Conserved arginines on the rim of Hfq catalyze base pair formation and exchange

Nucleic Acids Research

Volumn 41, Issue 15, 2013, Pages 7536-7546

  Panja, Subrata ^a   Schu, Daniel J ^b   Woodson, Sarah A ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; BACTERIAL PROTEIN; CHAPERONE; COMPLEMENTARY RNA; LYSINE; OLIGONUCLEOTIDE; PROTEIN HFQ; SMALL UNTRANSLATED RNA; UNCLASSIFIED DRUG;

ANISOTROPY; ARTICLE; BASE PAIRING; BINDING SITE; CATALYSIS; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA BINDING; RNA STRUCTURE; STATIC ELECTRICITY;

ARGININE; BACTERIAL PROTEINS; BASE PAIRING; BASE SEQUENCE; CATALYTIC DOMAIN; CONSERVED SEQUENCE; ESCHERICHIA COLI PROTEINS; HOST FACTOR 1 PROTEIN; LYSINE; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RNA FOLDING; RNA, BACTERIAL; RNA, MESSENGER; RNA, SMALL UNTRANSLATED; SIGMA FACTOR;

EID: 84883478358     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt521     Document Type: Article

References (68)

1. Vogel,J. and Luisi,B.F. (2011) Hfq and its constellation of RNA. Nat. Rev. Microbiol., 9, 578-589
2. 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 Harb. Symp. Quant. Biol., 71, 1-11
3. Beisel,C.L. and Storz,G. (2010) Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol. Rev., 34, 866-882
4. Kaberdin,V.R. and Blasi,U. (2006) Translation initiation and the fate of bacterial mRNAs. FEMS Microbiol. Rev., 30, 967-979
5. Caron,M.P., Lafontaine,D.A. and Masse,E. (2010) Small RNA-mediated regulation at the level of transcript stability. RNA Biol., 7, 140-144
6. Aiba,H. (2007) Mechanism of RNA silencing by Hfq-binding small RNAs. Curr. Opin. Microbiol., 10, 134-139
7. 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
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. USA, 107, 9602-9607
9. 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
10. 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
11. Rajkowitsch,L. and Schroeder,R. (2007) Dissecting RNA chaperone activity. RNA, 13, 2053-2060
12. 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., 37, 6205-6213
13. 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
14. 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
15. 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
16. 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
17. Sauer,E. and Weichenrieder,O. (2011) Structural basis for RNA 30-end recognition by Hfq. Proc. Natl Acad. Sci. USA, 108, 13065-13070
18. Link,T.M., Valentin-Hansen,P. and Brennan,R.G. (2009) Structure of Escherichia coli Hfq bound to polyriboadenylate RNA. Proc. Natl Acad. Sci. USA, 106, 19292-19297
19. Soper,T.J. and Woodson,S.A. (2008) The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA, 14, 1907-1917
20. Beich-Frandsen,M., Vecerek,B., Konarev,P.V., Sjoblom,B., Kloiber,K., Hammerle,H., Rajkowitsch,L., Miles,A.J., Kontaxis,G., Wallace,B.A. et al. (2011) Structural insights into the dynamics and function of the C-terminus of the E coli RNA chaperone Hfq. Nucleic Acids Res., 39, 4900-4915
21. Updegrove,T.B. and Wartell,R.M. (2011) The influence of Escherichia coli Hfq mutations on RNA binding and sRNA mRNA duplex formation in rpoS riboregulation. Biochim. Biophys. Acta, 1809, 532-540
22. Olejniczak,M. (2011) Despite similar binding to the Hfq protein regulatory RNAs widely differ in their competition performance. Biochemistry, 50, 4427-4440
23. 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
24. 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., 39, 5193-5202
25. Adamson,D.N. and Lim,H.N. (2011) Essential requirements for robust signaling in Hfq dependent small RNA networks. PLoS Comput. Biol., 7, e1002138
26. 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
27. Majdalani,N., Chen,S., Murrow,J., St John,K. and Gottesman,S. (2001) Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol. Microbiol., 39, 1382-1394
28. 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
29. 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 50 rpoS mRNA leader region. Biochemistry, 47, 11184-11195
30. Panja,S. and Woodson,S.A. (2012) Hfq proximity and orientation controls RNA annealing. Nucleic Acids Res., 40, 8690-8697
31. Sauer,E., Schmidt,S. and Weichenrieder,O. (2012) Small RNA binding to the lateral surface of Hfq hexamers and structural rearrangements upon mRNA target recognition. Proc. Natl Acad. Sci. USA, 109, 9396-9401
32. Lee,T. and Feig,A.L. (2008) The RNA binding protein Hfq interacts specifically with tRNAs. RNA, 14, 514-523
33. Updegrove,T.B., Correia,J.J., Galletto,R., Bujalowski,W. and Wartell,R.M. (2010) E coli DNA associated with isolated Hfq interacts with Hfq's distal surface and C-terminal domain. Biochim. Biophys. Acta, 1799, 588-596
34. Zhang,A., Schu,D.J., Tjaden,B.C., Storz,G. and Gottesman,S. (2013) Mutations in interaction surfaces differentially impact E coli Hfq association with small RNAs and their mRNA targets. J. Mol. Biol., in press. doi: 10.1016/j.jmb.2013.01.006
