Home LiteratureArticle Details
PMID: 16166379 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs.

Genes & development ·Vol. 19 ·No. 18 ·2005-09-15 ·Pages 2176-86

Morita T, Maki K, Aiba H

Abstract

Hfq-binding antisense small RNAs of Escherichia coli, SgrS and RyhB, mediate the destabilization of target mRNAs in an RNase E-dependent manner. SgrS, whose expression is induced in response to phosphosugar stress, act on the ptsG mRNA encoding a major glucose transporter, while RyhB, whose expression is induced in response to Fe depletion, acts on several mRNAs encoding Fe-binding proteins. In this report, we addressed the question of how SgrS and RyhB RNAs cooperate with RNase E to destabilize the target mRNAs. We demonstrate that Hfq along with SgrS and RyhB copurified with RNase E but not with truncated RNase E. In addition, we show that RNase E but not other degradosome components copurified with Hfq. Taken together, we conclude that RNase E forms variable ribonucleoprotein complexes with Hfq/small RNAs through its C-terminal scaffold region. These complexes, distinct from the RNA degradosome, may act as specialized RNA decay machines that initiate the degradation of mRNAs targeted by each small RNA. The present finding has uncovered the mechanical basis of mRNA destabilization mediated by bacterial small RNAs. The formation of ribonucleoprotein complexes containing RNases could be a general way by which small RNAs destabilize target mRNAs in both prokaryotes and eukaryotes.

