Mimicry, deception and competition: The life of competing endogenous RNAs

Advanced Review

Marc P. Grüll, Eric Massé

Published Online: Feb 13 2019

DOI: 10.1002/wrna.1525

Full article on Wiley Online Library: HTML PDF

Can't access this content? Tell your librarian.

Since their discovery, small regulatory RNAs (sRNAs) were thought to be regulated exclusively at the transcriptional level. However, accumulating data from recent reports indicate that posttranscriptional signals can also modulate the function and stability of sRNAs. One of these posttranscriptional signals are competing endogenous RNAs (ceRNAs). Commonly called RNA sponges, ceRNAs can effectively sequester sRNAs and prevent them from binding their cognate target messenger RNAs (mRNAs). Subsequently, they prevent sRNA‐dependent regulation of translation and stability of mRNA targets. While some ceRNAs seem to be expressed constitutively, others are intricately regulated according to environmental conditions. The outcome of ceRNA binding to a sRNA reaches beyond simple sequestration. Various effects observed on sRNA functions extend from reducing transcriptional noise to promote RNA turnover. Here, we present a historical perspective of the discovery of ceRNAs in eukaryotic organisms and mainly focus on the synthesis and function of select, well‐described, ceRNAs in bacterial cells. This article is categorized under: RNA Interactions with Proteins and Other Molecules > Small Molecule–RNA Interactions Translation > Translation Regulation RNA Turnover and Surveillance > Regulation of RNA Stability

Regulation of chitosugar uptake by the ceRNA ChiX

[ Normal View | Magnified View ]

Target‐mediated derepression of the GcvB regulon

[ Normal View | Magnified View ]

ceRNA activity of the tRNA‐derived 3′ETS^leuZ

[ Normal View | Magnified View ]

