Despite similar binding to the Hfq protein regulatory RNAs widely differ in their competition performance

Biochemistry

Volumn 50, Issue 21, 2011, Pages 4427-4440

  Olejniczak, Mikozaj ^a  

^a INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ASSOCIATION RATES; BINDING AFFINITIES; E. COLI; HIGH-THROUGHPUT; SALT DEPENDENCE; SECONDARY STRUCTURES;

BINDING ENERGY; COMPETITION; DISSOCIATION; ESCHERICHIA COLI; RNA;

PROTEINS;

HFQ PROTEIN; PROTEIN SM; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; DIFFUSION; DILUTION; DISSOCIATION; KINETICS; MUTANT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; REGULATORY RNA SEQUENCE; THERMODYNAMICS;

BASE SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HOST FACTOR 1 PROTEIN; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RNA, BACTERIAL;

EID: 79958095433     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi102043f     Document Type: Article

References (55)

1. Waters, L. S., and Storz, G. (2009) Regulatory RNAs in bacteria. Cell 136, 615-628.
2. Romby, P., Vandenesch, F., and Wagner, E. G. (2006) The role of RNAs in the regulation of virulence-gene expression. Curr. Opin. Microbiol. 9, 229-236.
3. Altuvia, S., Weinstein-Fischer, D., Zhang, A., Postow, L., and Storz, G. (1997) A small, stable RNA induced by oxidative stress: Role as a pleiotropic regulator and antimutator. Cell 90, 43-53. (Pubitemid 28009417)
4. Sledjeski, D. D., Gupta, A., and 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. (Pubitemid 26289809)
5. Rice, P. W., and Dahlberg, J. E. (1982) A gene between polA and glnA retards growth of Escherichia coli when present in multiple copies: Physiological effects of the gene for spot 42 RNA. J. Bacteriol. 152, 1196-1210. (Pubitemid 13190426)
6. Moller, T., Franch, T., Udesen, C., Gerdes, K., and Valentin- Hansen, P. (2002) Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. Genes Dev. 16, 1696-1706. (Pubitemid 34743329)
7. Udekwu, K. I., Darfeuille, F., Vogel, J., Reimegard, J., Holmqvist, E., and Wagner, E. G. (2005) Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev. 19, 2355-2366. (Pubitemid 41396912)
8. Soper, T., Mandin, P., Majdalani, N., Gottesman, S., and Woodson, S. A. (2010) Positive regulation by small RNAs and the role of Hfq. Proc. Natl. Acad. Sci. U.S.A.
9. Urban, J. H., and Vogel, J. (2007) Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res. 35, 1018-1037. (Pubitemid 46344726)
10. Schumacher, M. A., Pearson, R. F., Moller, T., Valentin-Hansen, P., and Brennan, R. G. (2002) Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: A bacterial Sm-like protein. EMBO J. 21, 3546-3556. (Pubitemid 34760584)
11. Zhang, A., Wassarman, K. M., Ortega, J., Steven, A. C., and Storz, G. (2002) The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol. Cell 9, 11-22. (Pubitemid 34127767)
12. Geissmann, T. A., and Touati, D. (2004) Hfq, a new chaperoning role: Binding to messenger RNA determines access for small RNA regulator. EMBO J. 23, 396-405. (Pubitemid 38294504)
13. Moller, T., Franch, T., Hojrup, P., Keene, D. R., Bachinger, H. P., Brennan, R. G., and Valentin-Hansen, P. (2002) Hfq: A bacterial Sm-like protein that mediates RNA-RNA interaction. Mol. Cell 9, 23-30. (Pubitemid 34127768)
14. Mikulecky, P. J., Kaw, M. K., Brescia, C. C., Takach, J. C., Sledjeski, D. D., and Feig, A. L. (2004) Escherichia coli Hfq has distinct interaction surfaces for DsrA, rpoS and poly(A) RNAs. Nat. Struct. Mol. Biol. 11, 1206-1214.
15. Hopkins, J. F., Panja, S., and Woodson, S. A. (2011) Rapid binding and release of Hfq from ternary complexes during RNA annealing. Nucleic Acids Res.
16. Lease, R. A., and Woodson, S. A. (2004) Cycling of the Sm-like protein Hfq on the DsrA small regulatory RNA. J. Mol. Biol. 344, 1211-1223. (Pubitemid 39550474)
