The Staphylococcus aureus proteome

International Journal of Medical Microbiology

Volumn 304, Issue 2, 2014, Pages 110-120

  Otto, Andreas ^a   van Dijl, Jan Maarten ^b   Hecker, Michael ^a   Becher, Dörte ^a  

^a UNIVERSITY OF GREIFSWALD   (Germany)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

2D gel electrophoresis; Biofilms; Entire proteome; Membrane vesicles; MS based proteomics; Physiological proteomics; Stress starvation responses; Surfacome; Virulence factors

Indexed keywords

2D GEL ELECTROPHORESIS; BIOFILMS; ENTIRE PROTEOME; MEMBRANE VESICLES; MS-BASED PROTEOMICS; PHYSIOLOGICAL PROTEOMICS; STRESS/STARVATION RESPONSES; SURFACOME; VIRULENCE FACTORS;

ANIMALS; BACTERIAL PROTEINS; HUMANS; PROTEOME; PROTEOMICS; STAPHYLOCOCCUS AUREUS;

EID: 84893754633     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2013.11.007     Document Type: Short Survey

References (119)

1. Bandow J.E., Metzler-Nolte N. New ways of killing the beast: prospects for inorganic-organic hybrid nanomaterials as antibacterial agents. ChemBioChem 2009, 10:2847-2850.
2. Bäsell K., Otto A., Zühlke D., Rappen G.M., Schmidt S., Hentschker C., Macek B., Ohlsen K., Hecker M., Becher D. The phosphoproteome and its physiological dynamics in Staphylococcus aureus. Int. J. Med. Microbiol. 2013, 10.1016/j.ijmm.2013.11.020.
3. Becher D., Hempel K., Sievers S., Zühlke D., Pané-Farré J., Otto A., Fuchs S., Albrecht D., Bernhardt J., Engelmann S., Völker U., van Dijl J.M., Hecker M. A proteomic view of an important human pathogen - towards the quantification of the entire Staphylococcus aureus proteome. PLoS One 2009, 4:e8176.
4. Bernhardt J., Büttner K., Scharf C., Hecker M. Dual channel imaging of two-dimensional electropherograms in Bacillus subtilis. Electrophoresis 1999, 20:2225-2240.
5. Bernhardt J., Weibezahn J., Scharf C., Hecker M. Bacillus subtilis during feast and famine: visualization of the overall regulation of protein synthesis during glucose starvation by proteome analysis. Genome Res. 2003, 13:224-237.
6. Berth M., Moser F.M., Kolbe M., Bernhardt J. The state of the art in the analysis of two-dimensional gel electrophoresis images. Appl. Microbiol. Biotechnol. 2007, 76:1223-1243.
7. Bestebroer J., De Haas C.J., Van Strijp J.A. How microorganisms avoid phagocyte attraction. FEMS Microbiol. Rev. 2010, 34:395-414.
8. Birdsell D.C., Cota-Robles E.H. Production and ultrastructure of lysozyme and ethylenediaminetetraacetate-lysozyme spheroplasts of Escherichia coli. J. Bacteriol. 1967, 93:427-437.
9. Brötz-Oesterhelt H., Bandow J.E., Labischinski H. Bacterial proteomics and its role in antibacterial drug discovery. Mass Spectrom. Rev. 2005, 24:549-565.
10. Bumann D. Pathogen proteomes during infection: a basis for infection research and novel control strategies. J Proteomics 2010, 73:2267-2276.
11. CDC Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus - Minnesota and North Dakota, 1997-1999. MMWR. Morb. Mortal. Wkly. Rep. 1999, 48:707-710.
12. Chatterjee S.S., Joo H.S., Duong A.C., Dieringer T.D., Tan V.Y., Song Y., Fischer E.R., Cheung G.Y., Li M., Otto M. Essential Staphylococcus aureus toxin export system. Nat. Med. 2013, 19:364-367.
13. Cox J., Mann M. Quantitative, high-resolution proteomics for data-driven systems biology. Annu. Rev. Biochem. 2011, 80:273-299.
14. Deatherage B.L., Cookson B.T. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect. Immun. 2012, 80:1948-1957.
15. Delauné A., Dubrac S., Blanchet C., Poupel O., Mäder U., Hiron A., Leduc A., Fitting C., Nicolas P., Cavaillon J.-M. The WalKR system controls major staphylococcal virulence genes and is involved in triggering the host inflammatory response. Infect. Immun. 2012, 80:3438-3453.
