Cycling of RNAs on Hfq

RNA Biology

Volumn 10, Issue 4, 2013, Pages 619-626

  Wagner, E Gerhart H ^a,b  

^a UPPSALA UNIVERSITY   (Sweden)

^b SCIENCE FOR LIFE LABORATORY   (Sweden)

Author keywords

Binding kinetics; Protein RNA interaction; RNA chaperone; RNA exchange; sRNA mediated regulation

Indexed keywords

CHAPERONE; HFQ PROTEIN; MESSENGER RNA; RNA; TRANSFER RNA; UNCLASSIFIED DRUG;

DISSOCIATION; NONHUMAN; PHENOTYPE; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RESPONSE TIME; REVIEW; RNA METABOLISM;

EID: 84879014020     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.24044     Document Type: Review

References (94)

1. Lau NC, Lim LP, Weinstein EG, Bartel DP. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 2001; 294:858-62; PMID:11679671; http://dx.doi.org/10.1126/science.1065062.
2. Lee RC, Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001; 294:862-4; PMID:11679672; http://dx.doi.org/10.1126/ science.1065329.
3. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001; 294:853-8; PMID:11679670; http://dx.doi.org/10.1126/science.1064921.
4. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EGH, 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.
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. Waters LS, Storz G. Regulatory RNAs in bacteria. Cell 2009; 136:615-28; PMID:19239884; http://dx.doi.org/10.1016/j.cell.2009.01.043.
7. 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.
8. Holmqvist E, Unoson C, Reimegård J, Wagner EGH. A mixed double negative feedback loop between the sRNA MicF and the global regulator Lrp. Mol Microbiol 2012; 84:414-27; PMID:22324810; http://dx.doi.org/10.1111/j.1365-2958. 2012.07994.x.
9. Franze de Fernandez MT, Eoyang L, August JT. Factor fraction required for the synthesis of bacteriophage Qbeta-RNA. Nature 1968; 219:588-90; PMID:4874917; http://dx.doi.org/10.1038/219588a0.
10. Schumacher MA, Pearson RF, Møller T, Valentin-Hansen P, Brennan RG. Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein. EMBO J 2002; 21:3546-56; PMID:12093755; http://dx.doi.org/10.1093/emboj/cdf322.
11. Sauter C, Basquin J, Suck D. Sm-like proteins in Eubacteria: the crystal structure of the Hfq protein from Escherichia coli. Nucleic Acids Res 2003; 31:4091-8; PMID:12853626; http://dx.doi.org/10.1093/nar/gkg480.
12. Nikulin A, Stolboushkina E, Perederina A, Vassilieva I, Blaesi U, Moll I, et al. Structure of Pseudomonas aeruginosa Hfq protein. Acta Crystallogr D Biol Crystallogr 2005; 61:141-6; PMID:15681864; http://dx.doi.org/10.1107/ S0907444904030008.
13. Link TM, Valentin-Hansen P, Brennan RG. Structure of Escherichia coli Hfq bound to polyriboadenylate RNA. Proc Natl Acad Sci USA 2009; 106:19292-7; PMID:19889981; http://dx.doi.org/10.1073/pnas.0908744106.
14. 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.
15. Doetsch M, Stampfl S, Fürtig B, Beich-Frandsen M, Saxena K, Lybecker M, et al. Study of E. coli Hfq's RNA annealing acceleration and duplex destabilization activities using substrates with different GC-contents. Nucleic Acids Res 2013; 41:487-97; PMID:23104381; http://dx.doi.org/10.1093/nar/gks942.
