRNA) plays a role in Salmonella enterica serovar Typhimurium pathogenesis. J Bacteriol 2000; 182:1558-63; PMID:10692360; http://dx.doi.org/10.1128/ JB.182.6.1558-1563.2000.
52. Moore SD, Sauer RT. The tmRNA system for translational surveillance and ribosome rescue. Annu Rev Biochem 2007; 76:101-24; PMID:17291191; http://dx.doi.org/10.1146/annurev. biochem.75.103004.142733.
53. Bäumler AJ, Kusters JG, Stojiljkovic I, Heffron F. Salmonella typhimurium loci involved in survival within macrophages. Infect Immun 1994; 62:1623-30; PMID:8168923.
54. Ansong C, Yoon H, Porwollik S, Mottaz-Brewer H, Petritis BO, Jaitly N, et al. Global systems-level analysis of Hfq and SmpB deletion mutants in Salmonella: implications for virulence and global protein translation. PLoS One 2009; 4:e4809; PMID:19277208; http:// dx.doi.org/10.1371/journal.pone.0004809.
55. Schlosser-Silverman E, Elgrably-Weiss M, Rosenshine I, Kohen R, Altuvia S. Characterization of Escherichia coli DNA lesions generated within J774 macrophages. J Bacteriol 2000; 182:5225-30; PMID:10960109; http:// dx.doi.org/10.1128/JB.182.18.5225-5230.2000.
56. Ortega A, Gonzalo-Asensio J, García-Del Portillo F. Dynamics of Salmonella small RNA expression in nongrowing bacteria located inside eukaryotic cells. RNA Biol 2012; 9:9; PMID:22336761.
57. Gong H, Vu GP, Bai Y, Chan E, Wu R, Yang E, et al. A Salmonella small non-coding RNA facilitates bacterial invasion and intracellular replication by modulating the expression of virulence factors. PLoS Pathog 2011; 7:e1002120; PMID:21949647; http://dx.doi. org/10.1371/journal.ppat.1002120.
58. Fu Y, Galán JE. A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 1999; 401:293-7; PMID:10499590; http://dx.doi.org/10.1038/45829.
59. Zhang S, Santos RL, Tsolis RM, Stender S, Hardt WD, Bäumler AJ, et al. The Salmonella enterica serotype typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect Immun 2002; 70:3843- 55; PMID:12065528; http://dx.doi.org/10.1128/ IAI.70.7.3843-3855.2002.
60. Baxter MA, Fahlen TF, Wilson RL, Jones BD. HilE interacts with HilD and negatively regulates hilA transcription and expression of the Salmonella enterica serovar Typhimurium invasive phenotype. Infect Immun 2003; 71:1295-305; PMID:12595445; http:// dx.doi.org/10.1128/IAI.71.3.1295-1305.2003.
61. Santiviago CA, Reynolds MM, Porwollik S, Choi SH, Long F, Andrews-Polymenis HL, et al. Analysis of pools of targeted Salmonella deletion mutants identifies novel genes affecting fitness during competitive infection in mice. PLoS Pathog 2009; 5:e1000477; PMID:19578432; http://dx.doi.org/10.1371/ journal. ppat.1000477.
62. Vogel J, Argaman L, Wagner EG, Altuvia S. The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr Biol 2004; 14:2271-6; PMID:15620655; http://dx.doi.org/10.1016/j.cub.2004.12.003.
63. Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jäger JG, Hüttenhofer A, et al. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res 2003; 31:6435-43; PMID:14602901; http://dx.doi. org/10.1093/nar/gkg867.
64. Webb E, Claas K, Downs D. thiBPQ encodes an ABC transporter required for transport of thiamine and thiamine pyrophosphate in Salmonella typhimurium. J Biol Chem 1998; 273:8946-50; PMID:9535878; http://dx.doi.org/10.1074/jbc.273.15. 8946.
65. Zhang A, Altuvia S, Storz G. The novel oxyS RNA regulates expression of the sigma s subunit of Escherichia coli RNA polymerase. Nucleic Acids Symp Ser 1997; 36:27-8; PMID:9478196.
66. Retamal P, Castillo-Ruiz M, Mora GC. Characterization of MgtC, a virulence factor of Salmonella enterica Serovar Typhi. PLoS One 2009; 4:e5551; PMID:19436747; http://dx.doi.org/10.1371/journal. pone.0005551.
