CoChat
Sign Up
Cited by 98Bacterial Genetics and BiotechnologyRNA and protein synthesis mechanismsRNA Research and Splicing

Hfq CLASH uncovers sRNA-target interaction networks linked to nutrient availability adaptation

Open access
Iosub, Ira Alexandra, van Nues, Robert Willem, McKellar, Stuart William, Nieken, Karen Jule, Marchioretto, Marta, Sy, Brandon, Tree, Jai Justin, Viero, Gabriella +1 more·2020·eLife
DOI 10.7554/elife.54655PMC PMC7213987

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

Abstract By shaping gene expression profiles, small RNAs (sRNAs) enable bacteria to very efficiently adapt to constant changes in their environment. To better understand how Escherichia coli acclimatizes to changes in nutrient availability, we performed UV cross-linking, ligation and sequencing of hybrids (CLASH) to uncover sRNA-target interactions. Strikingly, we uncovered hundreds of novel Hfq-mediated sRNA-target interactions at specific growth stages, involving many novel 3’UTR-derived sRNAs and a plethora of sRNA-sRNA interactions. We discovered sRNA-target interaction networks that play a role in adaptation to changes in nutrient availability. We characterized a novel 3’UTR-derived sRNA (MdoR), which is part of a regulatory cascade that enhances maltose uptake by (a) inactivating repressive pathways that block the accumulation of maltose transporters and (b) by reducing the flux of general porins to the outer membrane. Our work provides striking examples of how bacteria utilize sRNAs to integrate multiple regulatory pathways to enhance nutrient stress adaptation.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.7554/elife.54655

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • CLASH with PIWI protein has been used to reveal mechanisms of piRNA targeting, and CLASH using E. Coli Hfq to enrich for sRNA-mRNA interactions revealed principles of small RNAs in bacteria.

    “CLASH with PIWI protein has been used to reveal mechanisms of piRNA targeting (Shen et al., 2018), and CLASH using E. Coli Hfq to enrich for sRNA-mRNA interactions revealed principles of small RNAs in bacteria (Iosub et al., 2020).”

    From Scalable and deep profiling of mRNA targets for individual microRNAs with chimeric eCLIP (2022) · cites this paper as Iosub et al., 2020