16. Dinges M.M., Orwin P.M., Schlievert P.M. Exotoxins of Staphylococcus aureus. Clin. Microbiol. Rev. 2000, 13:16-34.
17. Domon B., Aebersold R. Mass spectrometry and protein analysis. Science 2006, 312:212-217.
18. Dreisbach A., Hempel K., Buist G., Hecker M., Becher D., van Dijl J.M. Profiling the surfacome of Staphylococcus aureus. Proteomics 2010, 10:3082-3096.
19. Dreisbach A., van der Kooi-Pol M.M., Otto A., Gronau K., Bonarius H.P., Westra H., Groen H., Becher D., Hecker M., van Dijl J.M. Surface shaving as a versatile tool to profile global interactions between human serum proteins and the Staphylococcus aureus cell surface. Proteomics 2011, 11:2921-2930.
20. Dreisbach A., van Dijl J.M., Buist G. The cell surface proteome of Staphylococcus aureus. Proteomics 2011, 11:3154-3168.
21. Dubrac S., Msadek T. Identification of genes controlled by the essential YycG/YycF two-component system of Staphylococcus aureus. J. Bacteriol. 2004, 186:1175-1181.
22. Dutow P., Schmidl S.R., Ridderbusch M., Stülke J. Interactions between glycolytic enzymes of Mycoplasma pneumoniae. J. Mol. Microbiol. Biotechnol. 2010, 19:134-139.
23. Elsholz A.K., Turgay K., Michalik S., Hessling B., Gronau K., Oertel D., Mäder U., Bernhardt J., Becher D., Hecker M., Gerth U. Global impact of protein arginine phosphorylation on the physiology of Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:7451-7456.
24. Engelmann S., Hecker M. A proteomics view of virulence factors of Staphylococcus aureus. Genome Dyn. 2009, 6:187-197.
25. Feng J., Michalik S., Varming A.N., Andersen J.H., Albrecht D., Jelsbak L., Krieger S., Ohlsen K., Hecker M., Gerth U., Ingmer H., Frees D. Trapping and proteomic identification of cellular substrates of the ClpP protease in Staphylococcus aureus. J. Proteome Res. 2013, 12:547-558.
26. Fischer A., Yang S.J., Bayer A.S., Vaezzadeh A.R., Herzig S., Stenz L., Girard M., Sakoulas G., Scherl A., Yeaman M.R., Proctor R.A., Schrenzel J., Francois P. Daptomycin resistance mechanisms in clinically derived Staphylococcus aureus strains assessed by a combined transcriptomics and proteomics approach. J. Antimicrob. Chemother. 2011, 66:1696-1711.
27. Foster T.J., Hook M. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol. 1998, 6:484-488.
28. Francois P., Scherl A., Hochstrasser D., Schrenzel J. Proteomic approaches to study Staphylococcus aureus pathogenesis. J. Proteomics 2010, 73:701-708.
29. Fuchs S., Mehlan H., Kusch H., Teumer A., Zühlke D., Berth M., Wolf C., Dandekar T., Hecker M., Engelmann S., Bernhardt J. Protecs, a comprehensive and powerful storage and analysis system for OMICS data, applied for profiling the anaerobiosis response of Staphylococcus aureus COL. Proteomics 2010, 10:2982-3000.
30. Fuchs S., Pané-Farré J., Kohler C., Hecker M., Engelmann S. Anaerobic gene expression in Staphylococcus aureus. J. Bacteriol. 2007, 189:4275-4289.
31. Gerber S.A., Rush J., Stemman O., Kirschner M.W., Gygi S.P. Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:6940-6945.
32. Glowalla E., Tosetti B., Kronke M., Krut O. Proteomics-based identification of anchorless cell wall proteins as vaccine candidates against Staphylococcus aureus. Infect. Immun. 2009, 77:2719-2729.
33. Götz F. Staphylococcus and biofilms. Mol. Microbiol. 2002, 43:1367-1378.
34. Gurung M., Moon D.C., Choi C.W., Lee J.H., Bae Y.C., Kim J., Lee Y.C., Seol S.Y., Cho D.T., Kim S.I., Lee J.C. Staphylococcus aureus produces membrane-derived vesicles that induce host cell death. PLoS One 2011, 6:e27958.
