The poly(A) binding protein Hfq protects RNA from RNase E and exoribonucleolytic degradation

Nucleic Acids Research

Volumn 31, Issue 24, 2003, Pages 7302-7310

  Folichon, Marc ^b   Arluison, Véronique ^b   Pellegrini, Olivier ^b   Huntzinger, Eric ^a   Régnier, Philippe ^b   Hajnsdorf, Eliane ^b  

^a INST DE BIOL MOLEC ET CELLULAIRE   (France)

^b INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; ESCHERICHIA COLI PROTEIN; ESTERASE; EXORIBONUCLEASE; HFQ PROTEIN; MESSENGER RNA; POLYADENYLIC ACID BINDING PROTEIN; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RIBONUCLEASE; RIBONUCLEASE E; RIBONUCLEASE II; RIBOSOME PROTEIN; RNA; UNCLASSIFIED DRUG; URACIL;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; IN VITRO STUDY; IN VIVO STUDY; MODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RNA DEGRADATION; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS;

BASE SEQUENCE; BINDING SITES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENDORIBONUCLEASES; ESCHERICHIA COLI PROTEINS; EXORIBONUCLEASES; HOST FACTOR 1 PROTEIN; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; POLY A; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RIBOSOMAL PROTEINS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

ESCHERICHIA; ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0347519274     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkg915     Document Type: Article

References (51)

