Cross talk between ABC transporter mRNAs via a target mRNA-derived sponge of the GcvB small RNA

EMBO Journal

Volumn 34, Issue 11, 2015, Pages 1478-1492

  Miyakoshi, Masatoshi ^a   Chao, Yanjie ^a   Vogel, Jörg ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

GcvB; Hfq; noncoding RNA; RNase E; SroC

Indexed keywords

ABC TRANSPORTER; CARBON; GCVB SMALL RNA; MESSENGER RNA; NITROGEN; RIBONUCLEASE E; TRANSFER RNA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BACTERIAL RNA; SMALL UNTRANSLATED RNA;

AMINO ACID TRANSPORT; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BASE PAIRING; CARBON SOURCE; DOWN REGULATION; ENZYME DEGRADATION; GENE LOCUS; GENE REPRESSION; GENE TARGETING; NONHUMAN; PRIORITY JOURNAL; RNA PROCESSING; RNA STABILITY; SALMONELLA; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE; GENETICS; METABOLISM; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM;

BACTERIA (MICROORGANISMS);

ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; RNA, BACTERIAL; RNA, MESSENGER; RNA, SMALL UNTRANSLATED; SALMONELLA TYPHIMURIUM;

EID: 84931570743     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201490546     Document Type: Article

References (102)