35. Harro J.M., Peters B.M., O'May G.A., Archer N., Kerns P., Prabhakara R., Shirtliff M.E. Vaccine development in Staphylococcus aureus: taking the biofilm phenotype into consideration. FEMS Immunol. Med. Microbiol. 2010, 59:306-323.
36. Hecker M., Antelmann H., Büttner K., Bernhardt J. Gel-based proteomics of Gram-positive bacteria: a powerful tool to address physiological questions. Proteomics 2008, 8:4958-4975.
37. Hecker M., Becher D., Fuchs S., Engelmann S. A proteomic view of cell physiology and virulence of Staphylococcus aureus. Int. J. Med. Microbiol. 2010, 300:76-87.
38. Hecker M., Pané-Farré J., Völker U. SigB-dependent general stress response in Bacillus subtilis and related Gram-positive bacteria. Annu. Rev. Microbiol. 2007, 61:215-236.
39. Hecker M., Reder A., Fuchs S., Pagels M., Engelmann S. Physiological proteomics and stress/starvation responses in Bacillus subtilis and Staphylococcus aureus. Res. Microbiol. 2009, 160:245-258.
40. Hempel K., Herbst F.A., Moche M., Hecker M., Becher D. Quantitative proteomic view on secreted, cell surface-associated, and cytoplasmic proteins of the methicillin-resistant human pathogen Staphylococcus aureus under iron-limited conditions. J. Proteome Res. 2011, 10:1657-1666.
41. Hempel K., Pané-Farré J., Otto A., Sievers S., Hecker M., Becher D. Quantitative cell surface proteome profiling for SigB-dependent protein expression in the human pathogen Staphylococcus aureus via biotinylation approach. J. Proteome Res. 2010, 9:1579-1590.
42. Hoch J.A. Two-component and phosphorelay signal transduction. Curr. Opin. Microbiol. 2000, 3:165-170.
43. Hochgräfe F., Mostertz J., Albrecht D., Hecker M. Fluorescence thiol modification assay: oxidatively modified proteins in Bacillus subtilis. Mol. Microbiol. 2005, 58:409-425.
44. Hochgräfe F., Wolf C., Fuchs S., Liebeke M., Lalk M., Engelmann S., Hecker M. Nitric oxide stress induces different responses but mediates comparable protein thiol protection in Bacillus subtilis and Staphylococcus aureus. J. Bacteriol. 2008, 190:4997-5008.
45. Høiby N., Bjarnsholt T., Givskov M., Molin S., Ciofu O. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 2010, 35:322-332.
46. Hong S.W., Kim M.R., Lee E.Y., Kim J.H., Kim Y.S., Jeon S.G., Yang J.M., Lee B.J., Pyun B.Y., Gho Y.S., Kim Y.K. Extracellular vesicles derived from Staphylococcus aureus induce atopic dermatitis-like skin inflammation. Allergy 2011, 66:351-359.
47. Kiedrowski M.R., Kavanaugh J.S., Malone C.L., Mootz J.M., Voyich J.M., Smeltzer M.S., Bayles K.W., Horswill A.R. Nuclease modulates biofilm formation in community-associated methicillin-resistant Staphylococcus aureus. PLoS One 2011, 6:e26714.
48. Klevens R.M., Morrison M.A., Nadle J., Petit S., Gershman K., Ray S., Harrison L.H., Lynfield R., Dumyati G., Townes J.M., Craig A.S., Zell E.R., Fosheim G.E., McDougal L.K., Carey R.B., Fridkin S.K. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 2007, 298:1763-1771. Active Bacterial Core Surveillance, M.I.
49. Knox K.W., Vesk M., Work E. Relation between excreted lipopolysaccharide complexes and surface structures of a lysine-limited culture of Escherichia coli. J. Bacteriol. 1966, 92:1206-1217.
50. Kocher T., Swart R., Mechtler K. Ultra-high-pressure RPLC hyphenated to an LTQ-Orbitrap Velos reveals a linear relation between peak capacity and number of identified peptides. Anal. Chem. 2011, 83:2699-2704.
51. Kohler C., von Eiff C., Liebeke M., McNamara P.J., Lalk M., Proctor R.A., Hecker M., Engelmann S. A defect in menadione biosynthesis induces global changes in gene expression in Staphylococcus aureus. J. Bacteriol. 2008, 190:6351-6364.