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 87

  1. Andrade JM Dos Santos RF Chelysheva I Ignatova Z Arraiano CM 2018 The RNA-binding protein hfq is important for ribosome biogenesis and affects translation fidelity The EMBO Journal 37 e97631 10.15252/embj.201797631 29669858 PMC5983149 · DOI
  2. Azam MS Vanderpool CK 2015 Talk among yourselves: rna sponges mediate cross talk between functionally related messenger RNAs The EMBO Journal 34 1436 1438 10.15252/embj.201591492 25916829 PMC4474520 · DOI
  3. Baev MV Baev D Radek AJ Campbell JW 2006a Growth of Escherichia coli MG1655 on LB medium: monitoring utilization of amino acids, peptides, and nucleotides with transcriptional microarrays Applied Microbiology and Biotechnology 71 317 322 10.1007/s00253-005-0310-5 16575570 · DOI
  4. Baev MV Baev D Radek AJ Campbell JW 2006b Growth of Escherichia coli MG1655 on LB medium: determining metabolic strategy with transcriptional microarrays Applied Microbiology and Biotechnology 71 323 328 10.1007/s00253-006-0392-8 16645822 · DOI
  5. Bailey TL Boden M Buske FA Frith M Grant CE Clementi L Ren J Li WW Noble WS 2009 MEME SUITE: tools for motif discovery and searching Nucleic Acids Research 37 W202 W208 10.1093/nar/gkp335 19458158 PMC2703892 · DOI · Paper page
  6. Balleza E López-Bojorquez LN Martínez-Antonio A Resendis-Antonio O Lozada-Chávez I Balderas-Martínez YI Encarnación S Collado-Vides J 2009 Regulation by transcription factors in Bacteria: beyond description FEMS Microbiology Reviews 33 133 151 10.1111/j.1574-6976.2008.00145.x 19076632 PMC2704942 · DOI
  7. Bandyra KJ Said N Pfeiffer V Górna 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 Molecular Cell 47 943 953 10.1016/j.molcel.2012.07.015 22902561 PMC3469820 · DOI
  8. Beisel CL Storz G 2011 The base-pairing RNA spot 42 participates in a multioutput feedforward loop to help enact catabolite repression in Escherichia coli Molecular Cell 41 286 297 10.1016/j.molcel.2010.12.027 21292161 PMC3072601 · DOI
  9. Bianco CM Fröhlich KS Vanderpool CK 2019 Bacterial cyclopropane fatty acid synthase mRNA is targeted by activating and repressing small RNAs Journal of Bacteriology 201 19 10.1128/JB.00461-19 PMC6755755 31308070 · DOI
  10. Blattner FR Plunkett G Bloch CA Perna NT Burland V Riley M Collado-Vides J Glasner JD Rode CK Mayhew GF Gregor J Davis NW Kirkpatrick HA Goeden MA Rose DJ Mau B Shao Y 1997 The complete genome sequence of Escherichia coli K-12 Science 277 1453 1462 10.1126/science.277.5331.1453 9278503 · DOI
  11. Bouvier M Sharma CM Mika F Nierhaus KH Vogel J 2008 Small RNA binding to 5' mRNA coding region inhibits translational initiation Molecular Cell 32 827 837 10.1016/j.molcel.2008.10.027 19111662 · DOI
  12. Bruce HA Du D Matak-Vinkovic D Bandyra KJ Broadhurst RW Martin E Sobott F Shkumatov AV Luisi BF 2018 Analysis of the natively unstructured RNA/protein-recognition core in the Escherichia coli RNA degradosome and its interactions with regulatory RNA/Hfq complexes Nucleic Acids Research 46 387 402 10.1093/nar/gkx1083 29136196 PMC5758883 · DOI
  13. 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 The EMBO Journal 31 4005 4019 10.1038/emboj.2012.229 22922465 PMC3474919 · DOI
  14. Chao Y Li L Girodat D Förstner KU Said N Corcoran C Śmiga M Papenfort K Reinhardt R Wieden HJ Luisi BF Vogel J 2017 In Vivo cleavage map illuminates the central role of RNase E in coding and Non-coding RNA pathways Molecular Cell 65 39 51 10.1016/j.molcel.2016.11.002 28061332 PMC5222698 · DOI
  15. Chao Y Vogel J 2016 A 3' UTR-Derived small RNA provides the regulatory noncoding arm of the inner membrane stress response Molecular Cell 61 352 363 10.1016/j.molcel.2015.12.023 26805574 · DOI
  16. De Lay N Gottesman S 2009 The Crp-activated small noncoding regulatory RNA CyaR (RyeE) links nutritional status to group behavior Journal of Bacteriology 191 461 476 10.1128/JB.01157-08 18978044 PMC2620814 · DOI