16. Hopkins JF, Panja S, Woodson SA. Rapid binding and release of Hfq from ternary complexes during RNA annealing. Nucleic Acids Res 2011; 39:5193-202; PMID:21378124; http://dx.doi.org/10.1093/nar/gkr062.
17. Hwang W, Arluison V, Hohng S. Dynamic competition of DsrA and rpoS fragments for the proximal binding site of Hfq as a means for efficient annealing. Nucleic Acids Res 2011; 39:5131-9; PMID:21357187; http://dx.doi.org/10.1093/nar/gkr075.
18. Chao Y, Vogel J. The role of Hfq in bacterial pathogens. Curr Opin Microbiol 2010; 13:24-33; PMID:20080057; http://dx.doi.org/10.1016/j.mib.2010. 01.001.
19. Valentin-Hansen P, Eriksen M, Udesen C. The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol Microbiol 2004; 51:1525-33; PMID:15009882; http://dx.doi.org/10.1111/j.1365-2958.2003.03935.x.
20. Berghoff BA, Glaeser J, Sharma CM, Zobawa M, Lottspeich F, Vogel J, et al. Contribution of Hfq to photooxidative stress resistance and global regulation in Rhodobacter sphaeroides. Mol Microbiol 2011; 80:1479-95; PMID:21535243; http://dx.doi.org/10.1111/j.1365-2958.2011.07658.x.
21. Ding Y, Davis BM, Waldor MK. Hfq is essential for Vibrio cholerae virulence and downregulates sigma expression. Mol Microbiol 2004; 53:345-54; PMID:15225327; http://dx.doi.org/10.1111/j.1365-2958.2004.04142.x.
22. Guisbert E, Rhodius VA, Ahuja N, Witkin E, Gross CA. Hfq modulates the sigmaE-mediated envelope stress response and the sigma32-mediated cytoplasmic stress response in Escherichia coli. J Bacteriol 2007; 189:1963-73; PMID:17158661; http://dx.doi.org/10.1128/JB.01243-06.
23. Sonnleitner E, Schuster M, Sorger-Domenigg T, Greenberg EP, Bläsi U. Hfq-dependent alterations of the transcriptome profile and effects on quorum sensing in Pseudomonas aeruginosa. Mol Microbiol 2006; 59:1542-58; PMID:16468994; http://dx.doi.org/10.1111/j.1365-2958.2006.05032.x.
24. 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.
25. Ikeda Y, Yagi M, Morita T, Aiba H. Hfq binding at RhlB-recognition region of RNase E is crucial for the rapid degradation of target mRNAs mediated by sRNAs in Escherichia coli. Mol Microbiol 2011; 79:419-32; PMID:21219461; http://dx.doi.org/10.1111/j.1365-2958.2010.07454.x.
26. Sukhodolets MV, Garges S. Interaction of Escherichia coli RNA polymerase with the ribosomal protein S1 and the Sm-like ATPase Hfq. Biochemistry 2003; 42:8022-34; PMID:12834354; http://dx.doi.org/10.1021/bi020638i.
27. De Lay N, Gottesman S. Role of polynucleotide phosphorylase in sRNA function in Escherichia coli. RNA 2011; 17:1172-89; PMID:21527671; http://dx.doi.org/10.1261/rna.2531211.
28. 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.
29. 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.
30. 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.
31. Massé E, Escorcia FE, Gottesman S. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev 2003; 17:2374-83; PMID:12975324; http://dx.doi.org/10.1101/gad.1127103.
32. rd, Brennan RG. Structural mechanism of Staphylococcus aureus Hfq binding to an RNA A-tract. Nucleic Acids Res 2012; 40:11023-35; PMID:22965117; http://dx.doi.org/10.1093/nar/gks809.