17. Fender, A., Elf, J., Hampel, K., Zimmermann, B., and Wagner, E. G. (2010) RNAs actively cycle on the Sm-like protein Hfq. Genes Dev. 24, 2621-2626.
18. Moll, I., Afonyushkin, T., Vytvytska, O., Kaberdin, V. R., and Blasi, U. (2003) Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs. RNA 9, 1308-1314. (Pubitemid 37310861)
19. Link, T. M., Valentin-Hansen, P., and Brennan, R. G. (2009) Structure of Escherichia coli Hfq bound to polyriboadenylate RNA. Proc. Natl. Acad. Sci. U.S.A. 106, 19292-19297.
20. Sun, X., and Wartell, R. M. (2006) Escherichia coli Hfq binds A18 and DsrA domain II with similar 2:1 Hfq6/RNA stoichiometry using different surface sites. Biochemistry 45, 4875-4887.
21. de Haseth, P. L., and Uhlenbeck, O. C. (1980) Interaction of Escherichia coli host factor protein with oligoriboadenylates. Biochemistry 19, 6138-6146. (Pubitemid 11134695)
22. Soper, T. J., and Woodson, S. A. (2008) The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 14, 1907-1917.
23. Salim, N. N., and Feig, A. L. (2010) An upstream Hfq binding site in the fhlA mRNA leader region facilitates the OxyS-fhlA interaction. PLoS One 5, pii: E13028.
24. Lorenz, C., Gesell, T., Zimmermann, B., Schoeberl, U., Bilusic, I., Rajkowitsch, L., Waldsich, C., von Haeseler, A., and Schroeder, R. (2010) Genomic SELEX for Hfq-binding RNAs identifies genomic aptamers predominantly in antisense transcripts. Nucleic Acids Res.
25. Arluison, V., Hohng, S., Roy, R., Pellegrini, O., Regnier, P., and Ha, T. (2007) Spectroscopic observation of RNA chaperone activities of Hfq in post-transcriptional regulation by a small non-coding RNA. Nucleic Acids Res. 35, 999-1006. (Pubitemid 46344724)
26. Brescia, C. C., Mikulecky, P. J., Feig, A. L., and Sledjeski, D. D. (2003) Identification of the Hfq-binding site on DsrA RNA: Hfq binds without altering DsrA secondary structure. RNA 9, 33-43. (Pubitemid 36206300)
27. Darfeuille, F., Unoson, C., Vogel, J., and Wagner, E. G. (2007) An antisense RNA inhibits translation by competing with standby ribosomes. Mol. Cell 26, 381-392. (Pubitemid 46687099)
28. Majdalani, N., Hernandez, D., and Gottesman, S. (2002) Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol. Microbiol. 46, 813-826. (Pubitemid 35365616)
29. Zhang, A., Altuvia, S., Tiwari, A., Argaman, L., Hengge-Aronis, R., and Storz, G. (1998) The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J. 17, 6061-6068. (Pubitemid 28474799)
30. Antal, M., Bordeau, V., Douchin, V., and Felden, B. (2005) A small bacterial RNA regulates a putative ABC transporter. J. Biol. Chem. 280, 7901-7908. (Pubitemid 40349687)
31. Milligan, J. F., Groebe, D. R., Witherell, G. W., and Uhlenbeck, O. C. (1987) Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res. 15, 8783-8798.
32. Fahlman, R. P., and Uhlenbeck, O. C. (2004) Contribution of the esterified amino acid to the binding of aminoacylated tRNAs to the ribosomal P- and A-sites. Biochemistry 43, 7575-7583. (Pubitemid 38745773)
33. Wong, I., and Lohman, T. M. (1993) A double-filter method for nitrocellulose-filter binding: Application to protein-nucleic acid interactions. Proc. Natl. Acad. Sci. U.S.A. 90, 5428-5432. (Pubitemid 23176173)
34. Updegrove, T.,Wilf, N., Sun, X., andWartell, R.M. (2008) Effect of Hfq on RprA-rpoSmRNApairing: Hfq-RNA binding and the influence of the 50 rpoS mRNA leader region. Biochemistry 47, 11184-11195.
35. Zhang, A., Wassarman, K. M., Rosenow, C., Tjaden, B. C., Storz, G., and Gottesman, S. (2003) Global analysis of small RNA and mRNA targets of Hfq. Mol. Microbiol. 50, 1111-1124. (Pubitemid 37475847)