  17. De Mets F Van Melderen L Gottesman S 2019 Regulation of acetate metabolism and coordination with the TCA cycle via a processed small RNA PNAS 116 1043 1052 10.1073/pnas.1815288116 30591570 PMC6338826 · DOI
  18. El MY Gaviria-Cantin T Sá Nchez-Romero MA Gibert M Westermann AJ Rg Vogel J Balsalobre C 2018 CRP-cAMP mediates silencing of Salmonella virulence at the Post-Transcriptional level 1 PLOS Genetics 26 e1007401 10.1371/journal.pgen.1007401 PMC5991649 29879120 · DOI
  19. Faigenbaum-Romm R Reich A Gatt YE Barsheshet M Argaman L Margalit H 2020 Hierarchy in hfq chaperon occupancy of small RNA targets plays a major role in their regulation Cell Reports 30 3127 3138 10.1016/j.celrep.2020.02.016 32130912 PMC7059120 · DOI
  20. Feng L Rutherford ST Papenfort K Bagert JD van Kessel JC Tirrell DA Wingreen NS Bassler BL 2015 A qrr noncoding RNA deploys four different regulatory mechanisms to optimize quorum-sensing dynamics Cell 160 228 240 10.1016/j.cell.2014.11.051 25579683 PMC4313533 · DOI
  21. Figueroa-Bossi N Bossi L 2018 Sponges and predators in the small RNA WorldRegulating with RNA in Bacteria and archaea American Society of Microbiology 441 451 10.1128/9781683670247.ch25 · DOI
  22. Granneman S Kudla G Petfalski E Tollervey D 2009 Identification of protein binding sites on U3 snoRNA and pre-rRNA by UV cross-linking and high-throughput analysis of cDNAs PNAS 106 9613 9618 10.1073/pnas.0901997106 19482942 PMC2688437 · DOI
  23. Gulliver EL Wright A Lucas DD Mégroz M Kleifeld O Schittenhelm RB Powell DR Seemann T Bulitta JB Harper M Boyce JD 2018 Determination of the small RNA GcvB regulon in the Gram-negative bacterial pathogen Pasteurella multocida and identification of the GcvB seed binding region RNA 24 704 720 10.1261/rna.063248.117 29440476 PMC5900567 · DOI
  24. Guo MS Updegrove TB Gogol EB Shabalina SA Gross CA Storz G 2014 MicL, a new σE-dependent sRNA, combats envelope stress by repressing synthesis of lpp, the major outer membrane lipoprotein Genes & Development 28 1620 1634 10.1101/gad.243485.114 25030700 PMC4102768 · DOI
  25. Han K Tjaden B Lory S 2017 GRIL-seq provides a method for identifying direct targets of bacterial small regulatory RNA by in vivo proximity ligation Nature Microbiology 2 16239 10.1038/nmicrobiol.2016.239 PMC5567838 28005055 · DOI
  26. Helwak A Kudla G Dudnakova T Tollervey D 2013 Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding Cell 153 654 665 10.1016/j.cell.2013.03.043 23622248 PMC3650559 · DOI · Paper page
  27. Holmqvist E Wright PR Li L Bischler T Barquist L Reinhardt R Backofen R Vogel J 2016 Global RNA recognition patterns of post-transcriptional regulators hfq and CsrA revealed by UV crosslinking in vivo The EMBO Journal 35 991 1011 10.15252/embj.201593360 27044921 PMC5207318 · DOI
  28. Holmqvist E Vogel J 2018 RNA-binding proteins in bacteria Nature Reviews Microbiology 16 601 615 10.1038/s41579-018-0049-5 29995832 · DOI
  29. Holmqvist E Wagner EGH 2017 Impact of bacterial sRNAs in stress responses Biochemical Society Transactions 45 1203 1212 10.1042/BST20160363 29101308 PMC5730939 · DOI
  30. Hör J Gorski SA Vogel J 2018 Bacterial RNA biology on a genome scale Molecular Cell 70 785 799 10.1016/j.molcel.2017.12.023 29358079 · DOI
  31. Hör J Vogel J 2017 Global snapshots of bacterial RNA networks The EMBO Journal 36 245 247 10.15252/embj.201696072 28031253 PMC5286387 · DOI
  32. Jost D Nowojewski A Levine E 2013 Regulating the many to benefit the few: role of weak small RNA targets Biophysical Journal 104 1773 1782 10.1016/j.bpj.2013.02.020 23601324 PMC3627871 · DOI
  33. Kavita K de Mets F Gottesman S 2018 New aspects of RNA-based regulation by hfq and its partner sRNAs Current Opinion in Microbiology 42 53 61 10.1016/j.mib.2017.10.014 29125938 PMC10367044 · DOI
