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PMID: 15678100 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression.

The EMBO journal ·Vol. 24 ·No. 4 ·2005-02-23 ·Pages 824-35

Huntzinger E, Boisset S, Saveanu C, Benito Y, Geissmann T, Namane A, Lina G, Etienne J, Ehresmann B, Ehresmann C, Jacquier A, Vandenesch F, Romby P

Abstract

Staphylococcus aureus RNAIII is one of the largest regulatory RNAs, which controls several virulence genes encoding exoproteins and cell-wall-associated proteins. One of the RNAIII effects is the repression of spa gene (coding for the surface protein A) expression. Here, we show that spa repression occurs not only at the transcriptional level but also by RNAIII-mediated inhibition of translation and degradation of the stable spa mRNA by the double-strand-specific endoribonuclease III (RNase III). The 3' end domain of RNAIII, partially complementary to the 5' part of spa mRNA, efficiently anneals to spa mRNA through an initial loop-loop interaction. Although this annealing is sufficient to inhibit in vitro the formation of the translation initiation complex, the coordinated action of RNase III is essential in vivo to degrade the mRNA and irreversibly arrest translation. Our results further suggest that RNase III is recruited for targeting the paired RNAs. These findings add further complexity to the expression of the S. aureus virulon.

MeSH Terms
Antigens, Bacterial/genetics,metabolism Bacterial Proteins/metabolism Base Sequence Binding Sites Gene Expression Regulation, Bacterial Molecular Sequence Data Nucleic Acid Conformation Protein Biosynthesis RNA Stability RNA, Antisense/chemistry,genetics,metabolism RNA, Bacterial/chemistry,genetics,metabolism RNA, Messenger/genetics,metabolism Ribonuclease III/metabolism Ribosomes/metabolism Staphylococcal Protein A/genetics,metabolism Staphylococcus aureus/enzymology,genetics Transcription, Genetic/genetics
Chemicals
Antigens, Bacterial Bacterial Proteins RNA, Antisense RNA, Bacterial RNA, Messenger RNAIII, Staphylococcus aureus Staphylococcal Protein A streptococcal protective antigen Ribonuclease III
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Huntzinger Eric
UPR 9002 du CNRS, Institut de Biologie Moléculaire et Cellulaire, Strasbourg Cedex, France.
Boisset Sandrine
Saveanu Cosmin
Benito Yvonne
Geissmann Thomas
Namane Abdelkader
Lina Gérard
Etienne Jerome
Ehresmann Bernard
Ehresmann Chantal
Jacquier Alain
Vandenesch François
Romby Pascale
References (46)
46 references, click to expand
  1. Structure, reactivity, and biology of double-stranded RNA.
    Prog Nucleic Acid Res Mol Biol. 1996;52:1-65 PMID: 8821257
  2. Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1.
    Nat Med. 2004 Aug;10(8):842-8 PMID: 15247912
  3. Identification of structural elements critical for inter-domain interactions in a group II self-splicing intron.
    EMBO J. 1997 May 15;16(10):2945-54 PMID: 9184238
  4. Antisense RNA-regulated programmed cell death.
    Annu Rev Genet. 1997;31:1-31 PMID: 9442888
  5. A broad-host-range mobilizable shuttle vector for the construction of transcriptional fusions to beta-galactosidase in gram-positive bacteria.
    FEMS Microbiol Lett. 1997 Nov 15;156(2):193-8 PMID: 9513264
  6. trans-complementation of a Staphylococcus aureus agr mutant by Staphylococcus lugdunensis agr RNAIII.
    J Bacteriol. 1998 Nov;180(21):5780-3 PMID: 9791134
  7. ANALYSIS BY TRANSDUCTION OF MUTATIONS AFFECTING PENICILLINASE FORMATION IN STAPHYLOCOCCUS AUREUS.
    J Gen Microbiol. 1963 Oct;33:121-36 PMID: 14072829
  8. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria.
    Appl Environ Microbiol. 2004 Nov;70(11):6887-91 PMID: 15528558
  9. Probing the structure of RNAIII, the Staphylococcus aureus agr regulatory RNA, and identification of the RNA domain involved in repression of protein A expression.
    RNA. 2000 May;6(5):668-79 PMID: 10836788
  10. fhlA repression by OxyS RNA: kissing complex formation at two sites results in a stable antisense-target RNA complex.
    J Mol Biol. 2000 Jul 28;300(5):1101-12 PMID: 10903857
  11. Protein A is the von Willebrand factor binding protein on Staphylococcus aureus.
    Blood. 2000 Sep 15;96(6):2149-56 PMID: 10979960
  12. Endoribonuclease RNase III is essential in Bacillus subtilis.
    Mol Microbiol. 2000 Dec;38(5):1027-33 PMID: 11123676
  13. Group A streptococcal growth phase-associated virulence factor regulation by a novel operon (Fas) with homologies to two-component-type regulators requires a small RNA molecule.
    Mol Microbiol. 2001 Jan;39(2):392-406 PMID: 11136460
  14. Staphylococcal toxin induced preferential and prolonged in vivo deletion of innate-like B lymphocytes.
