Emerging Functions for the Staphylococcus aureus RNome

PLoS Pathogens

Volumn 9, Issue 12, 2013, Pages 1-13

  Guillet, Julien ^a   Hallier, Marc ^a   Felden, Brice ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID; MICRORNA; TRANSCRIPTION FACTOR; TRANSFER RNA; BACTERIAL RNA; COMPLEMENTARY RNA; SMALL INTERFERING RNA; TRANSCRIPTOME;

5' UNTRANSLATED REGION; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; ENVIRONMENTAL STRESS; HOSPITAL INFECTION; HUMAN; METABOLISM; NONHUMAN; OPEN READING FRAME; PATHOGENICITY ISLAND; PROTEIN EXPRESSION; REGULATORY RNA SEQUENCE; REVIEW; RNA BINDING; RNA TRANSLATION; SEQUENCE HOMOLOGY; STAPHYLOCOCCUS AUREUS; TRANS SPLICING; ANIMAL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; MICROBIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; STAPHYLOCOCCUS INFECTION;

ANIMALS; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; HUMANS; RNA, ANTISENSE; RNA, BACTERIAL; RNA, SMALL INTERFERING; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

EID: 84892854028     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003767     Document Type: Review

References (123)

1. David MZ, Daum RS, (2010) Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23: 616-687.
2. Xu SX, McCormick JK, (2012) Staphylococcal superantigens in colonization and disease. Front Cell Infect Microbiol 2: 52.
3. Morrison JM, Miller EW, Benson MA, Alonzo F 3rd, Yoong P, et al. (2012) Characterization of SSR42, a novel virulence factor regulatory RNA that contributes to the pathogenesis of a Staphylococcus aureus USA300 representative. J Bacteriol 194: 2924-2938.
4. Roux CM, DeMuth JP, Dunman PM, (2011) Characterization of components of the Staphylococcus aureus mRNA degradosome holoenzyme-like complex. J Bacteriol 193: 5520-5526.
5. 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 U S A 108: 20172-20177.
6. Felden B, Vandenesch F, Bouloc P, Romby P, (2011) The Staphylococcus aureus RNome and its commitment to virulence. PLoS Pathog 7: e1002006 doi:10.1371/journal.ppat.1002006.
7. 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.
8. 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.
9. Anderson KL, Roberts C, Disz T, Vonstein V, Hwang K, et al. (2006) Characterization of the Staphylococcus aureus heat shock, cold shock, stringent, and SOS responses and their effects on log-phase mRNA turnover. J Bacteriol 188: 6739-6756.
10. 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 doi:10.1371/journal.pone.0010725.
11. 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.
12. Geissmann T, Chevalier C, Cros MJ, Boisset S, Fechter P, et al. (2009) A search for small noncoding RNAs in Staphylococcus aureus reveals a conserved sequence motif for regulation. Nucleic Acids Res 37: 7239-7257.
13. Novick RP, Iordanescu S, Projan SJ, Kornblum J, Edelman I, (1989) pT181 plasmid replication is regulated by a countertranscript-driven transcriptional attenuator. Cell 59: 395-404.
14. 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.
15. 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 U S A 102: 14249-14254.
16. Gottesman S, Storz G, (2011) Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol 3: a003798.
17. Waters LS, Storz G, (2009) Regulatory RNAs in bacteria. Cell 136: 615-628.
18. Storz G, Vogel J, Wassarman KM, (2011) Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 43: 880-891.
19. Papenfort K, Vogel J, (2010) Regulatory RNA in bacterial pathogens. Cell Host Microbe 8: 116-127.
20. Romby P, Vandenesch F, Wagner EG, (2006) The role of RNAs in the regulation of virulence-gene expression. Curr Opin Microbiol 9: 229-236.
21. Gaballa A, Antelmann H, Aguilar C, Khakh SK, Song KB, et al. (2008) The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins. Proc Natl Acad Sci U S A 105: 11927-11932.
