Novel aspects of RNA regulation in Staphylococcus aureus

FEBS Letters

Volumn 588, Issue 15, 2014, Pages 2523-2529

  Fechter, Pierre ^a   Caldelari, Isabelle ^a   Lioliou, Efthimia ^a   Romby, Pascale ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Post transcriptional regulation; Regulatory RNAs; Staphylococcus aureus; Virulence

Indexed keywords

BACTERIAL RNA; CIS ACTING ELEMENT; PEPTIDE; REGULATOR PROTEIN; RNA; TRANS ACTING RNA; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; HOST PATHOGEN INTERACTION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; RNA BINDING; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS;

POST-TRANSCRIPTIONAL REGULATION; REGULATORY RNAS; STAPHYLOCOCCUS AUREUS; VIRULENCE;

GENE EXPRESSION REGULATION, BACTERIAL; QUORUM SENSING; RNA, BACTERIAL; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION, GENETIC; VIRULENCE;

EID: 84904253051     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.05.037     Document Type: Review

References (69)

1. T.R. Cech, and J.A. Steitz The noncoding RNA revolution-trashing old rules to forge new ones Cell 157 1 2014 77 94
2. I. Caldelari, Y. Chao, P. Romby, and J. Vogel RNA-mediated regulation in pathogenic bacteria Cold Spring Harb. Perspect. Med. 3 2013 a010298
3. G. Storz, J. Vogel, and K.M. Wassarman Regulation by small RNAs in bacteria: expanding frontiers Mol. Cell 43 2011 880 891
4. P.C. Fineran, and E. Charpentier Memory of viral infections by CRISPR-Cas adaptive immune systems: acquisition of new information Virology 434 2012 202 209
5. S.S. Krajewski, and F. Narberhaus Temperature-driven differential gene expression by RNA thermosensors Biochim. Biophys. Acta 2014 10.1016/j.bbagrm. 2014.03.006 in press, pii: S1874-9399(14)00058-3
6. A. Serganov, and E. Nudler A decade of riboswitches Cell 152 2013 17 24
7. E. Loh, O. Dussurget, J. Gripenland, K. Vaitkevicius, T. Tiensuu, P. Mandin, F. Repoila, C. Buchrieser, P. Cossart, and J. Johansson A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes Cell 139 2009 770 779
8. J.R. Mellin, T. Tiensuu, C. Becavin, E. Gouin, J. Johansson, and P. Cossart A riboswitch-regulated antisense RNA in Listeria monocytogenes Proc. Natl. Acad. Sci. U.S.A. 110 2013 13132 13137
9. J. Mulhbacher, P. St-Pierre, and D.A. Lafontaine Therapeutic applications of ribozymes and riboswitches Curr. Opin. Pharmacol. 10 2010 551 556
10. J. Vazquez-Anderson, and L.M. Contreras Regulatory RNAs: charming gene management styles for synthetic biology applications RNA Biol. 10 2013 1778 1797
11. A. Tomasini, P. Francois, B.P. Howden, P. Fechter, P. Romby, and I. Caldelari The importance of regulatory RNAs in Staphylococcus aureus Infect. Genet. Evol. 21 2014 616 626
12. I. Lasa, A. Toledo-Arana, and T.R. Gingeras An effort to make sense of antisense transcription in bacteria RNA Biol. 9 2012 1039 1044
13. J. Guillet, M. Hallier, and B. Felden Emerging functions for the Staphylococcus aureus RNome PLoS Pathog. 9 2013 e1003767
14. B. Felden, F. Vandenesch, P. Bouloc, and P. Romby The Staphylococcus aureus RNome and its commitment to virulence PLoS Pathog. 7 2011 e1002006
15. H.F. Chambers, and F.R. Deleo Waves of resistance: Staphylococcus aureus in the antibiotic era Nat. Rev. Microbiol. 7 2009 629 641
16. R.P. Novick, and E. Geisinger Quorum sensing in staphylococci Annu. Rev. Genet. 42 2008 541 564
17. R.P. Novick Autoinduction and signal transduction in the regulation of staphylococcal virulence Mol. Microbiol. 48 2003 1429 1449