35. Sievers,F., Wilm,A., Dineen,D., Gibson,T.J., Karplus,K., Li,W., Lopez,R., McWilliam,H., Remmert,M., Soding,J. et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol., 7, 539
36. Mandin,P. and Gottesman,S. (2010) Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J., 29, 3094-3107
37. 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
38. Panja,S. and Woodson,S.A. (2012) Hexamer to monomer equilibrium of E coli Hfq in solution and its impact on RNA annealing. J. Mol. Biol., 417, 406-412
39. Wang,W., Wang,L., Zou,Y., Zhang,J., Gong,Q., Wu,J. and Shi,Y. (2011) Cooperation of Escherichia coli Hfq hexamers in DsrA binding. Genes Dev., 25, 2106-2117
40. Soper,T.J., Doxzen,K. and Woodson,S.A. (2011) Major role for mRNA binding and restructuring in sRNA recruitment by Hfq. RNA, 17, 1544-1550
41. 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
42. 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
43. de Haseth,P.L. and Uhlenbeck,O.C. (1980) Interaction of Escherichia coli host factor protein with oligoriboadenylates. Biochemistry, 19, 6138-6146
44. Vincent,H.A., Henderson,C.A., Stone,C.M., Cary,P.D., Gowers,D.M., Sobott,F., Taylor,J.E. and Callaghan,A.J. (2012) The low-resolution solution structure of Vibrio cholerae Hfq in complex with Qrr1 sRNA. Nucleic Acids Res., 40, 8698-8710
45. Ribeiro Ede,A. Jr, Beich-Frandsen,M., Konarev,P.V., Shang,W., Vecerek,B., Kontaxis,G., Hammerle,H., Peterlik,H., Svergun,D.I., Blasi,U. et al. (2012) Structural flexibility of RNA as molecular basis for Hfq chaperone function. Nucleic Acids Res., 40, 8072-8084
46. Craig,M.E., Crothers,D.M. and Doty,P. (1971) Relaxation kinetics of dimer formation by self complementary oligonucleotides. J. Mol. Biol., 62, 383-401
47. Porschke,D. and Eigen,M. (1971) Co-operative non-enzymic base recognition
48. 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
49. Porschke,D. (1974) A direct measurement of the unzippering rate of a nucleic acid double helix. Biophys. Chem., 2, 97-101
50. Turner,D.H. (2000) In: Bloomfield,V.A., Tinoco,I.J. and Crothers,D.M. (eds), Nucleic Acids: Structures, Properties, Functions. University Science Books, Sausalito, pp
51. 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
52. Levin,J.G., Guo,J., Rouzina,I. and Musier-Forsyth,K. (2005) Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Prog. Nucleic Acid Res. Mol. Biol., 80, 217-286
53. Doetsch,M., Gstrein,T., Schroeder,R. and Furtig,B. (2010) Mechanisms of StpA-mediated RNA remodeling. RNA Biol., 7, 735-743
54. Doublie,S., Tabor,S., Long,A.M., Richardson,C.C. and Ellenberger,T. (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 A resolution [see comments]. Nature, 391, 251-258
55. Storz,G., Opdyke,J.A. and Zhang,A. (2004) Controlling mRNA stability and translation with small, noncoding RNAs. Curr. Opin. Microbiol., 7, 140-144
56. Desnoyers,G. and Masse,E. (2012) Noncanonical repression of translation initiation through small RNA recruitment of the RNA chaperone Hfq. Genes Dev., 26, 726-739
57. 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
58. Sittka,A., Lucchini,S., Papenfort,K., Sharma,C.M., Rolle,K., Binnewies,T.T., Hinton,J.C. and Vogel,J. (2008) Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet., 4, e1000163
59. Vecerek,B., Rajkowitsch,L., Sonnleitner,E., Schroeder,R. and Blasi,U. (2008) The C-terminal domain of Escherichia coli Hfq is required for regulation. Nucleic Acids Res., 36, 133-143
60. Olsen,A.S., Moller-Jensen,J., Brennan,R.G. and Valentin-Hansen,P. (2010) C-terminally truncated derivatives of Escherichia coli Hfq are proficient in riboregulation. J. Mol. Biol., 404, 173-182
61. Nielsen,J.S., Lei,L.K., Ebersbach,T., Olsen,A.S., Klitgaard,J.K., Valentin-Hansen,P. and Kallipolitis,B.H. (2010) Defining a role for Hfq in Gram-positive bacteria: evidence for Hfq-dependent antisense regulation in Listeria monocytogenes. Nucleic Acids Res., 38, 907-919
62. Heidrich,N., Moll,I. and 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
63. Gaballa,A., Antelmann,H., Aguilar,C., Khakh,S.K., Song,K.B., Smaldone,G.T. and Helmann,J.D. (2008) The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins. Proc. Natl Acad. Sci. USA, 105, 11927-11932
64. Felden,B., Vandenesch,F., Bouloc,P. and Romby,P. (2011) The Staphylococcus aureus RNome and its commitment to virulence. PLoS Pathog., 7, e1002006
65. Bohn,C., Rigoulay,C. and Bouloc,P. (2007) No detectable effect of RNA-binding protein Hfq absence in Staphylococcus aureus. BMC Microbiol., 7, 10
66. Rochat,T., Bouloc,P., Yang,Q., Bossi,L. and Figueroa-Bossi,N. (2012) Lack of interchangeability of Hfq-like proteins. Biochimie, 94, 1554-1559
67. Wilusz,C.J. and Wilusz,J. (2013) Lsm proteins and Hfq: Life at the 30 end. RNA Biol., 10, 592-601
68. Bandyra,K.J., Said,N., Pfeiffer,V., Gorna,M.W., Vogel,J. and Luisi,B.F. (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.