33. Nielsen JS, Bøggild A, Andersen CB, Nielsen G, Boysen A, Brodersen DE, et al. An Hfq-like protein in archaea: crystal structure and functional characterization of the Sm protein from Methanococcus jannaschii. RNA 2007; 13:2213-23; PMID:17959927; http://dx.doi.org/10.1261/rna.689007.
34. Sauer E, Weichenrieder O. Structural basis for RNA 3′-end recognition by Hfq. Proc Natl Acad Sci USA 2011; 108:13065-70; PMID:21737752; http://dx.doi.org/10.1073/pnas.1103420108.
35. Someya T, Baba S, Fujimoto M, Kawai G, Kumasaka T, Nakamura K. Crystal structure of Hfq from Bacillus subtilis in complex with SELEX-derived RNA aptamer: insight into RNA-binding properties of bacterial Hfq. Nucleic Acids Res 2012; 40:1856-67; PMID:22053080; http://dx.doi.org/10.1093/nar/gkr892.
36. Otaka H, Ishikawa H, Morita T, Aiba H. PolyU tail of rho-independent terminator of bacterial small RNAs is essential for Hfq action. Proc Natl Acad Sci USA 2011; 108:13059-64; PMID:21788484; http://dx.doi.org/10.1073/pnas. 1107050108.
37. Ishikawa H, Otaka H, Maki K, Morita T, Aiba H. The functional Hfq-binding module of bacterial sRNAs consists of a double or single hairpin preceded by a U-rich sequence and followed by a 3′ poly(U) tail. RNA 2012; 18:1062-74; PMID:22454537; http://dx.doi.org/10.1261/rna.031575.111.
38. Olejniczak M. Despite similar binding to the Hfq protein regulatory RNAs widely differ in their competition performance. Biochemistry 2011; 50:4427-40; PMID:21510661; http://dx.doi.org/10.1021/bi102043f.
39. 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.
40. Mikulecky PJ, Kaw MK, Brescia CC, Takach JC, Sledjeski DD, Feig AL. Escherichia coli Hfq has distinct interaction surfaces for DsrA, rpoS and poly(A) RNAs. Nat Struct Mol Biol 2004; 11:1206-14; PMID:15531892; http://dx.doi.org/10.1038/nsmb858.
41. Salim NN, Faner MA, Philip JA, Feig AL. Requirement of upstream Hfq-binding (ARN)x elements in glmS and the Hfq C-terminal region for GlmS upregulation by sRNAs GlmZ and GlmY. Nucleic Acids Res 2012; 40:8021-32; PMID:22661574; http://dx.doi.org/10.1093/nar/gks392.
42. Fender A, Elf J, Hampel K, Zimmermann B, Wagner EGH. RNAs actively cycle on the Sm-like protein Hfq. Genes Dev 2010; 24:2621-6; PMID:21123649; http://dx.doi.org/10.1101/gad.591310.
43. Salim NN, Feig AL. An upstream Hfq binding site in the fhlA mRNA leader region facilitates the OxyS-fhlA interaction. PLoS One 2010; 5:5; PMID:20927406; http://dx.doi.org/10.1371/journal.pone.0013028.
44. Wang W, Wang L, Zou Y, Zhang J, Gong Q, Wu J, et al. Cooperation of Escherichia coli Hfq hexamers in DsrA binding. Genes Dev 2011; 25:2106-17; PMID:21979921; http://dx.doi.org/10.1101/gad.16746011.
45. Sauer E, Schmidt S, Weichenrieder O. Small RNA binding to the lateral surface of Hfq hexamers and structural rearrangements upon mRNA target recognition. Proc Natl Acad Sci USA 2012; 109:9396-401; PMID:22645344; http://dx.doi.org/10.1073/pnas.1202521109.
46. Vecerek B, Rajkowitsch L, Sonnleitner E, Schroeder R, Bläsi U. The C-terminal domain of Escherichia coli Hfq is required for regulation. Nucleic Acids Res 2008; 36:133-43; PMID:18000007; http://dx.doi.org/10.1093/nar/gkm985.
