Riboregulation in plant-associated alpha-proteobacteria
Becker A, Overloeper A, Schlueter J-P, Reinkensmeier J, Robledo M, Giegerich R, Narberhaus F, Evguenieva-Hackenberg E (2014)
RNA Biology 11(5): 550-562.
Zeitschriftenaufsatz
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Autor*in
Becker, Anke;
Overloeper, Aaron;
Schlueter, Jan-Philip;
Reinkensmeier, JanUniBi;
Robledo, Marta;
Giegerich, RobertUniBi;
Narberhaus, Franz;
Evguenieva-Hackenberg, Elena
Einrichtung
Abstract / Bemerkung
The symbiotic alpha-rhizobia Sinorhizobium meliloti, Bradyrhizobium japonicum, Rhizobium etli and the related plant pathogen Agrobacterium tumefaciens are important model organisms for studying plant-microbe interactions. These metabolically versatile soil bacteria are characterized by complex lifestyles and large genomes. Here we summarize the recent knowledge on their small non-coding RNAs (sRNAs) including conservation, function, and interaction of the sRNAs with the RNA chaperone Hfq. In each of these organisms, an inventory of hundreds of cis- and trans-encoded sRNAs with regulatory potential was uncovered by high-throughput approaches and used for the construction of 39 sRNA family models. Genome-wide analyses of hfq mutants and co-immunoprecipitation with tagged Hfq revealed a major impact of the RNA chaperone on the physiology of plant-associated alpha-proteobacteria including symbiosis and virulence. Highly conserved members of the SmelC411 family are the AbcR sRNAs, which predominantly regulate ABC transport systems. AbcR1 of A. tumefaciens controls the uptake of the plant-generated signaling molecule GABA and is a central regulator of nutrient uptake systems. It has similar functions in S. meliloti and the human pathogen Brucella abortus. As RNA degradation is an important process in RNA-based gene regulation, a short overview on ribonucleases in plant-associated alpha-proteobacteria concludes this review.
Stichworte
RNA-seq;
ribolysis;
RNA-binding protein;
sRNA;
antisense RNA;
non-coding RNA;
riboregulation;
alpha-proteobacteria;
Rhizobiales
Erscheinungsjahr
2014
Zeitschriftentitel
RNA Biology
Band
11
Ausgabe
5
Seite(n)
550-562
ISSN
1547-6286
eISSN
1555-8584
Page URI
https://pub.uni-bielefeld.de/record/2699792
Zitieren
Becker A, Overloeper A, Schlueter J-P, et al. Riboregulation in plant-associated alpha-proteobacteria. RNA Biology. 2014;11(5):550-562.
Becker, A., Overloeper, A., Schlueter, J. - P., Reinkensmeier, J., Robledo, M., Giegerich, R., Narberhaus, F., et al. (2014). Riboregulation in plant-associated alpha-proteobacteria. RNA Biology, 11(5), 550-562. doi:10.4161/rna.29625
Becker, Anke, Overloeper, Aaron, Schlueter, Jan-Philip, Reinkensmeier, Jan, Robledo, Marta, Giegerich, Robert, Narberhaus, Franz, and Evguenieva-Hackenberg, Elena. 2014. “Riboregulation in plant-associated alpha-proteobacteria”. RNA Biology 11 (5): 550-562.
Becker, A., Overloeper, A., Schlueter, J. - P., Reinkensmeier, J., Robledo, M., Giegerich, R., Narberhaus, F., and Evguenieva-Hackenberg, E. (2014). Riboregulation in plant-associated alpha-proteobacteria. RNA Biology 11, 550-562.
Becker, A., et al., 2014. Riboregulation in plant-associated alpha-proteobacteria. RNA Biology, 11(5), p 550-562.
A. Becker, et al., “Riboregulation in plant-associated alpha-proteobacteria”, RNA Biology, vol. 11, 2014, pp. 550-562.
Becker, A., Overloeper, A., Schlueter, J.-P., Reinkensmeier, J., Robledo, M., Giegerich, R., Narberhaus, F., Evguenieva-Hackenberg, E.: Riboregulation in plant-associated alpha-proteobacteria. RNA Biology. 11, 550-562 (2014).
