The C-terminal domain of Escherichia coli Hfq is required for regulation

Nucleic Acids Research

Volumn 36, Issue 1, 2008, Pages 133-143

  Večerek, Branislav ^a   Rajkowitsch, Lukas ^a   Sonnleitner, Elisabeth ^a   Schroeder, Renée ^a   Bläsi, Udo ^a  

^a UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; BETA GALACTOSIDASE; MESSENGER RNA; RNA BINDING PROTEIN; UNTRANSLATED RNA;

ARTICLE; BACTERIAL GENETICS; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIABILITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; GEL MOBILITY SHIFT ASSAY; GENE TARGETING; GENETIC CONSERVATION; GENETIC REGULATION; GENETIC VARIABILITY; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEOBACTERIA; RNA BINDING; RNA STRUCTURE;

BACTERIAL PROTEINS; BINDING SITES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HOST FACTOR 1 PROTEIN; PROTEIN STRUCTURE, TERTIARY; RNA, MESSENGER; RNA, UNTRANSLATED; SEQUENCE DELETION; SIGMA FACTOR; SUCCINIC ACID; SUPEROXIDE DISMUTASE;

BETAPROTEOBACTERIA; ESCHERICHIA COLI;

EID: 38349138513     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm985     Document Type: Article

References (77)