1. Anupama K, Leela JK, Gowrishankar J, (2011) Two pathways for RNase E action in Escherichia coli in vivo and bypass of its essentiality in mutants defective for Rho-dependent transcription termination. Mol Microbiol 82: 1330-1348
2. Bandyra KJ, Said N, Pfeiffer V, Gorna MW, Vogel J, Luisi BF, (2012) The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E. Mol Cell 47: 943-953
3. Beisel CL, Storz G, (2010) Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev 34: 866-882
4. Berghoff BA, Glaeser J, Sharma CM, Zobawa M, Lottspeich F, Vogel J, Klug G, (2011) Contribution of Hfq to photooxidative stress resistance and global regulation in Rhodobacter sphaeroides. Mol Microbiol 80: 1479-1495
5. Blank K, Hensel M, Gerlach RG, (2011) Rapid and highly efficient method for scarless mutagenesis within the Salmonella enterica chromosome. PLoS One 6: e15763
6. Bohn C, Rigoulay C, Chabelskaya S, Sharma CM, Marchais A, Skorski P, Borezée-Durant E, Barbet R, Jacquet E, Jacq A, Gautheret D, Felden B, Vogel J, Bouloc P, (2010) Experimental discovery of small RNAs in Staphylococcus aureus reveals a riboregulator of central metabolism. Nucleic Acids Res 38: 6620-6636
7. Boos W, Lucht JM, (1996). Periplasmic binding protein-dependent ABC transporters. In Escherichia coli and Salmonella: Cellular and Molecular Biology, Neidhardt FC, Curtiss R III, Ingraham JL, Lin CC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE, (eds), pp. 1175-1209. Washington, DC: ASM Press
8. Bowden SD, Ramachandran VK, Knudsen GM, Hinton JC, Thompson A, (2010) An incomplete TCA cycle increases survival of Salmonella Typhimurium during infection of resting and activated murine macrophages. PLoS One 5: e13871
9. Brochado AR, Typas A, (2013) High-throughput approaches to understanding gene function and mapping network architecture in bacteria. Curr Opin Microbiol 16: 199-206
10. Busi F, Le Derout J, Cerciat M, Régnier P, Hajnsdorf E, (2010) Is the secondary putative RNA-RNA interaction site relevant to GcvB mediated regulation of oppA mRNA in Escherichia coli? Biochimie 92: 1458-1461
11. Callaghan AJ, Marcaida MJ, Stead JA, McDowall KJ, Scott WG, Luisi BF, (2005) Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature 437: 1187-1191
12. Cao Y, Wu J, Liu Q, Zhao Y, Ying X, Cha L, Wang L, Li W, (2010) sRNATarBase: a comprehensive database of bacterial sRNA targets verified by experiments. RNA 16: 2051-2057
13. Caswell CC, Gaines JM, Ciborowski P, Smith D, Borchers CH, Roux CM, Sayood K, Dunman PM, Roop II RM, (2012) Identification of two small regulatory RNAs linked to virulence in Brucella abortus 2308. Mol Microbiol 85: 345-360
14. Cazalla D, Yario T, Steitz JA, (2010) Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science 328: 1563-1566
15. Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I, (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147: 358-369
16. Chao Y, Papenfort K, Reinhardt R, Sharma CM, Vogel J, (2012) An atlas of Hfq-bound transcripts reveals 3′ UTRs as a genomic reservoir of regulatory small RNAs. EMBO J 31: 4005-4019
17. Cho BK, Barrett CL, Knight EM, Park YS, Palsson BØ, (2008) Genome-scale reconstruction of the Lrp regulatory network in Escherichia coli. Proc Natl Acad Sci USA 105: 19462-19467
18. Cho BK, Federowicz S, Park YS, Zengler K, Palsson BØ, (2011) Deciphering the transcriptional regulatory logic of amino acid metabolism. Nat Chem Biol 8: 65-71
19. Coornaert A, Chiaruttini C, Springer M, Guillier M, (2013) Post-transcriptional control of the Escherichia coli PhoQ-PhoP two-component system by multiple sRNAs involves a novel pairing region of GcvB. PLoS Genet 9: e1003156
20. Datsenko KA, Wanner BL, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645
21. De Lay N, Gottesman S, (2012) A complex network of small non-coding RNAs regulate motility in Escherichia coli. Mol Microbiol 86: 524-538
22. De Lay N, Schu DJ, Gottesman S, (2013) Bacterial small RNA-based negative regulation: Hfq and its accomplices. J Biol Chem 288: 7996-8003
23. Ebert MS, Sharp PA, (2010) Emerging roles for natural microRNA sponges. Curr Biol 20: R858-R861
24. Fender A, Elf J, Hampel K, Zimmermann B, Wagner EG, (2010) RNAs actively cycle on the Sm-like protein Hfq. Genes Dev 24: 2621-2626
25. Figueroa-Bossi N, Valentini M, Malleret L, Fiorini F, Bossi L, (2009) Caught at its own game: regulatory small RNA inactivated by an inducible transcript mimicking its target. Genes Dev 23: 2004-2015
26. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Paz-Ares J, (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39: 1033-1037