  34. Kortmann J Narberhaus F 2012 Bacterial RNA thermometers: molecular zippers and switches Nature Reviews Microbiology 10 255 265 10.1038/nrmicro2730 22421878 · DOI
  35. Lalaouna D Carrier MC Semsey S Brouard JS Wang J Wade JT Massé E 2015a A 3' external transcribed spacer in a tRNA transcript acts as a sponge for small RNAs to prevent transcriptional noise Molecular Cell 58 393 405 10.1016/j.molcel.2015.03.013 25891076 · DOI
  36. Lalaouna D Morissette A Carrier MC Massé E 2015b DsrA regulatory RNA represses both hns and rbsD mRNAs through distinct mechanisms in Escherichia coli Molecular Microbiology 98 357 369 10.1111/mmi.13129 26175201 · DOI
  37. Lalaouna D Prévost K Laliberté G Houé V Massé E 2018 Contrasting silencing mechanisms of the same target mRNA by two regulatory RNAs in Escherichia coli Nucleic Acids Research 46 2600 2612 10.1093/nar/gkx1287 29294085 PMC5861431 · DOI
  38. Lalaouna D Eyraud A Devinck A Prévost K Massé E 2019 GcvB small RNA uses two distinct seed regions to regulate an extensive targetome Molecular Microbiology 111 473 486 10.1111/mmi.14168 30447071 · DOI
  39. Lorenz R Bernhart SH Höner Zu Siederdissen C Tafer H Flamm C Stadler PF Hofacker IL 2011 ViennaRNA package 2.0 Algorithms for Molecular Biology 6 26 10.1186/1748-7188-6-26 22115189 PMC3319429 · DOI · Paper page
  40. Mäder U Nicolas P Depke M Pané-Farré J Debarbouille M van der Kooi-Pol MM Guérin C Dérozier S Hiron A Jarmer H Leduc A Michalik S Reilman E Schaffer M Schmidt F Bessières P Noirot P Hecker M Msadek T Völker U van Dijl JM 2016 Staphylococcus aureus transcriptome architecture: from laboratory to Infection-Mimicking conditions PLOS Genetics 12 e1005962 10.1371/journal.pgen.1005962 27035918 PMC4818034 · DOI
  41. Magoč T Salzberg SL 2011 FLASH: fast length adjustment of short reads to improve genome assemblies Bioinformatics 27 2957 2963 10.1093/bioinformatics/btr507 21903629 PMC3198573 · DOI · Paper page
  42. Martínez-Antonio A Janga SC Thieffry D 2008 Functional organisation of Escherichia coli transcriptional regulatory network Journal of Molecular Biology 381 238 247 10.1016/j.jmb.2008.05.054 18599074 PMC2726282 · DOI
  43. Melamed S Peer A Faigenbaum-Romm R Gatt YE Reiss N Bar A Altuvia Y Argaman L Margalit H 2016 Global mapping of small RNA-Target interactions in resource global mapping of small RNA-Target interactions in Bacteria Molecular Cell 63 884 897 10.1016/j.molcel.2016.07.026 27588604 PMC5145812 · DOI
  44. Melamed S Faigenbaum-Romm R Peer A Reiss N Shechter O Bar A Altuvia Y Argaman L Margalit H 2018 Mapping the small RNA interactome in Bacteria using RIL-seq Nature Protocols 13 1 33 10.1038/nprot.2017.115 29215635 · DOI
  45. Melamed S Adams PP Zhang A Zhang H Storz G 2020 RNA-RNA interactomes of ProQ and hfq reveal overlapping and competing roles Molecular Cell 77 411 425 10.1016/j.molcel.2019.10.022 31761494 PMC6980735 · DOI
  46. Miyakoshi M Chao Y Vogel J 2015a Regulatory small RNAs from the 3' regions of bacterial mRNAs Current Opinion in Microbiology 24 132 139 10.1016/j.mib.2015.01.013 25677420 · DOI
  47. Miyakoshi M Chao Y Vogel J 2015b Cross talk between ABC transporter mRNAs via a target mRNA-derived sponge of the GcvB small RNA The EMBO Journal 34 1478 1492 10.15252/embj.201490546 25630703 PMC4474525 · DOI
  48. Miyakoshi M Matera G Maki K Sone Y Vogel J 2018 Functional expansion of a TCA cycle operon mRNA by a 3′ end-derived small RNA Nucleic Acids Research 47 2075 2088 10.1093/nar/gky1243 PMC6393394 30541135 · DOI
  49. Mohammad F Green R Buskirk AR 2019 A systematically-revised ribosome profiling method for Bacteria reveals pauses at single-codon resolution eLife 8 e42591 10.7554/eLife.42591 30724162 PMC6377232 · DOI
  50. Monteiro C Papenfort K Hentrich K Ahmad I Le Guyon S Reimann R Grantcharova N Römling U 2012 Hfq and Hfq-dependent small RNAs are major contributors to multicellular development in Salmonella enterica serovar typhimurium RNA Biology 9 489 502 10.4161/rna.19682 22336758 · DOI
