Structure and function of surface polysaccharides of Staphylococcus aureus

Current Topics in Microbiology and Immunology

Volumn 409, Issue , 2017, Pages 57-93

  Weidenmaier, Christopher ^a   Lee, Jean C ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL POLYSACCHARIDE; BACTERIOPHAGE RECEPTOR; BETA LACTAM ANTIBIOTIC; CARRIER PROTEIN; CELL MEMBRANE PROTEIN; DAPTOMYCIN; DIPHTHERIA TOXOID CRM197; F 598; MEMBRANE LIPID; METICILLIN; MONOCLONAL ANTIBODY; OXACILLIN; PENTAVAX; PEPTIDOGLYCAN; PLACEBO; PROTEIN CP; PROTEIN CP5; PROTEIN CP8; PROTEIN PIA; PROTEIN PNAG; PROTEIN WTA; SAR 279356; STAPHYLOCOCCUS VACCINE; TETANUS TOXOID; UNCLASSIFIED DRUG; VIRULENCE FACTOR; POLYSACCHARIDE;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL VIABILITY; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; DRUG TARGETING; HORIZONTAL GENE TRANSFER; HUMAN; IMMUNE EVASION; IMMUNITY; IN VITRO STUDY; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; STAPHYLOCOCCAL BACTEREMIA; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; UNSPECIFIED SIDE EFFECT;

POLYSACCHARIDES; POLYSACCHARIDES, BACTERIAL; STAPHYLOCOCCUS AUREUS;

EID: 85041360220     PISSN: 0070217X     EISSN: 21969965     Source Type: Book Series    
DOI: 10.1007/82_2015_5018     Document Type: Chapter

References (208)

1. Aly R, Shinefield HR, Litz C, Maibach HI (1980) Role of teichoic acid in the binding of Staphylococcus aureus to nasal epithelial cells. J Infect Dis 141:463–465
2. Araki Y, Ito E (1989) Linkage units in cell walls of gram-positive bacteria. Crit Rev Microbiol 17 (2):121–135
3. Atilano ML, Pereira PM, Yates J, Reed P, Veiga H, Pinho MG, Filipe SR (2010) Teichoic acids are temporal and spatial regulators of peptidoglycan cross-linking in Staphylococcus aureus. Proc Natl Acad Sci USA 107(44):18991–18996
4. Baddour LM, Lowrance C, Albus A, Lowrance JH, Anderson SK, Lee JC (1992) Staphylococcus aureus microcapsule expression attenuates bacterial virulence in a rat model of experimental endocarditis. J Infect Dis 165:749–753
5. Badurina DS, Zolli-Juran M, Brown ED (2003) CTP:glycerol 3-phosphate cytidylyltransferase (TarD) from Staphylococcus aureus catalyzes the cytidylyl transfer via an ordered Bi-Bi reaction mechanism with micromolar K(m) values. Biochim Biophys Acta 1646(1–2):196–206
6. Barreteau H, Magnet S, El Ghachi M, Touze T, Arthur M, Mengin-Lecreulx D, Blanot D (2009) Quantitative high-performance liquid chromatography analysis of the pool levels of undecaprenyl phosphate and its derivatives in bacterial membranes. J Chromatogr B Anal Technol Biomed Life Sci 877(3):213–220
7. Baur S, Rautenberg M, Faulstich M, Grau T, Severin Y, Unger C, Hoffmann WH, Rudel T, Autenrieth IB, Weidenmaier C (2014) A nasal epithelial receptor for Staphylococcus aureus WTA governs adhesion to epithelial cells and modulates nasal colonization. PLoS Pathog 10 (5):e1004089
8. Bertsche U, Weidenmaier C, Kuehner D, Yang SJ, Baur S, Wanner S, Francois P, Schrenzel J, Yeaman MR, Bayer AS (2011) Correlation of daptomycin-resistance in a clinical Staphylococcus aureus strain with increased cell wall teichoic acid production and D-alanylation. Antimicrob Agents Chemother 55:3922
9. Bertsche U, Yang SJ, Kuehner D, Wanner S, Mishra NN, Roth T, Nega M, Schneider A, Mayer C, Grau T, Bayer AS, Weidenmaier C (2013) Increased cell wall teichoic acid production and D-alanylation are common phenotypes among daptomycin-resistant methicillin-resistant Staphylococcus aureus (MRSA) clinical isolates. PLoS ONE 8(6):e67398
10. Bhasin N, Albus A, Michon F, Livolsi PJ, Park J-S, Lee JC (1998) Identification of a gene essential for O-acetylation of the Staphylococcus aureus type 5 capsular polysaccharide. Mol Microbiol 27:9–21
11. Bhavsar AP, Truant R, Brown ED (2005) The TagB protein in Bacillus subtilis 168 is an intracellular peripheral membrane protein that can incorporate glycerol phosphate onto a membrane-bound acceptor in vitro. J Biol Chem 280(44):36691–36700
12. Bierbaum G, Sahl HG (1985) Induction of autolysis of staphylococci by the basic peptide antibiotics Pep 5 and nisin and their influence on the activity of autolytic enzymes. Arch Microbiol 141(3):249–254
13. Bischoff M, Dunman P, Kormanec J, Macapagal D, Murphy E, Mounts W, Berger-Bachi B, Projan S (2004) Microarray-based analysis of the Staphylococcus aureus sigmaB regulon. J Bacteriol 186(13):4085–4099
14. Biswas R, Martinez RE, Gohring N, Schlag M, Josten M, Xia G, Hegler F, Gekeler C, Gleske AK, Gotz F, Sahl HG, Kappler A, Peschel A (2012) Proton-binding capacity of Staphylococcus aureus wall teichoic acid and its role in controlling autolysin activity. PLoS ONE 7(7):e41415