47. Sonnleitner E, Napetschnig J, Afonyushkin T, Ecker K, Vecerek B, Moll I, et al. Functional effects of variants of the RNA chaperone Hfq. Biochem Biophys Res Commun 2004; 323:1017-23; PMID:15381101; http://dx.doi.org/10.1016/j.bbrc. 2004.08.190.
48. Olsen AS, Møller-Jensen J, Brennan RG, Valentin-Hansen P. C-terminally truncated derivatives of Escherichia coli Hfq are proficient in riboregulation. J Mol Biol 2010; 404:173-82; PMID:20888338; http://dx.doi.org/ 10.1016/j.jmb.2010.09.038.
49. Lorenz C, Gesell T, Zimmermann B, Schoeberl U, Bilusic I, Rajkowitsch L, et al. Genomic SELEX for Hfq-binding RNAs identifies genomic aptamers predominantly in antisense transcripts. Nucleic Acids Res 2010; 38:3794-808; PMID:20348540; http://dx.doi.org/10.1093/nar/gkq032.
50. 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.
51. Chao Y, Papenfort K, Reinhardt R, Sharma CM, Vogel J. An atlas of Hfq-bound transcripts reveals 3′ UTRs as a genomic reservoir of regulatory small RNAs. EMBO J 2012; 31:4005-19; PMID:22922465; http://dx.doi.org/10.1038/ emboj.2012.229.
52. Sonnleitner E, Sorger-Domenigg T, Madej MJ, Findeiss S, Hackermüller J, Hüttenhofer A, et al. Detection of small RNAs in Pseudomonas aeruginosa by RNomics and structure-based bioinformatic tools. Microbiology 2008; 154:3175-87; PMID:18832323; http://dx.doi.org/10.1099/mic.0.2008/019703-0.
53. 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.
54. Udekwu KI, Darfeuille F, Vogel J, Reimegård J, Holmqvist E, Wagner EGH. Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev 2005; 19:2355-66; PMID:16204185; http://dx.doi.org/10.1101/gad. 354405.
55. Folichon M, Arluison V, Pellegrini O, Huntzinger E, Régnier P, Hajnsdorf E. The poly(A) binding protein Hfq protects RNA from RNase E and exoribonucleolytic degradation. Nucleic Acids Res 2003; 31:7302-10; PMID:14654705; http://dx.doi.org/10.1093/nar/gkg915.
56. 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.
57. Zhang A, Wassarman KM, Ortega J, Steven AC, Storz G. The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol Cell 2002; 9:11-22; PMID:11804582; http://dx.doi.org/10.1016/S1097-2765(01)00437-3.
58. Soper T, Mandin P, Majdalani N, Gottesman S, Woodson SA. Positive regulation by small RNAs and the role of Hfq. Proc Natl Acad Sci USA 2010; 107:9602-7; PMID:20457943; http://dx.doi.org/10.1073/pnas.1004435107.
59. Lease RA, Woodson SA. Cycling of the Sm-like protein Hfq on the DsrA small regulatory RNA. J Mol Biol 2004; 344:1211-23; PMID:15561140; http://dx.doi.org/10.1016/j.jmb.2004.10.006.
60. Sun X, Wartell RM. Escherichia coli Hfq binds A18 and DsrA domain II with similar 2:1 Hfq6/RNA stoichiometry using different surface sites. Biochemistry 2006; 45:4875-87; PMID:16605255; http://dx.doi.org/10.1021/bi0523613.
61. Panja S, Woodson SA. Hfq proximity and orientation controls RNA annealing. Nucleic Acids Res 2012; 40:8690-7; PMID:22761405; http://dx.doi.org/10.1093/nar/gks618.
62. Beisel CL, Updegrove TB, Janson BJ, Storz G. Multiple factors dictate target selection by Hfq-binding small RNAs. EMBO J 2012; 31:1961-74; PMID:22388518; http://dx.doi.org/10.1038/emboj.2012.52.
63. Rajkowitsch L, Schroeder R. Dissecting RNA chaperone activity. RNA 2007; 13:2053-60; PMID:17901153; http://dx.doi.org/10.1261/rna.671807.