  51. Moon K Gottesman S 2011 Competition among Hfq-binding small RNAs in Escherichia coli Molecular Microbiology 82 1545 1562 10.1111/j.1365-2958.2011.07907.x 22040174 PMC7394283 · DOI
  52. Morita T Maki K Aiba H 2005 RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs Genes & Development 19 2176 2186 10.1101/gad.1330405 16166379 PMC1221888 · DOI
  53. Navarro Llorens JM Tormo A Martínez-García E 2010 Stationary phase in gram-negative Bacteria FEMS Microbiology Reviews 34 476 495 10.1111/j.1574-6976.2010.00213.x 20236330 · DOI
  54. Nitzan M Rehani R Margalit H 2017 Integration of bacterial small RNAs in regulatory networks Annual Review of Biophysics 46 131 148 10.1146/annurev-biophys-070816-034058 28532217 · DOI
  55. 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 Molecular Microbiology 68 890 906 10.1111/j.1365-2958.2008.06189.x 18399940 · DOI
  56. Papenfort K Said N Welsink T Lucchini S Hinton JCD Vogel J 2009 Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA Molecular Microbiology 74 139 158 10.1111/j.1365-2958.2009.06857.x 19732340 · DOI
  57. Pei XY Dendooven T Sonnleitner E Chen S Bläsi U Luisi BF 2019 Architectural principles for hfq/Crc-mediated regulation of gene expression eLife 8 e43158 10.7554/eLife.43158 30758287 PMC6422490 · DOI
  58. Pletnev P Osterman I Sergiev P Bogdanov A Dontsova O 2015 Survival guide: Escherichia coli in the stationary phase Acta Naturae 7 22 33 10.32607/20758251-2015-7-4-22-33 26798489 PMC4717247 · DOI
  59. Quinlan AR Hall IM 2010 BEDTools: a flexible suite of utilities for comparing genomic features Bioinformatics 26 841 842 10.1093/bioinformatics/btq033 20110278 PMC2832824 · DOI · Paper page
  60. Ritchie ME Phipson B Wu D Hu Y Law CW Shi W Smyth GK 2015 Limma powers differential expression analyses for RNA-sequencing and microarray studies Nucleic Acids Research 43 e47 10.1093/nar/gkv007 25605792 PMC4402510 · DOI · Paper page
  61. 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 The EMBO Journal 32 2764 2778 10.1038/emboj.2013.205 24065131 PMC3801439 · DOI
  62. Santiago-Frangos A Woodson SA 2018 Hfq chaperone brings speed dating to bacterial sRNA Wiley Interdisciplinary Reviews: RNA 9 e1475 10.1002/wrna.1475 29633565 PMC6002925 · DOI
  63. Sedlyarova N Shamovsky I Bharati BK Epshtein V Chen J Gottesman S Schroeder R Nudler E 2016 sRNA-Mediated control of transcription termination in E. coli Cell 167 111 121 10.1016/j.cell.2016.09.004 27662085 PMC5040353 · DOI
  64. Sezonov G Joseleau-Petit D D'Ari R 2007 Escherichia coli physiology in Luria-Bertani broth Journal of Bacteriology 189 8746 8749 10.1128/JB.01368-07 17905994 PMC2168924 · DOI
  65. 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 Molecular Microbiology 81 1144 1165 10.1111/j.1365-2958.2011.07751.x 21696468 · DOI
  66. Sharma E Sterne-Weiler T O'Hanlon D Blencowe BJ 2016 Global mapping of human RNA-RNA interactions Molecular Cell 62 618 626 10.1016/j.molcel.2016.04.030 27184080 · DOI
  67. Shimoni Y Friedlander G Hetzroni G Niv G Altuvia S Biham O Margalit H 2007 Regulation of gene expression by small non-coding RNAs: a quantitative view Molecular Systems Biology 3 138 10.1038/msb4100181 17893699 PMC2013925 · DOI
  68. Sittka A Pfeiffer V Tedin K Vogel J 2007 The RNA chaperone hfq is essential for the virulence of Salmonella typhimurium Molecular Microbiology 63 193 217 10.1111/j.1365-2958.2006.05489.x 17163975 PMC1810395 · DOI
  69. Smirnov A Förstner KU Holmqvist E Otto A Günster R Becher D Reinhardt R Vogel J 2016 Grad-seq guides the discovery of ProQ as a major small RNA-binding protein PNAS 113 11591 11596 10.1073/pnas.1609981113 27671629 PMC5068311 · DOI
  70. Smirnov A Wang C Drewry LL Vogel J 2017 Molecular mechanism of mRNA repression in trans by a ProQ-dependent small RNA The EMBO Journal 36 1029 1045 10.15252/embj.201696127 28336682 PMC5391140 · DOI