Becker, Anke, Overloeper, Aaron, Schlueter, Jan-Philip, Reinkensmeier, Jan, Robledo, Marta, Giegerich, Robert, Narberhaus, Franz, and Evguenieva-Hackenberg, Elena. “Riboregulation in plant-associated alpha-proteobacteria”. RNA Biology 11.5 (2014): 550-562.
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Small RNA-mediated control of the Agrobacterium tumefaciens GABA binding protein.
Wilms I, Voss B, Hess WR, Leichert LI, Narberhaus F., Mol. Microbiol. 80(2), 2011
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Evidence for a second class of S-adenosylmethionine riboswitches and other regulatory RNA motifs in alpha-proteobacteria.
Corbino KA, Barrick JE, Lim J, Welz R, Tucker BJ, Puskarz I, Mandal M, Rudnick ND, Breaker RR., Genome Biol. 6(8), 2005
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Expression of small RNAs in Rhizobiales and protection of a small RNA and its degradation products by Hfq in Sinorhizobium meliloti.
Voss B, Holscher M, Baumgarth B, Kalbfleisch A, Kaya C, Hess WR, Becker A, Evguenieva-Hackenberg E., Biochem. Biophys. Res. Commun. 390(2), 2009
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6S RNA regulates E. coli RNA polymerase activity.
Wassarman KM, Storz G., Cell 101(6), 2000
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Wassarman KM, Saecker RM., Science 314(5805), 2006
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Reinkensmeier J, Schluter JP, Giegerich R, Becker A., Genes (Basel) 2(4), 2011
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Nawrocki EP, Kolbe DL, Eddy SR., Bioinformatics 25(10), 2009
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Locomotif: from graphical motif description to RNA motif search.
Reeder J, Reeder J, Giegerich R., Bioinformatics 23(13), 2007
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Bellman's GAP--a language and compiler for dynamic programming in sequence analysis.
Sauthoff G, Mohl M, Janssen S, Giegerich R., Bioinformatics 29(5), 2013
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del Val C, Romero-Zaliz R, Torres-Quesada O, Peregrina A, Toro N, Jimenez-Zurdo JI., RNA Biol 9(2), 2012
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del Val C, Romero-Zaliz R, Torres-Quesada O, Peregrina A, Toro N, Jimenez-Zurdo JI., RNA Biol 9(2), 2012
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The genome of Rhizobium leguminosarum has recognizable core and accessory components.
Young JP, Crossman LC, Johnston AW, Thomson NR, Ghazoui ZF, Hull KH, Wexler M, Curson AR, Todd JD, Poole PS, Mauchline TH, East AK, Quail MA, Churcher C, Arrowsmith C, Cherevach I, Chillingworth T, Clarke K, Cronin A, Davis P, Fraser A, Hance Z, Hauser H, Jagels K, Moule S, Mungall K, Norbertczak H, Rabbinowitsch E, Sanders M, Simmonds M, Whitehead S, Parkhill J., Genome Biol. 7(4), 2006
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Torres-Quesada O, Millan V, Nisa-Martinez R, Bardou F, Crespi M, Toro N, Jimenez-Zurdo JI., PLoS ONE 8(7), 2013
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Caswell CC, Gaines JM, Ciborowski P, Smith D, Borchers CH, Roux CM, Sayood K, Dunman PM, Roop Ii RM., Mol. Microbiol. 85(2), 2012
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Contribution of Hfq to photooxidative stress resistance and global regulation in Rhodobacter sphaeroides.
Berghoff BA, Glaeser J, Sharma CM, Zobawa M, Lottspeich F, Vogel J, Klug G., Mol. Microbiol. 80(6), 2011
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Babitzke P, Romeo T., Curr. Opin. Microbiol. 10(2), 2007
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Watson RJ, Heys R., Plasmid 55(2), 2005
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Sobrero P, Valverde C., Crit. Rev. Microbiol. 38(4), 2012
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The expression of nifA in Azorhizobium caulinodans requires a gene product homologous to Escherichia coli HF-I, an RNA-binding protein involved in the replication of phage Q beta RNA.
