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2016 | 63 | 4 | 701-707

Article title

Contributions of the Hfq protein to translation regulation by small noncoding RNAs binding to the mRNA coding sequence

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EN

Abstracts

EN
The bacterial Sm-like protein Hfq affects the regulation of translation by small noncoding RNAs (sRNAs). In this way, Hfq participates in the cell adaptation to environmental stress, regulation of cellular metabolism, and bacterial virulence. The majority of known sRNAs bind complementary sequences in the 5'-untranslated mRNA regions. However, recent studies have shown that sRNAs can also target the mRNA coding sequence, even far downstream of the AUG start codon. In this review, we discuss how Hfq contributes to the translation regulation by those sRNAs which bind to the mRNA coding sequence.

Keywords

EN

Year

Volume

63

Issue

4

Pages

701-707

Physical description

Dates

published
2016
received
2016-06-06
revised
2016-10-11
accepted
2016-10-13
(unknown)
2016-11-23

Contributors

  • Department of Biochemistry, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University in Poznań, Poznań, Poland
  • Department of Biochemistry, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University in Poznań, Poznań, Poland

References

  • Andrade JM, Pobre V, Matos AM, Arraiano CM (2012) The crucial role of PNPase in the degradation of small RNAs that are not associated with Hfq. RNA 18: 844-855. https://doi.org/10.1261/rna.029413.111.
  • Argaman L, Altuvia S (2000) fhlA repression by OxyS RNA: kissing complex formation at two sites results in a stable antisense-target RNA complex. J Mol Biol 300: 1101-1112. https://doi.org/10.1006/jmbi.2000.3942.
  • Balbontin R, Fiorini F, Figueroa-Bossi N, Casadesus J, Bossi L (2010) Recognition of heptameric seed sequence underlies multi-target regulation by RybB small RNA in Salmonella enterica. Mol Microbiol 78: 380-394. https://doi.org/10.1111/j.1365-2958.2010.07342.x.
  • Bandyra KJ, Said N, Pfeiffer V, Gorna 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. Mol Cell 47: 943-953. https://doi.org/10.1016/j.molcel.2012.07.015.
  • 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. Mol Cell 41: 286-297. https://doi.org/10.1016/j.molcel.2010.12.027.
  • Bobrovskyy M, Vanderpool CK (2016) Diverse mechanisms of post-transcriptional repression by the small RNA regulator of glucose-phosphate stress. Mol Microbiol 99: 254-273. https://doi.org/10.1111/mmi.13230.
  • Bouvier M, Sharma CM, Mika F, Nierhaus KH, Vogel J (2008) Small RNA binding to 5' mRNA coding region inhibits translational initiation. Mol Cell 32: 827-837. https://doi.org/10.1016/j.molcel.2008.10.027.
  • Cech GM, Pakula B, Kamrowska D, Wegrzyn G, Arluison V, Szalewska-Palasz A (2014) Hfq protein deficiency in Escherichia coli affects ColE1-like but not lambda plasmid DNA replication. Plasmid 73: 10-15. https://doi.org/10.1016/j.plasmid.2014.04.005.
  • Chao Y, Vogel J (2010) The role of Hfq in bacterial pathogens. Curr Opin Microbiol 13: 24-33. 10.1016/j.mib.2010.01.001.
  • Chao Y, Vogel J (2016) A 3' UTR-Derived Small RNA provides the regulatory noncoding arm of the inner membrane stress response. Mol Cell 61: 352-363. https://doi.org/10.1016/j.molcel.2015.12.023.
