Effect of salt and RNA structure on annealing and strand displacement by Hfq

Nucleic Acids Research

Volumn 37, Issue 18, 2009, Pages 6205-6213

  Hopkins, Julia F ^a   Panja, Subrata ^b   McNeil, Stephanie A N ^a   Woodson, Sarah A ^b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; MESSENGER RNA; OLIGONUCLEOTIDE; PROTEIN DSRA; PROTEIN HFQ; SIGMA FACTOR RPOS; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; GENE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; RNA BINDING; RNA HYBRIDIZATION; RNA PURIFICATION; RNA STRUCTURE; SPECTROSCOPY;

ADENINE; BACTERIAL PROTEINS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENT DYES; HOST FACTOR 1 PROTEIN; KINETICS; NUCLEIC ACID CONFORMATION; NUCLEIC ACID HYBRIDIZATION; OLIGONUCLEOTIDE PROBES; RNA, ANTISENSE; RNA, UNTRANSLATED; SALTS; SIGMA FACTOR; SPECTROMETRY, FLUORESCENCE; URIDINE;

EID: 70350699443     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp646     Document Type: Article

References (45)

1. 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.
2. Masse,E. and Gottesman,S. (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl Acad. Sci. USA, 99, 4620-4625.
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.
4. Storz,G., Opdyke,J.A. and Zhang,A. (2004) Controlling mRNA stability and translation with small, noncoding RNAs. Curr. Opin. Microbiol., 7, 140-144.
5. Gottesman,S., McCullen,C.A., Guillier,M., Vanderpool,C.K., Majdalani,N., Benhammou,J., Thompson,K.M., FitzGerald,P.C., Sowa,N.A. and FitzGerald,D.J. (2006) Small RNA regulators and the bacterial response to stress. Cold Spring Harbor Symp. Quant. Biol., 71, 1-11.
6. Masse,E., Escorcia,F.E. and Gottesman,S. (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev., 17, 2374-2383.
7. Brennan,R.G. and Link,T.M. (2007) Hfq structure, function and ligand binding. Curr. Opin. Microbiol., 10, 125-133.
8. Aiba,H. (2007) Mechanism of RNA silencing by Hfq-binding small RNAs. Curr. Opin. Microbiol., 10, 134-139.
9. 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.
10. 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.
11. Sun,X., Zhulin,I. and Wartell,R.M. (2002) Predicted structure and phyletic distribution of the RNA-binding protein Hfq. Nucleic Acids Res., 30, 3662-3671.
12. Senear,A.W. and Steitz,J.A. (1976) Site-specific interaction of Qbeta host factor and ribosomal protein S1 with Qbeta and R17 bacteriophage RNAs. J. Biol. Chem., 251, 1902-1912.
13. Vytvytska,O., Moll,I., Kaberdin,V.R., von Gabain,A. and Blasi,U. (2000) Hfq (HF1) stimulates ompA mRNA decay by interfering with ribosome binding. Genes Dev., 14, 1109-1118.
14. 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.
15. Sledjeski,D.D., Whitman,C. and Zhang,A. (2001) Hfq is necessary for regulation by the untranslated RNA DsrA. J. Bacteriol., 183, 1997-2005.
16. Folichon,M., Arluison,V., Pellegrini,O., Huntzinger,E., Regnier,P. and Hajnsdorf,E. (2003) The poly(A) binding protein Hfq protects RNA from RNase E and exoribonucleolytic degradation. Nucleic Acids Res., 31, 7302-7310.
17. 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.
18. Moll,I., Leitsch,D., Steinhauser,T. and Blasi,U. (2003) RNA chaperone activity of the Sm-like Hfq protein. EMBO Rep., 4, 284-289.
19. 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.
20. Arluison,V., Mura,C., Guzman,M.R., Liquier,J., Pellegrini,O., Gingery,M., Regnier,P. and Marco,S. (2006) Three-dimensional structures of fibrillar Sm proteins: Hfq and other Sm-like proteins. J. Mol. Biol., 356, 86-96.
21. Majdalani,N., Cunning,C., Sledjeski,D., Elliott,T. and Gottesman,S. (1998) 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. USA, 95, 12462-12467.
22. Lease,R.A., Cusick,M.E. and Belfort,M. (1998) Riboregulation in Escherichia coli: DsrA RNA acts by RNA:RNA interactions at multiple loci. Proc. Natl Acad. Sci. USA, 95, 12456-12461.