    Proc Natl Acad Sci U S A. 2004 Aug 3;101(31):11392-7 PMID: 15273292
  15. Synthesis of group A streptococcal virulence factors is controlled by a regulatory RNA molecule.
    Mol Microbiol. 2004 Sep;53(5):1515-27 PMID: 15387826
  16. Nucleotide sequence and functional map of pC194, a plasmid that specifies inducible chloramphenicol resistance.
    J Bacteriol. 1982 May;150(2):815-25 PMID: 6950931
  17. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage.
    Nature. 1983 Oct 20-26;305(5936):709-12 PMID: 6226876
  18. Virulence of protein A-deficient and alpha-toxin-deficient mutants of Staphylococcus aureus isolated by allele replacement.
    Infect Immun. 1987 Dec;55(12):3103-10 PMID: 3679545
  19. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus.
    J Bacteriol. 1988 Sep;170(9):4365-72 PMID: 2457579
  20. Control of replication of plasmid R1: kinetics of in vitro interaction between the antisense RNA, CopA, and its target, CopT.
    EMBO J. 1988 Oct;7(10):3279-88 PMID: 2460339
  21. Extension inhibition analysis of translation initiation complexes.
    Methods Enzymol. 1988;164:419-25 PMID: 2468068
  22. The IS10 transposase mRNA is destabilized during antisense RNA control.
    EMBO J. 1990 Apr;9(4):1259-66 PMID: 1691096
  23. The role of the delta-lysin gene (hld) in the regulation of virulence genes by the accessory gene regulator (agr) in Staphylococcus aureus.
    EMBO J. 1990 May;9(5):1391-9 PMID: 2328718
  24. RNase III-dependent hydrolysis of lambda cII-O gene mRNA mediated by lambda OOP antisense RNA.
    Genes Dev. 1990 Dec;4(12A):2223-33 PMID: 2148537
  25. Replication control in plasmid R1: duplex formation between the antisense RNA, CopA, and its target, CopT, is not required for inhibition of RepA synthesis.
    EMBO J. 1992 Mar;11(3):1195-203 PMID: 1372249
  26. Regulation of the protein A-encoding gene in Staphylococcus aureus.
    Gene. 1992 May 1;114(1):25-34 PMID: 1587482
  27. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule.
    EMBO J. 1993 Oct;12(10):3967-75 PMID: 7691599
  28. Activation of alpha-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII.
    EMBO J. 1995 Sep 15;14(18):4569-77 PMID: 7556100
  29. The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs.
    Mol Cell. 2002 Jan;9(1):11-22 PMID: 11804582
  30. Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction.
    Mol Cell. 2002 Jan;9(1):23-30 PMID: 11804583
  31. A model B-cell superantigen and the immunobiology of B lymphocytes.
    Clin Immunol. 2002 Feb;102(2):117-34 PMID: 11846453
  32. Clostridial VirR/VirS regulon involves a regulatory RNA molecule for expression of toxins.
    Mol Microbiol. 2002 Jan;43(1):257-65 PMID: 11849553
  33. Antisense RNAs in bacteria and their genetic elements.
    Adv Genet. 2002;46:361-98 PMID: 11931231
  34. A 5' stem-loop and ribosome binding but not translation are important for the stability of Bacillus subtilis aprE leader mRNA.
    Microbiology. 2002 Jun;148(Pt 6):1795-803 PMID: 12055299
  35. Global regulation of Staphylococcus aureus genes by Rot.
    J Bacteriol. 2003 Jan;185(2):610-9 PMID: 12511508
  36. Autoinduction and signal transduction in the regulation of staphylococcal virulence.
    Mol Microbiol. 2003 Jun;48(6):1429-49 PMID: 12791129
  37. RNA processing and degradation in Bacillus subtilis.
    Microbiol Mol Biol Rev. 2003 Jun;67(2):157-74, table of contents PMID: 12794188
  38. RNA-mediated control of virulence gene expression in bacterial pathogens.
    Trends Microbiol. 2003 Jun;11(6):280-5 PMID: 12823945
  39. Effect of translational signals on mRNA decay in Bacillus subtilis.
    J Bacteriol. 2003 Sep;185(18):5372-9 PMID: 12949089
  40. 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
  41. Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator.
    EMBO J. 2004 Jan 28;23(2):396-405 PMID: 14739933
  42. Controlling mRNA stability and translation with small, noncoding RNAs.
    Curr Opin Microbiol. 2004 Apr;7(2):140-4 PMID: 15063850
  43. Regulatory elements of the Staphylococcus aureus protein A (Spa) promoter.
    J Bacteriol. 2004 Jun;186(12):3738-48 PMID: 15175287
  44. Hfq is essential for Vibrio cholerae virulence and downregulates sigma expression.
    Mol Microbiol. 2004 Jul;53(1):345-54 PMID: 15225327
  45. 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
  46. Regulation of protein A synthesis by the sar and agr loci of Staphylococcus aureus.
    Infect Immun. 1997 Jun;65(6):2243-9 PMID: 9169758
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2005-02-23
Epub
2005-00-27
Pages
824-35
Language
English
Region
England
NLM ID
8208664
PMCID
PMC549626
Subset
IM
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