52. Kohler C., von Eiff C., Peters G., Proctor R.A., Hecker M., Engelmann S. Physiological characterization of a heme-deficient mutant of Staphylococcus aureus by a proteomic approach. J. Bacteriol. 2003, 185:6928-6937.
53. Kohler C., Wolff S., Albrecht D., Fuchs S., Becher D., Büttner K., Engelmann S., Hecker M. Proteome analyses of Staphylococcus aureus in growing and non-growing cells: a physiological approach. Int. J. Med. Microbiol. 2005, 295:547-565.
54. Kriegeskorte A., König S., Sander G., Pirkl A., Mahabir E., Proctor R.A., von Eiff C., Peters G., Becker K. Small colony variants of Staphylococcus aureus reveal distinct protein profiles. Proteomics 2011, 11:2476-2490.
55. Lee E.Y., Choi D.Y., Kim D.K., Kim J.W., Park J.O., Kim S., Kim S.H., Desiderio D.M., Kim Y.K., Kim K.P., Gho Y.S. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics 2009, 9:5425-5436.
56. Lee J.C. Staphylococcus aureus membrane vesicles and its potential role in bacterial pathogenesis. J. Bacteriol. Virol. 2012, 42:181-188.
57. Lina G., Jarraud S., Ji G., Greenland T., Pedraza A., Etienne J., Novick R.P., Vandenesch F. Transmembrane topology and histidine protein kinase activity of AgrC, the agr signal receptor in Staphylococcus aureus. Mol. Microbiol. 1998, 28:655-662.
58. Lindsay J.A., Holden M.T. Staphylococcus aureus: superbug, super genome?. Trends Microbiol. 2004, 12:378-385.
59. Lowy F.D. Staphylococcus aureus infections. N. Engl. J. Med. 1998, 339:520-532.
60. Maass S., Sievers S., Zühlke D., Kuzinski J., Sappa P.K., Muntel J., Hessling B., Bernhardt J., Sietmann R., Völker U., Hecker M., Becher D. Efficient, global-scale quantification of absolute protein amounts by integration of targeted mass spectrometry and two-dimensional gel-based proteomics. Anal. Chem. 2011, 83:2677-2684.
61. MacDonald I.A., Kuehn M.J. Offense and defense: microbial membrane vesicles play both ways. Res. Microbiol. 2012, 163:607-618.
62. McCarthy A.J., Lindsay J.A. Staphylococcus aureus innate immune evasion is lineage-specific: a bioinformatics study. Infect. Genet. Evol. 2013, 19C:7-14.
63. Merino N., Toledo-Arana A., Vergara-Irigaray M., Valle J., Solano C., Calvo E., Lopez J.A., Foster T.J., Penadés J.R., Lasa I. Protein A-mediated multicellular behavior in Staphylococcus aureus. J. Bacteriol. 2009, 191:832-843.
64. Meyer F.M., Gerwig J., Hammer E., Herzberg C., Commichau F.M., Völker U., Stülke J. Physical interactions between tricarboxylic acid cycle enzymes in Bacillus subtilis: evidence for a metabolon. Metab. Eng. 2011, 13:18-27.
65. Michalik S., Bernhardt J., Otto A., Moche M., Becher D., Meyer H., Lalk M., Schurmann C., Schluter R., Kock H., Gerth U., Hecker M. Life and death of proteins: a case study of glucose-starved Staphylococcus aureus. Mol. Cell. Proteomics 2012, 11:558-570.
66. Michalik S., Liebeke M., Zühlke D., Lalk M., Bernhardt J., Gerth U., Hecker M. Proteolysis during long-term glucose starvation in Staphylococcus aureus COL. Proteomics 2009, 9:4468-4477.
67. Mijakovic I., Macek B. Impact of phosphoproteomics on studies of bacterial physiology. FEMS Microbiol. Rev. 2012, 36:877-892.
68. Miller M., Dreisbach A., Otto A., Becher D., Bernhardt J., Hecker M., Peppelenbosch M.P., van Dijl J.M. Mapping of interactions between human macrophages and Staphylococcus aureus reveals an involvement of MAP kinase signaling in the host defense. J. Proteome Res. 2011, 10:4018-4032.