  • Corcoran CP, Podkaminski D, Papenfort K, Urban JH, Hinton JC, Vogel J (2012) Superfolder GFP reporters validate diverse new mRNA targets of the classic porin regulator, MicF RNA. Mol Microbiol 84: 428-445. https://doi.org/10.1111/j.1365-2958.2012.08031.x.
  • de Haseth PL, Uhlenbeck OC (1980) Interaction of Escherichia coli host factor protein with oligoriboadenylates. Biochemistry 19: 6138-6146. https://doi.org/10.1021/bi00567a029.
  • Desnoyers G, Masse E (2012) Noncanonical repression of translation initiation through small RNA recruitment of the RNA chaperone Hfq. Genes Dev 26: 726-739. https://doi.org/10.1101/gad.182493.111.
  • Ellis MJ, Trussler RS, Haniford DB (2015) Hfq binds directly to the ribosome-binding site of IS10 transposase mRNA to inhibit translation. Mol Microbiol 96: 633-650. https://doi.org/10.1111/mmi.12961.
  • Fender A, Elf J, Hampel K, Zimmermann B, Wagner EG (2010) RNAs actively cycle on the Sm-like protein Hfq. Genes Dev 24: 2621-2626. https://doi.org/10.1101/gad.591310.
  • Fontaine F, Gasiorowski E, Gracia C, Ballouche M, Caillet J, Marchais A, Hajnsdorf E (2016) The small RNA SraG participates in PNPase homeostasis. RNA 22: 1560-1573. https://doi.org/10.1261/rna.055236.115.
  • Frohlich KS, Haneke K, Papenfort K, Vogel J (2016) The target spectrum of SdsR small RNA in Salmonella. Nucleic Acids Res. https://doi.org/10.1093/nar/gkw632.
  • Frohlich KS, Papenfort K, Berger AA, Vogel J (2012) A conserved RpoS-dependent small RNA controls the synthesis of major porin OmpD. Nucleic Acids Res 40: 3623-3640. https://doi.org/10.1093/nar/gkr1156.
  • Geissmann TA, Touati D (2004) Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator. EMBO J 23: 396-405. https://doi.org/10.1038/sj.emboj.7600058.
  • Groszewska A, Wroblewska Z, Olejniczak M (2016) The structure of fadL mRNA and its interactions with RybB sRNA. Acta Biochim Pol 63: 835-840. https://doi.org/10.18388/abp.2016_1361.
  • 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 Dev 28: 1620-1634. 10.1101/gad.243485.114.
  • Gutierrez A, Laureti L, Crussard S, Abida H, Rodriguez-Rojas A, Blazquez J, Baharoglu Z, Mazel D, Darfeuille F, Vogel J, Matic I (2013) β-Lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity. Nat Commun 4: 1610. 10.1038/ncomms2607.
  • Hao Y, Updegrove TB, Livingston NN, Storz G (2016) Protection against deleterious nitrogen compounds: role of sigmaS-dependent small RNAs encoded adjacent to sdiA. Nucleic Acids Res. https://doi.org/10.1093/nar/gkw404.
  • Heidrich N, Chinali A, Gerth U, Brantl S (2006) The small untranslated RNA SR1 from the Bacillus subtilis genome is involved in the regulation of arginine catabolism. Mol Microbiol 62: 520-536. https://doi.org/10.1111/j.1365-2958.2006.05384.x.
  • Heidrich N, Moll I, Brantl S (2007) In vitro analysis of the interaction between the small RNA SR1 and its primary target ahrC mRNA. Nucleic Acids Res 35: 4331-4346. https://doi.org/10.1093/nar/gkm439.
  • Henderson CA, Vincent HA, Casamento A, Stone CM, Phillips JO, Cary PD, Sobott F, Gowers DM, Taylor JE, Callaghan AJ (2013) Hfq binding changes the structure of Escherichia coli small noncoding RNAs OxyS and RprA, which are involved in the riboregulation of rpoS. RNA 19: 1089-1104. https://doi.org/10.1261/rna.034595.112.
