A Non-Coding RNA Promotes Bacterial Persistence and Decreases Virulence by Regulating a Regulator in Staphylococcus aureus

PLoS Pathogens

Volumn 10, Issue 3, 2014, Pages

  Romilly, Cédric ^a,h   Lays, Claire ^b,c,d,e   Tomasini, Arnaud ^a   Caldelari, Isabelle ^a   Benito, Yvonne ^b,c,d,e,f   Hammann, Philippe ^g   Geissmann, Thomas ^b,c,d,e   Boisset, Sandrine ^b,c,d,e,f   Romby, Pascale ^a   Vandenesch, François ^b,c,d,e,f  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^c UNIVERSITÉ DE LYON   (France)

^d UNIVERSITÉ LYON 1   (France)

^e CNRS   (France)

^f HOSPICES CIVILS DE LYON   (France)

^g INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^h UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; MGRA REGULATOR PROTEIN; REGULATOR PROTEIN; RSAA; SMALL UNTRANSLATED RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CAPSULE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BINDING SITE; BIOFILM; CATHETER INFECTION; COMMENSAL; CONTROLLED STUDY; FEMALE; HOST PATHOGEN INTERACTION; MASS SPECTROMETRY; MOUSE; NEUTROPHIL; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; OPSONIZATION; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN RNA BINDING; PROTEOMICS; QUORUM SENSING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PROCESSING; RNA RNA HYBRIDIZATION; RNA TRANSCRIPTION; SAPROTROPH; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; WESTERN BLOTTING;

ANIMALS; BACTEREMIA; BACTERIAL PROTEINS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CATHETER-RELATED INFECTIONS; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PARASITE INTERACTIONS; MICE; MICE, INBRED C57BL; PROTEOMICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, BACTERIAL; RNA, UNTRANSLATED; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE;

EID: 84897385784     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003979     Document Type: Article

References (61)