15. Bittersuermann D (1993) Influence of bacterial polysialic capsules on host defense - masquerade and mimicry. Polysialic Acid. Birkhauser, Basel
16. Boles BR, Thoendel M, Roth AJ, Horswill AR (2010) Identification of genes involved in polysaccharide-independent Staphylococcus aureus biofilm formation. PLoS ONE 5(4):e10146
17. Bouhss A, Trunkfield AE, Bugg TD, Mengin-Lecreulx D (2008) The biosynthesis of peptidoglycan lipid-linked intermediates. FEMS Microbiol Rev 32(2):208–233
18. Boyle-Vavra S, Li X, Alam MT, Read TD, Sieth J, Cywes-Bentley C, Dobbins G, David MZ, Kumar N, Eells SJ, Miller LG, Boxrud DJ, Chambers HF, Lynfield R, Lee JC, Daum RS (2015) USA300 and USA500 clonal lineages of Staphylococcus aureus do not produce a capsular polysaccharide due to conserved mutations in the cap5 locus. mBio 6(2):e02585– 02514
19. Brown S, Meredith T, Swoboda J, Walker S (2010) Staphylococcus aureus and Bacillus subtilis W23 make polyribitol wall teichoic acids using different enzymatic pathways. Chem Biol 17 (10):1101–1110
20. Brown S, Santa Maria JP Jr, Walker S (2013) Wall teichoic acids of gram-positive bacteria. Annu Rev Microbiol 67:313–336
21. Brown S, Xia G, Luhachack LG, Campbell J, Meredith TC, Chen C, Winstel V, Gekeler C, Irazoqui JE, Peschel A, Walker S (2012) Methicillin resistance in Staphylococcus aureus requires glycosylated wall teichoic acids. Proc Natl Acad Sci USA 109(46):18909–18914
22. Brown S, Zhang YH, Walker S (2008) A revised pathway proposed for Staphylococcus aureus wall teichoic acid biosynthesis based on in vitro reconstitution of the intracellular steps. Chem Biol 15(1):12–21
23. Bubeck Wardenburg J, Patel RJ, Schneewind O (2007) Surface proteins and exotoxins are required for the pathogenesis of Staphylococcus aureus pneumonia. Infect Immun 75(2):1040–1044
24. Campbell J, Singh AK, Santa Maria JP Jr, Kim Y, Brown S, Swoboda JG, Mylonakis E, Wilkinson BJ, Walker S (2011) Synthetic lethal compound combinations reveal a fundamental connection between wall teichoic acid and peptidoglycan biosyntheses in Staphylococcus aureus. ACS Chem Biol 6(1):106–116
25. Campbell J, Singh AK, Swoboda JG, Gilmore MS, Wilkinson BJ, Walker S (2012) An antibiotic that inhibits a late step in wall teichoic acid biosynthesis induces the cell wall stress stimulon in Staphylococcus aureus. Antimicrob Agents Chemother 56(4):1810–1820
26. Cerca N, Brooks JL, Jefferson KK (2008) Regulation of the intercellular adhesin locus regulator (icaR) by SarA, sigmaB, and IcaR in Staphylococcus aureus. J Bacteriol 190(19):6530–6533
27. Cerca N, Jefferson KK, Maira-Litran T, Pier DB, Kelly-Quintos C, Goldmann DA, Azeredo J, Pier GB (2007) Molecular basis for preferential protective efficacy of antibodies directed to the poorly-acetylated form of staphylococcal poly-N-acetyl-{beta}-(1-6)-glucosamine. Infect Immun 75(13):3406–3413
28. Chan YG, Frankel MB, Dengler V, Schneewind O, Missiakas D (2013) Staphylococcus aureus mutants lacking the LytR-CpsA-Psr family of enzymes release cell wall teichoic acids into the extracellular medium. J Bacteriol 195(20):4650–4659
29. Chan YG, Kim HK, Schneewind O, Missiakas D (2014) The capsular polysaccharide of Staphylococcus aureus is attached to peptidoglycan by the LytR-CpsA-Psr (LCP) family of enzymes. J Biol Chem 289(22):15680–15690
30. Cocchiaro JL, Gomez MI, Risley A, Solinga R, Sordelli DO, Lee JC (2006) Molecular characterization of the capsule locus from non-typeable Staphylococcus aureus. Mol Microbiol 59(3):948–960
31. Cramton SE, Gerke C, Schnell NF, Nichols WW, Gotz F (1999) The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 67(10):5427–5433
32. Cramton SE, Ulrich M, Gotz F, Doring G (2001) Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun 69(6):4079–4085
33. Cunnion KM, Lee JC, Frank MM (2001) Capsule production and growth phase influence binding of complement to Staphylococcus aureus. Infect Immun 69:6796–6803
34. Cywes-Bentley C, Skurnik D, Zaidi T, Roux D, Deoliveira RB, Garrett WS, Lu X, O’Malley J, Kinzel K, Zaidi T, Rey A, Perrin C, Fichorova RN, Kayatani AK, Maira-Litran T, Gening ML, Tsvetkov YE, Nifantiev NE, Bakaletz LO, Pelton SI, Golenbock DT, Pier GB (2013) Antibody to a conserved antigenic target is protective against diverse prokaryotic and eukaryotic pathogens. Proc Natl Acad Sci USA 110(24):E2209–2218
35. D’Elia MA, Henderson JA, Beveridge TJ, Heinrichs DE, Brown ED (2009) The N-acetylmannosamine transferase catalyzes the first committed step of teichoic acid assembly in Bacillus subtilis and Staphylococcus aureus. J Bacteriol 191(12):4030–4034
36. D’Elia MA, Millar KE, Beveridge TJ, Brown ED (2006a) Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis. J Bacteriol 188(23):8313–8316