  • Holmqvist E, Unoson C, Reimegard J, Wagner EG (2012) A mixed double negative feedback loop between the sRNA MicF and the global regulator Lrp. Mol Microbiol 84: 414-427. https://doi.org/10.1111/j.1365-2958.2012.07994.x.
  • 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. EMBO J 35: 991-1011. https://doi.org/10.15252/embj.201593360.
  • Huttenhofer A, Noller HF (1994) Footprinting mRNA-ribosome complexes with chemical probes. EMBO J 13: 3892-3901. http://www.ncbi.nlm.nih.gov/pubmed/8070416.
  • Ikeda Y, Yagi M, Morita T, Aiba H (2011) 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 79: 419-432. https://doi.org/10.1111/j.1365-2958.2010.07454.x.
  • Jorgensen MG, Thomason MK, Havelund J, Valentin-Hansen P, Storz G (2013) Dual function of the McaS small RNA in controlling biofilm formation. Genes Dev 27: 1132-1145. https://doi.org/10.1101/gad.214734.113.
  • Kakoschke TK, Kakoschke SC, Zeuzem C, Bouabe H, Adler K, Heesemann J, Rossier O (2016) The RNA chaperone Hfq is essential for virulence and modulates the expression of four adhesins in Yersinia enterocolitica. Sci Rep 6: 29275. https://doi.org/10.1038/srep29275.
  • Lalaouna D, Morissette A, Carrier MC, Masse E (2015) DsrA regulatory RNA represses both hns and rbsD mRNAs through distinct mechanisms in Escherichia coli. Mol Microbiol 98: 357-369. https://doi.org/10.1111/mmi.13129.
  • Lease RA, Woodson SA (2004) Cycling of the Sm-like protein Hfq on the DsrA small regulatory RNA. J Mol Biol 344: 1211-1223. https://doi.org/10.1016/j.jmb.2004.10.006.
  • Lee HJ, Gottesman S (2016) sRNA roles in regulating transcriptional regulators: Lrp and SoxS regulation by sRNAs. Nucleic Acids Res 44: 6907-6923. https://doi.org/10.1093/nar/gkw358.
  • Link TM, Valentin-Hansen P, Brennan RG (2009) Structure of Escherichia coli Hfq bound to polyriboadenylate RNA. Proc Natl Acad Sci U S A 106: 19292-19297. https://doi.org/10.1073/pnas.0908744106.
  • Malecka EM, Strozecka J, Sobanska D, Olejniczak M (2015) Structure of bacterial regulatory RNAs determines their performance in competition for the chaperone protein Hfq. Biochemistry 54: 1157-1170. https://doi.org/10.1021/bi500741d.
  • 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 bacteria. Mol Cell 63: 884-897. 10.1016/j.molcel.2016.07.026.
  • Mikulecky PJ, Kaw MK, Brescia CC, Takach JC, Sledjeski DD, Feig AL (2004) Escherichia coli Hfq has distinct interaction surfaces for DsrA, rpoS and poly(A) RNAs. Nat Struct Mol Biol 11: 1206-1214. https://doi.org/10.1038/nsmb858.
  • Moller T, Franch T, Hojrup P, Keene DR, Bachinger HP, Brennan RG, Valentin-Hansen P (2002a) Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction. Mol Cell 9: 23-30. https://doi.org/10.1016/S1097-2765(01)00436-1.
  • Moller T, Franch T, Udesen C, Gerdes K, Valentin-Hansen P (2002b) Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. Genes Dev 16: 1696-1706. https://doi.org/10.1101/gad.231702.
  • Moon K, Gottesman S (2009) A PhoQ/P-regulated small RNA regulates sensitivity of Escherichia coli to antimicrobial peptides. Mol Microbiol 74: 1314-1330. https://doi.org/10.1111/j.1365-2958.2009.06944.x.
  • Morita T, Maki K, Aiba H (2005) RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev 19: 2176-2186. https://doi.org/10.1101/gad.1330405.