27. Fröhlich KS, Papenfort K, Fekete A, Vogel J, (2013) A small RNA activates CFA synthase by isoform-specific mRNA stabilization. EMBO J 32: 2963-2979
28. Garrey SM, Blech M, Riffell JL, Hankins JS, Stickney LM, Diver M, Hsu YH, Kunanithy V, Mackie GA, (2009) Substrate binding and active site residues in RNases E and G: role of the 5′-sensor. J Biol Chem 284: 31843-31850
29. Geissmann T, Chevalier C, Cros MJ, Boisset S, Fechter P, Noirot C, Schrenzel J, François P, Vandenesch F, Gaspin C, Romby P, (2009) A search for small noncoding RNAs in Staphylococcus aureus reveals a conserved sequence motif for regulation. Nucleic Acids Res 37: 7239-7257
30. Ghrist AC, Heil G, Stauffer GV, (2001) GcvR interacts with GcvA to inhibit activation of the Escherichia coli glycine cleavage operon. Microbiology 147: 2215-2221
31. Göpel Y, Papenfort K, Reichenbach B, Vogel J, Görke B, (2013) Targeted decay of a regulatory small RNA by an adaptor protein for RNase E and counteraction by an anti-adaptor RNA. Genes Dev 27: 552-564
32. E-dependent sRNA, combats envelope stress by repressing synthesis of Lpp, the major outer membrane lipoprotein. Genes Dev 28: 1620-1634
33. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J, (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495: 384-388
34. Heil G, Stauffer LT, Stauffer GV, (2002) Glycine binds the transcriptional accessory protein GcvR to disrupt a GcvA/GcvR interaction and allow GcvA-mediated activation of the Escherichia coli gcvTHP operon. Microbiology 148: 2203-2214
35. Hiles ID, Higgins CF, (1986) Peptide uptake by Salmonella Typhimurium. The periplasmic oligopeptide-binding protein. Eur J Biochem 158: 561-567
36. Hui MP, Foley PL, Belasco JG, (2014) Messenger RNA degradation in bacterial cells. Annu Rev Genet 48: 537-559
37. Hussein R, Lim HN, (2011) Disruption of small RNA signaling caused by competition for Hfq. Proc Natl Acad Sci USA 108: 1110-1115
38. Jørgensen MG, Nielsen JS, Boysen A, Franch T, Møller-Jensen J, Valentin-Hansen P, (2012) Small regulatory RNAs control the multi-cellular adhesive lifestyle of Escherichia coli. Mol Microbiol 84: 36-50
39. Jørgensen MG, Thomason MK, Havelund J, Valentin-Hansen P, Storz G, (2013) Dual function of the McaS small RNA in controlling biofilm formation. Genes Dev 27: 1132-1145
40. Jourdan SS, McDowall KJ, (2008) Sensing of 5′ monophosphate by Escherichia coli RNase G can significantly enhance association with RNA and stimulate the decay of functional mRNA transcripts in vivo. Mol Microbiol 67: 102-115
41. Kim D, Hong JS, Qiu Y, Nagarajan H, Seo JH, Cho BK, Tsai SF, Palsson BØ, (2012) Comparative analysis of regulatory elements between Escherichia coli and Klebsiella pneumoniae by genome-wide transcription start site profiling. PLoS Genet 8: e1002867
42. Kim HM, Shin JH, Cho YB, Roe JH, (2014) Inverse regulation of Fe- and Ni-containing SOD genes by a Fur family regulator Nur through small RNA processed from 3′UTR of the sodF mRNA. Nucleic Acids Res 42: 2003-2014
43. Kröger C, Dillon SC, Cameron AD, Papenfort K, Sivasankaran SK, Hokamp K, Chao Y, Sittka A, Hébrard M, Händler K, Colgan A, Leekitcharoenphon P, Langridge GC, Lohan AJ, Loftus B, Lucchini S, Ussery DW, Dorman CJ, Thomson NR, Vogel J, et al, (2012) The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc Natl Acad Sci USA 109: E1277-E1286
44. Kröger C, Colgan A, Srikumar S, Händler K, Sivasankaran SK, Hammarlöf DL, Canals R, Grissom JE, Conway T, Hokamp K, Hinton JC, (2013) An infection-relevant transcriptomic compendium for Salmonella enterica Serovar Typhimurium. Cell Host Microbe 14: 683-695
45. Lutz R, Bujard H, (1997) Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res 25: 1203-1210
46. Mandin P, Gottesman S, (2009a) A genetic approach for finding small RNAs regulators of genes of interest identifies RybC as regulating the DpiA/DpiB two-component system. Mol Microbiol 72: 551-565
47. Mandin P, Gottesman S, (2009b) Regulating the regulator: an RNA decoy acts as an OFF switch for the regulation of an sRNA. Genes Dev 23: 1981-1985
48. Marcinowski L, Tanguy M, Krmpotic A, Rädle B, Lisnic VJ, Tuddenham L, Chane-Woon-Ming B, Ruzsics Z, Erhard F, Benkartek C, Babic M, Zimmer R, Trgovcich J, Koszinowski UH, Jonjic S, Pfeffer S, Dölken L, (2012) Degradation of cellular mir-27 by a novel, highly abundant viral transcript is important for efficient virus replication in vivo. PLoS Pathog 8: e1002510
49. Massé E, Escorcia FE, Gottesman S, (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev 17: 2374-2383
50. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, Loewer A, Ziebold U, Landhaler M, Kocks C, le Noble F, Rajewsky N, (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495: 333-338
51. Mika F, Busse S, Possling A, Berkholz J, Tschowri N, Sommerfeldt N, Pruteanu M, Hengge R, (2012) Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli. Mol Microbiol 84: 51-65
52. Modi SR, Camacho DM, Kohanski MA, Walker GC, Collins JJ, (2011) Functional characterization of bacterial sRNAs using a network biology approach. Proc Natl Acad Sci USA 108: 15522-15527
53. Möller P, Overlöper A, Förstner KU, Wen TN, Sharma CM, Lai EM, Narberhaus F, (2014) Profound Impact of Hfq on Nutrient Acquisition, Metabolism and Motility in the Plant Pathogen Agrobacterium tumefaciens. PLoS One 9: e110427
54. Moon K, Gottesman S, (2011) Competition among Hfq-binding small RNAs in Escherichia coli. Mol Microbiol 82: 1545-1562
55. 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
56. Mutalik VK, Nonaka G, Ades SE, Rhodius VA, Gross CA, (2009) Promoter strength properties of the complete sigma E regulon of Escherichia coli and Salmonella enterica. J Bacteriol 191: 7279-7287
57. Nichols RJ, Sen S, Choo YJ, Beltrao P, Zietek M, Chaba R, Lee S, Kazmierczak KM, Lee KJ, Wong A, Shales M, Lovett S, Winkler ME, Krogan NJ, Typas A, Gross CA, (2011) Phenotypic landscape of a bacterial cell. Cell 144: 143-156
58. Ortega AD, Gonzalo-Asensio J, García-del Portillo F, (2012) Dynamics of Salmonella small RNA expression in non-growing bacteria located inside eukaryotic cells. RNA Biol 9: 469-488
59. Overgaard M, Johansen J, Møller-Jensen J, Valentin-Hansen P, (2009) Switching off small RNA regulation with trap-mRNA. Mol Microbiol 73: 790-800
60. Overlöper A, Kraus A, Gurski R, Wright PR, Georg J, Hess WR, Narberhaus F, (2014) Two separate modules of the conserved regulatory RNA AbcR1 address multiple target mRNAs in and outside of the translation initiation region. RNA Biol 11: 624-640
61. E-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol Microbiol 62: 1674-1688
62. Papenfort K, Pfeiffer V, Lucchini S, Sonawane A, Hinton JC, Vogel J, (2008) Systematic deletion of Salmonella small RNA genes identifies CyaR, a conserved CRP-dependent riboregulator of OmpX synthesis. Mol Microbiol 68: 890-906
63. Papenfort K, Said N, Welsink T, Lucchini S, Hinton JC, Vogel J, (2009) Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 74: 139-158
64. Papenfort K, Bouvier M, Mika F, Sharma CM, Vogel J, (2010) Evidence for an autonomous 5′ target recognition domain in an Hfq-associated small RNA. Proc Natl Acad Sci USA 107: 20435-20440
65. Papenfort K, Sun Y, Miyakoshi M, Vanderpool CK, Vogel J, (2013) Small RNA-mediated activation of sugar phosphatase mRNA regulates glucose homeostasis. Cell 153: 426-437
66. Papenfort K, Vogel J, (2014) Small RNA functions in carbon metabolism and virulence of enteric pathogens. Front Cell Infect Microbiol 4: 91
67. Pfeiffer V, Sittka A, Tomer R, Tedin K, Brinkmann V, Vogel J, (2007) A small non-coding RNA of the invasion gene island (SPI-1) represses outer membrane protein synthesis from the Salmonella core genome. Mol Microbiol 66: 1174-1191
68. Plumbridge J, Bossi L, Oberto J, Wade JT, Figueroa-Bossi N, (2014) Interplay of transcriptional and small RNA-dependent control mechanisms regulates chitosugar uptake in Escherichia coli and Salmonella. Mol Microbiol 92: 648-658
69. Pulvermacher SC, Stauffer LT, Stauffer GV, (2008) The role of the small regulatory RNA GcvB in GcvB/mRNA posttranscriptional regulation of oppA and dppA in Escherichia coli. FEMS Microbiol Lett 281: 42-50
70. Pulvermacher SC, Stauffer LT, Stauffer GV, (2009) Role of the sRNA GcvB in regulation of cycA in Escherichia coli. Microbiology 155: 106-114
71. 54-dependent genes in Escherichia coli. Microbiol Mol Biol Rev 65: 422-444
72. Reitzer L, (2004). Biosynthesis of glutamate, aspartate, asparagine, L-alanine, and D-alanine. In EcoSal Plus, Curtiss R, Kaper JB, Karp PD, Neidhardt FC, Slauch JM, (eds). Washington, DC: ASM Press
73. Reitzer L,. (2005). Catabolism of amino acids and related compounds. In EcoSal Plus, Curtiss R, Kaper JB, Karp PD, Neidhardt FC, Slauch JM, (eds). Washington, DC: ASM Press.
74. Rubio-Somoza I, Weigel D, Franco-Zorilla JM, García JA, Paz-Ares J, (2011) ceRNAs: miRNA target mimic mimics. Cell 147: 1431-1432
75. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP, (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146: 353-358