MeSH Terms
Endoribonucleases/isolation & purification,metabolism Escherichia coli/genetics,growth & development,metabolism Escherichia coli Proteins/analysis,genetics,metabolism Gene Deletion Gene Expression Regulation, Bacterial Host Factor 1 Protein/analysis,genetics,metabolism Models, Biological Multienzyme Complexes/metabolism Polyribonucleotide Nucleotidyltransferase/metabolism RNA Helicases/metabolism RNA Stability RNA, Antisense/metabolism RNA, Bacterial/metabolism RNA, Messenger/metabolism Ribonucleoproteins/analysis,genetics,metabolism
Chemicals
Escherichia coli Proteins Hfq protein, E coli Host Factor 1 Protein Multienzyme Complexes RNA, Antisense RNA, Bacterial RNA, Messenger Ribonucleoproteins degradosome Polyribonucleotide Nucleotidyltransferase Endoribonucleases ribonuclease E RNA Helicases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Morita Teppei
Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa, Nagoya 464-8602, Japan.
Maki Kimika
Aiba Hiroji
References (35)
35 references, click to expand
  1. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products.
    Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5 PMID: 10829079
  2. RNase E is required for the maturation of ssrA RNA and normal ssrA RNA peptide-tagging activity.
    Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12406-11 PMID: 10535935
  3. Epitope tagging of chromosomal genes in Salmonella.
    Proc Natl Acad Sci U S A. 2001 Dec 18;98(26):15264-9 PMID: 11742086
  4. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli.
    Proc Natl Acad Sci U S A. 2002 Apr 2;99(7):4620-5 PMID: 11917098
  5. The Escherichia coli RNA degradosome: structure, function and relationship in other ribonucleolytic multienzyme complexes.
    Biochem Soc Trans. 2002 Apr;30(2):150-5 PMID: 12035760
  6. Regulation and mode of action of the second small RNA activator of RpoS translation, RprA.
    Mol Microbiol. 2002 Nov;46(3):813-26 PMID: 12410838
  7. Accumulation of glucose 6-phosphate or fructose 6-phosphate is responsible for destabilization of glucose transporter mRNA in Escherichia coli.
    J Biol Chem. 2003 May 2;278(18):15608-14 PMID: 12578824
  8. Interaction of Escherichia coli RNA polymerase with the ribosomal protein S1 and the Sm-like ATPase Hfq.
    Biochemistry. 2003 Jul 8;42(26):8022-34 PMID: 12834354
  9. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli.
    Genes Dev. 2003 Oct 1;17(19):2374-83 PMID: 12975324
  10. Global analysis of small RNA and mRNA targets of Hfq.
    Mol Microbiol. 2003 Nov;50(4):1111-24 PMID: 14622403
  11. The RNA degradosome and poly(A) polymerase of Escherichia coli are required in vivo for the degradation of small mRNA decay intermediates containing REP-stabilizers.
    Mol Microbiol. 2004 Feb;51(3):777-90 PMID: 14731278
  12. MicroRNAs: genomics, biogenesis, mechanism, and function.
    Cell. 2004 Jan 23;116(2):281-97 PMID: 14744438
  13. The bacterial Sm-like protein Hfq: a key player in RNA transactions.
    Mol Microbiol. 2004 Mar;51(6):1525-33 PMID: 15009882
  14. Controlling mRNA stability and translation with small, noncoding RNAs.
    Curr Opin Microbiol. 2004 Apr;7(2):140-4 PMID: 15063850
  15. Studies of the RNA degradosome-organizing domain of the Escherichia coli ribonuclease RNase E.
    J Mol Biol. 2004 Jul 23;340(5):965-79 PMID: 15236960
  16. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae.
    Cell. 2004 Jul 9;118(1):69-82 PMID: 15242645
  17. MicC, a second small-RNA regulator of Omp protein expression in Escherichia coli.
    J Bacteriol. 2004 Oct;186(20):6689-97 PMID: 15466019
  18. The small RNA regulators of Escherichia coli: roles and mechanisms*.
    Annu Rev Microbiol. 2004;58:303-28 PMID: 15487940
  19. Evidence for two functional gal promoters in intact Escherichia coli cells.
    J Biol Chem. 1981 Nov 25;256(22):11905-10 PMID: 6271763
  20. Copurification of E. coli RNAase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation.
    Cell. 1994 Mar 11;76(5):889-900 PMID: 7510217
  21. A lowered concentration of cAMP receptor protein caused by glucose is an important determinant for catabolite repression in Escherichia coli.
    Mol Microbiol. 1993 Oct;10(2):341-50 PMID: 7934825
  22. The N-terminal domain of the rne gene product has RNase E activity and is non-overlapping with the arginine-rich RNA-binding site.
    J Mol Biol. 1996 Jan 26;255(3):349-55 PMID: 8568879
  23. A DEAD-box RNA helicase in the Escherichia coli RNA degradosome.
    Nature. 1996 May 9;381(6578):169-72 PMID: 8610017
  24. Proteins associated with RNase E in a multicomponent ribonucleolytic complex.
    Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):3865-9 PMID: 8632981
  25. RNA components of Escherichia coli degradosome: evidence for rRNA decay.
    Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3157-61 PMID: 9501232
  26. Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome.
    Genes Dev. 1998 Sep 1;12(17):2770-81 PMID: 9732274
  27. 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 U S A. 1998 Oct 13;95(21):12462-7 PMID: 9770508
  28. Reconstitution of a minimal RNA degradosome demonstrates functional coordination between a 3' exonuclease and a DEAD-box RNA helicase.
    Genes Dev. 1999 Oct 1;13(19):2594-603 PMID: 10521403
  29. The Sm-like protein Hfq regulates polyadenylation dependent mRNA decay in Escherichia coli.
    Mol Microbiol. 2004 Nov;54(4):905-20 PMID: 15522076
  30. Enolase in the RNA degradosome plays a crucial role in the rapid decay of glucose transporter mRNA in the response to phosphosugar stress in Escherichia coli.
    Mol Microbiol. 2004 Nov;54(4):1063-75 PMID: 15522087
  31. Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system.
    Mol Microbiol. 2004 Nov;54(4):1076-89 PMID: 15522088
  32. Physical and functional interactions among RNase E, polynucleotide phosphorylase and the cold-shock protein, CsdA: evidence for a 'cold shock degradosome'.
    Mol Microbiol. 2004 Dec;54(5):1409-21 PMID: 15554978
  33. Implication of membrane localization of target mRNA in the action of a small RNA: mechanism of post-transcriptional regulation of glucose transporter in Escherichia coli.
    Genes Dev. 2005 Feb 1;19(3):328-38 PMID: 15650111
  34. Noncoding RNAs at the membrane.
    Nat Struct Mol Biol. 2005 Apr;12(4):285-6 PMID: 15809646
  35. Expression of the glucose transporter gene, ptsG, is regulated at the mRNA degradation step in response to glycolytic flux in Escherichia coli.
    EMBO J. 2001 Jul 2;20(13):3587-95 PMID: 11432845
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
Published
2005-09-15
Pages
2176-86
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC1221888
Subset
IM
Corrections
ErratumIn
-
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com