1. Braun,F., Hajnsdorf,E. and Régnier,P. (1996) Polynucleotide phosphorylase is required for the rapid degradation of the RNase E-processed rpsO mRNA of Escherichia coli devoid of its 3′ hairpin. Mol. Microbiol., 19, 997-1005.
2. Hajnsdorf,E., Steier,O., Coscoy,L., Teysset,L. and Régnier,P. (1994) Roles of RNase E, RNase II and PNPase in the degradation of the rpsO transcripts of Escherichia coli: stabilizing function of RNase II and evidence for efficient degradation in an ams-rnb-pnp mutant. EMBO J., 13, 3368-3377.
3. Hajnsdorf,E. and Régnier,P. (1999) E. coli rpsO mRNA decay: RNase E processing at the beginning of the coding sequence stimulates poly(A)-dependent degradation of the mRNA. J. Mol. Biol., 286, 1033-1043.
4. Haugel-Nielsen,J., Hajnsdorf,E. and Regnier,P. (1996) The rpsO mRNA of Escherichia coli is polyadenylated at multiple sites resulting from endonucleolytic processing and exonucleolytic degradation. EMBO J., 15, 3144-3152.
5. Coburn,G.A. and Mackie,G.A. (1999) Degradation of mRNA in Escherichia coli: an old problem with some new twists. Prog. Nucleic Acid Res. Mol. Biol., 62, 55-108.
6. Jerome,L.J., van Biesen,T. and Frost,L.S. (1999) Degradation of FinP antisense RNA from F-like plasmids: the RNA-binding protein, FinO, protects FinP from ribonuclease E. J. Mol. Biol., 285, 1457-1473.
7. Iost,I. and Dreyfus,M. (1994) mRNAs can be stabilized by DEAD-box proteins. Nature, 372, 193-196.
8. Braun,F., Le Derout,J. and Régnier,P. (1998) Ribosomes inhibit an RNase E cleavage which induces the decay of the rpsO mRNA of Escherichia coli. EMBO J., 17, 4790-4797.
9. Bechhofer,D.H. and Zen,K.H. (1989) Mechanism of erythromycin-induced ermC mRNA stability in Bacillus subtilis. J. Bacteriol., 171, 5803-5811.
10. Bouvet,P. and Belasco,J. (1992) RNA degradation in E. coli by endonuclease RNase E: control by 5′-terminal base pairing. Nature, 360, 488-491.
11. Joyce,S.A. and Dreyfus,M. (1998) In the absence of translation, RNase E can bypass 5′ mRNA stabilizers in Escherichia coli. J. Mol. Biol., 282, 241-254.
12. Vytvytska,O., Moll,I., Kaberdin,V.R., van Gabain,A. and Bläsi,U. (2000) HFq (HFI) stimulates ompA mRNA decay by interfering with ribosomes binding. Genes Dev., 14, 1109-1118.
13. Tsui,H.-C.,T., Leung,H.-C.,E. 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.
14. S subunit of RNA polymerase in Escherichia coli. J. Bacteriol., 179, 297-300.
15. Wachi,M., Takada,A. and Nagai,K. (1999) Overproduction of the outer-membrane proteins FepA and FhuE responsible for iron transport in Escherichia coli hfq::cat mutant. Biochem. Biophys. Res. Commun., 264, 525-529.
16. 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.
17. 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.
18. Muffler,A., Fischer,D. and Hengge-Aronis,R. (1996) The RNA-binding protein HF-I, known as a host factor for phage Qβ RNA replication, is essential for rpoS translation in Escherichia coli. Genes Dev., 10, 1143-1151.
19. Brown,L. and Elliott,T. (1996) 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., 178, 3763-3770.
20. Vytvytska,O., Jakobsen,J.S., Balcunate,G., Andersen,J.S., Baccarini,M. and von Gabain,A. (1998) Host-factor I, Hfq, binds to Escherichia coli ompA mRNA in a growth rate-dependent fashion and regulates its stability. Proc. Natl Acad. Sci. USA, 95, 14118-14123.
21. Takada,A., Wachi,M. and Nagai,K. (1999) Negative regulatory role of the Escherichia coli hfq gene in cell division. Biochem. Biophys. Res. Commun., 266, 579-583.
22. Sledjeski,D.D., Whitman,C. and Zhang,A. (2001) HFq is necessary for regulation by the untranslated RNA DsrA. J. Bacteriol., 183, 1997-2005.
23. Tsui,H.-C.T., 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.
24. Hajnsdorf,E. and Régnier,P. (2000) Host factor HFq of Escherichia coli stimulates elongation of poly(A) tails by poly(A)polymerase I. Proc. Natl Acad. Sci. USA, 97, 1501-1505.
25. Le Derout,J., Folichon,M., Briani,F., Dehò,G., Régnier,P. and Hajnsdorf,E. (2003) Hfq affects the length and the frequency of short oligo(A) tails at the 3′ end of Escherichia coli rpsO mRNAs. Nucleic Acids Res., 31, 4017-4023.
26. Senear,A.W. and Steitz,J.A. (1976) Site-specific interaction of Qβ host factor and ribosomal protein S1 with Qβ and R17 bacteriophage RNAs. J. Biol. Chem., 251, 1902-1912.
27. 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-1) protein. EMBO J., 17, 6061-6068.
28. Moller,T., Franch,T., Hojrup,P., Keene,D., 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.
29. Schuppli,D., Miranda,G., Tsui,H.-C.T., Winckler,M.E., Sogo,J.M. and Weber,H. (1997) Altered 3′-terminal RNA structure in phage Qβ adapted to host factor-less Escherichia coli. Proc. Natl Acad. Sci. USA, 94, 10239-10242.
30. Miranda,G., Schuppli,D., Barrera,I., Hausherr,C., Sogo,J.M. and Weber,H. (1997) Recognition of bacteriophage Qβ plus strand RNA as a template by Qβ replicase: role of RNA interactions mediated by ribosomal proteins S1 and host factors. J. Mol. Biol., 267, 1089-1103.
31. 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.
32. Hajnsdorf,E., Braun,F., Haugel-Nielsen,J. and Regnier,P. (1995) Polyadenylylation destabilizes the rpsO mRNA of Escherichia coli. Proc. Natl Acad. Sci. USA, 92, 3973-3977.
33. Régnier,P. and Hajnsdorf E. (1991) Decay of mRNA encoding ribosomal protein S15 of Escherichia coli is initiated by an RNase E-dependent endonucleolytic cleavage that removes the 3′ stabilizing stem and loop structure. J. Mol. Biol., 217, 283-292.
34. Coburn,G.A. and Mackie,G.A. (1996) Overexpression, purification and properties of Escherichia coli ribonuclease II. J. Biol. Chem., 271, 1048-1053.
35. Carpousis,A.J., van Houwe,G., Ehretsmann,C. and Krisch,H.M. (1994) Co-purification of E. coli RNase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation. Cell, 76, 889-900.
36. Donis-Keller,H., Maxam,A.M. and Gilbert,W. (1977) Mapping adenines, guanines and pyrimidines in RNA. Nucleic Acids Res., 4, 2527-2538.
37. O'Hara,E.B., Chekanova,J.A., Ingle,C.A., Kushner,Z.R., Peters,E. and Kushner,S.R. (1995) Polyadenylation helps regulate mRNA decay in Escherichia coli. Proc. Natl Acad. Sci. USA, 92, 1807-1811.
38. Mohanty,B.K. and Kushner,S.R. (2000) Polynucleotide phosphorylase, RNase II and RNase E play different roles in the in vivo modulation of polyadenylation in Escherichia coli. Mol. Microbiol., 6, 982-994.
39. Arluison,V., Derreumaux,P., Allemand,F., Folichon,M., Hajnsdorf,E. and Regnier,P. (2002) Structural modelling of the Sm-like protein Hfq from Escherichia coli. J. Mol. Biol., 320, 705-712.
40. Coburn,G.A. and Mackie,G.A. (1996) Differential sensitivities of portions of the mRNA for ribosomal protein S20 to 3′ exonucleases dependent on oligoadenylation and RNA secondary structure. J. Biol. Chem., 271, 15776-15781.
41. Azam,T.A., Iwata,A., Nishimura,A., Ueda,S. and Ishihama,A. (1999) Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol., 181, 6361-6370.
42. Marujo,P.E., Hajnsdorf,E., Le Derout,J., Andrade,R., Arraiano,C.M. and Régnier,P. (2000) RNase II removes the oligo(A) tails that destabilize the rpsO mRNA of Escherichia coli. RNA, 6, 1185-1193.
43. de Haseth,P.L. and Uhlenbeck,O.C. (1980) Interaction of Escherichia coli host factor protein with oligoriboadenylates. Biochemistry, 19, 6138-6146.
44. Schumacher,M.A., Rearson,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.
45. 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.
46. Thore,S., Mayer,C., Sauter,C., Weeks,S. and Suck,D. (2003) Crystal structures of the Pyrococcus abyssi Sm core and its complex with RNA: common features of RNA-binding in Archae and Eukarya. J. Biol. Chem., 278, 1239-1247.
47. Carmichael,G.G., Weber,K., Niveleau,A. and Wahba,A.J. (1975) The host factor required for RNA phage Qβ RNA replication in vitro. Intracellular location, quantitation and purification by polyadenylate-cellulose chromatography. J. Biol. Chem., 250, 3607-3612.
48. Azam,T.A. and Ishihama,A. (1999) Twelve species of the nucleoid-associated protein from Escherichia coli. J. Biol. Chem., 274, 33105-33113.
49. Moll,I., Leitsch,D., Steinhauser,T. and Bläsi,U. (2003) RNA chaperone activity of the Sm-like Hfq protein. EMBO Rep., 4, 284-289.
50. 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.
51. Mohanty,B.K. and Kushner,S.R. (1999) Analysis of the function of Escherichia coli poly(A) polymerase I in RNA metabolism. Mol. Microbiol., 34, 1094-1108.