References

Aiba,, H. (2007). Mechanism of RNA silencing by Hfq‐binding small RNAs. Current Opinion in Microbiology, 10(2), 134–139. https://doi.org/10.1016/j.mib.2007.03.010
Babitzke,, P., & Romeo,, T. (2007). CsrB sRNA family: Sequestration of RNA‐binding regulatory proteins. Current Opinion in Microbiology, 10(2), 156–163. https://doi.org/10.1016/j.mib.2007.03.007
Balbontin,, R., Villagra,, N., Pardos de la Gandara,, M., Mora,, G., Figueroa‐Bossi,, N., & Bossi,, L. (2016). Expression of IroN, the salmochelin siderophore receptor, requires mRNA activation by RyhB small RNA homologues. Molecular Microbiology, 100(1), 139–155. https://doi.org/10.1111/mmi.13307
Barria,, C., Malecki,, M., & Arraiano,, C. M. (2013). Bacterial adaptation to cold. Microbiology, 159(Pt. 12), 2437–2443. https://doi.org/10.1099/mic.0.052209-0
Bartel,, D. P. (2009). MicroRNAs: Target recognition and regulatory functions. Cell, 136(2), 215–233. https://doi.org/10.1016/j.cell.2009.01.002
Bartel,, D. P. (2018). Metazoan microRNAs. Cell, 173(1), 20–51. https://doi.org/10.1016/j.cell.2018.03.006
Beier,, S., & Bertilsson,, S. (2013). Bacterial chitin degradation‐mechanisms and ecophysiological strategies. Frontiers in Microbiology, 4, 149. https://doi.org/10.3389/fmicb.2013.00149
Bossi,, L., & Figueroa‐Bossi,, N. (2016). Competing endogenous RNAs: A target‐centric view of small RNA regulation in bacteria. Nature Reviews. Microbiology, 14(12), 775–784. https://doi.org/10.1038/nrmicro.2016.129
Bouvier,, M., Sharma,, C. M., Mika,, F., Nierhaus,, K. H., & Vogel,, J. (2008). Small RNA binding to 5′ mRNA coding region inhibits translational initiation. Molecular Cell, 32(6), 827–837. https://doi.org/10.1016/j.molcel.2008.10.027
Busi,, F., Le Derout,, J., Cerciat,, M., Regnier,, 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(10), 1458–1461. https://doi.org/10.1016/j.biochi.2010.06.020
Cesana,, M., Cacchiarelli,, D., Legnini,, I., Santini,, T., Sthandier,, O., Chinappi,, M., … Bozzoni,, I. (2011). A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell, 147(2), 358–369. https://doi.org/10.1016/j.cell.2011.09.028
Cesana,, M., & Daley,, G. Q. (2013). Deciphering the rules of ceRNA networks. Proceedings of the National Academy of Sciences, 110(18), 7112–7113. https://doi.org/10.1073/pnas.1305322110
Chao,, Y., Papenfort,, K., Reinhardt,, R., Sharma,, C. M., & Vogel,, J. (2012). An atlas of Hfq‐bound transcripts reveals 3′ UTRs as a genomic reservoir of regulatory small RNAs. EMBO Journal, 31(20), 4005–4019. https://doi.org/10.1038/emboj.2012.229
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(3), 352–363. https://doi.org/10.1016/j.molcel.2015.12.023
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 Genetics, 9(1), e1003156. https://doi.org/10.1371/journal.pgen.1003156
Desnoyers,, G., & Masse,, E. (2012). Noncanonical repression of translation initiation through small RNA recruitment of the RNA chaperone Hfq. Genes and Development, 26(7), 726–739. https://doi.org/10.1101/gad.182493.111
Ebert,, M. S., & Sharp,, P. A. (2010). MicroRNA sponges: Progress and possibilities. RNA, 16(11), 2043–2050. https://doi.org/10.1261/rna.2414110
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 and Development, 23(17), 2004–2015. https://doi.org/10.1101/gad.541609
Franco‐Zorrilla,, J. M., Valli,, A., Todesco,, M., Mateos,, I., Puga,, M. I., Rubio‐Somoza,, I., … Paz‐Ares,, J. (2007). Target mimicry provides a new mechanism for regulation of microRNA activity. Nature Genetics, 39(8), 1033–1037. https://doi.org/10.1038/ng2079
Friedman,, R. C., Farh,, K. K.‐H., Burge,, C. B., & Bartel,, D. P. (2009). Most mammalian mRNAs are conserved targets of microRNAs. Genome Research, 19(1), 92–105.
Geissmann,, T. A., & Touati,, D. (2004). Hfq, a new chaperoning role: Binding to messenger RNA determines access for small RNA regulator. EMBO Journal, 23(2), 396–405. https://doi.org/10.1038/sj.emboj.7600058