23. Lange,R. and Hengge-Aronis,R. (1991) Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol. Microbiol., 5, 49-59.
24. Brown,L. and Elliott,T. (1997) Mutations that increase expression of the rpoS gene and decrease its dependence on hfq function in Salmonella typhimurium. J. Bacteriol., 179, 656-662.
25. Muffler,A., Traulsen,D.D., Fischer,D., Lange,R. and Hengge-Aronis,R. (1997) The RNA-binding protein HF-I plays a global regulatory role which is largely, but not exclusively, due to its role in expression of the sigmaS subunit of RNA polymerase in Escherichia coli. J. Bacteriol. 179, 297-300.
26. 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.
27. Soper,T.J. and Woodson,S.A. (2008) The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA, 14, 1907-1917.
28. 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.
29. Rajkowitsch,L. and Schroeder,R. (2007) Dissecting RNA chaperone activity. RNA, 13, 2053-2060.
30. Mathews,D.H., Sabina,J., Zuker,M. and Turner,D.H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol., 288, 911-940.
31. Hopkins,J.F. and Woodson,S.A. (2005) Molecular beacons as probes of RNA unfolding under native conditions. Nucleic Acids Res., 33, 5763-5770.
32. Franze de Fernandez,M.T., Hayward,W.S. and August,J.T. (1972) Bacterial proteins required for replication of phage Q ribonucleic acid. Purification and properties of host factor I, a ribonucleic acid-binding protein. J. Biol. Chem., 247, 824-831.
33. Tyagi,S. and Kramer,F.R. (1996) Molecular beacons: Probes that fluoresce upon hybridization. Nat. Biotechnol., 14, 303-308.
34. 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.
35. Hopkins,J.F. (2007) Secondary structure rearrangements monitored by fluorescent probes in RNA folding and RNA-protein interactions. Ph.D. Thesis. Johns Hopkins University, Baltimore.
36. Record,M.T., Zhang,W.T. and Anderson,C.F. (1998) Analysis of effects of salts and uncharged solutes on protein and nucleic acid equilibria and processes: A practical guide to recognizing and interpreting polyelectrolyte effects, Hofmeister effects, and osmotic effects of salts. Adv. Protein Chem., 51, 281-353.
37. Porschke,D., Uhlenbec,O.C. and Martin,F.H. (1973) Thermodynamics and kinetics of helix-coil transition of oligomers containing Gc base pairs. Biopolymers, 12, 1313-1335.
38. Updegrove,T., Wilf,N., Sun,X. and Wartell,R.M. (2008) Effect of Hfq on RprA-rpoS mRNA pairing: Hfq-RNA binding and the influence of the 5′ rpoS mRNA leader region. Biochemistry, 47, 11184-11195.
39. Wagner,E.G., Altuvia,S. and Romby,P. (2002) Antisense RNAs in bacteria and their genetic elements. Adv. Genet., 46, 361-398.
40. Porschke,D. and Eigen,M. (1971) Co-operative non-enzymic base recognition. 3. Kinetics of the helix-coil transition of the oligoribouridylic-oligoriboadenylic acid system and of oligoriboadenylic acid alone at acidic pH. J. Mol. Biol., 62, 361-381.
41. Heilman-Miller,S.L., Wu,T. and Levin,J.G. (2004) Alteration of nucleic acid structure and stability modulates the efficiency of minus-strand transfer mediated by the HIV-1 nucleocapsid protein. J. Biol. Chem. 279, 44154-44165.
42. Vo,M.N., Barany,G., Rouzina,I. and Musier-Forsyth,K. (2009) HIV-1 nucleocapsid protein switches the pathway of transactivation response element RNA/DNA annealing from loop-loop "kissing" to "zipper". J. Mol. Biol., 386, 789-801.
43. Lease,R.A. and Belfort,M. (2000) A trans-acting RNA as a control switch in Escherichia coli: DsrA modulates function by forming alternative structures. Proc. Natl Acad. Sci. USA, 97, 9919-9924.
44. Jones,A.M., Goodwill,A. and Elliott,T. (2006) Limited role for the DsrA and RprA regulatory RNAs in rpoS regulation in Salmonella enterica. J. Bacteriol., 188, 5077-5088.
45. 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.