  • Morita T, Ueda M, Kubo K, Aiba H (2015) Insights into transcription termination of Hfq-binding sRNAs of Escherichia coli and characterization of readthrough products. RNA 21: 1490-1501. https://doi.org/10.1261/rna.051870.115.
  • Olejniczak M (2011) Despite similar binding to the Hfq protein regulatory RNAs widely differ in their competition performance. Biochemistry 50: 4427-4440. https://doi.org/10.1021/bi102043f.
  • Otaka H, Ishikawa H, Morita T, Aiba H (2011) PolyU tail of rho-independent terminator of bacterial small RNAs is essential for Hfq action. Proc Natl Acad Sci U S A 108: 13059-13064. https://doi.org/10.1073/pnas.1107050108.
  • Panja S, Santiago-Frangos A, Schu DJ, Gottesman S, Woodson SA (2015) Acidic residues in the Hfq chaperone increase the selectivity of sRNA binding and annealing. J Mol Biol 427: 3491-3500. https://doi.org/10.1016/j.jmb.2015.07.010.
  • Panja S, Schu DJ, Woodson SA (2013) Conserved arginines on the rim of Hfq catalyze base pair formation and exchange. Nucleic Acids Res 41: 7536-7546. https://doi.org/10.1093/nar/gkt521.
  • Papenfort K, Bouvier M, Mika F, Sharma CM, Vogel J (2010) Evidence for an autonomous 5' target recognition domain in an Hfq-associated small RNA. Proc Natl Acad Sci U S A 107: 20435-20440. https://doi.org/10.1073/pnas.1009784107.
  • Papenfort K, Espinosa E, Casadesus J, Vogel J (2015) Small RNA-based feedforward loop with AND-gate logic regulates extrachromosomal DNA transfer in Salmonella. Proc Natl Acad Sci U S A 112: E4772-E4781. https://doi.org/10.1073/pnas.1507825112.
  • Papenfort K, Pfeiffer V, Mika F, Lucchini S, Hinton JC, Vogel J (2006) SigmaE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol Microbiol 62: 1674-1688. https://doi.org/10.1111/j.1365-2958.2006.05524.x.
  • Papenfort K, Said N, Welsink T, Lucchini S, Hinton JC, Vogel J (2009) Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 74: 139-158. https://doi.org/10.1111/j.1365-2958.2009.06857.x.
  • Papenfort K, Sun Y, Miyakoshi M, Vanderpool CK, Vogel J (2013) Small RNA-mediated activation of sugar phosphatase mRNA regulates glucose homeostasis. Cell 153: 426-437. https://doi.org/10.1016/j.cell.2013.03.003.
  • Papenfort K, Vogel J (2014) Small RNA functions in carbon metabolism and virulence of enteric pathogens. Front Cell Infect Microbiol 4: 91. https://doi.org/10.3389/fcimb.2014.00091.
  • Parker A, Gottesman S (2016) Small RNA regulation of TolC, the outer membrane component of bacterial multidrug transporters. J Bacteriol 198: 1101-1113. 10.1128/JB.00971-15.
  • Peng Y, Curtis JE, Fang X, Woodson SA (2014a) Structural model of an mRNA in complex with the bacterial chaperone Hfq. Proc Natl Acad Sci U S A 111: 17134-17139. https://doi.org/10.1073/pnas.1410114111.
  • Peng Y, Soper TJ, Woodson SA (2014b) Positional effects of AAN motifs in rpoS regulation by sRNAs and Hfq. J Mol Biol 426: 275-285. https://doi.org/10.1016/j.jmb.2013.08.026.
  • Pfeiffer V, Papenfort K, Lucchini S, Hinton JC, Vogel J (2009) Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation. Nat Struct Mol Biol 16: 840-846. https://doi.org/10.1038/nsmb.1631.
  • Pfeiffer V, Sittka A, Tomer R, Tedin K, Brinkmann V, Vogel J (2007) A small non-coding RNA of the invasion gene island (SPI-1) represses outer membrane protein synthesis from the Salmonella core genome. Mol Microbiol 66: 1174-1191. https://doi.org/10.1111/j.1365-2958.2007.05991.x.