37. D’Elia MA, Pereira MP, Chung YS, Zhao W, Chau A, Kenney TJ, Sulavik MC, Black TA, Brown ED (2006b) Lesions in teichoic acid biosynthesis in Staphylococcus aureus lead to a lethal gain of function in the otherwise dispensable pathway. J Bacteriol 188(12):4183–4189
38. Dassy B, Hogan T, Foster TJ, Fournier JM (1993) Involvement of the accessory gene regulator (agr) in expression of type-5 capsular polysaccharide by Staphylococcus aureus. J Gen Microbiol 139:1301–1306
39. Dengler V, Meier PS, Heusser R, Kupferschmied P, Fazekas J, Friebe S, Staufer SB, Majcherczyk PA, Moreillon P, Berger-Bachi B, McCallum N (2012) Deletion of hypothetical wall teichoic acid ligases in Staphylococcus aureus activates the cell wall stress response. FEMS Microbiol Lett 333(2):109–120
40. Ding Y, Liu X, Chen F, Di H, Xu B, Zhou L, Deng X, Wu M, Yang CG, Lan L (2014) Metabolic sensor governing bacterial virulence in Staphylococcus aureus. Proc Natl Acad Sci USA 111 (46):E4981–4990
41. Endl J, Seidl HP, Fiedler F, Schleifer KH (1983) Chemical composition and structure of cell wall teichoic acids of staphylococci. Arch Microbiol 135(3):215–223
42. Endl J, Seidl PH, Fiedler F, Schleifer KH (1984) Determination of cell wall teichoic acid structure of staphylococci by rapid chemical and serological screening methods. Arch Microbiol 137 (3):272–280
43. Farha MA, Koteva K, Gale RT, Sewell EW, Wright GD, Brown ED (2014) Designing analogs of ticlopidine, a wall teichoic acid inhibitor, to avoid formation of its oxidative metabolites. Bioorg Med Chem Lett 24(3):905–910
44. Farha MA, Leung A, Sewell EW, D’Elia MA, Allison SE, Ejim L, Pereira PM, Pinho MG, Wright GD, Brown ED (2013) Inhibition of WTA synthesis blocks the cooperative action of PBPs and sensitizes MRSA to beta-lactams. ACS Chem Biol 8(1):226–233
45. Fattom A, Guidry A (1999) Response to letter to the editor—questions uniqueness of surface polysaccharide. Am J Vet Res 60(5):530
46. Fattom A, Matalon A, Buerkert J, Taylor K, Damaso S, Boutriau D (2015) Efficacy profile of a bivalent Staphylococcus aureus glycoconjugated vaccine in adults on hemodialysis: phase III randomized study. Hum Vaccin Immunother 11(3):632–641
47. Fattom A, Schneerson R, Szu SC, Vann WF, Shiloach J, Karakawa WW, Robbins JB (1990) Synthesis and immunologic properties in mice of vaccines composed of Staphylococcus aureus type 5 and type 8 capsular polysaccharides conjugated to Pseudomonas aeruginosa exotoxin A. Infect Immun 58(7):2367–2374
48. Fattom A, Schneerson R, Watson DC, Karakawa WW, Fitzgerald D, Pastan I, Li X, Shiloach J, Bryla DA, Robbins JB (1993) Laboratory and clinical evaluation of conjugate vaccines composed of Staphylococcus aureus type 5 and type 8 capsular polysaccharides bound to Pseudomonas aeruginosa recombinant exoprotein A. Infect Immun 61(3):1023–1032
49. Fattom AI, Sarwar J, Ortiz A, Naso R (1996) A Staphylococcus aureus capsular polysaccharide (CP) vaccine and CP-specific antibodies protect mice against bacterial challenge. Infect Immun 64(5):1659–1665
50. Fischer J, Lee JC, Peters G, Kahl BC (2014) Acapsular clinical Staphylococcus aureus isolates lack agr function. Clin Microbiol Infect 20(7):O414–417
51. Fischer W, Rosel P, Koch HU (1981) Effect of alanine ester substitution and other structural features of lipoteichoic acids on their inhibitory activity against autolysins of Staphylococcus aureus. J Bacteriol 146(2):467–475
52. Fluckiger U, Ulrich M, Steinhuber A, Doring G, Mack D, Landmann R, Goerke C, Wolz C (2005) Biofilm formation, icaADBC transcription, and polysaccharide intercellular adhesin synthesis by staphylococci in a device-related infection model. Infect Immun 73(3):1811–1819
53. Fournier B, Klier A, Rapoport G (2001) The two-component system ArlS-ArlR is a regulator of virulence gene expression in Staphylococcus aureus. Mol Microbiol 41(1):247–261
54. Fournier JM, Vann WF, Karakawa WW (1984) Purification and characterization of Staphylococcus aureus type 8 capsular polysaccharide. Infect Immun 45(1):87–93
55. Francois P, Tu Quoc PH, Bisognano C, Kelley WL, Lew DP, Schrenzel J, Cramton SE, Gotz F, Vaudaux P (2003) Lack of biofilm contribution to bacterial colonisation in an experimental model of foreign body infection by Staphylococcus aureus and Staphylococcus epidermidis. FEMS Immunol Med Microbiol 35(2):135–140
56. Frankel MB, Schneewind O (2012) Determinants of murein hydrolase targeting to cross-wall of Staphylococcus aureus peptidoglycan. J Biol Chem 287(13):10460–10471
57. Gening ML, Tsvetkov YE, Pier GB, Nifantiev NE (2007) Synthesis of beta-(1 → 6)-linked glucosamine oligosaccharides corresponding to fragments of the bacterial surface polysaccharide poly-N-acetylglucosamine. Carbohydr Res 342(3–4):567–575