Ghrist,, A. C., Heil,, G., & Stauffer,, G. V. (2001). GcvR interacts with GcvA to inhibit activation of the Escherichia coli glycine cleavage operon. Microbiology, 147, 2215–2221. https://doi.org/10.1099/00221287-147-8-2215
Gogol,, E. B., Rhodius,, V. A., Papenfort,, K., Vogel,, J., & Gross,, C. A. (2011). Small RNAs endow a transcriptional activator with essential repressor functions for single‐tier control of a global stress regulon. Proceedings of the National Academy of Sciences, 108(31), 12875–12880. https://doi.org/10.1073/pnas.1109379108
Gottesman,, S., & Storz,, G. (2011). Bacterial small RNA regulators: Versatile roles and rapidly evolving variations. Cold Spring Harbor Perspectives in Biology, 3(12). https://doi.org/10.1101/cshperspect.a003798
Guillier,, M., Gottesman,, S., & Storz,, G. (2006). Modulating the outer membrane with small RNAs. Genes and Development, 20(17), 2338–2348. https://doi.org/10.1101/gad.1457506
Guo,, H., Ingolia,, N. T., Weissman,, J. S., & Bartel,, D. P. (2010). Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature, 466(7308), 835–840. https://doi.org/10.1038/nature09267
Guo,, M. S., Updegrove,, T. B., Gogol,, E. B., Shabalina,, S. A., Gross,, C. A., & Storz,, G. (2014). MicL, a new sigmaE‐dependent sRNA, combats envelope stress by repressing synthesis of Lpp, the major outer membrane lipoprotein. Genes and Development, 28(14), 1620–1634. https://doi.org/10.1101/gad.243485.114
Han,, K., Tjaden,, B., & Lory,, S. (2016). GRIL‐seq provides a method for identifying direct targets of bacterial small regulatory RNA by in vivo proximity ligation. Nature Microbiology, 2, 16239. https://doi.org/10.1038/nmicrobiol.2016.239
Heil,, G., Stauffer,, L. T., & Stauffer,, G. V. (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. https://doi.org/10.1099/00221287-148-7-2203
Hucker,, S. M., Simon,, S., Scherer,, S., & Neuhaus,, K. (2017). Transcriptional and translational regulation by RNA thermometers, riboswitches and the sRNA DsrA in Escherichia coli O157:H7 Sakai under combined cold and osmotic stress adaptation. FEMS Microbiology Letters, 364(2). https://doi.org/10.1093/femsle/fnw262
Jacques,, J. F., Jang,, S., Prevost,, K., Desnoyers,, G., Desmarais,, M., Imlay,, J., & Masse,, E. (2006). RyhB small RNA modulates the free intracellular iron pool and is essential for normal growth during iron limitation in Escherichia coli. Molecular Microbiology, 62(4), 1181–1190. https://doi.org/10.1111/j.1365-2958.2006.05439.x
Johansen,, J., Rasmussen,, A. A., Overgaard,, M., & Valentin‐Hansen,, P. (2006). Conserved small non‐coding RNAs that belong to the sigmaE regulon: Role in down‐regulation of outer membrane proteins. Journal of Molecular Biology, 364(1), 1–8. https://doi.org/10.1016/j.jmb.2006.09.004
Jorgensen,, M. G., Nielsen,, J. S., Boysen,, A., Franch,, T., Moller‐Jensen,, J., & Valentin‐Hansen,, P. (2012). Small regulatory RNAs control the multi‐cellular adhesive lifestyle of Escherichia coli. Molecular Microbiology, 84(1), 36–50. https://doi.org/10.1111/j.1365-2958.2012.07976.x
Karreth,, F. A., Tay,, Y., Perna,, D., Ala,, U., Tan,, S. M., Rust,, A. G., … Pandolfi,, P. P. (2011). In vivo identification of tumor‐suppressive PTEN ceRNAs in an oncogenic BRAF‐induced mouse model of melanoma. Cell, 147(2), 382–395. https://doi.org/10.1016/j.cell.2011.09.032
Lalaouna,, D., Carrier,, M. C., Semsey,, S., Brouard,, J. S., Wang,, J., Wade,, J. T., & Masse,, E. (2015). A 3′ external transcribed spacer in a tRNA transcript acts as a sponge for small RNAs to prevent transcriptional noise. Molecular Cell, 58(3), 393–405. https://doi.org/10.1016/j.molcel.2015.03.013
Lalaouna,, D., Simoneau‐Roy,, M., Lafontaine,, D., & Masse,, E. (2013). Regulatory RNAs and target mRNA decay in prokaryotes. Biochimica et Biophysica Acta, 1829(6–7), 742–747. https://doi.org/10.1016/j.bbagrm.2013.02.013
Lapouge,, K., Schubert,, M., Allain,, F. H., & Haas,, D. (2008). Gac/Rsm signal transduction pathway of gamma‐proteobacteria: From RNA recognition to regulation of social behaviour. Molecular Microbiology, 67(2), 241–253. https://doi.org/10.1111/j.1365-2958.2007.06042.x
