Loop-loop interactions involved in antisense regulation are processed by the endoribonuclease III in Staphylococcus aureus

RNA Biology

Volumn 9, Issue 12, 2012, Pages 1461-1472

  Romilly, Cédric ^a   Chevalier, Clément ^b   Marzi, Stefano ^a   Masquida, Benoit ^a   Geissmann, Thomas ^c,d   Vandenesch, François ^c,d,e   Westhof, Eric ^a   Romby, Pascale ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITÉ DE LYON   (France)

^d INSERM   (France)

^e HOSPICES CIVILS DE LYON   (France)

Author keywords

Endoribonuclease; Gene regulation; Loop loop interaction; Processing; Regulatory RNA

Indexed keywords

RIBONUCLEASE; RIBONUCLEASE III; VIRULENCE FACTOR;

ARTICLE; MOLECULAR MODEL; NONHUMAN; QUORUM SENSING; RNA CLEAVAGE; RNA DEGRADATION; RNA STRUCTURE; STAPHYLOCOCCUS AUREUS;

EID: 84875206815     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.22710     Document Type: Article

References (42)

1. Dinges MM, Orwin PM, Schlievert PM. Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 2000; 13:16-34; PMID:10627489; http://dx.doi.org/10.1128/CMR. 13.1.16-34.2000. (Pubitemid 30039341)
2. Foster TJ, Höök M. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 1998; 6:484-8; PMID:10036727; http://dx.doi.org/10. 1016/S0966-842X(98)01400-0. (Pubitemid 29002881)
3. Novick R P. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 2003; 48:1429-49; PMID:12791129; http://dx.doi.org/10.1046/j.1365-2958.2003.03526.x. (Pubitemid 36751052)
4. Novick R P, Geisinger E. Quorum sensing in staphylococci. Annu Rev Genet 2008; 42:541-64; PMID:18713030; http://dx.doi.org/10.1146/annurev. genet.42.110807.091640.
5. Anderson KL, Dunman PM. Messenger RNA Turnover Processes in Escherichia coli, Bacillus sub-tilis, and Emerging Studies in Staphylococcus aureus. Int J Microbiol 2009; 2009:525491; PMID:19936110; http://dx.doi.org/10.1155/2009/ 525491.
6. Anderson KL, Roberts C, Disz T, Vonstein V, Hwang K, Overbeek R, et al. Characterization of the Staphylococcus aureus heat shock, cold shock, stringent, and SOS responses and their effects on log-phase mRNA turnover. J Bacteriol 2006; 188:6739-56; PMID:16980476; http://dx.doi.org/10.1128/JB.00609-06. (Pubitemid 44497886)
7. Anderson KL, Roux CM, Olson MW, Luong T T, Lee CY, Olson R, et al. Characterizing the effects of inorganic acid and alkaline shock on the Staphylococcus aureus transcriptome and messenger RNA turnover. FEMS Immunol Med Microbiol 2010; 60:208-50; PMID:21039920; http://dx.doi.org/10.1111/j.1574- 695X.2010.00736.x.
8. Jester BC, Romby P, Lioliou E. When ribo-nucleases come into play in pathogens: a survey of gram-positive bacteria. Int J Microbiol 2012; 2012:592196; PMID:22550495; http://dx.doi. org/10.1155/2012/592196.
9. Roux CM, DeMuth J P, Dunman PM. Characterization of components of the Staphylococcus aureus mRNA degradosome holoenzyme-like complex. J Bacteriol 2011; 193:5520-6; PMID:21764917; http://dx.doi. org/10.1128/JB.05485-11.
10. Kaberdin VR, Singh D, Lin-Chao S. Composition and conservation of the mRNA-degrading machinery in bacteria. J Biomed Sci 2011; 18:23-35; PMID:21418661; http://dx.doi.org/10.1186/1423-0127-18-23.
11. Olson PD, Kuechenmeister LJ, Anderson KL, Daily S, Beenken KE, Roux CM, et al. Small molecule inhibitors of Staphylococcus aureus RnpA alter cellular mRNA turnover, exhibit antimicrobial activity, and attenuate pathogenesis. PLoS Pathog 2011; 7:e1001287; PMID:21347352; http://dx.doi.org/10.1371/journal. ppat.1001287.
12. Marincola G, Schäfer T, Behler J, Bernhardt J, Ohlsen K, Goerke C, et al. RNase Y of Staphylococcus aureus and its role in the activation of virulence genes. Mol Microbiol 2012; 85:817-32; PMID:22780584; http://dx.doi.org/10.1111/j.1365-2958.2012.08144.x.