58. George SE, Nguyen T, Geiger T, Weidenmaier C, Lee JC, Liese J, Wolz C (2015) Phenotypic heterogeneity and temporal expression of the capsular polysaccharide in Staphylococcus aureus. Mol Microbiol 98(16):1073–1088
59. Gerke C, Kraft A, Sussmuth R, Schweitzer O, Gotz F (1998) Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J Biol Chem 273(29):18586–18593
60. Ginsberg C, Zhang YH, Yuan Y, Walker S (2006) In vitro reconstitution of two essential steps in wall teichoic acid biosynthesis. ACS Chem Biol 1(1):25–28
61. Goerke C, Koller J, Wolz C (2006a) Ciprofloxacin and trimethoprim cause phage induction and virulence modulation in Staphylococcus aureus. Antimicrob Agents Chemother 50(1):171–177
62. Goerke C, Wirtz C, Fluckiger U, Wolz C (2006b) Extensive phage dynamics in Staphylococcus aureus contributes to adaptation to the human host during infection. Mol Microbiol 61 (6):1673–1685
63. Grangeasse C, Cozzone AJ, Deutscher J, Mijakovic I (2007) Tyrosine phosphorylation: an emerging regulatory device of bacterial physiology. Trends Biochem Sci 32(2):86–94
64. Gruszczyk J, Olivares-Illana V, Nourikyan J, Fleurie A, Bechet E, Gueguen-Chaignon V, Freton C, Aumont-Nicaise M, Morera S, Grangeasse C, Nessler S (2013) Comparative analysis of the Tyr-kinases CapB1 and CapB2 fused to their cognate modulators CapA1 and CapA2 from Staphylococcus aureus. PLoS ONE 8(10):e75958
65. Guo H, Yi W, Song JK, Wang PG (2008) Current understanding on biosynthesis of microbial polysaccharides. Curr Top Med Chem 8(2):141–151
66. 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 208(11):1841–1848
67. Hansenova Manaskova S, Bikker FJ, Veerman EC, van Belkum A, van Wamel WJ (2013) Rapid detection and semi-quantification of IgG-accessible Staphylococcus aureus surface-associated antigens using a multiplex competitive Luminex assay. J Immunol Methods 397(1–2):18–27
68. Hartmann T, Baronian G, Nippe N, Voss M, Schulthess B, Wolz C, Eisenbeis J, Schmidt-Hohagen K, Gaupp R, Sunderkotter C, Beisswenger C, Bals R, Somerville GA, Herrmann M, Molle V, Bischoff M (2014) The catabolite control protein E (CcpE) affects virulence determinant production and pathogenesis of Staphylococcus aureus. J Biol Chem 289(43):29701–29711
69. Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Gotz F (1996) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20 (5):1083–1091
70. 2 . J Bacteriol 183:4609–4613
71. 2 inhibition in vitro and in vivo. J Infect Dis 176:431–438
72. Hilmi D, Parcina M, Stollewerk D, Ostrop J, Josten M, Meilaender A, Zaehringer U, Wichelhaus TA, Bierbaum G, Heeg K, Wolz C, Bekeredjian-Ding I (2014) Heterogeneity of host TLR2 stimulation by Staphylocoocus aureus isolates. PLoS ONE 9(5):e96416
73. Hochkeppel HK, Braun DG, Vischer W, Imm A, Sutter S, Staeubli U, Guggenheim R, Kaplan EL, Boutonnier A, Fournier JM (1987) Serotyping and electron microscopy studies of Staphylococcus aureus clinical isolates with monoclonal antibodies to capsular polysaccharide types 5 and 8. J Clin Microbiol 25(3):526–530
74. Horwitz MA (1980) The roles of the Fc and C3 receptors in the phagocytosis and killing of bacteria by human phagocytes. J Reticuloendothel Soc 28(Suppl):17s–26s
75. Jansen A, Szekat C, Schroder W, Wolz C, Goerke C, Lee JC, Turck M, Bierbaum G (2013) Production of capsular polysaccharide does not influence Staphylococcus aureus vancomycin susceptibility. BMC Microbiol 13:65
76. Jefferson KK, Cramton SE, Gotz F, Pier GB (2003) Identification of a 5-nucleotide sequence that controls expression of the ica locus in Staphylococcus aureus and characterization of the DNA-binding properties of IcaR. Mol Microbiol 48(4):889–899
77. Jenni R, Berger-Bachi B (1998) Teichoic acid content in different lineages of Staphylococcus aureus NCTC8325. Arch Microbiol 170(3):171–178
78. Jones C (2005) Revised structures for the capsular polysaccharides from Staphylococcus aureus types 5 and 8, components of novel glycoconjugate vaccines. Carbohydr Res 340 (6):1097–1106
79. Jung DJ, An JH, Kurokawa K, Jung YC, Kim MJ, Aoyagi Y, Matsushita M, Takahashi S, Lee HS, Takahashi K, Lee BL (2012) Specific serum Ig recognizing staphylococcal wall teichoic acid induces complement-mediated opsonophagocytosis against Staphylococcus aureus. J Immunol 189(10):4951–4959
80. Kawai Y, Marles-Wright J, Cleverley RM, Emmins R, Ishikawa S, Kuwano M, Heinz N, Bui NK, Hoyland CN, Ogasawara N, Lewis RJ, Vollmer W, Daniel RA, Errington J (2011) A widespread family of bacterial cell wall assembly proteins. EMBO J 30(24):4931–4941
81. Kelly-Quintos C, Cavacini LA, Posner MR, Goldmann D, Pier GB (2006) Characterization of the opsonic and protective activity against Staphylococcus aureus of fully human monoclonal antibodies specific for the bacterial surface polysaccharide poly-N-acetylglucosamine. Infect Immun 74(5):2742–2750