Lee,, H. J., & Gottesman,, S. (2016). sRNA roles in regulating transcriptional regulators: Lrp and SoxS regulation by sRNAs. Nucleic Acids Research, 44(14), 6907–6923. https://doi.org/10.1093/nar/gkw358
Li,, Z., & Deutscher,, M. P. (2002). RNase E plays an essential role in the maturation of Escherichia coli tRNA precursors. RNA, 8, 97–109.
Majdalani,, N., Cunning,, C., Sledjeski,, D., Elliott,, T., & Gottesman,, S. (1998). DsrA RNA regulates translation of RpoS message by an anti‐antisense mechanism, independent of its action as an antisilencer of transcription. Proceedings of the National Academy of Sciences, 95, 12462–12467.
Majdalani,, N., Vanderpool,, C. K., & Gottesman,, S. (2005). Bacterial small RNA regulators. Critical Reviews in Biochemistry and Molecular Biology, 40(2), 93–113. https://doi.org/10.1080/10409230590918702
Masse,, E., Escorcia,, F. E., & Gottesman,, S. (2003). Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes and Development, 17(19), 2374–2383. https://doi.org/10.1101/gad.1127103
Masse,, E., Salvail,, H., Desnoyers,, G., & Arguin,, M. (2007). Small RNAs controlling iron metabolism. Current Opinion in Microbiology, 10(2), 140–145. https://doi.org/10.1016/j.mib.2007.03.013
Masse,, E., Vanderpool,, C. K., & Gottesman,, S. (2005). Effect of RyhB small RNA on global iron use in Escherichia coli. Journal of Bacteriology, 187(20), 6962–6971. https://doi.org/10.1128/JB.187.20.6962-6971.2005
Melamed,, S., Peer,, A., Faigenbaum‐Romm,, R., Gatt,, Y. E., Reiss,, N., Bar,, A., … Margalit,, H. (2016). Global mapping of small RNA‐target interactions in bacteria. Molecular Cell, 63(5), 884–897. https://doi.org/10.1016/j.molcel.2016.07.026
Miyakoshi,, M., Chao,, Y., & Vogel,, J. (2015). Cross talk between ABC transporter mRNAs via a target mRNA‐derived sponge of the GcvB small RNA. EMBO Journal, 34(11), 1478–1492. https://doi.org/10.15252/embj.201490546
Modi,, S. R., Camacho,, D. M., Kohanski,, M. A., Walker,, G. C., & Collins,, J. J. (2011). Functional characterization of bacterial sRNAs using a network biology approach. Proceedings of the National Academy of Sciences, 108(37), 15522–15527. https://doi.org/10.1073/pnas.1104318108
Moll,, I. (2003). Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs. RNA, 9(11), 1308–1314. https://doi.org/10.1261/rna.5850703
Moller,, T., Franch,, T., Hojrup,, P., Keene,, D. R., Bächinger,, H. P., Brennan,, R. G., & Valentin‐Hansen,, P. (2002). Hfq. A bacterial Sm‐like protein that mediates RNA–RNA interaction. Molecular Cell, 9, 23–30.
Morita,, T., Mochizuki,, Y., & Aiba,, H. (2006). Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruction. Proceedings of the National Academy of Sciences, 103(13), 4858–4863. https://doi.org/10.1073/pnas.0509638103
Overgaard,, M., Johansen,, J., Moller‐Jensen,, J., & Valentin‐Hansen,, P. (2009). Switching off small RNA regulation with trap‐mRNA. Molecular Microbiology, 73(5), 790–800. https://doi.org/10.1111/j.1365-2958.2009.06807.x
Ow,, M. C., & Kushner,, S. R. (2002). Initiation of tRNA maturation by RNase E is essential for cell viability in E. coli. Genes and Development, 16, 1102–1115.
Papenfort,, K., Pfeiffer,, V., Mika,, F., Lucchini,, S., Hinton,, J. C. D., & Vogel,, J. (2006). σE‐dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Molecular Microbiology, 62(6), 1674–1688. https://doi.org/10.1111/j.1365-2958.2006.05524.x
Papenfort,, K., & Vogel,, J. (2014). Small RNA functions in carbon metabolism and virulence of enteric pathogens. Frontiers in Cellular and Infection Microbiology, 4, 91. https://doi.org/10.3389/fcimb.2014.00091
Plumbridge,, J., Bossi,, L., Oberto,, J., Wade,, J. T., & Figueroa‐Bossi,, N. (2014). Interplay of transcriptional and small RNA‐dependent control mechanisms regulates chitosugar uptake in Escherichia coli and Salmonella. Molecular Microbiology, 92(4), 648–658. https://doi.org/10.1111/mmi.12573
