Abstract
For a long time, the small regulatory RNA DsrA has been considered as a regulator with a narrow spectrum of action due to its restricted targetome. Since the first reports on DsrA characterization, only two targets of DsrA have been described: rpoS and hns mRNAs, encoding the sigma factor σS and the nucleoid-associated protein H-NS, respectively. Recently, the scope of DsrA targetome has been expanded by the characterization of two negatively regulated mRNAs, mreB and rbsD, involved in cell wall biosynthesis and ribose metabolism, respectively. In this review, we summarize new insights in DsrA-mediated regulation and emphasize the versatility of DsrA modes of action.
Similar content being viewed by others
References
Bak G, Han K, Kim D, Lee Y (2014) Roles of rpoS-activating small RNAs in pathways leading to acid resistance of Escherichia coli. Microbiologyopen 3:15–28. doi:10.1002/mbo3.143
Battesti A, Majdalani N, Gottesman S (2011) The RpoS-mediated general stress response in E. coli. Annu Rev Microbiol 65:189–213. doi:10.1146/annurev-micro-090110-102946
Cayrol B, Fortas E, Martret C, Cech G, Kloska A, Caulet S, Barbet M, Trépout S, Marco S, Taghbalout A, Busi F, Wegrzyn G, Arluison V (2015) Riboregulation of the bacterial actin-homolog MreB by DsrA small noncoding RNA. Integr Biol (Camb) 7:128–141. doi:10.1039/c4ib00102h
De Lay N, Gottesman S (2011) Role of polynucleotide phosphorylase in sRNA function in Escherichia coli. RNA 17:1172–1189. doi:10.1261/rna.2531211
De Lay N, Schu DJ, Gottesman S (2013) Bacterial small RNA-based negative regulation: Hfq and its accomplices. J Biol Chem 288:7996–8003. doi:10.1074/jbc.R112.441386
Dorman CJ (2004) H-NS: a universal regulator for a dynamic genome. Nat Rev Microbiol 2:391–400. doi:10.1038/nrmicro883
Guinote IB, Moreira RN, Barahona S, Freire P, Vicente M, Arraiano CM (2014) Breaking through the stress barrier: the role of BolA in Gram-negative survival. World J Microbiol Biotechnol 30:2559–2566. doi:10.1007/s11274-014-1702-4
Lalaouna D, Masse E (2015) Identification of sRNA interacting with a transcript of interest using MS2-affinity purification coupled with RNA sequencing (MAPS) technology. Genom Data 5:136–138. doi:10.1016/j.gdata.2015.05.033
Lalaouna D, Simoneau-Roy M, Lafontaine D, Masse E (2013) Regulatory RNAs and target mRNA decay in prokaryotes. Biochim Biophys Acta 1829:742–747. doi:10.1016/j.bbagrm.2013.02.013
Lalaouna D, Carrier MC, Semsey S, Brouard JS, Wang J, Wade JT, Masse E (2015a) A 3′ external transcribed spacer in a tRNA transcript acts as a sponge for small RNAs to prevent transcriptional noise. Mol Cell 58:393–405. doi:10.1016/j.molcel.2015.03.013
Lalaouna D, Morissette A, Carrier MC, Masse E (2015b) DsrA regulatory RNA represses both hns and rbsD mRNAs through distinct mechanisms in Escherichia coli. Mol Microbiol 98:357–369. doi:10.1111/mmi.13129
Lease RA, Cusick ME, Belfort M (1998) Riboregulation in Escherichia coli: DsrA RNA acts by RNA:RNA interactions at multiple loci. Proc Natl Acad Sci USA 95:12456–12461
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. Proc Natl Acad Sci USA 95:12462–12467
Majdalani N, Chen S, Murrow J, St John K, Gottesman S (2001) Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol Microbiol 39:1382–1394
Mandin P, Gottesman S (2010) Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 29:3094–3107. doi:10.1038/emboj.2010.179
McCullen CA, Benhammou JN, Majdalani N, Gottesman S (2010) Mechanism of positive regulation by DsrA and RprA small noncoding RNAs: pairing increases translation and protects rpoS mRNA from degradation. J Bacteriol 192:5559–5571. doi:10.1128/jb.00464-10
Repoila F, Gottesman S (2001) Signal transduction cascade for regulation of RpoS: temperature regulation of DsrA. J Bacteriol 183:4012–4023. doi:10.1128/jb.183.13.4012-4023.2001
Saramago M et al (2014) The role of RNases in the regulation of small RNAs. Curr Opin Microbiol 18:105–115. doi:10.1016/j.mib.2014.02.009
Schu DJ, Zhang A, Gottesman S, Storz G (2015) Alternative Hfq-sRNA interaction modes dictate alternative mRNA recognition. EMBO J. doi:10.15252/embj.201591569
Sledjeski D, Gottesman S (1995) A small RNA acts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli. Proc Natl Acad Sci USA 92:2003–2007
Sledjeski DD, Gupta A, Gottesman S (1996) The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J 15:3993–4000
Soper T, Mandin P, Majdalani N, Gottesman S, Woodson SA (2010) Positive regulation by small RNAs and the role of Hfq. Proc Natl Acad Sci USA 107:9602–9607. doi:10.1073/pnas.1004435107
Wagner EG, Romby P (2015) Small RNAs in bacteria and archaea: who they are what they do, and how they do it. Adv Genet 90:133–208. doi:10.1016/bs.adgen.2015.05.001
Zambrano N, Guichard PP, Bi Y, Cayrol B, Marco S, Arluison V (2009) Involvement of HFq protein in the post-transcriptional regulation of E. coli bacterial cytoskeleton and cell division proteins. Cell Cycle 8:2470–2472
Zhang A, Altuvia S, Tiwari A, Argaman L, Hengge-Aronis R, Storz G (1998) The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J 17:6061–6068. doi:10.1093/emboj/17.20.6061
Acknowledgments
This work has been supported by an operating grant from the Canadian Institutes of Health Research (CIHR) to EM. EM is a senior scholar from the Fonds de la Recherche en santé du Québec (FRSQ).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there are no conflicts of interest.
Additional information
Communicated by M. Kupiec.
Rights and permissions
About this article
Cite this article
Lalaouna, D., Massé, E. The spectrum of activity of the small RNA DsrA: not so narrow after all. Curr Genet 62, 261–264 (2016). https://doi.org/10.1007/s00294-015-0533-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00294-015-0533-7