82. Kelly-Quintos C, Kropec A, Briggs S, Ordonez C, Goldmann DA, Pier GB (2005) The role of epitope specificity in the human opsonic antibody response to the staphylococcal surface polysaccharide PNAG. J Infect Dis 192(11):2012–2019
83. Kern T, Giffard M, Hediger S, Amoroso A, Giustini C, Bui NK, Joris B, Bougault C, Vollmer W, Simorre JP (2010) Dynamics characterization of fully hydrated bacterial cell walls by solid-state NMR: evidence for cooperative binding of metal ions. J Am Chem Soc 132 (31):10911–10919
84. Kiser KB, Bhasin N, Deng L, Lee JC (1999a) Staphylococcus aureus cap5P encodes a UDP-N-acetylglucosamine 2-epimerase with functional redundancy. J Bacteriol 181 (16):4818–4824
85. Kiser KB, Cantey-Kiser JM, Lee JC (1999b) Development and characterization of a Staphylococcus aureus nasal colonization model in mice. Infect Immun 67(10):5001–5006
86. Kneidinger B, O’Riordan K, Li J, Brisson JR, Lee JC, Lam JS (2003) Three highly conserved proteins catalyze the conversion of UDP-N-acetyl-D-glucosamine to precursors for the biosynthesis of O antigen in Pseudomonas aeruginosa O11 and capsule in Staphylococcus aureus type 5. Implications for the UDP-N-acetyl-L-fucosamine biosynthetic pathway. J Biol Chem 278(6):3615–3627
87. Kojima N, Araki Y, Ito E (1985) Structure of the linkage units between ribitol teichoic acids and peptidoglycan. J Bacteriol 161:299–306
88. Kolata JB, Kuhbandner I, Link C, Normann N, Vu CH, Steil L, Weidenmaier C, Broker BM (2015) The fall of a dogma? Unexpected high T-cell memory response to Staphylococcus aureus in humans. J Infect Dis 212:830
89. Kropec A, Maira-Litran T, Jefferson KK, Grout M, Cramton SE, Gotz F, Goldmann DA, Pier GB, Kropec A, Maira-Litran T, Jefferson KK, Grout M, Cramton SE, Gotz F, Goldmann DA, Pier GB (2005) Poly-N-acetylglucosamine production in Staphylococcus aureus is essential for virulence in murine models of systemic infection. Infect Immun 73(10):6868–6876
90. Kurokawa K, Jung DJ, An JH, Fuchs K, Jeon YJ, Kim NH, Li X, Tateishi K, Park JA, Xia G, Matsushita M, Takahashi K, Park HJ, Peschel A, Lee BL (2013) Glycoepitopes of staphylococcal wall teichoic acid govern complement-mediated opsonophagocytosis via human serum antibody and mannose-binding lectin. J Biol Chem 288(43):30956–30968
91. Kuypers JM, Proctor RA (1989) Reduced adherence to traumatized rat heart valves by a low-fibronectin-binding mutant of Staphylococcus aureus. Infect Immun 57(8):2306–2312
92. Lazarevic V, Karamata D (1995) The tagGH operon of Bacillus subtilis 168 encodes a two-component ABC transporter involved in the metabolism of two wall teichoic acids. Mol Microbiol 16(2):345–355
93. Lee DC, Jia Z (2009) Emerging structural insights into bacterial tyrosine kinases. Trends Biochem Sci 34(7):351–357
94. Lee JC, Park JS, Shepherd SE, Carey V, Fattom A (1997) Protective efficacy of antibodies to the Staphylococcus aureus type 5 capsular polysaccharide in a modified model of endocarditis in rats. Infect Immun 65(10):4146–4151
95. Lee JC, Takeda S, Livolsi PJ, Paoletti LC (1993) Effects of in vitro and in vivo growth conditions on expression of type 8 capsular polysaccharide by Staphylococcus aureus. Infect Immun 61 (5):1853–1858
96. Lee JH, Kim NH, Winstel V, Kurokawa K, Larsen J, An JH, Khan A, Seong MY, Lee MJ, Andersen PS, Peschel A, Lee BL (2015) Surface-glycopolymers are crucial for in vitro anti-WTA IgG-mediated complement activation and opsonophagocytosis of Staphylococcus aureus. Infect Immun 83:4247
97. Lee K, Campbell J, Swoboda JG, Cuny GD, Walker S (2010) Development of improved inhibitors of wall teichoic acid biosynthesis with potent activity against Staphylococcus aureus. Bioorg Med Chem Lett 20(5):1767–1770
98. Levy J, Licini L, Haelterman E, Moris P, Lestrate P, Damaso S, Van Belle P, Boutriau D (2015) Safety and immunogenicity of an investigational 4-component Staphylococcus aureus vaccine with or without AS03B adjuvant: results of a randomized phase I trial. Hum Vaccin Immunother 11(3):620–631
99. Li W, Ulm H, Rausch M, Li X, O’Riordan K, Lee JC, Schneider T, Muller CE (2014) Analysis of the Staphylococcus aureus capsule biosynthesis pathway in vitro: characterization of the UDP-GlcNAc C6 dehydratases CapD and CapE and identification of enzyme inhibitors. Int J Med Microbiol 304(8):958–969
100. Liang X, Zheng L, Landwehr C, Lunsford D, Holmes D, Ji Y (2005) Global regulation of gene expression by ArlRS, a two-component signal transduction regulatory system of Staphylococcus aureus. J Bacteriol 187(15):5486–5492