Plumbridge,, J., & Pellegrini,, O. (2004). Expression of the chitobiose operon of Escherichia coli is regulated by three transcription factors: NagC, ChbR and CAP. Molecular Microbiology, 52(2), 437–449. https://doi.org/10.1111/j.1365-2958.2004.03986.x
Poliseno,, L., Salmena,, L., Zhang,, J., Carver,, B., Haveman,, W. J., & Pandolfi,, P. P. (2010). A coding‐independent function of gene and pseudogene mRNAs regulates tumour biology. Nature, 465(7301), 1033–1038. https://doi.org/10.1038/nature09144
Prevost,, K., Salvail,, H., Desnoyers,, G., Jacques,, J. F., Phaneuf,, E., & Masse,, E. (2007). The small RNA RyhB activates the translation of shiA mRNA encoding a permease of shikimate, a compound involved in siderophore synthesis. Molecular Microbiology, 64(5), 1260–1273. https://doi.org/10.1111/j.1365-2958.2007.05733.x
Pulvermacher,, S. C., Stauffer,, L. T., & Stauffer,, G. V. (2009). Role of the sRNA GcvB in regulation of cycA in Escherichia coli. Microbiology, 155(Pt. 1, 106–114. https://doi.org/10.1099/mic.0.023598-0
Rasmussen,, A. A., Eriksen,, M., Gilany,, K., Udesen,, C., Franch,, T., Petersen,, C., & Valentin‐Hansen,, P. (2005). Regulation of ompA mRNA stability: The role of a small regulatory RNA in growth phase‐dependent control. Molecular Microbiology, 58(5), 1421–1429. https://doi.org/10.1111/j.1365-2958.2005.04911.x
Repoila,, F., Majdalani,, N., & Gottesman,, S. (2003). Small non‐coding RNAs, co‐ordinators of adaptation processes in Escherichia coli: The RpoS paradigm. Molecular Microbiology, 48(4), 855–861.
Salmena,, L., Poliseno,, L., Tay,, Y., Kats,, L., & Pandolfi,, P. P. (2011). A ceRNA hypothesis: The Rosetta stone of a hidden RNA language? Cell, 146(3), 353–358. https://doi.org/10.1016/j.cell.2011.07.014
Salvail,, H., Caron,, M. P., Belanger,, J., & Masse,, E. (2013). Antagonistic functions between the RNA chaperone Hfq and an sRNA regulate sensitivity to the antibiotic colicin. EMBO Journal, 32(20), 2764–2778. https://doi.org/10.1038/emboj.2013.205
Salvail,, H., Lanthier‐Bourbonnais,, P., Sobota,, J. M., Caza,, M., Benjamin,, J. A., Mendieta,, M. E., … Masse,, E. (2010). A small RNA promotes siderophore production through transcriptional and metabolic remodeling. Proceedings of the National Academy of Sciences, 107(34), 15223–15228. https://doi.org/10.1073/pnas.1007805107
Seitz,, H. (2009). Redefining microRNA targets. Current Biology, 19(10), 870–873. https://doi.org/10.1016/j.cub.2009.03.059
Sharma,, C. M., Darfeuille,, F., Plantinga,, T. H., & 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 and Development, 21(21), 2804–2817. https://doi.org/10.1101/gad.447207
Sharma,, C. M., Papenfort,, K., Pernitzsch,, S. R., Mollenkopf,, H. J., Hinton,, J. C., & Vogel,, J. (2011). Pervasive post‐transcriptional control of genes involved in amino acid metabolism by the Hfq‐dependent GcvB small RNA. Molecular Microbiology, 81(5), 1144–1165. https://doi.org/10.1111/j.1365-2958.2011.07751.x
Sittka,, A., Lucchini,, S., Papenfort,, K., Sharma,, C. M., Rolle,, K., Binnewies,, T. T., … Vogel,, J. (2008). Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post‐transcriptional regulator, Hfq. PLoS Genetics, 4(8), e1000163. https://doi.org/10.1371/journal.pgen.1000163
Souza,, C. P., Almeida,, B. C., Colwell,, R. R., & Rivera,, I. N. (2011). The importance of chitin in the marine environment. Marine Biotechnology, 13(5), 823–830. https://doi.org/10.1007/s10126-011-9388-1
Stauffer,, L. T., & Stauffer,, G. V. (2005). GcvA interacts with both the α and σ subunits of RNA polymerase to activate the Escherichia coli gcvB gene and the gcvTHP operon. FEMS Microbiology Letters, 242(2), 333–338.
Stauffer,, L. T., & Stauffer,, G. V. (2012). Antagonistic roles for GcvA and GcvB in hdeAB expression in Escherichia coli. ISRN Microbiology, 2012, 1–10. https://doi.org/10.5402/2012/697308
Storz,, G., Opdyke,, J. A., & Zhang,, A. (2004). Controlling mRNA stability and translation with small, noncoding RNAs. Current Opinion in Microbiology, 7(2), 140–144. https://doi.org/10.1016/j.mib.2004.02.015