69. Muthukrishnan G., Quinn G.A., Lamers R.P., Diaz C., Cole A.L., Chen S., Cole A.M. Exoproteome of Staphylococcus aureus reveals putative determinants of nasal carriage. J. Proteome Res. 2011, 10:2064-2078.
70. Nandakumar R., Nandakumar M.P., Marten M.R., Ross J.M. Proteome analysis of membrane and cell wall associated proteins from Staphylococcus aureus. J. Proteome Res. 2005, 4:250-257.
71. O'Farrell P.H. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 1975, 250:4007-4021.
72. Ohlsen K., Donat S. The impact of serine/threonine phosphorylation in Staphylococcus aureus. Int. J. Med. Microbiol. 2010, 300:137-141.
73. Otto A., Bernhardt J., Hecker M., Becher D. Global relative and absolute quantitation in microbial proteomics. Curr. Opin. Microbiol. 2012, 15:364-372.
74. Otto A., Bernhardt J., Meyer H., Schaffer M., Herbst F.A., Siebourg J., Mäder U., Lalk M., Hecker M., Becher D. Systems-wide temporal proteomic profiling in glucose-starved Bacillus subtilis. Nat. Commun. 2010, 1:137.
75. Otto M. Staphylococcal biofilms. Bacterial Biofilms 2008, 207-228. Springer, Berlin Heidelberg.
76. Otto M. Basis of virulence in community-associated methicillin-resistant Staphylococcus aureus. Annu. Rev. Microbiol. 2010, 64:143-162.
77. Otto M. MRSA virulence and spread. Cell. Microbiol. 2012, 14:1513-1521.
78. Otto M. Community-associated MRSA: what makes them special?. Int. J. Med. Microbiol. 2013, 303:324-330.
79. Otto M. Staphylococcal infections: mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity. Annu. Rev. Med. 2013, 64:175-188.
80. Pagels M., Fuchs S., Pané-Farré J., Kohler C., Menschner L., Hecker M., McNamarra P.J., Bauer M.C., von Wachenfeldt C., Liebeke M., Lalk M., Sander G., von Eiff C., Proctor R.A., Engelmann S. Redox sensing by a Rex-family repressor is involved in the regulation of anaerobic gene expression in Staphylococcus aureus. Mol. Microbiol. 2010, 76:1142-1161.
81. Pané-Farré J., Jonas B., Förstner K., Engelmann S., Hecker M. The sigmaB regulon in Staphylococcus aureus and its regulation. Int. J. Med. Microbiol. 2006, 296:237-258.
82. Pasztor L., Ziebandt A.K., Nega M., Schlag M., Haase S., Franz-Wachtel M., Madlung J., Nordheim A., Heinrichs D.E., Götz F. Staphylococcal major autolysin (Atl) is involved in excretion of cytoplasmic proteins. J. Biol. Chem. 2010, 285:36794-36803.
83. Peacock S.J., Moore C.E., Justice A., Kantzanou M., Story L., Mackie K., O'Neill G., Day N.P. Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect. Immun. 2002, 70:4987-4996.
84. Periasamy S., Chatterjee S.S., Cheung G.Y., Otto M. Phenol-soluble modulins in staphylococci: what are they originally for?. Commun. Integr. Biol. 2012, 5:275-277.
85. Pöther D.C., Gierok P., Harms M., Mostertz J., Hochgräfe F., Antelmann H., Hamilton C.J., Borovok I., Lalk M., Aharonowitz Y., Hecker M. Distribution and infection-related functions of bacillithiol in Staphylococcus aureus. Int. J. Med. Microbiol. 2013, 303:114-123.
86. Pöther D.C., Liebeke M., Hochgräfe F., Antelmann H., Becher D., Lalk M., Lindequist U., Borovok I., Cohen G., Aharonowitz Y., Hecker M. Diamide triggers mainly S Thiolations in the cytoplasmic proteomes of Bacillus subtilis and Staphylococcus aureus. J. Bacteriol. 2009, 191:7520-7530.
87. Resch A., Leicht S., Saric M., Pasztor L., Jakob A., Gotz F., Nordheim A. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling. Proteomics 2006, 6:1867-1877.
88. Rivera J., Cordero R.J., Nakouzi A.S., Frases S., Nicola A., Casadevall A. Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:19002-19007.