36. de Haseth, P. L., and Uhlenbeck, O. C. (1980) Interaction of Escherichia coli host factor protein with Q beta ribonucleic acid. Biochemistry 19, 6146-6151. (Pubitemid 11134696)
37. Carmichael, G. G., Weber, K., Niveleau, A., and Wahba, A. J. (1975) The host factor required for RNA phage Qbeta RNA replication in vitro. Intracellular location, quantitation, and purification by polyadenylate- cellulose chromatography. J. Biol. Chem. 250, 3607-3612.
38. Hopkins, J. F., Panja, S., McNeil, S. A., and Woodson, S. A. (2009) Effect of salt and RNA structure on annealing and strand displacement by Hfq. Nucleic Acids Res.
39. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415. (Pubitemid 37442169)
40. Bassi, G. S., and Weeks, K. M. (2003) Kinetic and thermodynamic framework for assembly of the six-component bI3 group I intron ribonucleoprotein catalyst. Biochemistry 42, 9980-9988. (Pubitemid 37012874)
41. Ho, Y., and Waring, R. B. (1999) The maturase encoded by a group I intron from Aspergillus nidulans stabilizes RNA tertiary structure and promotes rapid splicing. J. Mol. Biol. 292, 987-1001. (Pubitemid 29481712)
42. Rose, M. A., and Weeks, K. M. (2001) Visualizing induced fit in early assembly of the human signal recognition particle. Nat. Struct. Biol. 8, 515-520. (Pubitemid 32525010)
43. Olejniczak, M., Dale, T., Fahlman, R. P., and Uhlenbeck, O. C. (2005) Idiosyncratic tuning of tRNAs to achieve uniform ribosome binding. Nat. Struct. Mol. Biol. 12, 788-793. (Pubitemid 43086253)
44. Vecerek, B., Beich-Frandsen, M., Resch, A., and Blasi, U. (2010) Translational activation of rpoS mRNA by the non-coding RNA DsrA and Hfq does not require ribosome binding. Nucleic Acids Res. 38, 1284-1293.
45. Lee, T., and Feig, A. L. (2008) The RNA binding protein Hfq interacts specifically with tRNAs. RNA 14, 514-523. (Pubitemid 351397816)
46. Rolle, K., Zywicki, M., Wyszko, E., Barciszewska, M. Z., and Barciszewski, J. (2006) Evaluation of the dynamic structure of DsrA RNA from E. coli and its functional consequences. J. Biochem. 139, 431-438. (Pubitemid 43667107)
47. Hwang, W., Arluison, V., and Hohng, S. (2011) Dynamic competition of DsrA and rpoS fragments for the proximal binding site of Hfq as a means for efficient annealing. Nucleic Acids Res.
48. Afonyushkin, T., Vecerek, B., Moll, I., Blasi, U., and Kaberdin, V. R. (2005) Both RNase E and RNase III control the stability of sodB mRNA upon translational inhibition by the small regulatory RNA RyhB. Nucleic Acids Res. 33, 1678-1689. (Pubitemid 41418396)
49. Galluppi, G. R., and Richardson, J. P. (1980) ATP-induced changes in the binding of RNA synthesis termination protein Rho to RNA. J. Mol. Biol. 138, 513-539.
50. Steinmetz, E. J., and Platt, T. (1994) Evidence supporting a tethered tracking model for helicase activity of Escherichia coli Rho factor. Proc. Natl. Acad. Sci. U.S.A. 91, 1401-1405. (Pubitemid 24059019)
51. Sledjeski, D. D., Whitman, C., and Zhang, A. (2001) Hfq is necessary for regulation by the untranslated RNA DsrA. J. Bacteriol. 183, 1997-2005. (Pubitemid 32225995)
52. Record, M. T., Jr., Lohman, M. L., and De Haseth, P. (1976) Ion effects on ligand-nucleic acid interactions. J. Mol. Biol. 107, 145-158.
53. Hussein, R., and Lim, H. N. (2011) Disruption of small RNA signaling caused by competition for Hfq. Proc. Natl. Acad. Sci. U.S.A. 108, 1110-1115.
54. Papenfort, K., Said, N., Welsink, T., Lucchini, S., Hinton, J. C., and Vogel, J. (2009) Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol. Microbiol. 74, 139-158.
55. Kajitani, M., Kato, A., Wada, A., Inokuchi, Y., and Ishihama, A. (1994) Regulation of the Escherichia coli hfq gene encoding the host factor for phage Q beta. J. Bacteriol. 176, 531-534. (Pubitemid 24034076)