The Essential yhcSR Two-Component Signal Transduction System Directly Regulates the lac and opuCABCD Operons of Staphylococcus aureus

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Yan, Meiying ^a   Hall, Jeffrey W ^a   Yang, Junshu ^a   Ji, Yinduo ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; BETAINE; CARNITINE; CHOLINE; COMPLEMENTARY RNA; GALACTOSE 6 PHOSPHATASE ISOMERASE LACA PROTEIN; PHOSPHATASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; LACTOSE OPERON; NONHUMAN; OPERON; OPUC OPERON; OPUCABCD OPERON; PROMOTER REGION; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION REGULATION; YHCSR;

ANIMALS; BACTERIAL PROTEINS; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; LAC OPERON; PROMOTER REGIONS, GENETIC; RNA, ANTISENSE; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION, GENETIC;

STAPHYLOCOCCUS AUREUS;

EID: 84870619546     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050608     Document Type: Article

References (49)

1. Grundmann H, Aires-de-Sousa M, Boyce J, Tiemersma E, (2006) Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat. Lancet 368: 874-885 doi:10.1016/S0140-6736(06)68853-3.
2. Kazakova SV, Hageman JC, Matava M, Srinivasan A, Phelan L, et al. (2005) A clone of methicillin-resistant Staphylococcus aureus among professional football players. N Engl J Med 352: 468-475 doi:10.1056/NEJMoa042859.
3. Rice LB (2006) Antimicrobial resistance in gram-positive bacteria. Am J Med 119: S11-19; discussion S62-70. doi:10.1016/j.amjmed.2006.03.012.
4. Gross R, (1993) Signal transduction and virulence regulation in human and animal pathogens. FEMS Microbiol Rev 10: 301-326.
5. Stock AM, Robinson VL, Goudreau PN, (2000) Two-component signal transduction. Annu Rev Biochem 69: 183-215 doi:10.1146/annurev.biochem.69.1.183.
6. Li Y-H, Lau PCY, Tang N, Svensäter G, Ellen RP, et al. (2002) Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans. J Bacteriol 184: 6333-6342.
7. Novick RA, Microbiology AS for (2006) Staphylococcal pathogenesis and pathogenicity factors: genetics and regulation. Gram-positive pathogens. Wiley-Blackwell.
8. Barrett JF, Hoch JA, (1998) Two-Component Signal Transduction as a Target for Microbial Anti-Infective Therapy. Antimicrob Agents Chemother 42: 1529-1536.
9. Martin PK, Li T, Sun D, Biek DP, Schmid MB, (1999) Role in cell permeability of an essential two-component system in Staphylococcus aureus. J Bacteriol 181: 3666-3673.
10. Sun J, Zheng L, Landwehr C, Yang J, Ji Y, (2005) Identification of a novel essential two-component signal transduction system, YhcSR, in Staphylococcus aureus. Journal of bacteriology 187: 7876.
11. Sun F, Ji Q, Jones MB, Deng X, Liang H, et al. (2011) AirSR, a [2Fe-2S] Cluster-Containing Two-Component System, Mediates Global Oxygen Sensing and Redox Signaling in Staphylococcus aureus. J Am Chem Soc 134: 305-314 doi:10.1021/ja2071835.
12. Fabret C, Hoch JA, (1998) A Two-Component Signal Transduction System Essential for Growth of Bacillus subtilis: Implications for Anti-Infective Therapy. J Bacteriol 180: 6375-6383.
13. Throup JP, Koretke KK, Bryant AP, Ingraham KA, Chalker AF, et al. (2000) A genomic analysis of two-component signal transduction in Streptococcus pneumoniae. Mol Microbiol 35: 566-576.
14. Fukuchi K, Kasahara Y, Asai K, Kobayashi K, Moriya S, et al. (2000) The essential two-component regulatory system encoded by yycF and yycG modulates expression of the ftsAZ operon in Bacillus subtilis. Microbiology (Reading, Engl) 146 (Pt 7): 1573-1583.
15. Bisicchia P, Noone D, Lioliou E, Howell A, Quigley S, et al. (2007) The essential YycFG two-component system controls cell wall metabolism in Bacillus subtilis. Molecular Microbiology 65: 180-200 doi:10.1111/j.1365-2958.2007.05782.x.