22. Mandin P, Repoila F, Vergassola M, Geissmann T, Cossart P, (2007) Identification of new noncoding RNAs in Listeria monocytogenes and prediction of mRNA targets. Nucleic Acids Res 35: 962-974.
23. Nielsen JS, Olsen AS, Bonde M, Valentin-Hansen P, Kallipolitis BH, (2008) Identification of a sigma B-dependent small noncoding RNA in Listeria monocytogenes. J Bacteriol 190: 6264-6270.
24. 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.
25. Fozo EM, Hemm MR, Storz G, (2008) Small toxic proteins and the antisense RNAs that repress them. Microbiol Mol Biol Rev 72: 579-589.
26. Fozo EM, Makarova KS, Shabalina SA, Yutin N, Koonin EV, et al. (2010) Abundance of type I toxin-antitoxin systems in bacteria: searches for new candidates and discovery of novel families. Nucleic Acids Res 38: 3743-3759.
27. Sayed N, Jousselin A, Felden B, (2011) 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.
28. 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.
29. Greenfield TJ, Ehli E, Kirshenmann T, Franch T, Gerdes K, et al. (2000) The antisense RNA of the par locus of pAD1 regulates the expression of a 33-amino-acid toxic peptide by an unusual mechanism. Mol Microbiol 37: 652-660.
30. Dulebohn D, Choy J, Sundermeier T, Okan N, Karzai AW, (2007) Trans-translation: the tmRNA-mediated surveillance mechanism for ribosome rescue, directed protein degradation, and nonstop mRNA decay. Biochemistry 46: 4681-4693.
31. Gillet R, Felden B, (2001) Emerging views on tmRNA-mediated protein tagging and ribosome rescue. Mol Microbiol 42: 879-885.
32. Haebel PW, Gutmann S, Ban N, (2004) Dial tm for rescue: tmRNA engages ribosomes stalled on defective mRNAs. Curr Opin Struct Biol 14: 58-65.
33. Keiler KC, (2008) Biology of trans-translation. Annu Rev Microbiol 62: 133-151.
34. Liu Y, Wu N, Dong J, Gao Y, Zhang X, et al. (2010) SsrA (tmRNA) acts as an antisense RNA to regulate Staphylococcus aureus pigment synthesis by base pairing with crtMN mRNA. FEBS Lett 584: 4325-4329.
35. Novick RP, Geisinger E, (2008) Quorum sensing in staphylococci. Annu Rev Genet 42: 541-564.
36. Benito Y, Kolb FA, Romby P, Lina G, Etienne J, et al. (2000) 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 6: 668-679.
37. Kreger AS, Kim KS, Zaboretzky F, Bernheimer AW, (1971) Purification and properties of staphylococcal delta hemolysin. Infect Immun 3: 449-465.
38. Mellor IR, Thomas DH, Sansom MS, (1988) Properties of ion channels formed by Staphylococcus aureus delta-toxin. Biochim Biophys Acta 942: 280-294.
39. Verdon J, Berjeaud JM, Lacombe C, Hechard Y, (2008) Characterization of anti-Legionella activity of warnericin RK and delta-lysin I from Staphylococcus warneri. Peptides 29: 978-984.
40. 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.
41. Liu Y, Mu C, Ying X, Li W, Wu N, et al. (2011) RNAIII activates map expression by forming an RNA-RNA complex in Staphylococcus aureus. FEBS Lett 585: 899-905.
42. Chavakis T, Hussain M, Kanse SM, Peters G, Bretzel RG, et al. (2002) Staphylococcus aureus extracellular adherence protein serves as anti-inflammatory factor by inhibiting the recruitment of host leukocytes. Nat Med 8: 687-693.
43. 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.
44. 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 doi:10.1371/journal.ppat.1000809.
45. 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.
46. Link TM, Valentin-Hansen P, Brennan RG, (2009) Structure of Escherichia coli Hfq bound to polyriboadenylate RNA. Proc Natl Acad Sci U S A 106: 19292-19297.
