The influence of Escherichia coli Hfq mutations on RNA binding and sRNA•mRNA duplex formation in rpoS riboregulation

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1809, Issue 10, 2011, Pages 532-540

  Updegrove, Taylor B ^a   Wartell, Roger M ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

DsrA; Hfq protein; OxyS; RprA; SRNA rpoS mRNA regulation

Indexed keywords

BACTERIAL PROTEIN; MESSENGER RNA; PROTEIN HFQ; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; DSRA GENE; ESCHERICHIA COLI; GENE MUTATION; NONHUMAN; OXYS GENE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; RIBOSOME; RPOS GENE; RPRA GENE;

BACTERIAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HOST FACTOR 1 PROTEIN; KINETICS; MUTATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; RNA, BACTERIAL; RNA, MESSENGER; SIGMA FACTOR;

ESCHERICHIA COLI;

EID: 80053440900     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2011.08.006     Document Type: Article

References (43)

1. Tsui H.C., Leung H.C., Winkler M.E. Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol. Microbiol. 1994, 13:35-49.
2. Aiba H. Mechanism of RNA silencing by Hfq-binding small RNAs. Curr. Opin. Microbiol. 2007, 10:134-139.
3. Waters L.S., Storz G. Regulatory RNAs in bacteria. Cell 2009, 136:615-628.
4. Valentin-Hansen P., Eriksen M., Udesen C. The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol. Microbiol. 2004, 51:1525-1533.
5. Majdalani N., Vanderpool C.K., Gottesman S. Bacterial small RNA regulators. Crit. Rev. Biochem. Mol. Biol. 2005, 40:93-113.
6. Moller T., Franch T., Hojrup P., Keene D.R., Bachinger H.P., Brennan R.G., Valentin-Hansen P. Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction. Mol. Cell 2002, 9:23-30.
7. Zhang A., Wassarman K.M., Ortega J., Steven A.C., Storz G. The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol. Cell 2002, 9:11-22.
8. Geissmann T.A., Touati D. Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator. EMBO J. 2004, 23:396-405.
9. Repoila F., Majdalani N., Gottesman S. Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm. Mol. Microbiol. 2003, 48:855-861.
10. Hengge-Aronis R. Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 2002, 66:373-395. table of contents.
11. Majdalani N., Cunning C., Sledjeski D., Elliott T., Gottesman S. 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. U. S. A. 1998, 95:12462-12467.
12. Majdalani N., Hernandez D., Gottesman S. Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol. Microbiol. 2002, 46:813-826.
13. Brown L., Elliott T. Mutations that increase expression of the rpoS gene and decrease its dependence on hfq function in Salmonella typhimurium. J. Bacteriol. 1997, 179:656-662.
14. Lease R.A., Woodson S.A. Cycling of the Sm-like protein Hfq on the DsrA small regulatory RNA. J. Mol. Biol. 2004, 344:1211-1223.
15. Zhang A., Altuvia S., Tiwari A., Argaman L., Hengge-Aronis R., Storz G. The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J. 1998, 17:6061-6068.
16. Schumacher M.A., Pearson R.F., Moller T., Valentin-Hansen P., Brennan R.G. Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein. EMBO J. 2002, 21:3546-3556.
17. Sauter C., Basquin J., Suck D. Sm-like proteins in Eubacteria: the crystal structure of the Hfq protein from Escherichia coli. Nucleic Acids Res. 2003, 31:4091-4098.
18. Nikulin A., Stolboushkina E., Perederina A., Vassilieva I., Blaesi U., Moll I., Kachalova G., Yokoyama S., Vassylyev D., Garber M., Nikonov S. Structure of Pseudomonas aeruginosa Hfq protein. Acta Crystallogr. D Biol. Crystallogr. 2005, 61:141-146.
19. Beich-Frandsen M., Vecerek B., Sjoblom B., Blasi U., Djinovic-Carugo K. Structural analysis of full-length Hfq from Escherichia coli. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2011, 67:536-540.
20. Updegrove T.B., Correia J.J., Chen Y., Terry C., Wartell R.M. The stoichiometry of the Escherichia coli Hfq protein bound to RNA. RNA 2011, 17:489-500.