18. N.K. Priest, J.K. Rudkin, E.J. Feil, J.M. van den Elsen, A. Cheung, S.J. Peacock, M. Laabei, D.A. Lucks, M. Recker, and R.C. Massey From genotype to phenotype: can systems biology be used to predict Staphylococcus aureus virulence? Nat. Rev. Microbiol. 10 2012 791 797
19. S.Y. Queck, M. Jameson-Lee, A.E. Villaruz, T.H. Bach, B.A. Khan, D.E. Sturdevant, S.M. Ricklefs, M. Li, and M. Otto RNAIII-independent target gene control by the agr quorum-sensing system: insight into the evolution of virulence regulation in Staphylococcus aureus Mol. Cell 32 2008 150 158
20. Y. Benito, G. Lina, T. Greenland, J. Etienne, and F. Vandenesch Trans-complementation of a Staphylococcus aureus agr mutant by Staphylococcus lugdunensis agr RNAIII J. Bacteriol. 180 1998 5780 5783
21. N. Balaban, and R.P. Novicl Translation of RNAIII, the Staphylococcus aureus agr regulatory RNA molecule, can be activated by a 3′-end deletion FEMS Microbiol. Lett. 133 1995 155 161
22. E. Huntzinger, S. Boisset, C. Saveanu, Y. Benito, T. Geissmann, A. Namane, G. Lina, J. Etienne, B. Ehresmann, C. Ehresmann, A. Jacquier, F. Vandenesch, and P. Romby Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression EMBO J. 24 2005 824 835
23. C. Chevalier, S. Boisset, C. Romilly, B. Masquida, P. Fechter, T. Geissmann, F. Vandenesch, and P. Romby Staphylococcus aureus RNAIII binds to two distant regions of coa mRNA to arrest translation and promote mRNA degradation PLoS Pathog. 6 2010 e1000809
24. S. Boisset, T. Geissmann, E. Huntzinger, P. Fechter, N. Bendridi, M. Possedko, C. Chevalier, A.C. Helfer, Y. Benito, A. Jacquier, C. Gaspin, F. Vandenesch, and P. Romby Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism Genes Dev. 21 2007 1353 1366
25. S. Chabelskaya, V. Bordeau, and B. Felden Dual RNA regulatory control of a Staphylococcus aureus virulence factor Nucleic Acids Res. 42 2014 4847 4858
26. A. Eyraud, P. Tattevin, S. Chabelskaya, and B. Felden A small RNA controls a protein regulator involved in antibiotic resistance in Staphylococcus aureus Nucleic Acids Res. 42 2014 4892 4905
27. E.J. Smith, L. Visai, S.W. Kerrigan, P. Speziale, and T.J. Foster The Sbi protein is a multifunctional immune evasion factor of Staphylococcus aureus Infect. Immun. 79 2011 3801 3809
28. E. Geisinger, R.P. Adhikari, R. Jin, H.F. Ross, and R.P. Novick Inhibition of rot translation by RNAIII, a key feature of agr function Mol. Microbiol. 61 2006 1038 1048
29. C.L. Beisel, and G. Storz Base pairing small RNAs and their roles in global regulatory networks FEMS Microbiol. Rev. 34 2010 866 882
30. M. Chunhua, L. Yu, G. Yaping, D. Jie, L. Qiang, T. Xiaorong, and Y. Guang The expression of LytM is down-regulated by RNAIII in Staphylococcus aureus J. Basic Microbiol. 52 2012 636 641
31. J. Song, C. Lays, F. Vandenesch, Y. Benito, M. Bes, Y. Chu, G. Lina, P. Romby, T. Geissmann, and S. Boisset The expression of small regulatory RNAs in clinical samples reflects the different life styles of Staphylococcus aureus in colonization vs. infection PLoS ONE 7 2012 e37294
32. S. Oun, P. Redder, J.P. Didier, P. Francois, A.R. Corvaglia, E. Buttazzoni, C. Giraud, M. Girard, J. Schrenzel, and P. Linder The CshA DEAD-box RNA helicase is important for quorum sensing control in Staphylococcus aureus RNA Biol. 10 2013 157 165
33. E. Levine, Z. Zhang, T. Kuhlman, and T. Hwa Quantitative characteristics of gene regulation by small RNA PLoS Biol. 5 2007 e229
34. Y. Shimoni, G. Friedlander, G. Hetzroni, G. Niv, S. Altuvia, O. Biham, and H. Margalit Regulation of gene expression by small non-coding RNAs: a quantitative view Mol. Syst. Biol. 3 2007 138