1. Chambers HF, Deleo FR, (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7: 629-641.
2. Priest NK, Rudkin JK, Feil EJ, van den Elsen JM, Cheung A, et al. (2012) From genotype to phenotype: can systems biology be used to predict Staphylococcus aureus virulence? Nat Rev Microbiol 10: 791-797.
3. Novick RP, Geisinger E, (2008) Quorum sensing in staphylococci. Annu Rev Genet 42: 541-564.
4. Felden B, Vandenesch F, Bouloc P, Romby P, (2011) The Staphylococcus aureus RNome and its commitment to virulence. PLoS Pathog 7: e1002006.
5. Romilly C, Caldelari I, Parmentier D, Lioliou E, Romby P, et al. (2012) Current knowledge on regulatory RNAs and their machineries in Staphylococcus aureus. RNA Biol 9: 402-413.
6. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, et al. (1993) Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 12: 3967-3975.
7. Morfeldt E, Taylor D, von Gabain A, Arvidson S, (1995) Activation of alpha-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J 14: 4569-4577.
8. Geisinger E, Adhikari RP, Jin R, Ross HF, Novick RP, (2006) Inhibition of rot translation by RNAIII, a key feature of agr function. Mol Microbiol 61: 1038-1048.
9. Huntzinger E, Boisset S, Saveanu C, Benito Y, Geissmann T, et al. (2005) Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J 24: 824-835.
10. Boisset S, Geissmann T, Huntzinger E, Fechter P, Bendridi N, et al. (2007) Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 21: 1353-1366.
11. Chevalier C, Boisset S, Romilly C, Masquida B, Fechter P, et al. (2010) Staphylococcus aureus RNAIII binds to two distant regions of coa mRNA to arrest translation and promote mRNA degradation. PLoS Pathog 6: e1000809.
12. Pichon C, Felden B, (2005) Small RNA genes expressed from Staphylococcus aureus genomic and pathogenicity islands with specific expression among pathogenic strains. Proc Natl Acad Sci USA 102: 14249-14254.
13. 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.
14. Beaume M, Hernandez D, Farinelli L, Deluen C, Linder P, et al. (2010) Cartography of methicillin-resistant S. aureus transcripts: detection, orientation and temporal expression during growth phase and stress conditions. PLoS One 5: e10725.
15. Nielsen JS, Larsen MH, Lillebaek EM, Bergholz TM, Christiansen MH, et al. (2011) A small RNA controls expression of the chitinase ChiA in Listeria monocytogenes. PLoS One 6: e19019.
16. Sayed N, Jousselin A, Felden B, (2012) A cis-antisense RNA acts in trans in Staphylococcus aureus to control translation of a human cytolytic peptide. Nat Struct Mol Biol 19: 105-112.
17. Sayed N, Nonin-Lecomte S, Rety S, Felden B, (2012) Functional and structural insights of a Staphylococcus aureus apoptotic-like membrane peptide from a toxin-antitoxin module. J Biol Chem 287: 43454-43463.
18. 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.
19. Abu-Qatouseh LF, Chinni SV, Seggewiss J, Proctor RA, Brosius J, et al. (2010) Identification of differentially expressed small non-protein-coding RNAs in Staphylococcus aureus displaying both the normal and the small-colony variant phenotype. J Mol Med (Berl) 88: 565-575.
20. Geissmann T, Marzi S, Romby P, (2009) The role of mRNA structure in translational control in bacteria. RNA Biol 6: 153-160.
21. Bohn C, Rigoulay C, Chabelskaya S, Sharma CM, Marchais A, et al. (2010) Experimental discovery of small RNAs in Staphylococcus aureus reveals a riboregulator of central metabolism. Nucleic Acids Res 38: 6620-6636.
22. Lasa I, Toledo-Arana A, Dobin A, Villanueva M, de los Mozos IR, et al. (2011) Genome-wide antisense transcription drives mRNA processing in bacteria. Proc Natl Acad Sci USA 108: 20172-20177.
23. 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.
24. Luong TT, Newell SW, Lee CY, (2003) Mgr, a novel global regulator in Staphylococcus aureus. J Bacteriol 185: 3703-3710.
25. Ingavale S, van Wamel W, Luong TT, Lee CY, Cheung AL, (2005) Rat/MgrA, a regulator of autolysis, is a regulator of virulence genes in Staphylococcus aureus. Infect Immun 73: 1423-1431.
26. Luong TT, Dunman PM, Murphy E, Projan SJ, Lee CY, (2006) Transcription Profiling of the mgrA Regulon in Staphylococcus aureus. J Bacteriol 188: 1899-1910.
27. Ingavale SS, Van Wamel W, Cheung AL, (2003) Characterization of RAT, an autolysis regulator in Staphylococcus aureus. Mol Microbiol 48: 1451-1466.
28. Gupta RK, Alba J, Xiong YQ, Bayer AS, Lee CY, (2013) MgrA activates expression of capsule genes, but not the alpha-toxin gene in experimental Staphylococcus aureus endocarditis. J Infect Dis.
29. Meier S, Goerke C, Wolz C, Seidl K, Homerova D, et al. (2007) sigmaB and the sigmaB-dependent arlRS and yabJ-spoVG loci affect capsule formation in Staphylococcus aureus. Infect Immun 75: 4562-4571.
30. Busch A, Richter AS, Backofen R, (2008) IntaRNA: efficient prediction of bacterial sRNA targets incorporating target site accessibility and seed regions. Bioinformatics 24: 2849-2856.
31. Tjaden B, (2008) TargetRNA: a tool for predicting targets of small RNA action in bacteria. Nucleic Acids Res 36: W109-13.
32. Trotonda MP, Tamber S, Memmi G, Cheung AL, (2008) MgrA represses biofilm formation in Staphylococcus aureus. Infect Immun 76: 5645-5654.