67. Lee EJ, Groisman EA. An antisense RNA that governs the expression kinetics of a multifunctional virulence gene. Mol Microbiol 2010; 76:1020-33; PMID:20398218; http://dx.doi.org/10.1111/j.1365- 2958.2010.07161.x.
68. Zhang A, Altuvia S, Tiwari A, Argaman L, Hengge-Aronis R, Storz G. The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J 1998; 17:6061-8; PMID:9774349; http:// dx.doi.org/10.1093/emboj/17.20. 6061.
69. Wilmes-Riesenberg MR, Foster JW, Curtiss R 3rd. An altered rpoS allele contributes to the avirulence of Salmonella typhimurium LT2. Infect Immun 1997; 65:203-10; PMID:8975913.
70. Guiney DG, Fierer J. The Role of the spv Genes in Salmonella Pathogenesis. Front Microbiol 2011; 2:129; PMID:21716657; http://dx.doi.org/10. 3389/ fmicb.2011.00129.
71. Majdalani N, Cunning C, Sledjeski D, Elliott T, Gottesman S. DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proc Natl Acad Sci U S A 1998; 95:12462-7; PMID:9770508; http://dx.doi.org/10.1073/pnas.95.21. 12462.
72. Majdalani N, Chen S, Murrow J, St John K, Gottesman S. Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol Microbiol 2001; 39:1382-94; PMID:11251852; http://dx.doi. org/10.1111/j.1365-2958.2001.02329.x.
73. Mandin P, Gottesman S. Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 2010; 29:3094- 107; PMID:20683441; http://dx.doi.org/10.1038/ emboj.2010.179.
74. Papenfort K, Said N, Welsink T, Lucchini S, Hinton JC, Vogel J. Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 2009; 74:139-58; PMID:19732340; http://dx.doi.org/10. 1111/j.1365- 2958.2009.06857.x.
75. Jones AM, Goodwill A, Elliott T. Limited role for the DsrA and RprA regulatory RNAs in rpoS regulation in Salmonella enterica. J Bacteriol 2006; 188:5077- 88; PMID:16816180; http://dx.doi.org/10.1128/ JB.00206-06.
76. Sittka A, Pfeiffer V, Tedin K, Vogel J. The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol Microbiol 2007; 63:193-217; PMID:17163975; http://dx.doi.org/10.1111/j.1365- 2958.2006.05489.x.
77. Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, Binnewies TT, et al. Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 2008; 4:e1000163; PMID:18725932; http://dx.doi. org/10.1371/journal.pgen.1000163.
78. Fröhlich KS, Vogel J. Activation of gene expression by small RNA. Curr Opin Microbiol 2009; 12:674- 82; PMID:19880344; http://dx.doi.org/10.1016/ j. mib.2009.09.009.
79. Soper TJ, Woodson SA. The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 2008; 14:1907-17; PMID:18658123; http:// dx.doi.org/10.1261/rna.1110608.
80. Moll I, Afonyushkin T, Vytvytska O, Kaberdin VR, Bläsi U. Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs. RNA 2003; 9:1308-14; PMID:14561880; http://dx.doi. org/10.1261/rna.5850703.
81. Soper T, Mandin P, Majdalani N, Gottesman S, Woodson SA. Positive regulation by small RNAs and the role of Hfq. Proc Natl Acad Sci U S A 2010; 107:9602-7; PMID:20457943; http://dx.doi. org/10.1073/pnas.1004435107.
82. Kawamoto H, Koide Y, Morita T, Aiba H. Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol Microbiol 2006; 61:1013-22; PMID:16859494; http://dx.doi.org/10.1111/j.1365- 2958.2006.05288.x.
83. Mohanty BK, Maples VF, Kushner SR. The Sm-like protein Hfq regulates polyadenylation dependent mRNA decay in Escherichia coli. Mol Microbiol 2004; 54:905-20; PMID:15522076; http://dx.doi. org/10.1111/j.1365-2958.2004.04337.x.
84. Rabhi M, Espéli O, Schwartz A, Cayrol B, Rahmouni AR, Arluison V, et al. The Sm-like RNA chaperone Hfq mediates transcription antitermination at Rhodependent terminators. EMBO J 2011; 30:2805- 16; PMID:21673658; http://dx.doi.org/10.1038/ emboj.2011.192.
85. Hussein R, Lim HN. Disruption of small RNA signaling caused by competition for Hfq. Proc Natl Acad Sci USA 2010; PMID:21189298.