  71. Sonnleitner E Bläsi U 2014 Regulation of hfq by the RNA CrcZ in Pseudomonas aeruginosa carbon catabolite repression PLOS Genetics 10 e1004440 10.1371/journal.pgen.1004440 24945892 PMC4063720 · DOI
  72. Storz G Vogel J Wassarman KM 2011 Regulation by small RNAs in Bacteria: expanding frontiers Molecular Cell 43 880 891 10.1016/j.molcel.2011.08.022 21925377 PMC3176440 · DOI
  73. Thomason MK Bischler T Eisenbart SK Förstner KU Zhang A Herbig A Nieselt K Sharma CM Storz G 2015 Global transcriptional start site mapping using differential RNA sequencing reveals novel antisense RNAs in Escherichia coli Journal of Bacteriology 197 18 28 10.1128/JB.02096-14 25266388 PMC4288677 · DOI · Paper page
  74. Tjaden B 2015 De novo assembly of bacterial transcriptomes from RNA-seq data Genome Biology 16 1 10 10.1186/s13059-014-0572-2 25583448 PMC4316799 · DOI
  75. Travis AJ Moody J Helwak A Tollervey D Kudla G 2014 Hyb: a bioinformatics pipeline for the analysis of CLASH (crosslinking, ligation and sequencing of hybrids) data Methods 65 263 273 10.1016/j.ymeth.2013.10.015 24211736 PMC3969109 · DOI
  76. Tree JJ Granneman S McAteer SP Tollervey D Gally DL 2014 Identification of bacteriophage-encoded anti-sRNAs in pathogenic Escherichia coli Molecular Cell 55 199 213 10.1016/j.molcel.2014.05.006 24910100 PMC4104026 · DOI
  77. Updegrove TB Zhang A Storz G 2016 Hfq: the flexible RNA matchmaker Current Opinion in Microbiology 30 133 138 10.1016/j.mib.2016.02.003 26907610 PMC4821791 · DOI
  78. van Nues RW Castro-Roa D Yuzenkova Y Zenkin N 2016 Ribonucleoprotein particles of bacterial small non-coding RNA IsrA (IS61 or McaS) and its interaction with RNA polymerase core may link transcription to mRNA fate Nucleic Acids Research 44 2577 2592 10.1093/nar/gkv1302 26609136 PMC4824073 · DOI
  79. van Nues R Schweikert G de Leau E Selega A Langford A Franklin R Iosub I Wadsworth P Sanguinetti G Granneman S 2017 Kinetic CRAC uncovers a role for Nab3 in determining gene expression profiles during stress Nature Communications 8 12 10.1038/s41467-017-00025-5 28400552 PMC5432031 · DOI
  80. Vogel J Luisi BF 2011 Hfq and its constellation of RNA Nature Reviews Microbiology 9 578 589 10.1038/nrmicro2615 21760622 PMC4615618 · DOI
  81. Wang J Rennie W Liu C Carmack CS Prévost K Caron M-P Massé E Ding Y Wade JT 2015 Identification of bacterial sRNA regulatory targets using ribosome profiling Nucleic Acids Research 197 gkv1158 10.1093/nar/gkv1158 PMC4666370 26546513 · DOI
  82. Wang J Liu T Zhao B Lu Q Wang Z Cao Y Li W 2016 sRNATarBase 3.0: an updated database for sRNA-target interactions in Bacteria Nucleic Acids Research 44 D248 D253 10.1093/nar/gkv1127 26503244 PMC4702819 · DOI
  83. Waters SA McAteer SP Kudla G Pang I Deshpande NP Amos TG Leong KW Wilkins MR Strugnell R Gally DL Tollervey D Tree JJ 2017 Small RNA interactome of pathogenic E. coli revealed through crosslinking of RNase E The EMBO Journal 36 374 387 10.15252/embj.201694639 27836995 PMC5286369 · DOI
  84. Waters LS Storz G 2009 Regulatory RNAs in bacteria Cell 136 615 628 10.1016/j.cell.2009.01.043 19239884 PMC3132550 · DOI
  85. Webb S Hector RD Kudla G Granneman S 2014 PAR-CLIP data indicate that Nrd1-Nab3-dependent transcription termination regulates expression of hundreds of protein coding genes in yeast Genome Biology 15 R8 10.1186/gb-2014-15-1-r8 24393166 PMC4053934 · DOI
  86. Wilson KS Von HPH 1995 Transcription termination at intrinsic terminators: the role of the RNA hairpin (Escherichia coli/RNA polymerase/rho-independent termination) PNAS 92 8793 8797 10.1073/pnas.92.19.8793 7568019 PMC41053 · DOI
  87. Wu X Bartel DP 2017 kpLogo: positional k-mer analysis reveals hidden specificity in biological sequences Nucleic Acids Research 45 W534 W538 10.1093/nar/gkx323 28460012 PMC5570168 · DOI