89. Rogasch K., Rühmling V., Pané-Farré J., Höper D., Weinberg C., Fuchs S., Schmudde M., Bröker B.M., Wolz C., Hecker M., Engelmann S. Influence of the two-component system SaeRS on global gene expression in two different Staphylococcus aureus strains. J. Bacteriol. 2006, 188:7742-7758.
90. Scherl A., Francois P., Charbonnier Y., Deshusses J.M., Koessler T., Huyghe A., Bento M., Stahl-Zeng J., Fischer A., Masselot A., Vaezzadeh A., Galle F., Renzoni A., Vaudaux P., Lew D., Zimmermann-Ivol C.G., Binz P.A., Sanchez J.C., Hochstrasser D.F., Schrenzel J. Exploring glycopeptide-resistance in Staphylococcus aureus: a combined proteomics and transcriptomics approach for the identification of resistance-related markers. BMC Genomics 2006, 7:296.
91. Schmidt F., Scharf S.S., Hildebrandt P., Burian M., Bernhardt J., Dhople V., Kalinka J., Gutjahr M., Hammer E., Völker U. Time-resolved quantitative proteome profiling of host-pathogen interactions: the response of Staphylococcus aureus RN1HG to internalisation by human airway epithelial cells. Proteomics 2010, 10:2801-2811.
92. Schmidt F., Völker U. Proteome analysis of host-pathogen interactions: investigation of pathogen responses to the host cell environment. Proteomics 2011, 11:3203-3211.
93. Scott J.R., Barnett T.C. Surface proteins of Gram-positive bacteria and how they get there. Annu. Rev. Microbiol. 2006, 60:397-423.
94. Seidl K., Müller S., Francois P., Kriebitzsch C., Schrenzel J., Engelmann S., Bischoff M., Berger-Bachi B. Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus. BMC Microbiol. 2009, 9:95.
95. Sibbald M.J., Ziebandt A.K., Engelmann S., Hecker M., de Jong A., Harmsen H.J., Raangs G.C., Stokroos I., Arends J.P., Dubois J.Y., van Dijl J.M. Mapping the pathways to staphylococcal pathogenesis by comparative secretomics. Microbiol. Mol. Biol. Rev. 2006, 70:755-788.
96. Sievers S., Ernst C.M., Geiger T., Hecker M., Wolz C., Becher D., Peschel A. Changing the phospholipid composition of Staphylococcus aureus causes distinct changes in membrane proteome and membrane-sensory regulators. Proteomics 2010, 10:1685-1693.
97. Solis N., Larsen M.R., Cordwell S.J. Improved accuracy of cell surface shaving proteomics in Staphylococcus aureus using a false-positive control. Proteomics 2010, 10:2037-2049.
98. Spaan A.N., Surewaard B.G., Nijland R., van Strijp J.A. Neutrophils versus Staphylococcus aureus: a biological tug of war. Annu. Rev. Microbiol. 2013, 67:629-650.
99. Stauff D.L., Torres V.J., Skaar E.P. Signaling and DNA-binding activities of the Staphylococcus aureus HssR-HssS two-component system required for heme sensing. J. Biol. Chem. 2007, 282:26111-26121.
100. Thakur S.S., Geiger T., Chatterjee B., Bandilla P., Fröhlich F., Cox J., Mann M. Deep and highly sensitive proteome coverage by LC-MS/MS without prefractionation. Mol. Cell. Proteomics 2011, 10. M110.003699.
101. Thay B., Wai S.N., Oscarsson J. Staphylococcus aureus alpha-toxin-dependent induction of host cell death by membrane-derived vesicles. PLoS One 2013, 8:e54661.
102. Truong-Bolduc Q.C., Ding Y., Hooper D.C. Posttranslational modification influences the effects of MgrA on norA expression in Staphylococcus aureus. J. Bacteriol. 2008, 190:7375-7381.
103. Truong-Bolduc Q.C., Hooper D.C. Phosphorylation of MgrA and its effect on expression of the NorA and NorB efflux pumps of Staphylococcus aureus. J. Bacteriol. 2010, 192:2525-2534.
104. Tsompanidou E., Denham E.L., Becher D., de Jong A., Buist G., van Oosten M., Manson W.L., Back J.W., van Dijl J.M., Dreisbach A. Distinct roles of phenol-soluble modulins in spreading of Staphylococcus aureus on wet surfaces. Appl. Environ. Microbiol. 2013, 79:886-895.