Kaminski PA, Desnoues N, Elmerich C., Proc. Natl. Acad. Sci. U.S.A. 91(11), 1994
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Kaminski PA, Desnoues N, Elmerich C., Proc. Natl. Acad. Sci. U.S.A. 91(11), 1994
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Sobrero P, Valverde C., Arch. Microbiol. 193(9), 2011
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Storz G, Vogel J, Wassarman KM., Mol. Cell 43(6), 2011
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Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, Binnewies TT, Hinton JC, Vogel J., PLoS Genet. 4(8), 2008
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Sittka A, Sharma CM, Rolle K, Vogel J., RNA Biol 6(3), 2009
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Lorenz C, Gesell T, Zimmermann B, Schoeberl U, Bilusic I, Rajkowitsch L, Waldsich C, von Haeseler A, Schroeder R., Nucleic Acids Res. 38(11), 2010
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Chao Y, Papenfort K, Reinhardt R, Sharma CM, Vogel J., EMBO J. 31(20), 2012
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Dambach M, Irnov I, Winkler WC., PLoS ONE 8(2), 2013
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Hfq (HF1) stimulates ompA mRNA decay by interfering with ribosome binding.
Vytvytska O, Moll I, Kaberdin VR, von Gabain A, Blasi U., Genes Dev. 14(9), 2000
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Mohanty BK, Maples VF, Kushner SR., Mol. Microbiol. 54(4), 2004
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The Sinorhizobium meliloti RNA chaperone Hfq mediates symbiosis of S. meliloti and alfalfa.
Barra-Bily L, Pandey SP, Trautwetter A, Blanco C, Walker GC., J. Bacteriol. 192(6), 2010
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Wilms I, Moller P, Stock AM, Gurski R, Lai EM, Narberhaus F., J. Bacteriol. 194(19), 2012
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The control of Azorhizobium caulinodans nifA expression by oxygen, ammonia and by the HF-I-like protein, NrfA.
Kaminski PA, Elmerich C., Mol. Microbiol. 28(3), 1998
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Zhang Y, Hong G., Acta Biochim. Biophys. Sin. (Shanghai) 41(9), 2009
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Barra-Bily L, Fontenelle C, Jan G, Flechard M, Trautwetter A, Pandey SP, Walker GC, Blanco C., J. Bacteriol. 192(6), 2010
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Role of the Sinorhizobium meliloti global regulator Hfq in gene regulation and symbiosis.
Gao M, Barnett MJ, Long SR, Teplitski M., Mol. Plant Microbe Interact. 23(4), 2010
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The Sinorhizobium meliloti RNA chaperone Hfq influences central carbon metabolism and the symbiotic interaction with alfalfa.
Torres-Quesada O, Oruezabal RI, Peregrina A, Jofre E, Lloret J, Rivilla R, Toro N, Jimenez-Zurdo JI., BMC Microbiol. 10(), 2010
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Sobrero P, Schluter JP, Lanner U, Schlosser A, Becker A, Valverde C., PLoS ONE 7(10), 2012
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The Hfq-like protein NrfA of the phototrophic purple bacterium Rhodobacter capsulatus controls nitrogen fixation via regulation of nifA and anfA expression.
Drepper T, Raabe K, Giaourakis D, Gendrullis M, Masepohl B, Klipp W., FEMS Microbiol. Lett. 215(2), 2002
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Mutation of GOGAT prevents pea bacteroid formation and N2 fixation by globally downregulating transport of organic nitrogen sources.
Mulley G, White JP, Karunakaran R, Prell J, Bourdes A, Bunnewell S, Hill L, Poole PS., Mol. Microbiol. 80(1), 2011
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The Brucella abortus host factor I (HF-I) protein contributes to stress resistance during stationary phase and is a major determinant of virulence in mice.
Robertson GT, Roop RM Jr., Mol. Microbiol. 34(4), 1999
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Roop RM 2nd, Robertson GT, Ferguson GP, Milford LE, Winkler ME, Walker GC., Vet. Microbiol. 90(1-4), 2002
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A highly conserved protein of unknown function in Sinorhizobium meliloti affects sRNA regulation similar to Hfq.