101. Ling LL, Schneider T, Peoples AJ, Spoering AL, Engels I, Conlon BP, Mueller A, Schaberle TF, Hughes DE, Epstein S, Jones M, Lazarides L, Steadman VA, Cohen DR, Felix CR, Fetterman KA, Millett WP, Nitti AG, Zullo AM, Chen C, Lewis K (2015) A new antibiotic kills pathogens without detectable resistance. Nature 517 (7535):455-459
102. Luong T, Sau S, Gomez M, Lee JC, Lee CY (2002a) Regulation of Staphylococcus aureus capsular polysaccharide expression by agr and sarA. Infect Immun 70:444–450
103. Luong TT, Lee CY (2006) The arl locus positively regulates Staphylococcus aureus type 5 capsule via an mgrA-dependent pathway. Microbiology 152(Pt 10):3123–3131
104. Luong TT, Newell SW, Lee CY (2003) Mgr, a novel global regulator in Staphylococcus aureus. J Bacteriol 185(13):3703–3710
105. Luong TT, Ouyang S, Bush K, Lee CY (2002b) Type 1 capsule genes of Staphylococcus aureus are carried in a staphylococcal cassette chromosome genetic element. J Bacteriol 184 (13):3623–3629
106. Luong TT, Sau K, Roux C, Sau S, Dunman PM, Lee CY (2011) Staphylococcus aureus ClpC divergently regulates capsule via sae and codY in strain Newman but activates capsule via codY in strain UAMS-1 and in strain Newman with repaired saeS. J Bacteriol 193(3):686–694
107. Mack D, Fischer W, Krokotsch A, Leopold K, Hartmann R, Egge H, Laufs R (1996a) The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol 178:175–183
108. Mack D, Haeder M, Siemssen N, Laufs R (1996b) Association of biofilm production of coagulase-negative staphylococci with expression of a specific polysaccharide intercellular adhesin. J Infect Dis 174(4):881–884
109. Maira-Litran T, Kropec A, Abeygunawardana C, Joyce J, Mark G 3rd, Goldmann DA, Pier GB (2002) Immunochemical properties of the staphylococcal poly-N-acetylglucosamine surface polysaccharide. Infect Immun 70(8):4433–4440
110. Maira-Litran T, Kropec A, Goldmann DA, Pier GB (2005) Comparative opsonic and protective activities of Staphylococcus aureus conjugate vaccines containing native or deacetylated Staphylococcal Poly-N-acetyl-beta-(1-6)-glucosamine. Infect Immun 73(10):6752–6762
111. Majerczyk CD, Dunman PM, Luong TT, Lee CY, Sadykov MR, Somerville GA, Bodi K, Sonenshein AL (2010) Direct targets of CodY in Staphylococcus aureus. J Bacteriol 192 (11):2861–2877
112. Majerczyk CD, Sadykov MR, Luong TT, Lee C, Somerville GA, Sonenshein AL (2008) Staphylococcus aureus CodY negatively regulates virulence gene expression. J Bacteriol 190 (7):2257–2265
113. Matias VR, Beveridge TJ (2005) Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol Microbiol 56 (1):240–251
114. Matias VR, Beveridge TJ (2006) Native cell wall organization shown by cryo-electron microscopy confirms the existence of a periplasmic space in Staphylococcus aureus. J Bacteriol 188 (3):1011–1021
115. May JJ, Finking R, Wiegeshoff F, Weber TT, Bandur N, Koert U, Marahiel MA (2005) Inhibition of the D-alanine: D-alanyl carrier protein ligase from Bacillus subtilis increases the bacterium’s susceptibility to antibiotics that target the cell wall. FEBS J 272(12):2993–3003
116. McKenney D, Pouliot KL, Wang Y, Murthy V, Ulrich M, Doring G, Lee JC, Goldmann DA, Pier GB (1999) Broadly protective vaccine for Staphylococcus aureus based on an in vivo-expressed antigen. Science 284:1523–1527
117. McLoughlin RM, Solinga RM, Rich J, Zaleski KJ, Cocchiaro JL, Risley A, Tzianabos AO, Lee JC (2006) CD4 + T cells and CXC chemokines modulate the pathogenesis of Staphylococcus aureus wound infections. Proc Natl Acad Sci USA 103(27):10408–10413
118. Meier S, Goerke C, Wolz C, Seidl K, Homerova D, Schulthess B, Kormanec J, Berger-Bachi B, Bischoff M (2007) sigmaB and the sigmaB-dependent arlRS and yabJ-spoVG loci affect capsule formation in Staphylococcus aureus. Infect Immun 75(9):4562–4571
119. Meredith TC, Swoboda JG, Walker S (2008) Late-stage polyribitol phosphate wall teichoic acid biosynthesis in Staphylococcus aureus. J Bacteriol 190(8):3046–3056
120. Misawa Y, Kelley KA, Wang X, Wang L, Park WB, Birtel J, Saslowsky D, Lee JC (2015) Staphylococcus aureus colonization of the mouse gastrointestinal tract is modulated by wall teichoic acid, capsule, and surface proteins. PLoS Pathog 11(7):e1005061
121. Mishra NN, Bayer AS, Weidenmaier C, Grau T, Wanner S, Stefani S, Cafiso V, Bertuccio T, Yeaman MR, Nast CC, Yang SJ (2014) Phenotypic and genotypic characterization of daptomycin-resistant methicillin-resistant Staphylococcus aureus strains: relative roles of mprF and dlt operons. PLoS ONE 9(9):e107426
122. Montgomery CP, Boyle-Vavra S, Adem PV, Lee JC, Husain AN, Clasen J, Daum RS (2008) Comparison of virulence in community-associated methicillin-resistant Staphylococcus aureus pulsotypes USA300 and USA400 in a rat model of pneumonia. J Infect Dis 198(4):561–570