  • Qu X, Wen JD, Lancaster L, Noller HF, Bustamante C, Tinoco I, Jr. (2011) The ribosome uses two active mechanisms to unwind messenger RNA during translation. Nature 475: 118-121. https://doi.org/10.1038/nature10126.
  • Rice JB, Vanderpool CK (2011) The small RNA SgrS controls sugar-phosphate accumulation by regulating multiple PTS genes. Nucleic Acids Res 39: 3806-3819. https://doi.org/10.1093/nar/gkq1219.
  • Richards J, Belasco JG (2016) Distinct Requirements for 5'-Monophosphate-assisted RNA Cleavage by Escherichia coli RNase E and RNase G. J Biol Chem 291: 5038-5048. https://doi.org/10.1074/jbc.M115.702555.
  • Salim NN, Faner MA, Philip JA, Feig AL (2012) 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 40: 8021-8032. https://doi.org/10.1093/nar/gks392.
  • Salim NN, Feig AL (2010) An upstream Hfq binding site in the fhlA mRNA leader region facilitates the OxyS-fhlA interaction. PLoS One 5: e13028. https://doi.org/10.1371/journal.pone.0013028.
  • Salvail H, Caron MP, Belanger J, Masse E (2013) Antagonistic functions between the RNA chaperone Hfq and an sRNA regulate sensitivity to the antibiotic colicin. EMBO J 32: 2764-2778. https://doi.org/10.1038/emboj.2013.205.
  • Santiago-Frangos A, Kavita K, Schu DJ, Gottesman S, Woodson SA (2016) C-terminal domain of the RNA chaperone Hfq drives sRNA competition and release of target RNA. Proc Natl Acad Sci U S A 113: E6089-E6096. https://doi.org/10.1073/pnas.1613053113.
  • Saramago M, Barria C, Dos Santos RF, Silva IJ, Pobre V, Domingues S, Andrade JM, Viegas SC, Arraiano CM (2014) The role of RNases in the regulation of small RNAs. Curr Opin Microbiol 18: 105-115. https://doi.org/10.1016/j.mib.2014.02.009.
  • Sauer E, Schmidt S, Weichenrieder O (2012) Small RNA binding to the lateral surface of Hfq hexamers and structural rearrangements upon mRNA target recognition. Proc Natl Acad Sci U S A 109: 9396-9401. https://doi.org/10.1073/pnas.1202521109.
  • Sauer E, Weichenrieder O (2011) Structural basis for RNA 3'-end recognition by Hfq. Proc Natl Acad Sci U S A 108: 13065-13070. https://doi.org/10.1073/pnas.1103420108.
  • Schu DJ, Zhang A, Gottesman S, Storz G (2015) Alternative Hfq-sRNA interaction modes dictate alternative mRNA recognition. EMBO J 34: 2557-2573. https://doi.org/10.15252/embj.201591569.
  • Schumacher MA, Pearson RF, Moller T, Valentin-Hansen P, Brennan RG (2002) Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein. EMBO J 21: 3546-3556. https://doi.org/10.1093/emboj/cdf322.
  • Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, Binnewies TT, Hinton JC, Vogel J (2008) Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 4: e1000163. https://doi.org/10.1371/journal.pgen.1000163.
  • Sittka A, Sharma CM, Rolle K, Vogel J (2009) 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 6: 266-275. https://doi.org/10.4161/rna.6.3.8332.
  • Sledjeski DD, Whitman C, Zhang A (2001) Hfq is necessary for regulation by the untranslated RNA DsrA. J Bacteriol 183: 1997-2005. https://doi.org/10.1128/JB.183.6.1997-2005.2001.
  • Sonnleitner E, Blasi U (2014) Regulation of Hfq by the RNA CrcZ in Pseudomonas aeruginosa carbon catabolite repression. PLoS Genet 10: e1004440. https://doi.org/10.1371/journal.pgen.1004440.