1. Franze de Fernandez,M.T., Eoyang,L. and August,J.T. (1968) Factor fraction required for the synthesis of bacteriophage Qbeta-RNA. Nature, 219, 588-590.
2. Tsui,H.C., Leung,H.C. and Winkler,M.E. (1994) Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol. Microbiol., 13, 35-49.
3. 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.
4. Muffler,A., Fischer,D. and Hengge-Aronis,R. (1996) The RNA-binding protein HF-I, known as a host factor for phage Qbeta RNA replication, is essential for rpoS translation in Escherichia coli. Genes Dev. 10, 1143-1151.
5. Massé,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.
6. Vecerek,B., Moll,I., Afonyushkin,T., Kaberdin,V. and Bläsi,U. (2003) Interaction of the RNA chiperone Hfq with mRNAs: Direct and indirect roles of Hfq in iron metabolism of Escherichia coli. Mol. Microbiol. 50, 897-909.
7. Tsui,H.C., Feng,G. and Winkler,M.E. (1997) Negative regulation of mutS and mutH repair gene expression by the Hfq and RpoS global regulators of Escherichia coli K-12. J. Bacteriol., 179 7476-7487.
8. Vytvytska,O., Moll,I., Kaberdin,V.R., von Gabain,A. and Bläsi,U. (2000) Hfq (HFI) stimulates ompA mRNA decay by interfering with ribosome binding. Genes Dev., 14, 1109-1118.
9. 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.
10. Sledjeski,D.D., Whitman,C. and Zhang,A. (2001) Hfq is necessary for regulation by the untranslated RNA DsrA. J. Bacteriol., 183, 1997-2005.
11. Massé,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.
12. Moll,I., Afonyushkin,T., Vytvytska,O., Kaberdin,V.R. and Bläsi,U. (2003) Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs. RNA, 9, 1308-1314.
13. Afonyushkin,T., Vecerek,B., Moll,I., Bläsi,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.
14. 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.
15. Vecerek,B., Moll,I. and Bläsi,U. (2007) Control of Fur synthesis by the non-coding RNA RyhB and iron-responsive decoding. EMBO J., 26, 965-975.
16. Møller,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.
17. Kawamoto,H., Koide,Y., Morita,T. and Aiba,H. (2006) Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol. Microbiol., 61, 1013-1022.
18. Robertson,G.T. and Roop,R.M.Jr (1999) The Brucella abortus host factor I (HF-I) protein contributes to stress resistance during stationary phase and is a major determinant of virulence in mice. Mol. Microbiol., 34, 690-700.
19. Sonnleitner,E., Hagens,S., Rosenau,F., Wilhelm,S., Habel,A., Jäger,K.E. and Bläsi,U. (2003) Reduced virulence of a hfq mutant of Pseudomonas aeruginosa O1. Microb. Pathog., 35 217-228.
20. Christiansen,J.K., Larsen,M.H., Ingmer,H., Søgaard-Andersen,L. and Kallipolitis,B.H. (2004) The RNA-binding protein Hfq of Listeria monocytogenes: Role in stress tolerance and virulence. J. Bacteriol., 186, 3355-3362.
21. Ding,Y., Davis,B.M. and Waldor,M.K. (2004) Hfq is essential for Vibrio cholerae virulence and downregulates sigma expression. Mol. Microbiol., 53, 345-354.
22. Brennan,R.G. and Link,T.M. (2007) Hfq structure, function and ligand binding. Curr. Opin. Microbiol., 10, 125-133.
23. 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.
24. 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.
25. Wassarman,K.M., Repoila,F., Rosenow,C., Storz,G. and Gottesman,S. (2001) Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev., 15, 1637-1651.
26. Vogel,J. and Sharma,C.M. (2005) How to find small non-coding RNAs in bacteria. Biol. Chem., 386, 1219-1238.
27. 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.
28. Majdalani,N., Vanderpool,C.K. and Gottesman,S. (2005) Bacterial small RNA regulators. Crit. Rev. Biochem. Mol. Biol., 40, 93-113.
29. 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.
30. 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.
31. Moll,I., Leitsch,D., Steinhauser,T. and Bläsi,U. (2003) RNA chaperone activity of the Sm-like Hfq protein. EMBO Rep., 4, 284-289
32. 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.
33. Schumacher,M.A., Pearson,R.F., Møller,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.
34. Sauter,C., Basquin,J. and Suck,D. (2003) Sm-like proteins in Eubacteria: the crystal structure of the Hfq protein from Escherichia coli. Nucleic Acids Res., 31, 4091-4098.
35. Nikulin,A., Stolboushkina,E., Perederina,A., Vassilieva,I., Blaesi,U., Moll,I., Kachalova,G., Yokoyama,S., Vassylyev,D. et al. (2005) Structure of Pseudomonas aeruginosa Hfq protein. Acta Crystallogr. D Biol. Crystallogr., 61, 141-146.
36. Achsel,T., Stark,H. and Lührmann,R. (2001) The Sm domain is an ancient RNA-binding motif with oligo(U) specificity. Proc. Natl Acad. Sci. USA, 98, 3685-3689.
37. Večerek,B., Moll,I. and Bläsi,U. (2005) Translational autocontrol of the Escherichia coli hfq RNA chapserone gene. RNA, 11 976-984.
38. 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, 4206-1214.
39. 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.
40. 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.
41. Sonnleitner,E., Moll,I. and Bläsi,U. (2002) Functional replacement of the Escherichia coli hfq gene by the homologue of Pseudomonas aeruginosa. Microbiology, 148, 883-891.
42. Arluison,V., Folichon,M., Marco,S., Derreumaux,P., Pellegrini,O., Seguin,J., Hajnsdorf,E. and Regnier,P. (2004) The C-terminal domain of Escherichia coli Hfq increases the stability of the hexamer. Eur. J. Biochem., 271, 1258-1265.