123. Moreau M, Richards JC, Fournier JM, Byrd RA, Karakawa WW, Vann WF (1990) Structure of the type-5 capsular polysaccharide of Staphylococcus aureus. Carbohydrate Res 201(2):285–297
124. Moreillon P, Entenza JM, Francioli P, McDevitt D, Foster TJ, Francois P, Vaudaux P (1995) Role of Staphylococcus aureus coagulase and clumping factor in pathogenesis of experimental endocarditis. Infect Immun 63(12):4738–4743
125. Morona JK, Morona R, Miller DC, Paton JC (2002) Streptococcus pneumoniae capsule biosynthesis protein CpsB is a novel manganese-dependent phosphotyrosine-protein phosphatase. J Bacteriol 184(2):577–583
126. Muller E, Hubner J, Gutierrez N, Takeda S, Goldmann DA, Pier GB (1993) Isolation and characterization of transposon mutants of Staphylococcus epidermidis deficient in capsular polysaccharide/adhesin and slime. Infect Immun 61(2):551–558
127. Nanra JS, Buitrago SM, Crawford S, Ng J, Fink PS, Hawkins J, Scully IL, McNeil LK, Aste-Amézaga JM, Cooper D (2013) Capsular polysaccharides are an important immune evasion mechanism for Staphylococcus aureus. Hum Vaccines Immunotherapeutics 9 (3):480–487
128. Nemeth J, Lee JC (1995) Antibodies to capsular polysaccharides are not protective against experimental Staphylococcus aureus endocarditis. Infect Immun 63:375–380
129. Neuhaus FC, Baddiley J (2003) A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol Mol Biol Rev 67(4):686–723
130. Nilsson I-M, Lee JC, Bremell T, Ryden C, Tarkowski A (1997) The role of staphylococcal polysaccharide microcapsule expression in septicemia and septic arthritis. Infect Immun 65:4216–4221
131. Nissen M, Marshall H, Richmond P, Shakib S, Jiang Q, Cooper D, Rill D, Baber J, Eiden J, Gruber W, Jansen KU, Emini EA, Anderson AS, Zito ET, Girgenti D (2015) A randomized phase I study of the safety and immunogenicity of three ascending dose levels of a 3-antigen Staphylococcus aureus vaccine (SA3Ag) in healthy adults. Vaccine 33(15):1846–1854
132. Novick RP, Geisinger E (2008) Quorum sensing in staphylococci. Annu Rev Genet 42:541–564
133. O’Riordan K, Lee JC (2004) Staphylococcus aureus capsular polysaccharides. Clin Microbiol Rev 17(1):218–234
134. Park KH, Kurokawa K, Zheng L, Jung DJ, Tateishi K, Jin JO, Ha NC, Kang HJ, Matsushita M, Kwak JY, Takahashi K, Lee BL (2010) Human serum mannose-binding lectin senses wall teichoic acid glycopolymer of Staphylococcus aureus, which is restricted in infancy. J Biol Chem 285(35):27167–27175
135. Park S, Gerber S, Lee JC (2014) Antibodies to Staphylococcus aureus serotype 8 capsular polysaccharide react with and protect against serotype 5 and 8 isolates. Infect Immun 82 (12):5049–5055
136. Perego M, Glaser P, Minutello A, Strauch MA, Leopold K, Fischer W (1995) Incorporation of D-alanine into lipoteichoic acid and wall teichoic acid in Bacillus subtilis. Identification of genes and regulation. J Biol Chem 270(26):15598–15606
137. Pereira MP, Brown ED (2004) Bifunctional catalysis by CDP-ribitol synthase: convergent recruitment of reductase and cytidylyltransferase activities in Haemophilus influenzae and Staphylococcus aureus. Biochemistry 43(37):11802–11812
138. Pereira MP, D’Elia MA, Troczynska J, Brown ED (2008) Duplication of teichoic acid biosynthetic genes in Staphylococcus aureus leads to functionally redundant poly(ribitol phosphate) polymerases. J Bacteriol 190(16):5642–5649
139. Peschel A, Otto M, Jack RW, Kalbacher H, Jung G, Gotz F (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274(13):8405–8410
140. Peschel A, Vuong C, Otto M, Gotz F (2000) The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrob Agents Chemother 44(10):2845–2847
141. Pohl K, Francois P, Stenz L, Schlink F, Geiger T, Herbert S, Goerke C, Schrenzel J, Wolz C (2009) CodY in Staphylococcus aureus: a regulatory link between metabolism and virulence gene expression. J Bacteriol 191(9):2953–2963
142. Pohlmann-Dietze P, Ulrich M, Kiser KB, Doring G, Lee JC, Fournier JM, Botzenhart K, Wolz C (2000) Adherence of Staphylococcus aureus to endothelial cells: influence of capsular polysaccharide, global regulator agr, and bacterial growth phase. Infect Immun 68(9):4865– 4871
143. Portoles M, Kiser KB, Bhasin N, Chan KHN, Lee JC (2001) Staphylococcus aureus Cap5O has UDP-ManNAc dehydrogenase activity and is essential for capsule expression. Infect Immun 69:917–923
144. Poutrel B, Gilbert FB, Lebrun M (1995) Effects of culture conditions on production of type 5 capsular polysaccharide by human and bovine Staphylococcus aureus strains. Clin Diagn Lab Immunol 2:166–171
145. Poutrel B, Rainard P, Sarradin P (1997) Heterogeneity of cell-associated CP5 expression on Staphylococcus aureus strains demonstrated by flow cytometry. Clin Diagn Lab Immunol 4:275–278