  • 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 U S A 107: 9602-9607. https://doi.org/10.1073/pnas.1004435107.
  • Soper TJ, Doxzen K, Woodson SA (2011) Major role for mRNA binding and restructuring in sRNA recruitment by Hfq. RNA 17: 1544-1550. https://doi.org/10.1261/rna.2767211.
  • Soper TJ, Woodson SA (2008) The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 14: 1907-1917. https://doi.org/10.1261/rna.1110608.
  • Takyar S, Hickerson RP, Noller HF (2005) mRNA helicase activity of the ribosome. Cell 120: 49-58. https://doi.org/10.1016/j.cell.2004.11.042.
  • Tree JJ, Granneman S, McAteer SP, Tollervey D, Gally DL (2014) Identification of bacteriophage-encoded anti-sRNAs in pathogenic Escherichia coli. Mol Cell 55: 199-213. https://doi.org/10.1016/j.molcel.2014.05.006.
  • Tsui HC, Feng G, Winkler ME (1997) Negative regulation of mutS and mutH repair gene expression by the Hfq and RpoS global regulators of Escherichia coli K-12. J Bacteriol 179: 7476-7487. https://doi.org/10.1128/jb.179.23.7476-7487.1997.
  • Updegrove TB, Zhang A, Storz G (2016) Hfq: the flexible RNA matchmaker. Curr Opin Microbiol 30: 133-138. https://doi.org/10.1016/j.mib.2016.02.003.
  • Urban JH, Vogel J (2007) Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res 35: 1018-1037. https://doi.org/10.1093/nar/gkl1040.
  • Vogel J, Luisi BF (2011) Hfq and its constellation of RNA. Nat Rev Microbiol 9: 578-589. https://doi.org/10.1038/nrmicro2615.
  • Vytvytska O, Moll I, Kaberdin VR, von Gabain A, Blasi U (2000) Hfq (HF1) stimulates ompA mRNA decay by interfering with ribosome binding. Genes Dev 14: 1109-1118. https://doi.org/10.1101/gad.14.9.1109.
  • Wagner EG (2009) Kill the messenger: bacterial antisense RNA promotes mRNA decay. Nat Struct Mol Biol 16: 804-806. https://doi.org/10.1038/nsmb0809-804.
  • Waters LS, Storz G (2009) Regulatory RNAs in bacteria. Cell 136: 615-628. https://doi.org/10.1016/j.cell.2009.01.043.
  • Wright PR, Richter AS, Papenfort K, Mann M, Vogel J, Hess WR, Backofen R, Georg J (2013) Comparative genomics boosts target prediction for bacterial small RNAs. Proc Natl Acad Sci U S A 110: E3487-E3496. https://doi.org/10.1073/pnas.1303248110.
  • Wroblewska Z, Olejniczak M (2016) Hfq assists small RNAs in binding to the coding sequence of ompD mRNA and in rearranging its structure. RNA 22: 979-994. https://doi.org/10.1261/rna.055251.115.
  • Yusupova GZ, Yusupov MM, Cate JH, Noller HF (2001) The path of messenger RNA through the ribosome. Cell 106: 233-241. https://doi.org/10.1016/S0092-8674(01)00435-4.
  • Zhang A, Schu DJ, Tjaden BC, Storz G, Gottesman S (2013) Mutations in interaction surfaces differentially impact E. coli Hfq association with small RNAs and their mRNA targets. J Mol Biol 425: 3678-3697. https://doi.org/10.1016/j.jmb.2013.01.006.
  • Zhang A, Wassarman KM, Ortega J, Steven AC, Storz G (2002) The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol Cell 9: 11-22. https://doi.org/10.1016/S1097-2765(01)00437-3.
  • Zheng A, Panja S, Woodson SA (2016) Arginine patch predicts the RNA annealing activity of Hfq from gram-negative and gram-positive bacteria. J Mol Biol 428: 2259-2264. https://doi.org/10.1016/j.jmb.2016.03.027.

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bwmeta1.element.bwnjournal-article-abpv63p701kz
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