13. Kaito C, Kurokawa K, Matsumoto Y, Terao Y, Kawabata S, Hamada S, et al. Silkworm pathogenic bacteria infection model for identification of novel virulence genes. Mol Microbiol 2005; 56:934-44; PMID:15853881; http://dx.doi.org/10.1111/j.1365-2958.2005.04596.x. (Pubitemid 40646766)
14. Liu Y, Dong J, Wu N, Gao Y, Zhang X, Mu C, et al. The production of extracellular proteins is regulated by ribonuclease III via two different pathways in Staphylococcus aureus. PLoS One 2011; 6:e20554; PMID:21655230; http://dx.doi.org/10.1371/journal. pone.0020554.
15. Huntzinger E, Boisset S, Saveanu C, Benito Y, Geissmann T, Namane A, et al. Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J 2005; 24:824-35; PMID:15678100; http://dx.doi.org/10.1038/sj.emboj.7600572. (Pubitemid 40396111)
16. Lioliou E, Sharma CM, Caldelari I, Helfer AC, Fechter P, Vandenesch F, et al. Global regulatory functions of the Staphylococcus aureus endoribonuclease III in gene expression. PLoS Genet 2012; 8:e1002782; PMID:22761586; http://dx.doi.org/10.1371/journal. pgen.1002782.
17. MacRae IJ, Doudna JA. Ribonuclease revisited: structural insights into ribonuclease III family enzymes. Curr Opin Struct Biol 2007; 17:138-45; PMID:17194582; http://dx.doi.org/10.1016/j.sbi.2006.12.002. (Pubitemid 46240810)
18. Conrad C, Schmitt JG, Evguenieva-Hackenberg E, Klug G. One functional subunit is sufficient for catalytic activity and substrate specificity of Escherichia coli endoribonuclease III artificial heterodimers. FEBS Lett 2002; 518:93-6; PMID:11997024; http://dx.doi. org/10.1016/S0014-5793(02)02653-4. (Pubitemid 34454970)
19. Dasgupta S, Fernandez L, Kameyama L, Inada T, Nakamura Y, Pappas A, et al. Genetic uncoupling of the dsRNA-binding and RNA cleavage activities of the Escherichia coli endoribonuclease RNase III-the effect of dsRNA binding on gene expression. Mol Microbiol 1998; 28:629-40; PMID:9632264; http://dx.doi.org/10. 1046/j.1365-2958.1998.00828.x. (Pubitemid 28218406)
20. Sun W, Jun E, Nicholson AW. Intrinsic double-stranded-RNA processing activity of Escherichia coli ribonuclease III lacking the dsRNA-binding domain. Biochemistry 2001; 40:14976-84; PMID:11732918; http://dx.doi.org/10.1021/ bi011570u. (Pubitemid 33136119)
21. Chevalier C, Huntzinger E, Fechter P, Boisset S, Vandenesch F, Romby P, et al. Staphylococcus aureus endoribonuclease III purification and properties. Methods Enzymol 2008; 447:309-27; PMID:19161850; http://dx.doi.org/10.1016/ S0076-6879(08)02216-7.
22. Geisinger E, Adhikari R P, Jin R, Ross H F, Novick R P. Inhibition of rot translation by RNAIII, a key feature of agr function. Mol Microbiol 2006; 61:1038-48; PMID:16879652; http://dx.doi.org/10.1111/j.1365-2958.2006.05292.x. (Pubitemid 44134179)
23. Boisset S, Geissmann T, Huntzinger E, Fechter P, Bendridi N, Possedko M, et al. Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 2007; 21:1353-66; PMID:17545468; http://dx.doi.org/10.1101/gad. 423507. (Pubitemid 46871039)
24. Chevalier C, Boisset S, Romilly C, Masquida B, Fechter P, Geissmann T, et al. Staphylococcus aureus RNAIII binds to two distant regions of coa mRNA to arrest translation and promote mRNA degradation. PLoS Pathog 2010; 6:e1000809; PMID:20300607; http://dx.doi.org/10.1371/journal.ppat.1000809.
25. Lasa I, Toledo-Arana A, Dobin A, Villanueva M, de los Mozos IR, Vergara-Irigaray M, et al. Genome-wide antisense transcription drives mRNA processing in bacteria. Proc Natl Acad Sci USA 2011; 108:20172-7; PMID:22123973; http://dx.doi.org/10.1073/pnas.1113521108.
26. Pertzev AV, Nicholson AW. Characterization of RNA sequence determinants and antideterminants of processing reactivity for a minimal substrate of Escherichia coli ribonuclease III. Nucleic Acids Res 2006; 34:3708-21; PMID:16896014; http://dx.doi.org/10.1093/nar/gkl459. (Pubitemid 44400420)