Cited by

Sorted by citations

Authors
Iosub, I. A., van Nues, R. W., McKellar, S. W., Nieken, K. J., Marchioretto, M., Sy, B., Tree, J. J., Viero, G., & Granneman, S.
Affiliations
  • University of Edinburgh (GB)
  • Institute of Cell Biology, University of Edinburgh, Edinburgh, United Kingdom
  • National Research Council (IT)
  • UNSW Sydney (AU)
Corresponding author
Granneman, Sander
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2020-05-01
Volume
9
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.54655
PMC
PMC7213987
OpenAlex
W3023974221
Cited by
98
References
2
Citations by year
2026: 7 · 2025: 11 · 2024: 18 · 2023: 15 · 2022: 17 · 2021: 20 · 2020: 9 · 2019: 1
FWCI
8.94
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
Funders
  • Wellcome (102334, 091549)
  • Medical Research Council (MR/R008205/1)
  • National Health and Medical Research Council (GNT1067241, GNT1139313)
  • Axonomix
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Keywords
Hfq, small RNA, RNA-RNA interactions, CLASH, Escherichia coli, gene expression regulation
MeSH terms
Adaptation, Physiological, Energy Metabolism, Escherichia coli, Models, Genetic, Nucleic Acid Conformation, RNA Processing, Post-Transcriptional, RNA, Bacterial, RNA, Messenger, Gene Expression Regulation, Bacterial, 5' Untranslated Regions, 3' Untranslated Regions, RNA Stability, Escherichia coli Proteins, Databases, Genetic, Host Factor 1 Protein, RNA, Small Untranslated

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review