64. Geissmann TA, Touati D. Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator. EMBO J 2004; 23:396-405; PMID:14739933; http://dx.doi.org/10.1038/sj.emboj.7600058.
65. Ribeiro EdeA Jr., Beich-Frandsen M, Konarev PV, Shang W, Vecerek B, Kontaxis G, et al. Structural flexibility of RNA as molecular basis for Hfq chaperone function. Nucleic Acids Res 2012; 40:8072-84; PMID:22718981; http://dx.doi.org/10.1093/nar/gks510.
66. Moll I, Leitsch D, Steinhauser T, Bläsi U. RNA chaperone activity of the Sm-like Hfq protein. EMBO Rep 2003; 4:284-9; PMID:12634847; http://dx.doi.org/10.1038/sj.embor.embor772.
67. Vincent HA, Henderson CA, Stone CM, Cary PD, Gowers DM, Sobott F, et al. The low-resolution solution structure of Vibrio cholerae Hfq in complex with Qrr1 sRNA. Nucleic Acids Res 2012; 40:8698-710; PMID:22730296; http://dx.doi.org/10.1093/nar/gks582.
68. Holmqvist E, Reimegård J, Sterk M, Grantcharova N, Römling U, Wagner EGH. Two antisense RNAs target the transcriptional regulator CsgD to inhibit curli synthesis. EMBO J 2010; 29:1840-50; PMID:20407422; http://dx.doi.org/10.1038/emboj.2010.73.
69. Updegrove TB, Correia JJ, Chen Y, Terry C, Wartell RM. The stoichiometry of the Escherichia coli Hfq protein bound to RNA. RNA 2011; 17:489-500; PMID:21205841; http://dx.doi.org/10.1261/rna.2452111.
70. Hopkins JF, Panja S, McNeil SA, Woodson SA. Effect of salt and RNA structure on annealing and strand displacement by Hfq. Nucleic Acids Res 2009; 37:6205-13; PMID:19671524; http://dx.doi.org/10.1093/nar/gkp646.
71. 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.
72. Hussein R, Lim HN. Disruption of small RNA signaling caused by competition for Hfq. Proc Natl Acad Sci USA 2011; 108:1110-5; PMID:21189298; http://dx.doi.org/10.1073/pnas.1010082108.
73. Galluppi GR, Richardson JP. ATP-induced changes in the binding of RNA synthesis termination protein Rho to RNA. J Mol Biol 1980; 138:513-39; PMID:6157829; http://dx.doi.org/10.1016/S0022-2836(80)80016-7.
74. Steinmetz EJ, Platt T. Evidence supporting a tethered tracking model for helicase activity of Escherichia coli Rho factor. Proc Natl Acad Sci USA 1994; 91:1401-5; PMID:7509071; http://dx.doi.org/10.1073/pnas.91.4.1401.
75. Afonyushkin T, Vecerek B, Moll I, Bläsi U, Kaberdin VR. Both RNase E and RNase III control the stability of sodB mRNA upon translational inhibition by the small regulatory RNA RyhB. Nucleic Acids Res 2005; 33:1678-89; PMID:15781494; http://dx.doi.org/10.1093/nar/gki313.
76. Hämmerle H, Beich-Frandsen M, Veèerek B, Rajkowitsch L, Carugo O, Djinoviæ-Carugo K, et al. Structural and biochemical studies on ATP binding and hydrolysis by the Escherichia coli RNA chaperone Hfq. PLoS One 2012; 7:e50892; PMID:23226421; http://dx.doi.org/10.1371/journal.pone.0050892.
77. Vogel J, Argaman L, Wagner EGH, 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.
78. Panja S, Woodson SA. Hexamer to monomer equilibrium of E. coli Hfq in solution and its impact on RNA annealing. J Mol Biol 2012; 417:406-12; PMID:22326348; http://dx.doi.org/10.1016/j.jmb.2012.02.009.