35. C. Pichon, and B. Felden Small RNA genes expressed from Staphylococcus aureus genomic and pathogenicity islands with specific expression among pathogenic strains Proc. Natl. Acad. Sci. U.S.A 102 2005 14249 14254
36. S. Chabelskaya, O. Gaillot, and B. Felden A Staphylococcus aureus small RNA is required for bacterial virulence and regulates the expression of an immune-evasion molecule PLoS Pathog. 6 2010 e1000927
37. E.B. Gogol, V.A. Rhodius, K. Papenfort, J. Vogel, and C.A. Gross Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon Proc. Natl. Acad. Sci. U.S.A. 108 2011 12875 12880
38. T. Xue, X. Zhang, H. Sun, and B. Sun ArtR, a novel sRNA of Staphylococcus aureus, regulates alpha-toxin expression by targeting the 5′ UTR of sarT mRNA Med. Microbiol. Immunol. 203 2014 1 12
39. A.L. Cheung, A.S. Bayer, G. Zhang, H. Gresham, and Y.Q. Xiong Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus FEMS Immunol. Med. Microbiol. 40 2004 1 9
40. K.A. Schmidt, A.C. Manna, and A.L. Cheung SarT influences sarS expression in Staphylococcus aureus Infect. Immun. 71 2003 5139 5148
41. X. Han, H. Bai, L. Liu, H. Dong, R. Liu, J. Song, C. Ding, K. Qi, H. Liu, and S. Yu The luxS gene functions in the pathogenesis of avian pathogenic Escherichia coli Microb. Pathog. 55 2013 21 27
42. D. Yu, L. Zhao, T. Xue, and B. Sun Staphylococcus aureus autoinducer-2 quorum sensing decreases biofilm formation in an icaR-dependent manner BMC Microbiol. 12 2012 288
43. C. Kaito, Y. Saito, M. Ikuo, Y. Omae, H. Mao, G. Nagano, T. Fujiyuki, S. Numata, X. Han, K. Obata, S. Hasegawa, H. Yamaguchi, K. Inokuchi, T. Ito, K. Hiramatsu, and K. Sekimizu Mobile genetic element SCCmec-encoded psm-mec RNA suppresses translation of agrA and attenuates MRSA virulence PLoS Pathog. 9 2013 e1003269
44. L. Tuchscherr, B. Loffler, F.R. Buzzola, and D.O. Sordelli Staphylococcus aureus adaptation to the host and persistence: role of loss of capsular polysaccharide expression Future Microbiol. 5 2010 1823 1832
45. R.K. Gupta, J. Alba, Y.Q. Xiong, A.S. Bayer, and C.Y. Lee MgrA activates expression of capsule genes, but not the alpha-toxin gene in experimental Staphylococcus aureus endocarditis J. Infect. Dis. 208 2013 1841 1848
46. C. Romilly, C. Lays, A. Tomasini, I. Caldelari, Y. Benito, P. Hammann, T. Geissmann, S. Boisset, P. Romby, and F. Vandenesch A non-coding RNA promotes bacterial persistence and decreases virulence by regulating a regulator in Staphylococcus aureus PLoS Pathog. 10 2014 e1003979
47. T. Geissmann, S. Marzi, and P. Romby A search for small noncoding RNAs in Staphylococcus aureus reveals a conserved sequence motif for regulation Nucleic Acids Res. 37 2009 7239 7259
48. M. Bischoff, P. Dunman, J. Kormanec, D. Macapagal, E. Murphy, W. Mounts, B. Berger-Bachi, and S. Projan Microarray-based analysis of the Staphylococcus aureus sigmaB regulon J. Bacteriol. 186 2004 4085 4099
49. T.T. Luong, P.M. Dunman, E. Murphy, S.J. Projan, and C.Y. Lee Transcription profiling of the mgrA regulon in Staphylococcus aureus J. Bacteriol. 188 2006 1899 1910
50. S. Ingavale, W. van Wamel, T.T. Luong, C.Y. Lee, and A.L. Cheung Rat/MgrA, a regulator of autolysis, is a regulator of virulence genes in Staphylococcus aureus Infect. Immun. 73 2005 1423 1431
51. S.S. Ingavale, W. Van Wamel, and A.L. Cheung Characterization of RAT, an autolysis regulator in Staphylococcus aureus Mol. Microbiol. 48 2003 1451 1466
