Transcriptome-Wide Analyses of 5′-Ends in RNase J Mutants of a Gram-Positive Pathogen Reveal a Role in RNA Maturation, Regulation and Degradation

PLoS Genetics

Volumn 10, Issue 2, 2014, Pages

  Linder, Patrick ^a   Lemeille, Sylvain ^a   Redder, Peter ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE; MESSENGER RNA; RIBONUCLEASE; RIBONUCLEASE E; RIBOZYME; RNA; RNA 16S; TRANSCRIPTOME; 5' UNTRANSLATED REGION; REGULATORY RNA SEQUENCE;

ARTICLE; ENZYME ACTIVITY; ESCHERICHIA COLI; FEVER; FIRMICUTES; GENE MUTATION; GRAM POSITIVE BACTERIUM; IN VIVO STUDY; MATURATION; NONHUMAN; PHENOTYPE; QUALITY CONTROL; RATING SCALE; RIBOSOME; RNA DEGRADATION; STAPHYLOCOCCUS AUREUS; 5' UNTRANSLATED REGION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; REGULATORY RNA SEQUENCE; RNA STABILITY;

5' UNTRANSLATED REGIONS; ESCHERICHIA COLI; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RIBONUCLEASES; RIBOSOMES; RNA STABILITY; RNA, MESSENGER; STAPHYLOCOCCUS AUREUS;

EID: 84901743101     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004207     Document Type: Article

References (32)