105. Tsompanidou E., Denham E.L., Sibbald M.J., Yang X.-M., Seinen J., Friedrich A.W., Buist G., van Dijl J.M. The sortase A substrates FnbpA, FnbpB, ClfA and ClfB antagonize colony spreading of Staphylococcus aureus. PLoS One 2012, 7:e44646.
106. Tsompanidou E., Denham E.L., van Dijl J.M. Phenol-soluble modulins, hellhounds from the staphylococcal virulence-factor pandemonium. Trends Microbiol. 2013, 7:313-315.
107. van den Berg S., Bowden M.G., Bosma T., Buist G., van Dijl J.M., van Wamel W.J., de Vogel C.P., van Belkum A., Bakker-Woudenberg I.A. A multiplex assay for the quantification of antibody responses in Staphylococcus aureus infections in mice. J. Immunol. Methods 2011, 365:142-148.
108. Ventura C.L., Malachowa N., Hammer C.H., Nardone G.A., Robinson M.A., Kobayashi S.D., DeLeo F.R. Identification of a novel Staphylococcus aureus two-component leukotoxin using cell surface proteomics. PLoS One 2010, 5:e11634.
109. Wang R., Braughton K.R., Kretschmer D., Bach T.H.L., Queck S.Y., Li M., Kennedy A.D., Dorward D.W., Klebanoff S.J., Peschel A., Deleo F.R., Otto M. Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat. Med. 2007, 13:1510-1514.
110. Weber H., Engelmann S., Becher D., Hecker M. Oxidative stress triggers thiol oxidation in the glyceraldehyde-3-phosphate dehydrogenase of Staphylococcus aureus. Mol. Microbiol. 2004, 52:133-140.
111. Wenzel M., Patra M., Senges C.H., Ott I., Stepanek J.J., Pinto A., Prochnow P., Vuong C., Langklotz S., Metzler-Nolte N., Bandow J.E. Analysis of the mechanism of action of potent antibacterial hetero-tri-organometallic compounds: a structurally new class of antibiotics. ACS Chem. Biol. 2013, 8(7):1442-1450.
112. Wertheim H.F., Melles D.C., Vos M.C., van Leeuwen W., van Belkum A., Verbrugh H.A., Nouwen J.L. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect. Dis. 2005, 5:751-762.
113. Witney A.A., Marsden G.L., Holden M.T., Stabler R.A., Husain S.E., Vass J.K., Butcher P.D., Hinds J., Lindsay J.A. Design, validation, and application of a seven-strain Staphylococcus aureus PCR product microarray for comparative genomics. Appl. Environ. Microbiol. 2005, 71:7504-7514.
114. Wolf C., Hochgräfe F., Kusch H., Albrecht D., Hecker M., Engelmann S. Proteomic analysis of antioxidant strategies of Staphylococcus aureus: diverse responses to different oxidants. Proteomics 2008, 8:3139-3153.
115. Wolf C., Kusch H., Monecke S., Albrecht D., Holtfreter S., von Eiff C., Petzl W., Rainard P., Bröker B.M., Engelmann S. Genomic and proteomic characterization of Staphylococcus aureus mastitis isolates of bovine origin. Proteomics 2011, 11:2491-2502.
116. Wolff S., Hahne H., Hecker M., Becher D. Complementary analysis of the vegetative membrane proteome of the human pathogen Staphylococcus aureus. Mol. Cell. Proteomics 2008, 7:1460-1468.
117. Ziebandt A.K., Becher D., Ohlsen K., Hacker J., Hecker M., Engelmann S. The influence of agr and sigmaB in growth phase dependent regulation of virulence factors in Staphylococcus aureus. Proteomics 2004, 4:3034-3047.
118. Ziebandt A.K., Kusch H., Degner M., Jaglitz S., Sibbald M.J., Arends J.P., Chlebowicz M.A., Albrecht D., Pantucek R., Doskar J., Ziebuhr W., Bröker B.M., Hecker M., van Dijl J.M., Engelmann S. Proteomics uncovers extreme heterogeneity in the Staphylococcus aureus exoproteome due to genomic plasticity and variant gene regulation. Proteomics 2010, 10:1634-1644.
119. Ziebandt A.K., Weber H., Rudolph J., Schmid R., Höper D., Engelmann S., Hecker M. Extracellular proteins of Staphylococcus aureus and the role of SarA and sigma B. Proteomics 2001, 1:480-493.