Pandey SP, Minesinger BK, Kumar J, Walker GC., Nucleic Acids Res. 39(11), 2011
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Central role for RNase YbeY in Hfq-dependent and Hfq-independent small-RNA regulation in bacteria.
Pandey SP, Winkler JA, Li H, Camacho DM, Collins JJ, Walker GC., BMC Genomics 15(), 2014
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Davies BW, Kohrer C, Jacob AI, Simmons LA, Zhu J, Aleman LM, Rajbhandary UL, Walker GC., Mol. Microbiol. 78(2), 2010
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The Escherichia coli translation-associated heat shock protein YbeY is involved in rRNA transcription antitermination.
Grinwald M, Ron EZ., PLoS ONE 8(4), 2013
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Conserved bacterial RNase YbeY plays key roles in 70S ribosome quality control and 16S rRNA maturation.
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Egea PF, Stroud RM, Walter P., Curr. Opin. Struct. Biol. 15(2), 2005
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Egea PF, Stroud RM, Walter P., Curr. Opin. Struct. Biol. 15(2), 2005
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Discovery of a rhizobial RNA that is essential for symbiotic root nodule development.
Ebeling S, Kundig C, Hennecke H., J. Bacteriol. 173(20), 1991
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Ebeling S, Kundig C, Hennecke H., J. Bacteriol. 173(20), 1991
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tmRNAs that encode proteolysis-inducing tags are found in all known bacterial genomes: A two-piece tmRNA functions in Caulobacter.
Keiler KC, Shapiro L, Williams KP., Proc. Natl. Acad. Sci. U.S.A. 97(14), 2000
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The tmRNA Website: invasion by an intron.
Williams KP., Nucleic Acids Res. 30(1), 2002
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Williams KP., Nucleic Acids Res. 30(1), 2002
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The expression of a novel antisense gene mediates incompatibility within the large repABC family of alpha-proteobacterial plasmids.
MacLellan SR, Smallbone LA, Sibley CD, Finan TM., Mol. Microbiol. 55(2), 2005
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A small antisense RNA downregulates expression of an essential replicase protein of an Agrobacterium tumefaciens Ti plasmid.
Chai Y, Winans SC., Mol. Microbiol. 56(6), 2005
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Chai Y, Winans SC., Mol. Microbiol. 56(6), 2005
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GABA controls the level of quorum-sensing signal in Agrobacterium tumefaciens.
Chevrot R, Rosen R, Haudecoeur E, Cirou A, Shelp BJ, Ron E, Faure D., Proc. Natl. Acad. Sci. U.S.A. 103(19), 2006
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Planamente S, Morera S, Faure D., Commun Integr Biol 6(3), 2013
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Planamente S, Morera S, Faure D., Commun Integr Biol 6(3), 2013
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Overloper A, Kraus A, Gurski R, Wright PR, Georg J, Hess WR, Narberhaus F., RNA Biol 11(5), 2014
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Wright PR, Richter AS, Papenfort K, Mann M, Vogel J, Hess WR, Backofen R, Georg J., Proc. Natl. Acad. Sci. U.S.A. 110(37), 2013
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Wright PR, Richter AS, Papenfort K, Mann M, Vogel J, Hess WR, Backofen R, Georg J., Proc. Natl. Acad. Sci. U.S.A. 110(37), 2013
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Translational control and target recognition by Escherichia coli small RNAs in vivo.
Urban JH, Vogel J., Nucleic Acids Res. 35(3), 2007
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Urban JH, Vogel J., Nucleic Acids Res. 35(3), 2007
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Novel Sinorhizobium meliloti quorum sensing positive and negative regulatory feedback mechanisms respond to phosphate availability.
McIntosh M, Meyer S, Becker A., Mol. Microbiol. 74(5), 2009
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Modeling quorum sensing in Sinorhizobium meliloti.
McIntosh M, Czuppon P, Best K, Becker A, Pfaffelhuber P., 2013
McIntosh M, Czuppon P, Best K, Becker A, Pfaffelhuber P., 2013
MicC, a second small-RNA regulator of Omp protein expression in Escherichia coli.