47. Schumacher MA, Pearson RF, Moller T, Valentin-Hansen P, Brennan RG, (2002) Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein. Embo J 21: 3546-3556.
48. Bandyra KJ, Said N, Pfeiffer V, Gorna MW, Vogel J, et al. (2012) The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E. Mol Cell 47: 943-953.
49. Urban JH, Vogel J, (2007) Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res 35: 1018-1037.
50. Jousselin A, Metzinger L, Felden B, (2009) On the facultative requirement of the bacterial RNA chaperone, Hfq. Trends Microbiol 17: 399-405.
51. Bohn C, Rigoulay C, Bouloc P, (2007) No detectable effect of RNA-binding protein Hfq absence in Staphylococcus aureus. BMC Microbiol 7: 10.
52. 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.
53. Nielsen JS, Christiansen MH, Bonde M, Gottschalk S, Frees D, et al. (2011) Searching for small sigmaB-regulated genes in Staphylococcus aureus. Arch Microbiol 193: 23-34.
54. Liu Y, Wu N, Dong J, Gao Y, Zhang X, et al. (2010) Hfq is a global regulator that controls the pathogenicity of Staphylococcus aureus. PLoS One 5: e13069 doi:10.1371/journal.pone.0013069.
55. Castro SL, Nelman-Gonzalez M, Nickerson CA, Ott CM, (2011) Induction of attachment-independent biofilm formation and repression of Hfq expression by low-fluid-shear culture of Staphylococcus aureus. Appl Environ Microbiol 77: 6368-6378.
56. Salim NN, Faner MA, Philip JA, Feig AL, (2012) Requirement of upstream Hfq-binding (ARN)x elements in glmS and the Hfq C-terminal region for GlmS upregulation by sRNAs GlmZ and GlmY. Nucleic Acids Res 40: 8021-8032.
57. Chevalier C, Huntzinger E, Fechter P, Boisset S, Vandenesch F, et al. (2008) Staphylococcus aureus endoribonuclease III purification and properties. Methods Enzymol 447: 309-327.
58. Herskovitz MA, Bechhofer DH, (2000) Endoribonuclease RNase III is essential in Bacillus subtilis. Mol Microbiol 38: 1027-1033.
59. Stead MB, Marshburn S, Mohanty BK, Mitra J, Pena Castillo L, et al. (2011) Analysis of Escherichia coli RNase E and RNase III activity in vivo using tiling microarrays. Nucleic Acids Res 39: 3188-3203.
60. 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 doi:10.1371/journal.pgen.1002782.
61. Liu Y, Dong J, Wu N, Gao Y, Zhang X, et al. (2011) The production of extracellular proteins is regulated by ribonuclease III via two different pathways in Staphylococcus aureus. PLoS One 6: e20554 doi:10.1371/journal.pone.0020554.
62. Romilly C, Chevalier C, Marzi S, Masquida B, Geissmann T, et al. (2012) Loop-loop interactions involved in antisense regulation are processed by the endoribonuclease III in Staphylococcus aureus. RNA Biol 9: 1461-1472.
63. 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.
64. Lasa I, Toledo-Arana A, Gingeras TR, (2012) An effort to make sense of antisense transcription in bacteria. RNA Biol 9: 1039-1044.
65. Wurtzel O, Sesto N, Mellin JR, Karunker I, Edelheit S, et al. (2012) Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol Syst Biol 8: 583.
66. Sesto N, Wurtzel O, Archambaud C, Sorek R, Cossart P, (2013) The excludon: a new concept in bacterial antisense RNA-mediated gene regulation. Nat Rev Microbiol 11: 75-82.
67. Carpousis AJ, (2007) The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu Rev Microbiol 61: 71-87.
68. Lehnik-Habrink M, Newman J, Rothe FM, Solovyova AS, Rodrigues C, et al. (2011) RNase Y in Bacillus subtilis: a Natively disordered protein that is the functional equivalent of RNase E from Escherichia coli. J Bacteriol 193: 5431-5441.