33. Luong TT, Lee CY, (2006) The arl locus positively regulates Staphylococcus aureus type 5 capsule via an mgrA-dependent pathway. Microbiology 152: 3123-3131.
34. Vuong C, Voyich JM, Fischer ER, Braughton KR, Whitney AR, et al. (2004) Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell Microbiol 6: 269-275.
35. Thakker M, Park JS, Carey V, Lee JC, (1998) Staphylococcus aureus serotype 5 capsular polysaccharide is antiphagocytic and enhances bacterial virulence in a murine bacteremia model. Infect Immun 66: 5183-5189.
36. Xu S, Arbeit RD, Lee JC, (1992) Phagocytic killing of encapsulated and microencapsulated Staphylococcus aureus by human polymorphonuclear leukocytes. Infect Immun 60: 1358-1362.
37. Marincola G, Schafer T, Behler J, Bernhardt J, Ohlsen K, et al. (2012) RNase Y of Staphylococcus aureus and its role in the activation of virulence genes. Mol Microbiol 85: 817-832.
38. Ballal A, Manna AC, (2009) Expression of the sarA family of genes in different strains of Staphylococcus aureus. Microbiology 155: 2342-2352.
39. Wagner EG, Altuvia S, Romby P, (2002) Antisense RNAs in bacteria and their genetic elements. Adv Genet 46: 361-398.
40. Lioliou E, Sharma CM, Altuvia Y, Caldelari I, Romilly C, et al. (2013) In vivo mapping of RNA-RNA interactions in Staphylococcus aureus using the endoribonuclease III. Methods 63: 135-143.
41. Bischoff M, Dunman P, Kormanec J, Macapagal D, Murphy E, et al. (2004) Microarray-based analysis of the Staphylococcus aureus sigmaB regulon. J Bacteriol 186: 4085-4099.
42. Rashid MH, Rumbaugh K, Passador L, Davies DG, Hamood AN, et al. (2000) Polyphosphate kinase is essential for biofilm development, quorum sensing, and virulence of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 97: 9636-9641.
43. Valle J, Toledo-Arana A, Berasain C, Ghigo JM, Amorena B, et al. (2003) SarA and not sigmaB is essential for biofilm development by Staphylococcus aureus. Mol Microbiol 48: 1075-1087.
44. Sun F, Ding Y, Ji Q, Liang Z, Deng X, et al. (2012) Protein cysteine phosphorylation of SarA/MgrA family transcriptional regulators mediates bacterial virulence and antibiotic resistance. Proc Natl Acad Sci USA 109: 15461-15466.
45. Moscoso M, Garcia E, Lopez R, (2006) Biofilm formation by Streptococcus pneumoniae: role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion. J Bacteriol 188: 7785-7795.
46. Flahaut S, Vinogradov E, Kelley KA, Brennan S, Hiramatsu K, et al. (2008) Structural and biological characterization of a capsular polysaccharide produced by Staphylococcus haemolyticus. J Bacteriol 190: 1649-1657.
47. Novick RP, Christie GE, Penades JR, (2010) The phage-related chromosomal islands of Gram-positive bacteria. Nat Rev Microbiol 8: 541-551.
48. Maurelli AT, (2007) Black holes, antivirulence genes, and gene inactivation in the evolution of bacterial pathogens. FEMS Microbiol Lett 267: 1-8.
49. Bliven KA, Maurelli AT, (2012) Antivirulence genes: insights into pathogen evolution through gene loss. Infect Immun 80: 4061-4070.
50. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, et al. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459: 950-956.
51. Baek CH, Wang S, Roland KL, Curtiss Rr, (2009) Leucine-responsive regulatory protein (Lrp) acts as a virulence repressor in Salmonella enterica serovar Typhimurium. J Bacteriol 191: 1278-1292.
52. Lee EJ, Groisman EA, (2010) An antisense RNA that governs the expression kinetics of a multifunctional virulence gene. Mol Microbiol 76: 1020-1033.
53. Song J, Lays C, Vandenesch F, Benito Y, Bes M, et al. (2012) The expression of small regulatory RNAs in clinical samples reflects the different life styles of Staphylococcus aureus in colonization vs. infection. PLoS One 7: e37294.
54. Kreiswirth BN, Lofdahl S, Betley MJ, O'Reilly M, Schlievert PM, et al. (1983) The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305: 709-712.
55. Arnaud M, Chastanet A, Debarbouille M, (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70: 6887-6891.
56. Chevalier C, Geissmann T, Helfer AC, Romby P, (2009) Probing mRNA structure and sRNA-mRNA interactions in bacteria using enzymes and lead(II). Methods Mol Biol 540: 215-232.
57. Fechter P, Chevalier C, Yusupova G, Yusupov M, Romby P, et al. (2009) Ribosomal initiation complexes probed by toeprinting and effect of trans-acting translational regulators in bacteria. Methods Mol Biol 540: 247-263.
58. Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, et al. (1996) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20: 1083-1091.
59. Chavant P, Gaillard-Martinie B, Talon R, Hebraud M, Bernardi T, (2007) A new device for rapid evaluation of biofilm formation potential by bacteria. J Microbiol Methods 68: 605-612.
60. Cucarella C, Solano C, Valle J, Amorena B, Lasa I, et al. (2001) Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183: 2888-2896.
61. Kristian SA, Birkenstock TA, Sauder U, Mack D, Gotz F, et al. (2008) Biofilm formation induces C3a release and protects Staphylococcus aureus from IgG and complement deposition and from neutrophil-dependent killing. J Infect Dis 197: 1028-1035.