79. Carmichael GG, Weber K, Niveleau A, Wahba AJ. The host factor required for RNA phage Qbeta RNA replication in vitro. Intracellular location, quantitation, and purification by polyadenylate-cellulose chromatography. J Biol Chem 1975; 250:3602-12; PMID:165178.
80. Kajitani M, Kato A, Wada A, Inokuchi Y, Ishihama A. Regulation of the Escherichia coli hfq gene encoding the host factor for phage Q beta. J Bacteriol 1994; 176:531-4; PMID:8288550.
81. Ali Azam T, Iwata A, Nishimura A, Ueda S, Ishihama A. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 1999; 181:6361-70; PMID:10515926.
82. Sittka A, Sharma CM, Rolle K, Vogel J. Deep sequencing of Salmonella RNA associated with heterologous Hfq proteins in vivo reveals small RNAs as a major target class and identifies RNA processing phenotypes. RNA Biol 2009; 6:266-75; PMID:19333007; http://dx.doi.org/10.4161/rna.6.3.8332.
83. 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.
84. Montero Llopis P, Jackson AF, Sliusarenko O, Surovtsev I, Heinritz J, Emonet T, et al. Spatial organization of the flow of genetic information in bacteria. Nature 2010; 466:77-81; PMID:20562858; http://dx.doi.org/10.1038/ nature09152.
85. Diestra E, Cayrol B, Arluison V, Risco C. Cellular electron microscopy imaging reveals the localization of the Hfq protein close to the bacterial membrane. PLoS One 2009; 4:e8301; PMID:20011543; http://dx.doi.org/10.1371/ journal.pone.0008301.
86. Persson F, Lindén M, Unoson C, Elf J. Extracting intracellular diffusive states and transition rates from single-molecule tracking data. Nat Methods 2013; In press; PMID:23396281; http://dx.doi.org/10.1038/nmeth.2367.
87. Mehta P, Goyal S, Wingreen NS. A quantitative comparison of sRNA-based and protein-based gene regulation. Mol Syst Biol 2008; 4:221; PMID:18854820; http://dx.doi.org/10.1038/msb.2008.58.
88. Levine E, Zhang Z, Kuhlman T, Hwa T. Quantitative characteristics of gene regulation by small RNA. PLoS Biol 2007; 5:e229; PMID:17713988; http://dx.doi.org/10.1371/journal.pbio.0050229.
89. Slagter-Jäger JG. The role of Hfq in antisense RNA-mediated regulation: a comparison between trans- and cis-encoded RNAs. In: PhD thesis, Uppsala university 2003.
90. Wagner EGH, Altuvia S, Romby P. Antisense RNAs in bacteria and their genetic elements. Adv Genet 2002; 46:361-98; PMID:11931231; http://dx.doi.org/ 10.1016/S0065-2660(02)46013-0.
91. Romby P, Vandenesch F, Wagner EGH. The role of RNAs in the regulation of virulence-gene expression. Curr Opin Microbiol 2006; 9:229-36; PMID:16529986; http://dx.doi.org/10.1016/j.mib.2006.02.005.
92. Hao Y, Zhang ZJ, Erickson DW, Huang M, Huang Y, Li J, et al. Quantifying the sequence-function relation in gene silencing by bacterial small RNAs. Proc Natl Acad Sci USA 2011; 108:12473-8; PMID:21742981; http://dx.doi.org/10.1073/ pnas.1100432108.
93. Pandey SP, Minesinger BK, Kumar J, Walker GC. A highly conserved protein of unknown function in Sinorhizobium meliloti affects sRNA regulation similar to Hfq. Nucleic Acids Res 2011; 39:4691-708; PMID:21325267; http://dx.doi.org/10. 1093/nar/gkr060.
94. Bandyra KJ, Said N, Pfeiffer V, Górna MW, Vogel J, Luisi BF. The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E. Mol Cell 2012; 47:943-53; PMID:22902561; http://dx.doi.org/10.1016/j.molcel.2012.07.015.