Chen S, Zhang A, Blyn LB, Storz G., J. Bacteriol. 186(20), 2004
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Chen S, Zhang A, Blyn LB, Storz G., J. Bacteriol. 186(20), 2004
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An internal antisense RNA regulates expression of the photosynthesis gene isiA.
Duhring U, Axmann IM, Hess WR, Wilde A., Proc. Natl. Acad. Sci. U.S.A. 103(18), 2006
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Duhring U, Axmann IM, Hess WR, Wilde A., Proc. Natl. Acad. Sci. U.S.A. 103(18), 2006
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The influence of Hfq and ribonucleases on the stability of the small non-coding RNA OxyS and its target rpoS in E. coli is growth phase dependent.
Basineni SR, Madhugiri R, Kolmsee T, Hengge R, Klug G., RNA Biol 6(5), 2009
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Basineni SR, Madhugiri R, Kolmsee T, Hengge R, Klug G., RNA Biol 6(5), 2009
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Turn-over of the small non-coding RNA RprA in E. coli is influenced by osmolarity.
Madhugiri R, Basineni SR, Klug G., Mol. Genet. Genomics 284(4), 2010
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Madhugiri R, Basineni SR, Klug G., Mol. Genet. Genomics 284(4), 2010
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Regulation of 6S RNA biogenesis by switching utilization of both sigma factors and endoribonucleases.
Kim KS, Lee Y., Nucleic Acids Res. 32(20), 2004
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Kim KS, Lee Y., Nucleic Acids Res. 32(20), 2004
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Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA.
Papenfort K, Said N, Welsink T, Lucchini S, Hinton JCD, Vogel J., Mol. Microbiol. 74(1), 2009
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Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli.
Masse E, Escorcia FE, Gottesman S., Genes Dev. 17(19), 2003
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Masse E, Escorcia FE, Gottesman S., Genes Dev. 17(19), 2003
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Regulation of ompA mRNA stability: the role of a small regulatory RNA in growth phase-dependent control.
Rasmussen AA, Eriksen M, Gilany K, Udesen C, Franch T, Petersen C, Valentin-Hansen P., Mol. Microbiol. 58(5), 2005
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Both RNase E and RNase III control the stability of sodB mRNA upon translational inhibition by the small regulatory RNA RyhB.
Afonyushkin T, Vecerek B, Moll I, Blasi U, Kaberdin VR., Nucleic Acids Res. 33(5), 2005
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Afonyushkin T, Vecerek B, Moll I, Blasi U, Kaberdin VR., Nucleic Acids Res. 33(5), 2005
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Regulation of the small regulatory RNA MicA by ribonuclease III: a target-dependent pathway.
Viegas SC, Silva IJ, Saramago M, Domingues S, Arraiano CM., Nucleic Acids Res. 39(7), 2010
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The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E.
Bandyra KJ, Said N, Pfeiffer V, Gorna MW, Vogel J, Luisi BF., Mol. Cell 47(6), 2012
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Bandyra KJ, Said N, Pfeiffer V, Gorna MW, Vogel J, Luisi BF., Mol. Cell 47(6), 2012
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New aspects of RNA processing in prokaryotes.
Evguenieva-Hackenberg E, Klug G., Curr. Opin. Microbiol. 14(5), 2011
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Evguenieva-Hackenberg E, Klug G., Curr. Opin. Microbiol. 14(5), 2011
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Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs.
Moll I, Afonyushkin T, Vytvytska O, Kaberdin VR, Blasi U., RNA 9(11), 2003
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Moll I, Afonyushkin T, Vytvytska O, Kaberdin VR, Blasi U., RNA 9(11), 2003
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Characterization of the role of ribonucleases in Salmonella small RNA decay.
Viegas SC, Pfeiffer V, Sittka A, Silva IJ, Vogel J, Arraiano CM., Nucleic Acids Res. 35(22), 2007
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Viegas SC, Pfeiffer V, Sittka A, Silva IJ, Vogel J, Arraiano CM., Nucleic Acids Res. 35(22), 2007
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The critical role of RNA processing and degradation in the control of gene expression.
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