Storz,, G., Vogel,, J., & Wassarman,, K. M. (2011). Regulation by small RNAs in bacteria: Expanding frontiers. Molecular Cell, 43(6), 880–891. https://doi.org/10.1016/j.molcel.2011.08.022
Sumazin,, P., Yang,, X., Chiu,, H. S., Chung,, W. J., Iyer,, A., Llobet‐Navas,, D., … Califano,, A. (2011). An extensive microRNA‐mediated network of RNA–RNA interactions regulates established oncogenic pathways in glioblastoma. Cell, 147(2), 370–381. https://doi.org/10.1016/j.cell.2011.09.041
Tharanathan,, R. N., & Kittur,, F. S. (2003). Chitin—The undisputed biomolecule of great potential. Critical Reviews in Food Science and Nutrition, 43(1), 61–87. https://doi.org/10.1080/10408690390826455
Thomas,, M., Lieberman,, J., & Lal,, A. (2010). Desperately seeking microRNA targets. Nature Structural and Molecular Biology, 17(10), 1169–1174. https://doi.org/10.1038/nsmb.1921
Tree,, J. J., Granneman,, S., McAteer,, S. P., Tollervey,, D., & Gally,, D. L. (2014). Identification of bacteriophage‐encoded anti‐sRNAs in pathogenic Escherichia coli. Molecular Cell, 55(2), 199–213. https://doi.org/10.1016/j.molcel.2014.05.006
Udekwu,, K. I., Darfeuille,, F., Vogel,, J., Reimegård,, J., Holmqvist,, E., & Wagner,, E. G. H. (2005). Hfq‐dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes and Development, 19(19), 2355–2366.
Urbanowski,, M. L., Stauffer,, L. T., & Stauffer,, G. V. (2000). The gcvB gene encodes a small untranslated RNA involved in expression of the dipeptide and oligopeptide transport system in Escherichia coli. Molecular Microbiology, 37(4), 856–868.
Valentin‐Hansen,, P., Johansen,, J., & Rasmussen,, A. A. (2007). Small RNAs controlling outer membrane porins. Current Opinion in Microbiology, 10(2), 152–155. https://doi.org/10.1016/j.mib.2007.03.001
Vanderpool,, C. K. (2011). Combined experimental and computational strategies define an expansive regulon for GcvB small RNA. Molecular Microbiology, 81(5), 1129–1132. https://doi.org/10.1111/j.1365-2958.2011.07780.x
Vogel,, J., & Luisi,, B. F. (2011). Hfq and its constellation of RNA. Nature Reviews Microbiology, 9(8), 578–589. https://doi.org/10.1038/nrmicro2615
Vogel,, J., & Papenfort,, K. (2006). Small non‐coding RNAs and the bacterial outer membrane. Current Opinion in Microbiology, 9(6), 605–611. https://doi.org/10.1016/j.mib.2006.10.006
Wang,, H., Yang,, H., Shivalila,, C. S., Dawlaty,, M. M., Cheng,, A. W., Zhang,, F., & Jaenisch,, R. (2013). One‐step generation of mice carrying mutations in multiple genes by CRISPR/Cas‐mediated genome engineering. Cell, 153(4), 910–918. https://doi.org/10.1016/j.cell.2013.04.025
Waters,, S. A., McAteer,, S. P., Kudla,, G., Pang,, I., Deshpande,, N. P., Amos,, T. G., … Tree,, J. J. (2017). Small RNA interactome of pathogenic E. coli revealed through crosslinking of RNase E. EMBO Journal, 36(3), 374–387. https://doi.org/10.15252/embj.201694639
Wright,, P. R., Richter,, A. S., Papenfort,, K., Mann,, M., Vogel,, J., Hess,, W. R., … Georg,, J. (2013). Comparative genomics boosts target prediction for bacterial small RNAs. Proceedings of the National Academy of Sciences, 110(37), E3487–E3496. https://doi.org/10.1073/pnas.1303248110
Yang,, Q., Figueroa‐Bossi,, N., & Bossi,, L. (2014). Translation enhancing ACA motifs and their silencing by a bacterial small regulatory RNA. PLoS Genetics, 10(1), e1004026. https://doi.org/10.1371/journal.pgen.1004026
Zhang,, A., Wassarman,, K. M., Ortega,, J., Steven,, A. C., & Storz,, G. (2002). The Sm‐like Hfq protein increases OxyS RNA interaction with target mRNAs. Molecular Cell, 9, 11–22.
Zhou,, P., Xu,, W., Peng,, X., Luo,, Z., Xing,, Q., Chen,, X., … Jiang,, S. (2013). Large‐scale screens of miRNA–mRNA interactions unveiled that the 3′UTR of a gene is targeted by multiple miRNAs. PLoS One, 8(7), e68204. https://doi.org/10.1371/journal.pone.0068204

Access to this WIREs title is by subscription only.

Recommend to Your
Librarian Now!

Mimicry, deception and competition: The life of competing endogenous RNAs

Browse by Topic

Access to this WIREs title is by subscription only.

The latest WIREs articles in your inbox