21. Mikulecky P.J., Kaw M.K., Brescia C.C., Takach J.J., Sledjeski D., Feig A.L. Escherichia coli Hfq has distinct interaction surfaces for DsrA, rpoS and poly(A) RNAs. Nat. Struct. Mol. Biol. 2004, 11:1206-1214.
22. Sun X., Wartell R.M. Escherichia coli Hfq binds A18 and DsrA domain II with similar 2:1 Hfq6/RNA stoichiometry using different surface sites. Biochemistry 2006, 45:4875-4887.
23. Updegrove T., Wilf N., Sun X., Wartell R.M. Effect of Hfq on RprA-rpoS mRNA pairing: Hfq-RNA binding and the influence of the 5′ rpoS mRNA leader region. Biochemistry 2008, 47:11184-11195.
24. Olejniczak M. Despite similar binding to the Hfq protein regulatory RNAs widely differ in their competition performance. Biochemistry 2011, 50:4427-4440.
25. Soper T.J., Woodson S.A. The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 2008, 14:1907-1917.
26. Link T.M., Valentin-Hansen P., Brennan R.G. Structure of Escherichia coli Hfq bound to polyriboadenylate RNA. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:19292-19297.
27. Soper T., Mandin P., Majdalani N., Gottesman S., Woodson S.A. Positive regulation by small RNAs and the role of Hfq. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:9602-9607.
28. Vecerek B., Rajkowitsch L., Sonnleitner E., Schroeder R., Blasi U. The C-terminal domain of Escherichia coli Hfq is required for regulation. Nucleic Acids Res. 2008, 36:133-143.
29. Beich-Frandsen M., Vecerek B., Konarev P.V., Sjoblom B., Kloiber K., Hammerle H., Rajkowitsch L., Miles A.J., Kontaxis G., Wallace B.A., Svergun D.I., Konrat R., Blasi U., Djinovic-Carugo K. Structural insights into the dynamics and function of the C-terminus of the E. coli RNA chaperone Hfq. Nucleic Acids Res. 2011, 39:4900-4915.
30. Olsen A.S., Moller-Jensen J., Brennan R.G., Valentin-Hansen P. C-terminally truncated derivatives of Escherichia coli Hfq are proficient in riboregulation. J. Mol. Biol. 2010, 404:173-182.
31. Hussein R., Lim H.N. Disruption of small RNA signaling caused by competition for Hfq. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:1110-1115.
32. Fender A., Elf J., Hampel K., Zimmermann B., Wagner E.G. RNAs actively cycle on the Sm-like protein Hfq. Genes Dev. 2010, 24:2621-2626.
33. Updegrove T.B., Correia J.J., Galletto R., Bujalowski W., Wartell R.M. E. coli DNA associated with isolated Hfq interacts with Hfq's distal surface and C-terminal domain. Biochim. Biophys. Acta 2010, 1799:588-596.
34. Brescia C.C., Mikulecky P.J., Feig A.L., Sledjeski D.D. Identification of the Hfq-binding site on DsrA RNA: Hfq binds without altering DsrA secondary structure. RNA 2003, 9:33-43.
35. Sonnleitner E., Napetschnig J., Afonyushkin T., Ecker K., Vecerek B., Moll I., Kaberdin V.R., Blasi U. Functional effects of variants of the RNA chaperone Hfq. Biochem. Biophys. Res. Commun. 2004, 323:1017-1023.
36. Lange R., Fischer D., Hengge-Aronis R. Identification of transcriptional start sites and the role of ppGpp in the expression of rpoS, the structural gene for the sigma S subunit of RNA polymerase in Escherichia coli. J. Bacteriol. 1995, 177:4676-4680.
37. Brown L., Elliott T. Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the Hfq gene. J. Bacteriol. 1996, 178:3763-3770.
38. Sledjeski D.D., Gupta A., Gottesman S. The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J. 1996, 15:3993-4000.
39. E. Sauer, O. Weichenrieder, Structural basis for RNA 3′-end recognition by Hfq, Proc. Natl. Acad. Sci. U. S. A. (in press), doi:1103420108.
40. Brennan R.G., Link T.M. Hfq structure, function and ligand binding. Curr. Opin. Microbiol. 2007, 10:125-133.
41. Jing D., Agnew J., Patton W.F., Hendrickson J., Beechem J.M. A sensitive two-color electrophoretic mobility shift assay for detecting both nucleic acids and protein in gels. Proteomics 2003, 3:1172-1180.
42. Madhugiri R., Basineni S.R., Klug G. Turn-over of the small non-coding RNA RprA in E. coli is influenced by osmolarity. Mol. Genet. Genomics 2010, 284:307-318.
43. Sledjeski D.D., Whitman C., Zhang A. Hfq is necessary for regulation by the untranslated RNA DsrA. J. Bacteriol. 2001, 183:1997-2005.