69. 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.
70. 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.
71. Redder P, Linder P, (2012) DEAD-box RNA helicases in gram-positive RNA decay. Methods Enzymol 511: 369-383.
72. 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 doi:10.1371/journal.pgen.1002520.
73. Lehnik-Habrink M, Lewis RJ, Mader U, Stulke J, (2012) RNA degradation in Bacillus subtilis: an interplay of essential endo- and exoribonucleases. Mol Microbiol 84: 1005-1017.
74. Kaito C, Kurokawa K, Matsumoto Y, Terao Y, Kawabata S, et al. (2005) Silkworm pathogenic bacteria infection model for identification of novel virulence genes. Mol Microbiol 56: 934-944.
75. 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.
76. 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.
77. Pane-Farre J, Jonas B, Forstner K, Engelmann S, Hecker M, (2006) The sigmaB regulon in Staphylococcus aureus and its regulation. Int J Med Microbiol 296: 237-258.
78. Shaw LN, Aish J, Davenport JE, Brown MC, Lithgow JK, et al. (2006) Investigations into sigmaB-modulated regulatory pathways governing extracellular virulence determinant production in Staphylococcus aureus. J Bacteriol 188: 6070-6080.
79. Jonsson IM, Arvidson S, Foster S, Tarkowski A, (2004) Sigma factor B and RsbU are required for virulence in Staphylococcus aureus-induced arthritis and sepsis. Infect Immun 72: 6106-6111.
80. Pane-Farre J, Jonas B, Hardwick SW, Gronau K, Lewis RJ, et al. (2009) Role of RsbU in controlling SigB activity in Staphylococcus aureus following alkaline stress. J Bacteriol 191: 2561-2573.
81. Senn MM, Giachino P, Homerova D, Steinhuber A, Strassner J, et al. (2005) Molecular analysis and organization of the sigmaB operon in Staphylococcus aureus. J Bacteriol 187: 8006-8019.
82. Lauderdale KJ, Boles BR, Cheung AL, Horswill AR, (2009) Interconnections between Sigma B, agr, and proteolytic activity in Staphylococcus aureus biofilm maturation. Infect Immun 77: 1623-1635.
83. Horsburgh MJ, Wharton SJ, Cox AG, Ingham E, Peacock S, et al. (2002) MntR modulates expression of the PerR regulon and superoxide resistance in Staphylococcus aureus through control of manganese uptake. Mol Microbiol 44: 1269-1286.
84. Seidl K, Stucki M, Ruegg M, Goerke C, Wolz C, et al. (2006) Staphylococcus aureus CcpA affects virulence determinant production and antibiotic resistance. Antimicrob Agents Chemother 50: 1183-1194.
85. Zhu Y, Nandakumar R, Sadykov MR, Madayiputhiya N, Luong TT, et al. (2011) RpiR homologues may link Staphylococcus aureus RNAIII synthesis and pentose phosphate pathway regulation. J Bacteriol 193: 6187-6196.
86. Somerville GA, Chaussee MS, Morgan CI, Fitzgerald JR, Dorward DW, et al. (2002) Staphylococcus aureus aconitase inactivation unexpectedly inhibits post-exponential-phase growth and enhances stationary-phase survival. Infect Immun 70: 6373-6382.
87. Somerville GA, Said-Salim B, Wickman JM, Raffel SJ, Kreiswirth BN, et al. (2003) Correlation of acetate catabolism and growth yield in Staphylococcus aureus: implications for host-pathogen interactions. Infect Immun 71: 4724-4732.
88. Borezee-Durant E, Hiron A, Piard JC, Juillard V, (2009) Dual role of the oligopeptide permease Opp3 during growth of Staphylococcus aureus in milk. Appl Environ Microbiol 75: 3355-3357.