27. Zhang K, Nicholson AW. Regulation of ribonuclease III processing by double-helical sequence antideter-minants. Proc Natl Acad Sci USA 1997; 94:13437-41; PMID:9391043; http://dx.doi.org/10.1073/pnas.94.25.13437. (Pubitemid 28009600)
28. Felden B, Vandenesch F, Bouloc P, Romby P. The Staphylococcus aureus RNome and its commitment to virulence. PLoS Pathog 2011; 7:e1002006; PMID:21423670; http://dx.doi.org/10.1371/journal. ppat.1002006.
29. Gan J, Shaw G, Tropea JE, Waugh DS, Court DL, Ji X. A stepwise model for double-stranded RNA processing by ribonuclease III. Mol Microbiol 2008; 67:143-54; PMID:18047582; http://dx.doi. org/10.1111/j.1365-2958.2007.06032.x. (Pubitemid 350231141)
30. Robertson HD. Escherichia coli ribonuclease III cleavage sites. Cell 1982; 30:669-72; PMID:6754088; http://dx.doi.org/10.1016/0092-8674(82)90270-7. (Pubitemid 13204655)
31. Gan J, Tropea JE, Austin B P, Court DL, Waugh DS, Ji X. Structural insight into the mechanism of double-stranded RNA processing by ribonuclease III. Cell 2006; 124:355-66; PMID:16439209; http://dx.doi. org/10.1016/j.cell. 2005.11.034. (Pubitemid 43121983)
32. Blaszczyk J, Gan J, Tropea JE, Court DL, Waugh DS, Ji X. Noncatalytic assembly of ribonuclease III with double-stranded RNA. Structure 2004; 12:457-66; PMID:15016361; http://dx.doi.org/10.1016/j. str.2004.02.004. (Pubitemid 38353066)
33. Franch T, Thisted T, Gerdes K. Ribonuclease III processing of coaxially stacked RNA helices. J Biol Chem 1999; 274:26572-8; PMID:10473621; http://dx.doi. org/10.1074/jbc.274.37.26572.
34. Calin-Jageman I, Nicholson AW. Mutational analysis of an RNA internal loop as a reactivity epit-ope for Escherichia coli ribonuclease III substrates. Biochemistry 2003; 42:5025-34; PMID:12718545; http://dx.doi.org/10.1021/ bi030004r. (Pubitemid 36532056)
35. Wagner EG, Altuvia S, Romby P. Antisense RNAs in bacteria and their genetic elements. Adv Genet 2002; 46:361-98; PMID:11931231; http://dx.doi. org/10.1016/S0065-2660(02)46013-0.
36. Brantl S. Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr Opin Microbiol 2007; 10:102-9; PMID:17387036; http://dx.doi. org/10.1016/j.mib.2007.03.012. (Pubitemid 46590052)
37. Argaman L, Altuvia S. fhlA repression by OxyS RNA: kissing complex formation at two sites results in a stable antisense-target RNA complex. J Mol Biol 2000; 300:1101-12; PMID:10903857; http://dx.doi. org/10.1006/jmbi.2000. 3942.
38. Chanfreau G, Buckle M, Jacquier A. Recognition of a conserved class of RNA tetraloops by Saccharomyces cerevisiae RNase III. Proc Natl Acad Sci USA 2000; 97:3142-7; PMID:10716739; http://dx.doi. org/10.1073/pnas.97.7.3142. (Pubitemid 30183269)
39. Benito Y, Kolb FA, Romby P, Lina G, Etienne J, Vandenesch F. 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; 6:668-79; PMID:10836788; http://dx.doi.org/10.1017/S1355838200992550. (Pubitemid 30318462)
40. Fechter P, Chevalier C, Yusupova G, Yusupov M, Romby P, Marzi S. Ribosomal initiation complexes probed by toeprinting and effect of trans-acting trans-lational regulators in bacteria. Methods Mol Biol 2009; 540:247-63; PMID:19381565; http://dx.doi. org/10.1007/978-1-59745-558-9-18.
41. Westhof E, Masquida B, Jossinet F. Predicting and modeling RNA architecture. Cold Spring Harb Perspect Biol 2011; 3: In press; PMID:20504963; http://dx.doi.org/10.1101/cshperspect.a003632.
42. Jossinet F, Ludwig TE, Westhof E. Assemble: an interactive graphical tool to analyze and build RNA architectures at the 2D and 3D levels. Bioinformatics 2010; 26:2057-9; PMID:20562414; http://dx.doi. org/10.1093/bioinformatics/ btq321.