Central role for RNase YbeY in Hfq-dependent and Hfq-independent small-RNA regulation in bacteria

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Pandey, Shree P ^a   Winkler, Jonathan A ^b   Li, Hu ^b,d   Camacho, Diogo M ^b   Collins, James J ^b   Walker, Graham C ^c  

^a INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH KOLKATA   (India)

^b Boston University   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d MAYO GRADUATE SCHOOL   (United States)

Author keywords

E. coli; Hfq; Hydroxyurea; Small RNA; Stress adaptation; YbeY

Indexed keywords

BACTERIAL RNA; ESCHERICHIA COLI PROTEIN; HFQ PROTEIN, E COLI; HOST FACTOR 1; HYDROXYUREA; METALLOPROTEIN; YBEY PROTEIN, E COLI;

DRUG EFFECTS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; HOST FACTOR 1 PROTEIN; HYDROXYUREA; METALLOPROTEINS; RNA, BACTERIAL;

EID: 84893679350     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-121     Document Type: Article

References (42)

1. Huang HY, Chang HY, Chou CH, Tseng CP, Ho SY, Yang CD, Ju YW, Huang HD. sRNAMap: genomic maps for small non-coding RNAs, their regulators and their targets in microbial genomes. Nucleic Acids Res 2009, 37(Database issue):D150-D154. 2686527, 19015153.
2. Waters LS, Storz G. Regulatory RNAs in bacteria. Cell 2009, 136(4):615-628. 10.1016/j.cell.2009.01.043, 3132550, 19239884.
3. Storz G, Vogel J, Wassarman KM. Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 2011, 43(6):880-891. 10.1016/j.molcel.2011.08.022, 3176440, 21925377.
4. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120(1):15-20. 10.1016/j.cell.2004.12.035, 15652477.
5. Barra-Bily L, Pandey SP, Trautwetter A, Blanco C, Walker GC. The Sinorhizobium meliloti RNA chaperone Hfq mediates symbiosis of S. meliloti and alfalfa. J Bacteriol 2010, 192(6):1710-1718. 10.1128/JB.01427-09, 2832522, 20081033.
6. Brennan RG, Link TM. Hfq structure, function and ligand binding. Curr Opin Microbiol 2007, 10(2):125-133. 10.1016/j.mib.2007.03.015, 17395525.
7. Link TM, Valentin-Hansen P, Brennan RG. Structure of Escherichia coli Hfq bound to polyriboadenylate RNA. Proc Natl Acad Sci U S A 2009, 106(46):19292-19297. 10.1073/pnas.0908744106, 2773200, 19889981.
8. Bardill JP, Hammer BK. Non-coding sRNAs regulate virulence in the bacterial pathogen Vibrio cholerae. RNA Biol 2012, 9(4):392-401. 10.4161/rna.19975, 3384565, 22546941.
9. Vogel J, Luisi BF. Hfq and its constellation of RNA. Nat Rev Microbiol 2011, 9(8):578-589. 10.1038/nrmicro2615, 21760622.
10. Aiba H. Mechanism of RNA silencing by Hfq-binding small RNAs. Curr Opin Microbiol 2007, 10(2):134-139. 10.1016/j.mib.2007.03.010, 17383928.
11. Bandyra KJ, Said N, Pfeiffer V, Gorna MW, Vogel J, Luisi BF. The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E. Mol Cell 2012, 47(6):943-953. 10.1016/j.molcel.2012.07.015, 3469820, 22902561.
12. Sauer E, Schmidt S, Weichenrieder O. Small RNA binding to the lateral surface of Hfq hexamers and structural rearrangements upon mRNA target recognition. Proc Natl Acad Sci U S A 2012, 109(24):9396-9401. 10.1073/pnas.1202521109, 3386104, 22645344.
13. Sauer E, Weichenrieder O. Structural basis for RNA 3′-end recognition by Hfq. Proc Natl Acad Sci U S A 2011, 108(32):13065-13070. 10.1073/pnas.1103420108, 3156190, 21737752.
14. Papenfort K, Bouvier M, Mika F, Sharma CM, Vogel J. Evidence for an autonomous 5′ target recognition domain in an Hfq-associated small RNA. Proc Natl Acad Sci U S A 2010, 107(47):20435-20440. 10.1073/pnas.1009784107, 2996696, 21059903.
15. Hutvagner G, Simard MJ. Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 2008, 9(1):22-32. 10.1038/nrm2321, 18073770.
16. Pandey SP, Minesinger BK, Kumar J, Walker GC. A highly conserved protein of unknown function in Sinorhizobium meliloti affects sRNA regulation similar to Hfq. Nucleic Acids Res 2011, 39(11):4691-4708. 10.1093/nar/gkr060, 3113577, 21325267.
17. Gil R, Silva FJ, Pereto J, Moya A. Determination of the core of a minimal bacterial gene set. Microbiol Mol Biol Rev 2004, 68(3):518-537. 10.1128/MMBR.68.3.518-537.2004, 515251, 15353568.
18. Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK, Arnaud M, Asai K, Ashikaga S, Aymerich S, Bessieres P, et al. Essential Bacillus subtilis genes. Proc Natl Acad Sci U S A 2003, 100(8):4678-4683. 10.1073/pnas.0730515100, 153615, 12682299.
19. Akerley BJ, Rubin EJ, Novick VL, Amaya K, Judson N, Mekalanos JJ. A genome-scale analysis for identification of genes required for growth or survival of Haemophilus influenzae. Proc Natl Acad Sci U S A 2002, 99(2):966-971. 10.1073/pnas.012602299, 117414, 11805338.