43. Sonnleitner,E., Napetschnig,J., Afonyushkin,T., Ecker,K, Večerek,B., Moll.J., Kaberdin,V.R. and Bläsi,U. (2004) Functional effects of variants of the RNA chaperone Hfq. Biochem. Biophys. Res. Commun., 323, 1017-4023.
44. Steiner,M., Lubitz,W. and Bläsi,U. (1993) The missing link in phage lysis of gram-positive bacteria: Gene 14 of Bacillus subtilis phage phi 29 encodes the functional homolog of lambda S protein. J. Bacteriol., 175, 1038-1042.
45. Miller,J.H. (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Haror, NY.
46. Brückner,R. (1992) A series of shuttle vectors for Bacillus subtilis and Escherichia coli. Gene, 122, 187-192.
47. Takayanagi,Y., Tanaka,K. and Takahashi,H. (1994) Structure of the 5′ upstream region and the regulation of the rpoS gene of Escherichia coli. Mol. Gen. Genet., 243, 525-531.
48. Lin-Chao,S. and Bremer,H. (1986) Effect of the bacterial growth rate on replication control of plasmid pBR322 in Escherichia coli. Mol. Gen. Genet., 203, 143-149.
49. Sonnleitner,E., Schuster,M., Sorger-Domenigg,T., G~eenberg,E.P. and Bläsi,U. (2006) Hfq-dependent alterations of the transcriptome profile and effects on quorum sensing in Pseudomonas aerugmosa. Mol. Microbiol., 59, 1542-1558.
50. Mayer,O., Rajkowitsch,L., Lorenz,C., Konrat,R. and Schroeder,R. (2007) RNA chaperone activity and RNA-binding properties of the E. coli protein StpA. Nucleic Acids Res., 35, 1257-1269.
51. Gottesman,S., McCullen,C.A., Guillier,M., Vanderpool,C.K., Majdalani,N., Benhammou,J., Thompson,K.M., FitzGerald,P.C., Sowa,N.A. et al. (2006) Small RNA regulators and the bacterial response to stress. Cold Spring Harb. Symp. Quant Biol., 71, 1-11.
52. Morita,T., Mochizuki,Y.,and Aiba,H. (2006) Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruotion. Proc. Natl Acad. Sci. USA, 103, 4858-4863.
53. 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.
54. 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.
55. 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.
56. Zuker,M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
57. 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.
58. Tolstorukov,M.Y., Virnik,K.M., Adhya,S. and Zhurkin,V.B. (2005) A-tract clusters may facilitate DNA packaging it b~cterial nucleoid. Nucleic Acids Res., 33, 3907-3918.
59. Azam,T.A., Hiraga,S. and Ishihama,A. (2000) Two types of localization of the DNA-binding proteins within the Escherichia coli nucleoid. Genes Cells, 5, 613-626.
60. Zambrano,M.M., Siegele,D.A., Almiron.M., Tormo,A. and Kolter,R. (1993) Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science, 259, 1757-1760.
61. Tompa,P. and Csermely,P. (2004) The role of structural disorder in the function of RNA and protein chaperones. FASEB J., 18, 1169-1175.
62. Sukhodolets,M.V. and Garges.S. (2003) Interaction of Escherichia, coli RNA polymerase with the ribosomal protein S1 and the Sm-like ATPase Hfq. Biochemistry, 42, 8022-8034.
63. Morita,T., Maki,K. and Aiba,H. (2005) RNase E-based ribonucleoprotein complexes: Mechanical basis of mRNA destabilization mediated by bacterial noneoding RNAs. Genes Dev., 19, 2176-2186.
64. Mohanty,B.K., Maples,V.F. and Kushner,S.R. (2004) The Sm-like protein Hfq regulates polyadenylation dependent mRNA decay in Escherichia coli. Mol. Microbiol., 54, 905-920.
65. Bossi,L. and Figueroa-Bossi,N. (2007) A small RNA downregulates LamB maltoporin in Salmonella. Mol. Microbiol., 65, 799-810.
66. 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.
67. Lenz,D.H., Mok,K.C., Lilley,B.N., Kulkarni,R.V., Wingreen,N.S. and Bassler,B.L. (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell, 118, 69-82.
68. Heidrich,N., Chinali,A., Gerth,U. and Brantl,S. (2006) The small untranslated RNA SR 1 from the Bacillus subtilis genome is involved in the regulation of arginine catabolism. Mol. Microbiol. 62, 520-536.
69. 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.
70. Huntzinger,E., Boisset,S., Saveanu,C., Benito,Y., Geissmann,T., Namane,A., Lina,G., Etienne,J., Ehresmann,B. et al. (2005) Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J., 24, 824-835.
71. Boisset,S., Geissmann,T., Huntzinger,E., Fechter,P., Bendridi,N., Possedko,M., Chevalier,C., Helfer,A.C., Benito,Y. et al. (2007) Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev., 21, 1353-1366.
72. Sittka,A., Pfeiffer,V., Tedin,K. and Vogel,J. (2007) The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol. Microbiol., 63, 193-217.
73. Bohn,C., Rigoulay,C. and Bouloc,P. (2007) No detectable effect of RNA-binding protein Hfq absence in Staphylococcus aureus. BMC Microbiol., 7, 10.
74. Christiansen,J.K., Nielsen,J.S., Ebersbach,T., Valentin-Hansen,P., Søgaard-Anderseri,L. and Kallipolitis,B.H. (2006) Identification of small Hfq-binding RNAs in Listeria monocytogenes. RNA, 12, 1383-1396.
75. Romero,P., Obradovic,Z. and Dunker,A.K. (1997) Sequence data analysis for long disordered regions prediction in the calcineurin family. Genome Inform., 8, 110-124.
76. Li,X., Romero,P.,. Rani,M., Dunker,A.K. and Obradovic,Z. (1999) Predicting protein disorder for N-, C-, and internal regione. Genome Inform., 10, 30-40.
77. Romero,P., Obradovic,Z., Li,X., Garner,J., Brown,C. and Dunker,A.K. (2001) Proteins: Sequence complexity of disordered protein. Struct. Funct. Gen., 42, 38-48.