89. Hiron A, Borezee-Durant E, Piard JC, Juillard V, (2007) Only one of four oligopeptide transport systems mediates nitrogen nutrition in Staphylococcus aureus. J Bacteriol 189: 5119-5129.
90. Zhu Y, Xiong YQ, Sadykov MR, Fey PD, Lei MG, et al. (2009) Tricarboxylic acid cycle-dependent attenuation of Staphylococcus aureus in vivo virulence by selective inhibition of amino acid transport. Infect Immun 77: 4256-4264.
91. 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.
92. Oscarsson J, Harlos C, Arvidson S, (2005) Regulatory role of proteins binding to the spa (protein A) and sarS (staphylococcal accessory regulator) promoter regions in Staphylococcus aureus NTCC 8325-4. Int J Med Microbiol 295: 253-266.
93. Oscarsson J, Kanth A, Tegmark-Wisell K, Arvidson S, (2006) SarA is a repressor of hla (alpha-hemolysin) transcription in Staphylococcus aureus: its apparent role as an activator of hla in the prototype strain NCTC 8325 depends on reduced expression of sarS. J Bacteriol 188: 8526-8533.
94. Li D, Cheung A, (2008) Repression of hla by rot is dependent on sae in Staphylococcus aureus. Infect Immun 76: 1068-1075.
95. Jelsbak L, Hemmingsen L, Donat S, Ohlsen K, Boye K, et al. (2010) Growth phase-dependent regulation of the global virulence regulator Rot in clinical isolates of Staphylococcus aureus. Int J Med Microbiol 300: 229-236.
96. Said-Salim B, Dunman PM, McAleese FM, Macapagal D, Murphy E, et al. (2003) Global regulation of Staphylococcus aureus genes by Rot. J Bacteriol 185: 610-619.
97. Schmidt KA, Manna AC, Gill S, Cheung AL, (2001) SarT, a repressor of alpha-hemolysin in Staphylococcus aureus. Infect Immun 69: 4749-4758.
98. Xue T, Zhang X, Sun H, Sun B, (2013) ArtR, a novel sRNA of Staphylococcus aureus, regulates alpha-toxin expression by targeting the 5′ UTR of sarT mRNA. Med Microbiol Immunol E-pub ahead of print. doi: 10.1007/s00430-013-0307-0.
99. Kaito C, Saito Y, Nagano G, Ikuo M, Omae Y, et al. (2011) Transcription and translation products of the cytolysin gene psm-mec on the mobile genetic element SCCmec regulate Staphylococcus aureus virulence. PLoS Pathog 7: e1001267 doi:10.1371/journal.ppat.1001267.
100. Kaito C, Saito Y, Ikuo M, Omae Y, Mao H, et al. (2013) Mobile Genetic Element SCCmec-encoded psm-mec RNA Suppresses Translation of agrA and Attenuates MRSA Virulence. PLoS Pathog 9: e1003269 doi:10.1371/journal.ppat.1003269.
101. Novick RP, Christie GE, Penades JR, (2010) The phage-related chromosomal islands of Gram-positive bacteria. Nat Rev Microbiol 8: 541-551.
102. Chabelskaya S, Gaillot O, Felden B, (2010) A Staphylococcus aureus small RNA is required for bacterial virulence and regulates the expression of an immune-evasion molecule. PLoS Pathog 6: e1000927 doi:10.1371/journal.ppat.1000927.
103. Zhang L, Jacobsson K, Vasi J, Lindberg M, Frykberg L, (1998) A second IgG-binding protein in Staphylococcus aureus. Microbiology 144: 985-991.
104. Haupt K, Reuter M, van den Elsen J, Burman J, Halbich S, et al. (2008) The Staphylococcus aureus protein Sbi acts as a complement inhibitor and forms a tripartite complex with host complement Factor H and C3b. PLoS Pathog 4: e1000250 doi:10.1371/journal.ppat.1000250.