16. Dubrac S, Msadek T, (2004) Identification of Genes Controlled by the Essential YycG/YycF Two-Component System of Staphylococcus aureus. J Bacteriol 186: 1175-1181 doi:10.1128/JB.186.4.1175-1181.2004.
17. Howell A, Dubrac S, Andersen KK, Noone D, Fert J, et al. (2003) Genes controlled by the essential YycG/YycF two-component system of Bacillus subtilis revealed through a novel hybrid regulator approach. Mol Microbiol 49: 1639-1655.
18. Mohedano ML, Overweg K, de la Fuente A, Reuter M, Altabe S, et al. (2005) Evidence that the essential response regulator YycF in Streptococcus pneumoniae modulates expression of fatty acid biosynthesis genes and alters membrane composition. J Bacteriol 187: 2357-2367 doi:10.1128/JB.187.7.2357-2367.2005.
19. Ng W, Robertson GT, Kazmierczak KM, Zhao J, Gilmour R, et al. (2003) Constitutive expression of PcsB suppresses the requirement for the essential VicR (YycF) response regulator in Streptococcus pneumoniae R6§. Molecular Microbiology 50: 1647-1663 doi:10.1046/j.1365-2958.2003.03806.x.
20. Ng W, Kazmierczak KM, Winkler ME, (2004) Defective cell wall synthesis in Streptococcus pneumoniae R6 depleted for the essential PcsB putative murein hydrolase or the VicR (YycF) response regulator. Molecular Microbiology 53: 1161-1175 doi:10.1111/j.1365-2958.2004.04196.x.
21. Yan M, Yu C, Yang J, Ji Y, (2011) The Essential Two-Component System YhcSR Is Involved in Regulation of the Nitrate Respiratory Pathway of Staphylococcus aureus. Journal of Bacteriology 193: 1799-1805 doi:10.1128/JB.01511-10.
22. Yan M, Yu C, Yang J, Ji Y, (2009) Development of shuttle vectors for evaluation of essential regulator regulated gene expression in Staphylococcus aureus. Plasmid 61: 188-192 doi:10.1016/j.plasmid.2009.02.001.
23. Oskouian B, Stewart GC, (1990) Repression and catabolite repression of the lactose operon of Staphylococcus aureus. J Bacteriol 172: 3804-3812.
24. Kiran MD, Akiyoshi DE, Giacometti A, Cirioni O, Scalise G, et al. (2009) OpuC-an ABC transporter that is associated with Staphylococcus aureus pathogenesis. Int J Artif Organs 32: 600-610.
25. Ji Y, Yu C, Liang X (2007) Transcriptomic Analysis of ArlRS Two-Component Signaling Regulon, a Global Regulator, in Staphylococcus aureus. Two-Component Signaling Systems, Part B. Academic Press, Vol. Volume 423. 502-513. Available:http://www.sciencedirect.com/science/article/pii/S0076687907230241. Accessed 7 February 2012.
26. Liang X, Zheng L, Landwehr C, Lunsford D, Holmes D, et al. (2005) Global regulation of gene expression by ArlRS, a two-component signal transduction regulatory system of Staphylococcus aureus. J Bacteriol 187: 5486-5492 doi:10.1128/JB.187.15.5486-5492.2005.
27. Miller AA, Engleberg NC, DiRita VJ, (2001) Repression of virulence genes by phosphorylation-dependent oligomerization of CsrR at target promoters in S. pyogenes. Mol Microbiol 40: 976-990.
28. Manna AC, Ingavale SS, Maloney M, van Wamel W, Cheung AL, (2004) Identification of sarV (SA2062), a new transcriptional regulator, is repressed by SarA and MgrA (SA0641) and involved in the regulation of autolysis in Staphylococcus aureus. J Bacteriol 186: 5267-5280 doi:10.1128/JB.186.16.5267-5280.2004.
29. Manna AC, Cheung AL, (2006) Transcriptional regulation of the agr locus and the identification of DNA binding residues of the global regulatory protein SarR in Staphylococcus aureus. Mol Microbiol 60: 1289-1301 doi:10.1111/j.1365-2958.2006.05171.x.
30. Yin D, Fox B, Lonetto ML, Etherton MR, Payne DJ, et al. (2004) Identification of antimicrobial targets using a comprehensive genomic approach. Pharmacogenomics 5: 101-113 doi:10.1517/phgs.5.1.101.25679.
31. Vilhelmsson O, Miller KJ, (2002) Humectant Permeability Influences Growth and Compatible Solute Uptake by Staphylococcus aureus Subjected to Osmotic Stress. Journal of Food Protection 65: 1008-1015.