76. Salvail H, Caron MP, Bélanger J, Massé E, (2013) Antagonistic functions between the RNA chaperone Hfq and an sRNA regulate sensitivity to the antibiotic colicin. EMBO J 32: 2764-2778
77. Saramago M, Bárria C, Dos Santos RF, Silva IJ, Pobre V, Domingues S, Andrade JM, Viegas SC, Arraiano CM, (2014) The role of RNases in the regulation of small RNAs. Curr Opin Microbiol 18: 105-115
78. Schellenberg GD, Furlong CE, (1977) Resolution of the multiplicity of the glutamate and aspartate transport systems of Escherichia coli. J Biol Chem 252: 9055-9064
79. Seitz H, (2009) Redefining microRNA targets. Curr Biol 19: 870-873
80. Sharma CM, Darfeuille F, Plantinga TH, Vogel J, (2007) A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites. Genes Dev 21: 2804-2817
81. Sharma CM, Papenfort K, Pernitzsch SR, Mollenkopf HJ, Hinton JC, Vogel J, (2011) Pervasive post-transcriptional control of genes involved in amino acid metabolism by the Hfq-dependent GcvB small RNA. Mol Microbiol 81: 1144-1165
82. 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
83. Sobrero P, Valverde C, (2012) The bacterial protein Hfq: much more than a mere RNA-binding factor. Crit Rev Microbiol 38: 276-299
84. Sonnleitner E, Sorger-Domenigg T, Madej MJ, Findeiss S, Hackermüller J, Hüttenhofer A, Stadler PF, Bläsi U, Moll I, (2008) Detection of small RNAs in Pseudomonas aeruginosa by RNomics and structure-based bioinformatic tools. Microbiology 154: 3175-3187
85. Sonnleitner E, Gonzalez N, Sorger-Domenigg T, Heeb S, Richter AS, Backofen R, Williams P, Hüttenhofer A, Haas D, Bläsi U, (2011) The small RNA PhrS stimulates synthesis of the Pseudomonas aeruginosa quinolone signal. Mol Microbiol 80: 868-885
86. Stauffer LT, Stauffer GV, (2005) GcvA interacts with both the alpha and sigma subunits of RNA polymerase to activate the Escherichia coli gcvB gene and the gcvTHP operon. FEMS Microbiol Lett 242: 333-338
87. Stauffer LT, Stauffer GV, (2012) Antagonistic Roles for GcvA and GcvB in hdeAB Expression in Escherichia coli. ISRN Microbiol 2012: 697308
88. Stirling DA, Hulton CS, Waddell L, Park SF, Stewart GS, Booth IR, Higgins CF, (1989) Molecular characterization of the proU loci of Salmonella Typhimurium and Escherichia coli encoding osmoregulated glycine betaine transport systems. Mol Microbiol 3: 1025-1038
89. Storz G, Vogel J, Wassarman KM, (2011) Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 43: 880-891
90. Suzuki K, Babitzke P, Kushner SR, Romeo T, (2006) Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev 20: 2605-2617
91. Torres-Quesada O, Millán V, Nisa-Martínez R, Bardou F, Crespi M, Toro N, Jiménez-Zurdo JI, (2013) Independent activity of the homologous small regulatory RNAs AbcR1 and AbcR2 in the legume symbiont Sinorhizobium meliloti. PLoS One 8: e68147
92. Tree JJ, Granneman S, McAteer SP, Tollervey D, Gally DL, (2014) Identification of bacteriophage-encoded anti-sRNAs in pathogenic Escherichia coli. Mol Cell 55: 199-213
93. Urban JH, Vogel J, (2007) Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res 35: 1018-1037
94. Urbanowski ML, Stauffer LT, Stauffer GV, (2000) The gcvB gene encodes a small untranslated RNA involved in expression of the dipeptide and oligopeptide transport systems in Escherichia coli. Mol Microbiol 37: 856-868
95. Vanderpool CK, (2011) Combined experimental and computational strategies define an expansive regulon for GcvB small RNA. Mol Microbiol 81: 1129-1132
96. Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jäger JG, Hüttenhofer 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
97. Vogel J, Luisi BF, (2011) Hfq and its constellation of RNA. Nat Rev Microbiol 9: 578-589
98. Wahl A, Hubert P, Sturgis JN, Bouveret E, (2009) Tagging of Escherichia coli proteins with new cassettes allowing in vivo systematic fluorescent and luminescent detection, and purification from physiological expression levels. Proteomics 9: 5389-5393
99. Willis RC, Furlong CE, (1975) Purification and properties of a periplasmic glutamate-aspartate binding protein from Escherichia coli K12 strain W3092. J Biol Chem 250: 2574-2580
100. Wright PR, Richter AS, Papenfort K, Mann M, Vogel J, Hess WR, Backofen R, Georg J, (2013) Comparative genomics boosts target prediction for bacterial small RNAs. Proc Natl Acad Sci USA 110: E3487-E3496
101. Yang Q, Figueroa-Bossi N, Bossi L, (2014) Translation enhancing ACA motifs and their silencing by a bacterial small regulatory RNA. PLoS Genet 10: e1004026
102. Zhang A, Wassarman KM, Rosenow C, Tjaden BC, Storz G, Gottesman S, (2003) Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol 50: 1111-1124