86. Moon K, Gottesman S. Competition among Hfqbinding small RNAs in Escherichia coli. Mol Microbiol 2011; 82:1545-62; PMID:22040174; http://dx.doi. org/10.1111/j.1365-2958.2011.07907.x.
87. Croucher NJ, Thomson NR. Studying bacterial transcriptomes using RNA-seq. Curr Opin Microbiol 2010; 13:619-24; PMID:20888288; http://dx.doi. org/10.1016/j.mib.2010.09.009.
88. Perkins TT, Kingsley RA, Fookes MC, Gardner PP, James KD, Yu L, et al. A strand-specific RNA-Seq analysis of the transcriptome of the typhoid bacillus Salmonella typhi. PLoS Genet 2009; 5:e1000569; PMID:19609351; http://dx.doi.org/10.1371/journal. pgen.1000569.
89. Ozsolak F, Milos PM. Transcriptome profiling using single-molecule direct RNA sequencing. Methods Mol Biol 2011; 733:51-61; PMID:21431762; http:// dx.doi.org/10.1007/978-1-61779-089-8-4.
90. Mandlik A, Livny J, Robins WP, Ritchie JM, Mekalanos JJ, Waldor MK. RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression. Cell Host Microbe 2011; 10:165- 74; PMID:21843873; http://dx.doi.org/10.1016/j. chom.2011.07.007.
91. Vogel J, Wagner EG. Target identification of small noncoding RNAs in bacteria. Curr Opin Microbiol 2007; 10:262-70; PMID:17574901; http://dx.doi. org/10.1016/j.mib.2007.06.001.
92. Tjaden B, Goodwin SS, Opdyke JA, Guillier M, Fu DX, Gottesman S, et al. Target prediction for small, noncoding RNAs in bacteria. Nucleic Acids Res 2006; 34:2791-802; PMID:16717284; http://dx.doi. org/10.1093/nar/gkl356.
93. Papenfort K, Pfeiffer V, Lucchini S, Sonawane A, Hinton JC, Vogel J. Systematic deletion of Salmonella small RNA genes identifies CyaR, a conserved CRP-dependent riboregulator of OmpX synthesis. Mol Microbiol 2008; 68:890-906; PMID:18399940; http://dx.doi.org/10.1111/j.1365-2958.2008.06189.x.
94. Wadler CS, Vanderpool CK. Characterization of homologs of the small RNA SgrS reveals diversity in function. Nucleic Acids Res 2009; 37:5477-85; PMID:19620214; http://dx.doi.org/10.1093/nar/gkp591.
95. Corcoran CP, Podkaminski D, Papenfort K, Urban JH, Hinton JC, Vogel J. Superfolder GFP reporters validate diverse new mRNA targets of the classic porin regulator, MicF RNA. Mol Microbiol 2012; 84:428- 45; PMID:22458297; http://dx.doi.org/10.1111/j.1365-2958.2012.08031.x.
96. Bossi L, Figueroa-Bossi N. A small RNA downregulates LamB maltoporin in Salmonella. Mol Microbiol 2007; 65:799-810; PMID:17608792; http://dx.doi. org/10.1111/j.1365-2958.2007.05829.x.
97. Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4:44- 57; PMID:19131956; http://dx.doi.org/10.1038/nprot.2008.211.
98. Huang W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009; 37:1-13; PMID:19033363; http://dx.doi. org/10.1093/nar/gkn923.
99. Monteiro C, Papenfort K, Hentrich K, Ahmad I, Le Guyon S, Reimann R, et al. Hfq and Hfq-dependent small RNAs are major contributors to multicellular development in Salmonella enterica serovar Typhimurium. RNA Biol 2012; 9:9; PMID:22336758.
100. Altier C, Suyemoto M, Lawhon SD. Regulation of Salmonella enterica serovar typhimurium invasion genes by csrA. Infect Immun 2000; 68:6790- 7; PMID:11083797; http://dx.doi.org/10.1128/ IAI.68.12.6790-6797.2000.
101. Urbanowski ML, Stauffer LT, Stauffer GV. The gcvB gene encodes a small untranslated RNA involved in expression of the dipeptide and oligopeptide transport systems in Escherichia coli. Mol Microbiol 2000; 37:856-68; PMID:10972807; http://dx.doi. org/10.1046/j.1365-2958.2000.02051.x.
102. Urban JH, Vogel J. Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS Biol 2008; 6:e64; PMID:18351803; http://dx.doi.org/10.1371/journal.pbio.0060064.
