Ribosomes inhibit an RNase E cleavage which induces the decay of the rpsO mRNA of Escherichia coli

EMBO Journal

Volumn 17, Issue 16, 1998, Pages 4790-4797

  Braun, Frédérique ^b   Le Derout, Jacques ^a   Régnier, Philippe ^a  

^a INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

Author keywords

mRNA stability; Ribosomes; RNase E; Translation

Indexed keywords

MESSENGER RNA; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RIBONUCLEASE; RIBOSOME PROTEIN;

ARTICLE; AUTOREGULATION; CONTROLLED STUDY; ESCHERICHIA COLI; GENE MUTATION; NONHUMAN; OPERATOR GENE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; RIBOSOME; RNA DEGRADATION; RNA PROCESSING; RNA TRANSLATION; STOP CODON;

BASE SEQUENCE; CODON; ENDORIBONUCLEASES; ESCHERICHIA COLI; GENES, BACTERIAL; HYDROLYSIS; MUTAGENESIS, SITE-DIRECTED; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; RIBOSOMAL PROTEINS; RNA, MESSENGER;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0032541436     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.16.4790     Document Type: Article

References (51)

1. Arraiano,M.C., Yancey,S.D. and Kushner,S.R. (1988) Stabilization of discrete mRNA breakdown products in ams pnp rnb multiple mutant of Escherichia coli K 12. J. Bacteriol., 170, 4625-4633.
2. Baumeister,R., Flache,P., Melefors,Ö, von Gabain,A. and Hillen,W. (1991) Lack of a 5′ non-coding region in Tn1724 encoded tetR mRNA is associated with a low efficiency of translation and a short half-life in Escherichia coli. Nucleic Acids Res., 17, 4595-4600.
3. Bechhofer,D. (1993) 5′ mRNA stabilizers. In Belasco,J.G. and Brawerman,G. (eds), Control of Messenger RNA Stability. Academic Press Inc., New York, pp. 31-52.
4. Bouvet,P. and Belasco,J.G. (1992) Control of RNase E-mediated RNA degradation by 5′ terminal base pairing in E.coli. Nature, 360, 488-491.
5. 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.
6. Carpousis,A.G., 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.
7. Cohen,S.N. and McDowall,K.J. (1997) RNase E: still a wonderfully mysterious enzyme. Mol. Microbiol., 23, 1099-1106.
8. Cole,J.R. and Nomura,M. (1986) Changes in the half-life of ribosomal protein messenger RNA caused by translational repression. J. Mol. Biol., 188, 383-392.
9. Dotto,G.P., Enea,V. and Zinder,N.D. (1981) Functional analysis of bacteriophage F1 intergenic region. Virology, 114, 463-473.
10. Emory,S.A., Bouvet,P. and Belasco,J.G. (1992) A 5′-terminal stem-loop structure can stabilize mRNA in Escherichia coli. Genes Dev., 6, 135-148.
11. 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 transcript of Escherichia coli: stabilizing function and evidence for efficient degradation in an ams-pnp-rnb mutant. EMBO J., 13, 3368-3377.
12. Hajnsdorf,E., Braun,F., Haugel-Nielsen,J. and Régnier,P. (1995) Polyadenylylation destabilizes the rpsO mRNA of Escherichia coli. Proc. Natl Acad. Sci. USA, 92, 3973-3977.
13. Hajnsdorf,E., Braun,F., Haugel-Nielsen,J., Le Derout,J. and Régnier,P. (1996) Multiple degradation pathways of the rpsO mRNA of Escherichia coli. RNase E interacts with the 5′ and 3′ extremities of the primary transcript. Biochimie, 78, 416-424.
14. Hartz,D., McPheeters,D.S., Green,L. and Gold,L. (1991) Detection of Escherichia coli ribosome binding at translation initiation sites in the absence of tRNA. J. Mol. Biol., 218, 99-105.
15. Haugel-Nielsen,J., Hajnsdorf,E. and Régnier,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.
16. Higgins,C.F., Causton,H.C., Dance,G.S.C. and Mudd,E.A. (1993) The role of 3′ end in mRNA stability and decay. In Belasco,J.G. and Brawerman,G. (eds), Control of Messenger RNA Stability. Academic Press Inc., New York, pp. 13-30.
17. Huang,H., Liao,J. and Cohen,S.N. (1998) Poly(A) and poly(U) specific RNA 3′ tail shortening by E.coli ribonuclease E. Nature, 391, 99-102.
18. Iost,I. and Dreyfus,M. (1995) The stability of Escherichia coli lacZ mRNA depends upon the simultaneity of its synthesis and translation. EMBO J., 14, 3252-3261.
19. Jain,C. and Kleckner,N. (1993) IS10 mRNA stability and steady states levels in Escherichia coli: indirect effects of translation and role of rne function. Mol. Microbiol., 9, 233-247.
20. Keiler,K.C., Waller,P.R.H. and Sauer,R.T. (1996) Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science, 271, 990-993.
21. Kunkel,T.A., Roberts,J.D. and Zakour,R.A. (1987) Rapid and efficient site-specific mutagenesis without phenotipic selection. In Wu,R. and Grossman,L. (eds), Recombinani DNA. Academic Press Inc., San Diego, CA, pp. 367-382.
22. Lerner,C.G. and Inouye,M. (1990) Low copy number plasmids for regulated low-level expression of cloned genes in Escherichia coli with blue/white insert screening capability. Nucleic Acids Res., 18, 4631.
23. Mackie,G.A. (1987) Posttranscriptional regulation of ribosomal protein S20 and stability of the S20 mRNA species. J. Bacteriol., 169, 2697-2701.