1. Condon C, Bechhofer DH, (2011) Regulated RNA stability in the Gram positives. Curr Opin Microbiol 14: 148-154.
2. Roberts C, Anderson KL, Murphy E, Projan SJ, Mounts W, et al. (2006) Characterizing the effect of the Staphylococcus aureus virulence factor regulator, SarA, on log-phase mRNA half-lives. J Bacteriol 188: 2593-2603.
3. McDowall KJ, Kaberdin VR, Wu SW, Cohen SN, Lin-Chao S, (1995) Site-specific RNase E cleavage of oligonucleotides and inhibition by stem-loops. Nature 374: 287-290.
4. Carpousis AJ, (2007) The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu Rev Microbiol 61: 71-87.
5. Anderson KL, Roux CM, Olson MW, Luong TT, Lee CY, et al. (2010) Characterizing the effects of inorganic acid and alkaline shock on the Staphylococcus aureus transcriptome and messenger RNA turnover. FEMS Immunol Med Microbiol 60: 208-250.
6. Shahbabian K, Jamalli A, Zig L, Putzer H, (2009) RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. EMBO J 28: 3523-3533.
7. Even S, Pellegrini O, Zig L, Labas V, Vinh J, et al. (2005) Ribonucleases J1 and J2: two novel endoribonucleases in B.subtilis with functional homology to E.coli RNase E. Nucleic Acids Res 33: 2141-2152.
8. Mader U, Zig L, Kretschmer J, Homuth G, Putzer H, (2008) mRNA processing by RNases J1 and J2 affects Bacillus subtilis gene expression on a global scale. Mol Microbiol 70: 183-196.
9. Durand S, Gilet L, Bessieres P, Nicolas P, Condon C, (2012) Three essential ribonucleases-RNase Y, J1, and III-control the abundance of a majority of Bacillus subtilis mRNAs. PLoS Genet 8: e1002520.
10. Bugrysheva JV, Scott JR, (2010) The ribonucleases J1 and J2 are essential for growth and have independent roles in mRNA decay in Streptococcus pyogenes. Mol Microbiol 75: 731-743.
11. Lehnik-Habrink M, Pfortner H, Rempeters L, Pietack N, Herzberg C, et al. (2010) The RNA degradosome in Bacillus subtilis: identification of CshA as the major RNA helicase in the multiprotein complex. Mol Microbiol 77: 958-971.
12. Roux CM, Demuth JP, Dunman PM, (2011) Characterization of components of the Staphylococcus aureus messenger RNA degradosome holoenzyme-like complex. J Bacteriol 193: 5520-6.
13. Mathy N, Benard L, Pellegrini O, Daou R, Wen T, et al. (2007) 5′-to-3′ exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5′ stability of mRNA. Cell 129: 681-692.
14. Li de la Sierra-Gallay I, Zig L, Jamalli A, Putzer H, (2008) Structural insights into the dual activity of RNase J. Nat Struct Mol Biol 15: 206-212.
15. Dorleans A, Li de la Sierra-Gallay I, Piton J, Zig L, Gilet L, et al. (2011) Molecular basis for the recognition and cleavage of RNA by the bifunctional 5′-3′ exo/endoribonuclease RNase J. Structure 19: 1252-1261.
16. Newman JA, Hewitt L, Rodrigues C, Solovyova A, Harwood CR, et al. (2011) Unusual, dual endo- and exonuclease activity in the degradosome explained by crystal structure analysis of RNase J1. Structure 19: 1241-1251.
17. Britton RA, Wen T, Schaefer L, Pellegrini O, Uicker WC, et al. (2007) Maturation of the 5′ end of Bacillus subtilis 16S rRNA by the essential ribonuclease YkqC/RNase J1. Mol Microbiol 63: 127-138.
18. Mathy N, Hebert A, Mervelet P, Benard L, Dorleans A, et al. (2010) Bacillus subtilis ribonucleases J1 and J2 form a complex with altered enzyme behaviour. Mol Microbiol 75: 489-498.
19. Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK, et al. (2003) Essential Bacillus subtilis genes. Proc Natl Acad Sci U S A 100: 4678-4683.
20. Chaudhuri RR, Allen AG, Owen PJ, Shalom G, Stone K, et al. (2009) Comprehensive identification of essential Staphylococcus aureus genes using Transposon-Mediated Differential Hybridisation (TMDH). BMC Genomics 10: 291.
21. Redder P, Linder P, (2012) New Range of Vectors with a Stringent 5-Fluoroorotic Acid-Based Counterselection System for Generating Mutants by Allelic Replacement in Staphylococcus aureus. Appl Environ Microbiol 78: 3846-3854.
22. Figaro S, Durand S, Gilet L, Cayet N, Sachse M, et al. (2013) Bacillus subtilis mutants with knockouts of the genes encoding ribonucleases RNase Y and RNase J1 are viable, with major defects in cell morphology, sporulation, and competence. J Bacteriol 195: 2340-2348.
23. Papp-Wallace KM, Maguire ME, (2008) Regulation of CorA Mg2+ channel function affects the virulence of Salmonella enterica serovar typhimurium. J Bacteriol 190: 6509-6516.
24. Richards J, Liu Q, Pellegrini O, Celesnik H, Yao S, et al. (2011) An RNA pyrophosphohydrolase triggers 5′-exonucleolytic degradation of mRNA in Bacillus subtilis. Mol Cell 43: 940-949.
25. Lioliou E, Sharma CM, Caldelari I, Helfer AC, Fechter P, et al. (2012) Global regulatory functions of the Staphylococcus aureus endoribonuclease III in gene expression. PLoS Genet 8: e1002782.
26. Redko Y, Condon C, (2010) Maturation of 23S rRNA in Bacillus subtilis in the absence of Mini-III. J Bacteriol 192: 356-359.
27. Reiter NJ, Osterman A, Torres-Larios A, Swinger KK, Pan T, et al. (2010) Structure of a bacterial ribonuclease P holoenzyme in complex with tRNA. Nature 468: 784-789.
28. Howden BP, Beaume M, Harrison PF, Hernandez D, Schrenzel J, et al. (2013) Analysis of the Small RNA Transcriptional Response in Multidrug-Resistant Staphylococcus aureus after Antimicrobial Exposure. Antimicrob Agents Chemother 57: 3864-3874.
29. Daou-Chabo R, Mathy N, Benard L, Condon C, (2009) Ribosomes initiating translation of the hbs mRNA protect it from 5′-to-3′ exoribonucleolytic degradation by RNase J1. Mol Microbiol 71: 1538-1550.
30. Zuker M, (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415.
31. Kazantsev AV, Krivenko AA, Harrington DJ, Holbrook SR, Adams PD, et al. (2005) Crystal structure of a bacterial ribonuclease P RNA. Proc Natl Acad Sci U S A 102: 13392-13397.
32. Oun S, Redder P, Didier JP, Francois P, Corvaglia AR, et al. (2013) The CshA DEAD-box RNA helicase is important for quorum sensing control in Staphylococcus aureus. RNA Biol 10: 157-165.