20. Davies BW, Walker GC. A highly conserved protein of unknown function is required by Sinorhizobium meliloti for symbiosis and environmental stress protection. J Bacteriol 2008, 190(3):1118-1123. 10.1128/JB.01521-07, 2223554, 18055601.
21. Rasouly A, Davidovich C, Ron EZ. The heat shock protein YbeY is required for optimal activity of the 30S ribosomal subunit. J Bacteriol 2010, 192(18):4592-4596. 10.1128/JB.00448-10, 2937419, 20639334.
22. Rasouly A, Schonbrun M, Shenhar Y, Ron EZ. YbeY - a heat shock protein involved in translation in Escherichia coli. J Bacteriol 2009, 191:2649-2655. 10.1128/JB.01663-08, 2668401, 19181801.
23. Davies BW, Köhrer C, Jacob AI, Simmons LA, Zhu J, Aleman LM, Rajbhandhari UL, Walker GC. Role of Escherichia coli YbeY, a highly conserved protein, in rRNA processing. Mol Microbiol 2010, 78(2):506-518. 10.1111/j.1365-2958.2010.07351.x, 2959132, 20807199.
24. Jacob AI, Kohrer C, Davies BW, Rajbhandary UL, Walker GC. Conserved bacterial RNase YbeY plays Key roles in 70S ribosome quality control and 16S rRNA maturation. Mol Cell 2013, 49(3):427-438. 10.1016/j.molcel.2012.11.025, 3570609, 23273979.
25. Davies BW, Kohanski MA, Simmons LA, Winkler JA, Collins JJ, Walker GC. Hydroxyurea induces hydroxyl radical-mediated cell death in Escherichia coli. Mol Cell 2009, 36(5):845-860. 10.1016/j.molcel.2009.11.024, 2821657, 20005847.
26. Faith JJ, Hayete B, Thaden JT, Mogno I, Wierzbowski J, Cottarel G, Kasif S, Collins JJ, Gardner TS. Large-scale mapping and validation of Escherichia coli transcriptional regulation from a compendium of expression profiles. PLoS Biol 2007, 5(1):e8. 10.1371/journal.pbio.0050008, 1764438, 17214507.
27. Modi SR, Camacho DM, Kohanski MA, Walker GC, Collins JJ. Functional characterization of bacterial sRNAs using a network biology approach. Proc Natl Acad Sci U S A 2011, 108(37):15522-15527. 10.1073/pnas.1104318108, 3174649, 21876160.
28. Cao Y, Wu J, Liu Q, Zhao Y, Ying X, Cha L, Wang L, Li W. sRNATarBase: a comprehensive database of bacterial sRNA targets verified by experiments. RNA 2010, 16(11):2051-2057. 10.1261/rna.2193110, 2957045, 20843985.
29. Kohanski MA, Dwyer DJ, Wierzbowski J, Cottarel G, Collins JJ. Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 2008, 135(4):679-690. 10.1016/j.cell.2008.09.038, 2684502, 19013277.
30. Nakayashiki T, Mori H. Genome-wide screening with hydroxyurea reveals a link between nonessential ribosomal proteins and reactive oxygen species production. J Bacteriol 2013, 195(6):1226-1235. 10.1128/JB.02145-12, 3592001, 23292777.
31. Nakayashiki T, Saito N, Takeuchi R, Kadokura H, Nakahigashi K, Wanner BL, Mori H. The tRNA thiolaton pathway modulates the intracellular redox state in Escherchia coli. J Bacteriol 2013, 195(9):2039-2049. 10.1128/JB.02180-12, 3624572, 23457245.
32. Beisel CL, Storz G. Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev 2010, 34(5):866-882. 2920360, 20662934.
33. Papenfort K, Vogel J. Multiple target regulation by small noncoding RNAs rewires gene expression at the post-transcriptional level. Res Microbiol 2009, 160(4):278-287. 10.1016/j.resmic.2009.03.004, 19366629.
34. Henke JM, Bassler BL. Bacterial social engagements. Trends Cell Biol 2004, 14(11):648-656. 10.1016/j.tcb.2004.09.012, 15519854.
35. Mahoney TF, Silhavy TJ. The Cpx stress response confers resistance to some, but not all, bactericidal antibiotics. J Bacteriol 2013, 195(9):1869-1874. 10.1128/JB.02197-12, 3624577, 23335416.
36. Kint CI, Verstraeten N, Wens I, Liebens VR, Hofkens J, Versees W, Fauvart M, Michiels J. The Escherichia coli GTPase ObgE modulates hydroxyl radical levels in response to DNA replication fork arrest. FEBS J 2012, 279(19):3692-3704. 10.1111/j.1742-4658.2012.08731.x, 22863262.
37. Altuvia S, Weinstein-Fischer D, Zhang A, Postow L, Storz G. A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell 1997, 90(1):43-53. 10.1016/S0092-8674(00)80312-8, 9230301.
38. Bibi E. Early targeting events during membrane protein biogenesis in Escherichia coli. Biochim Biophys Acta 2011, 1808(3):841-850. 10.1016/j.bbamem.2010.07.025, 20682283.
39. Vogel J, Papenfort K. Small non-coding RNAs and the bacterial outer membrane. Curr Opin Microbiol 2006, 9(6):605-611. 10.1016/j.mib.2006.10.006, 17055775.
40. Faith JJ, Driscoll ME, Fusaro VA, Cosgrove EJ, Hayete B, Juhn FS, Schneider SJ, Gardner TS. Many microbe microarrays database: uniformly normalized affymetrix compendia with structured experimental metadata. Nucleic Acids Res 2008, 36(Database issue):D866-D870. 2238822, 17932051.
41. Cheadle C, Vawter MP, Freed WJ, Becker KG. Analysis of microarray data using Z score transformation. J Mol Diagn 2003, 5(2):73-81. 10.1016/S1525-1578(10)60455-2, 1907322, 12707371.
42. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4(1):44-57.