105. Lamers RP, Stinnett JW, Muthukrishnan G, Parkinson CL, Cole AM, (2011) Evolutionary analyses of Staphylococcus aureus identify genetic relationships between nasal carriage and clinical isolates. PLoS One 6: e16426 doi:10.1371/journal.pone.0016426.
106. Burian M, Wolz C, Goerke C, (2010) Regulatory adaptation of Staphylococcus aureus during nasal colonization of humans. PLoS One 5: e10040 doi:10.1371/journal.pone.0010040.
107. Cheung AL, Bayer AS, Zhang G, Gresham H, Xiong YQ, (2004) Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus. FEMS Immunol Med Microbiol 40: 1-9.
108. Goerke C, Campana S, Bayer MG, Doring G, Botzenhart K, et al. (2000) Direct quantitative transcript analysis of the agr regulon of Staphylococcus aureus during human infection in comparison to the expression profile in vitro. Infect Immun 68: 1304-1311.
109. Traber KE, Lee E, Benson S, Corrigan R, Cantera M, et al. (2008) agr function in clinical Staphylococcus aureus isolates. Microbiology 154: 2265-2274.
110. Shopsin B, Drlica-Wagner A, Mathema B, Adhikari RP, Kreiswirth BN, et al. (2008) Prevalence of agr dysfunction among colonizing Staphylococcus aureus strains. J Infect Dis 198: 1171-1174.
111. 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 doi:10.1371/journal.pone.0037294.
112. von Eiff C, Becker K, Machka K, Stammer H, Peters G, (2001) Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med 344: 11-16.
113. Wertheim HF, Vos MC, Ott A, van Belkum A, Voss A, et al. (2004) Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 364: 703-705.
114. von Eiff C, Heilmann C, Proctor RA, Woltz C, Peters G, et al. (1997) A site-directed Staphylococcus aureus hemB mutant is a small-colony variant which persists intracellularly. J Bacteriol 179: 4706-4712.
115. Proctor RA, von Eiff C, Kahl BC, Becker K, McNamara P, et al. (2006) Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 4: 295-305.
116. Vaudaux P, Kelley WL, Lew DP, (2006) Staphylococcus aureus small colony variants: difficult to diagnose and difficult to treat. Clin Infect Dis 43: 968-970.
117. von Eiff C, Becker K, Metze D, Lubritz G, Hockmann J, et al. (2001) Intracellular persistence of Staphylococcus aureus small-colony variants within keratinocytes: a cause for antibiotic treatment failure in a patient with darier's disease. Clin Infect Dis 32: 1643-1647.
118. Lannergard J, von Eiff C, Sander G, Cordes T, Seggewiss J, et al. (2008) Identification of the genetic basis for clinical menadione-auxotrophic small-colony variant isolates of Staphylococcus aureus. Antimicrob Agents Chemother 52: 4017-4022.
119. Chatterjee I, Kriegeskorte A, Fischer A, Deiwick S, Theimann N, et al. (2008) In vivo mutations of thymidylate synthase (encoded by thyA) are responsible for thymidine dependency in clinical small-colony variants of Staphylococcus aureus. J Bacteriol 190: 834-842.
120. Schmidt KA, Manna AC, Cheung AL, (2003) SarT influences sarS expression in Staphylococcus aureus. Infect Immun 71: 5139-5148.
121. Gao J, Stewart GC, (2004) Regulatory elements of the Staphylococcus aureus protein A (Spa) promoter. J Bacteriol 186: 3738-3748.
122. Reyes D, Andrey DO, Monod A, Kelley WL, Zhang G, et al. (2011) Coordinated regulation by AgrA, SarA, and SarR to control agr expression in Staphylococcus aureus. J Bacteriol 193: 6020-6031.
123. Manna AC, Cheung AL, (2003) sarU, a sarA homolog, is repressed by SarT and regulates virulence genes in Staphylococcus aureus. Infect Immun 71: 343-353.