24. Mackie,G.A. and Genereaux,J.L. (1993) The role of RNA structure in determining RNase E-dependent cleavage sites in the mRNA for ribosomal protein S20 in vitro. J. Mol. Biol., 234, 998-1012.
25. Mackie,G.A., Genereaux,J.L. and Masterman,S.K. (1997) Modulation of the activity of RNase E in vitro by RNA sequences and secondary structures 5′ to cleavage sites. J. Biol. Chem, 272, 609-616.
26. Marakova,O.V., Marakov,E.M., Sousa,R. and Dreyfus,M. (1995) Transcribing Escherichia coli genes with mutant T7 RNA polymerases: stability of lacZ mRNA inversely correlates with polymerase speed. Proc. Natl Acad. Sci. USA, 92, 12250-12254.
27. McDowall,K.J., Kaberdin,V.R:, Wu,S.W., Cohen,S.N. and Lin-Chao,S. (1995) Site-specific RNase E cleavage of oligonucleotides and inhibition by stem-loops. Nature, 374, 287-290.
28. Miller,J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
29. Naureckiene,S. and Uhlin,B.E. (1996) In vitro analysis of mRNA processing by RNase E in the pap operon of Escherichia coli. Mol. Microbiol., 21, 55-68.
30. Nilsson,G., Belasco,J.G., Cohen,S.N. and von Gabain,A. (1987) Effect of premature termination of translation on mRNA stability depends on the site of ribosome release. Proc. Natl Acad. Sci. USA, 84, 4890-4894.
31. Nilsson,P., Naureckiene,S. and Uhlin,B.E. (1996) Mutations affecting mRNA processing and fimbrial biogenesis in the Escherichia coli pap operon. J. Bacteriol., 178, 683-690.
32. O'Hara,E.B., Chekanova,J.A., Ingle,C.A., Kushner,Z.R., Peters,E. and Kushner,S.R. (1995) Polyadenylylation helps regulate mRNA decay in Escherichia coli. Proc. Natl Acad. Sci. USA, 92, 1807-1811.
33. Petersen,C. (1993) Translation and mRNA stability in bacteria: a complex relationship. In Belasco,J.G. and Brawerman,G. (eds), Control of Messenger RNA Stability. Academic Press Inc., New York, pp. 117-147.
34. Philippe,C., Eyermann,F., Bénard,L., Portier,C., Ehresmann,B. and Ehresmann,C. (1993) Ribosomal protein S15 from Escherichia coli modulates its own translation by trapping the ribosome on the mRNA initiation loading site. Proc. Natl Acad. Sci. USA, 90, 4394-4398.
35. Plumbridge,J., Dondon,J., Nakamura,Y. and Grunberg-Manago,M. (1985) Effect of NusA protein on expression of the nusA infB operon in E.coli. Nucleic Acids. Res., 13, 3371-3388.
36. Portier,C. Dondon,L. and Grunberg-Manago,M. (1990) Translational autocontrol of the E.coli ribosomal protein S15. J. Mol. Biol., 211, 407-414.
37. Py,B., Higgins,C.F., Krisch,H.M. and Carpousis,A.J. (1996) A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature, 381, 169-172.
38. Rapaport,L.R. and Mackie,G.A. (1994) Influence of translational efficiency on the stability of the mRNA for ribosomal protein S20 in Escherichia coli. J. Bacteriol., 176, 992-998.
39. 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.
40. Régnier,P. and Portier,C. (1986) Initiation, attenuation and RNase III processing of transcripts from the E.coli operon encoding ribosomal protein S15 and polynucleotide phosphorylase. J. Mol. Biol., 187, 23-32.
41. Régnier,P., Grunberg-Manago,M. and Portier,C. (1987) Nucleotide sequence of the pnp gene of E.coli encoding polynucleotide phosphorylase; homology of the primary structure of the protein with the RNA binding domain of ribosomal protein S1. J. Biol. Chem., 262, 63-68.
42. Sambrook,J., Fritsch,E.F. and Maniatis,T. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Simons,R.W., Houman,F. and Kleckner,N. (1987) Improved single and multicopy lacZ-based cloning vectors for protein and operon fusions. Gene, 53, 85-96.
44. Singer,P. and Nomura,M. (1985) Stability of ribosomal protein mRNA and translational feedback regulation in Escherichia coli. Mol. Gen. Genet., 199, 543-546.
45. Springer,M. et al. (1985) Autogeneous control of Escherichia coli threonyl-tRNA synthetase expression in vivo. J. Mol. Biol., 185, 93-104.
46. Steitz,J. (1969) Polypeptide chain initiation: nucleotide sequences of the three ribosomal binding sites in bacteriophage R17 RNA. Nature, 224, 957-964.
47. Xu,F., Lin-Chao,S. and Cohen,S.N. (1993) The Escherichia coli pcnB gene promotes adenylation of antisense RNAI of ColE1-type plasmids in vivo and degradation of RNAI decay intermediate. Proc. Natl Acad. Sci. USA, 90, 6756-6760.
48. Yano,R. and Yura,T. (1989) Suppression of the Escherichia coli rpoH opal mutation by ribosomes lacking S15 protein. J. Bacteriol., 171, 1712-1717.
49. Yarchuk,O., Iost,I. and Dreyfus,M. (1991) The relation between translation and mRNA degradation in the lacZ gene. Biochimie, 73, 1533-1541.
50. Zilhao,R., Camelo,L. and Arraiano,C.M. (1993) DNA sequencing and expression of the gene rnb encoding Escherichia coli ribonuclease II. Mol. Microbiol., 8, 43-51.
51. Zilhao,R., Plumbridge,J., Hajnsdorf,E., Régnier,P. and Arraiano,C.M. (1996) Escherichia coli RNase II: characterization of the promoters involved in the transcription of rnb. Microbiology, 142, 367-375.