52. T. Geissmann, S. Marzi, and P. Romby The role of mRNA structure in translational control in bacteria RNA Biol. 6 2009 153 160
53. I. Ruiz de los Mozos, M. Vergara-Irigaray, V. Segura, M. Villanueva, N. Bitarte, M. Saramago, S. Domingues, C.M. Arraiano, P. Fechter, P. Romby, J. Valle, C. Solano, I. Lasa, and A. Toledo-Arana Base pairing interaction between 5′- and 3′-UTRs controls icaR mRNA translation in Staphylococcus aureus PLoS Genet. 9 2013 e1004001
54. N.J. ten Broeke-Smits, T.E. Pronk, I. Jongerius, O. Bruning, F.R. Wittink, T.M. Breit, J.A. van Strijp, A.C. Fluit, and C.H. Boel Operon structure of Staphylococcus aureus Nucleic Acids Res. 38 2010 3263 3274
55. I. Lasa, A. Toledo-Arana, A. Dobin, M. Villanueva, I.R. de Los Mozos, M. Vergara-Irigaray, V. Segura, D. Fagegaltier, J.R. Penades, J. Valle, C. Solano, and T.R. Gingeras Genome-wide antisense transcription drives mRNA processing in bacteria Proc. Natl. Acad. Sci. U.S.A. 108 2011 20172 20177
56. E. Lioliou, C.M. Sharma, I. Caldelari, A.C. Helfer, P. Fechter, F. Vandenesch, J. Vogel, and P. Romby Global regulatory functions of the Staphylococcus aureus endoribonuclease III in gene expression PLoS Genet. 8 2012 e1002782
57. M.L. Pinel-Marie, R. Brielle, and B. Felden Dual toxic-peptide-coding Staphylococcus aureus RNA under antisense regulation targets host cells and bacterial rivals unequally Cell Rep. 16 2014 155 167
58. T. Dorr, M. Vulic, and K. Lewis Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli PLoS Biol. 8 2010 e1000317
59. N.Q. Balaban, K. Gerdes, K. Lewis, and J.D. McKinney A problem of persistence: still more questions than answers? Nat. Rev. Microbiol. 11 2013 587 591
60. O. Wurtzel, N. Sesto, J.R. Mellin, I. Karunker, S. Edelheit, C. Becavin, C. Archambaud, P. Cossart, and R. Sorek Comparative transcriptomics of pathogenic and non-pathogenic Listeria species Mol. Syst. Biol. 8 2012 583
61. N. Sesto, O. Wurtzel, C. Archambaud, R. Sorek, and P. Cossart The excludon: a new concept in bacterial antisense RNA-mediated gene regulation Nat. Rev. Microbiol. 11 2013 75 82
62. I. Caldelari, P. Fechter, E. Lioliou, C. Romilly, C. Chevalier, C. Gaspin, and P. Romby A current overview of regulatory RNAs in Staphylococcus aureus A. Marchfelder, W. Hess, Regulatory RNAs in Prokaryotes 2011 Springer-Verlag Wien and New York 51 75
63. C.R. Arciola, D. Campoccia, P. Speziale, L. Montanaro, and J.W. Costerton Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials Biomaterials 33 2012 5967 5982
64. Y. Chao, K. Papenfort, R. Reinhardt, C.M. Sharma, and J. Vogel An atlas of Hfq-bound transcripts reveals 3′ UTRs as a genomic reservoir of regulatory small RNAs EMBO J. 31 2012 4005 4019
65. J.M. Morrison, K.L. Anderson, K.E. Beenken, M.S. Smeltzer, and P.M. Dunman The staphylococcal accessory regulator, SarA, is an RNA-binding protein that modulates the mRNA turnover properties of late-exponential and stationary phase Staphylococcus aureus cells Front. Cell. Infect. Microbiol. 2 2012 26
66. G. Marincola, T. Schäfer, J. Behler, J. Bernhardt, K. Ohlsen, C. Goerke, and C. Wolz RNase Y of Staphylococcus aureus and its role in the activation of virulence gene Mol. Microbiol. 85 2012 817 832
67. P. Linder, S. Lemeille, and P. Redder 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 Genet. 10 2014 e1004207
68. A.J. Westermann, S.A. Gorski, and J. Vogel Dual RNA-seq of pathogen and host Nat. Rev. Microbiol. 10 2012 618 630
69. N.T. Ingolia Ribosome profiling: new views of translation, from single codons to genome scale Nat. Rev. Genet. 15 2014 205 213