103. Göpel Y, Lüttmann D, Heroven AK, Reichenbach B, Dersch P, Görke B. Common and divergent features in transcriptional control of the homologous small RNAs GlmY and GlmZ in Enterobacteriaceae. Nucleic Acids Res 2011; 39:1294-309; PMID:20965974; http:// dx.doi.org/10.1093/nar/gkq986.
104. Rasmussen AA, Eriksen M, Gilany K, Udesen C, Franch T, Petersen C, et al. Regulation of ompA mRNA stability: the role of a small regulatory RNA in growth phase-dependent control. Mol Microbiol 2005; 58:1421-9; PMID:16313626; http://dx.doi. org/10.1111/j.1365-2958.2005.04911.x.
105. Kint G, De Coster D, Marchal K, Vanderleyden J, De Keersmaecker SC. The small regulatory RNA molecule MicA is involved in Salmonella enterica serovar Typhimurium biofilm formation. BMC Microbiol 2010; 10:276; PMID:21044338; http://dx.doi. org/10.1186/1471-2180-10-276.
106. Mizuno T, Chou MY, Inouye M. A unique mechanism regulating gene expression: translational inhibition by a complementary RNA transcript (micRNA). Proc Natl Acad Sci U S A 1984; 81:1966-70; PMID:6201848; http://dx.doi.org/10. 1073/pnas.81.7.1966.
107. Esterling L, Delihas N. The regulatory RNA gene micF is present in several species of gram-negative bacteria and is phylogenetically conserved. Mol Microbiol 1994; 12:639-46; PMID:7523827; http://dx.doi. org/10.1111/j.1365- 2958.1994.tb01051.x.
108. Figueroa-Bossi N, Valentini M, Malleret L, Fiorini F, Bossi L. Caught at its own game: regulatory small RNA inactivated by an inducible transcript mimicking its target. Genes Dev 2009; 23:2004-15; PMID:19638370; http://dx.doi.org/10.1101/gad.541609.
109. Bouvier M, Sharma CM, Mika F, Nierhaus KH, Vogel J. Small RNA binding to 5¢ mRNA coding region inhibits translational initiation. Mol Cell 2008; 32:827-37; PMID:19111662; http://dx.doi. org/10.1016/j.molcel.2008.10.027.
110. Antal M, Bordeau V, Douchin V, Felden B. A small bacterial RNA regulates a putative ABC transporter. J Biol Chem 2005; 280:7901-8; PMID:15618228; http://dx.doi.org/10.1074/jbc.M413071200.
111. Balbontín R, Figueroa-Bossi N, Casadesús J, Bossi L. Insertion hot spot for horizontally acquired DNA within a bidirectional small-RNA locus in Salmonella enterica. J Bacteriol 2008; 190:4075-8; PMID:18390661; http://dx.doi.org/10.1128/JB.00220-08.
112. Vanderpool CK, Gottesman S. Involvement of a novel transcriptional activator and small RNA in posttranscriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol Microbiol 2004; 54:1076-89; PMID:15522088; http://dx.doi. org/10.1111/j.1365-2958.2004.04348.x.
113. Fozo EM, Kawano M, Fontaine F, Kaya Y, Mendieta KS, Jones KL, et al. Repression of small toxic protein synthesis by the Sib and OhsC small RNAs. Mol Microbiol 2008; 70:1076-93; PMID:18710431; http://dx.doi.org/10.1111/j.1365- 2958.2008.06394.x.
114. Han K, Kim KS, Bak G, Park H, Lee Y. Recognition and discrimination of target mRNAs by Sib RNAs, a cis-encoded sRNA family. Nucleic Acids Res 2010; 38:5851-66; PMID:20453032; http://dx.doi. org/10.1093/nar/gkq292.
115. Møller T, Franch T, Udesen C, Gerdes K, Valentin-Hansen P. Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. Genes Dev 2002; 16:1696-706; PMID:12101127; http://dx.doi. org/10.1101/gad.231702.
116. Beisel CL, Storz G. Discriminating tastes: Physiological contributions of the Hfq-binding small RNA Spot 42 to catabolite repression. RNA Biol 2011; 8:8; PMID:21788732; http://dx.doi.org/10.4161/ rna.8.5.16024.
117. Nechooshtan G, Elgrably-Weiss M, Sheaffer A, Westhof E, Altuvia S. A pH-responsive riboregulator. Genes Dev 2009; 23:2650-62; PMID:19933154; http://dx.doi.org/10.1101/gad.552209.