32. Vijaranakul U, Nadakavukaren MJ, Bayles DO, Wilkinson BJ, Jayaswal RK, (1997) Characterization of an NaCl-sensitive Staphylococcus aureus mutant and rescue of the NaCl-sensitive phenotype by glycine betaine but not by other compatible solutes. Appl Environ Microbiol 63: 1889-1897.
33. Kuroda M, Kuroda H, Oshima T, Takeuchi F, Mori H, et al. (2003) Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus. Mol Microbiol 49: 807-821.
34. Forsyth R, Haselbeck RJ, Ohlsen KL, Yamamoto RT, Xu H, et al. (2002) A genome-wide strategy for the identification of essential genes in Staphylococcus aureus. Molecular microbiology 43: 1387-1400.
35. Ji Y, (2001) Identification of Critical Staphylococcal Genes Using Conditional Phenotypes Generated by Antisense RNA. Science 293: 2266-2269 doi:10.1126/science.1063566.
36. Liang X, Yu C, Sun J, Liu H, Landwehr C, et al. (2006) Inactivation of a Two-Component Signal Transduction System, SaeRS, Eliminates Adherence and Attenuates Virulence of Staphylococcus aureus. Infection and Immunity 74: 4655-4665 doi:10.1128/IAI.00322-06.
37. Dunman PM, Murphy E, Haney S, Palacios D, Tucker-Kellogg G, et al. (2001) Transcription Profiling-Based Identification ofStaphylococcus aureus Genes Regulated by the agrand/or sarA Loci. J Bacteriol 183: 7341-7353 doi:10.1128/JB.183.24.7341-7353.2001.
38. 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 doi:10.1128/JB.188.5.1899-1910.2006.
39. Huang KJ, Lan CY, Igo MM, (1997) Phosphorylation stimulates the cooperative DNA-binding properties of the transcription factor OmpR. Proc Natl Acad Sci USA 94: 2828-2832.
40. Pragman AA, Yarwood JM, Tripp TJ, Schlievert PM, (2004) Characterization of Virulence Factor Regulation by SrrAB, a Two-Component System in Staphylococcus aureus. J Bacteriol 186: 2430-2438 doi:10.1128/JB.186.8.2430-2438.2004.
41. Head CG, Tardy A, Kenney LJ, (1998) Relative binding affinities of OmpR and OmpR-phosphate at the ompF and ompC regulatory sites. J Mol Biol 281: 857-870 doi:10.1006/jmbi.1998.1985.
42. Chen C, Beattie GA, (2007) Characterization of the osmoprotectant transporter OpuC from Pseudomonas syringae and demonstration that cystathionine-beta-synthase domains are required for its osmoregulatory function. J Bacteriol 189: 6901-6912 doi:10.1128/JB.00763-07.
43. Kappes RM, Kempf B, Kneip S, Boch J, Gade J, et al. (1999) Two evolutionarily closely related ABC transporters mediate the uptake of choline for synthesis of the osmoprotectant glycine betaine in Bacillus subtilis. Mol Microbiol 32: 203-216.
44. Verheul A, Glaasker E, Poolman B, Abee T, (1997) Betaine and L-carnitine transport by Listeria monocytogenes Scott A in response to osmotic signals. J Bacteriol 179: 6979-6985.
45. Kiran MD, Balaban N, (2009) TRAP plays a role in stress response in Staphylococcus aureus. Int J Artif Organs 32: 592-599.
46. Ogura M, Yamaguchi H, Yoshida Ki, Fujita Y, Tanaka T, (2001) DNA microarray analysis of Bacillus subtilis DegU, ComA and PhoP regulons: an approach to comprehensive analysis of B.subtilis two-component regulatory systems. Nucleic Acids Res 29: 3804-3813.
47. Kobayashi K, Ogura M, Yamaguchi H, Yoshida K, Ogasawara N, et al. (2001) Comprehensive DNA microarray analysis of Bacillus subtilis two-component regulatory systems. J Bacteriol 183: 7365-7370 doi:10.1128/JB.183.24.7365-7370.2001.
48. Dubrac S, Boneca IG, Poupel O, Msadek T, (2007) New insights into the WalK/WalR (YycG/YycF) essential signal transduction pathway reveal a major role in controlling cell wall metabolism and biofilm formation in Staphylococcus aureus. J Bacteriol 189: 8257-8269 doi:10.1128/JB.00645-07.
49. Kreiswirth BN, Löfdahl 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.