146. Qamar A, Golemi-Kotra D (2012) Dual roles of FmtA in Staphylococcus aureus cell wall biosynthesis and autolysis. Antimicrob Agents Chemother 56(7):3797–3805
147. Qian Z, Yin Y, Zhang Y, Lu L, Li Y, Jiang Y (2006) Genomic characterization of ribitol teichoic acid synthesis in Staphylococcus aureus: genes, genomic organization and gene duplication. BMC Genom 7:74
148. Rachid S, Ohlsen K, Wallner U, Hacker J, Hecker M, Ziebuhr W (2000) Alternative transcription factor sigma(B) is involved in regulation of biofilm expression in a Staphylococcus aureus mucosal isolate. J Bacteriol 182(23):6824–6826
149. Reichmann NT, Cassona CP, Grundling A (2013) Revised mechanism of D-alanine incorporation into cell wall polymers in Gram-positive bacteria. Microbiology 159(Pt 9):1868–1877
150. Risley AL, Loughman A, Cywes-Bentley C, Foster TJ, Lee JC (2007) Capsular polysaccharide masks clumping factor A-mediated adherence of Staphylococcus aureus to fibrinogen and platelets. J Infect Dis 196(6):919–927
151. Roberts IS, Saunders FK, Boulnois GJ (1989) Bacterial capsules and interactions with complement and phagocytes. Biochem Soc Trans 17(3):462–464
152. Roghmann M, Taylor KL, Gupte A, Zhan M, Johnson JA, Cross A, Edelman R, Fattom AI (2005) Epidemiology of capsular and surface polysaccharide in Staphylococcus aureus infections complicated by bacteraemia. J Hosp Infect 59(1):27–32
153. Romilly C, Lays C, Tomasini A, Caldelari I, Benito Y, Hammann P, Geissmann T, Boisset S, Romby P, Vandenesch F (2014) A non-coding RNA promotes bacterial persistence and decreases virulence by regulating a regulator in Staphylococcus aureus. PLoS Pathog 10(3): e1003979
154. Sadovskaya I, Vinogradov E, Flahaut S, Kogan G, Jabbouri S (2005) Extracellular carbohydrate-containing polymers of a model biofilm-producing strain, Staphylococcus epidermidis RP62A. Infect Immun 73(5):3007–3017
155. Sau S, Bhasin N, Wann ER, Lee JC, Foster TJ, Lee CY (1997a) The Staphylococcus aureus allelic genetic loci for serotype 5 and 8 capsule expression contain the type-specific genes flanked by common genes. Microbiol 143:2395–2405
156. Sau S, Sun J, Lee CY (1997b) Molecular characterization and transcriptional analysis of type 8 capsule genes in Staphylococcus aureus. J Bacteriol 179:1614–1621
157. Schaffer AC, Solinga RM, Cocchiaro J, Portoles M, Kiser KB, Risley A, Randall SM, Valtulina V, Speziale P, Walsh E, Foster T, Lee JC (2006) Immunization with Staphylococcus aureus clumping factor B, a major determinant in nasal carriage, reduces nasal colonization in a murine model. Infect Immun 74(4):2145–2153
158. Schlag M, Biswas R, Krismer B, Kohler T, Zoll S, Yu W, Schwarz H, Peschel A, Gotz F (2010) Role of staphylococcal wall teichoic acid in targeting the major autolysin Atl. Mol Microbiol 75(4):864–873
159. Schulthess B, Meier S, Homerova D, Goerke C, Wolz C, Kormanec J, Berger-Bachi B, Bischoff M (2009) Functional characterization of the sigmaB-dependent yabJ-spoVG operon in Staphylococcus aureus: role in methicillin and glycopeptide resistance. Antimicrob Agents Chemother 53(5):1832–1839
160. Scully IL, Liberator PA, Jansen KU, Anderson AS (2014) Covering all the bases: preclinical development of an effective Staphylococcus aureus vaccine. Front Immunol 5:109
161. Scully IL, Timofeyeva Y, Keeney D, Matsuka YV, Severina E, McNeil LK, Nanra J, Hu G, Liberator PA, Jansen KU, Anderson AS (2015) Demonstration of the preclinical correlate of protection for Staphylococcus aureus clumping factor A in a murine model of infection. Vaccine 33(41):5452–5457
162. Seidl K, Stucki M, Ruegg M, Goerke C, Wolz C, Harris L, Berger-Bachi B, Bischoff M (2006) Staphylococcus aureus CcpA affects virulence determinant production and antibiotic resistance. Antimicrob Agents Chemother 50(4):1183–1194
163. Sewell EW, Brown ED (2014) Taking aim at wall teichoic acid synthesis: new biology and new leads for antibiotics. J Antibiot (Tokyo) 67(1):43–51
164. Shinefield H, Black S, Fattom A, Horwith G, Rasgon S, Ordonez J, Yeoh H, Law D, Robbins JB, Schneerson R, Muenz L, Fuller S, Johnson J, Fireman B, Alcorn H, Naso R (2002) Use of a Staphylococcus aureus conjugate vaccine in patients receiving hemodialysis. N Engl J Med 346(7):491–496
165. Skurnik D, Merighi M, Grout M, Gadjeva M, Maira-Litran T, Ericsson M, Goldmann DA, Huang SS, Datta R, Lee JC, Pier GB (2010) Animal and human antibodies to distinct Staphylococcus aureus antigens mutually neutralize opsonic killing and protection in mice. J Clin Invest 120(9):3220–3233
166. Soldo B, Lazarevic V, Karamata D (2002a) tagO is involved in the synthesis of all anionic cell-wall polymers in Bacillus subtilis 168. Microbiology 148(Pt 7):2079–2087
167. Soldo B, Lazarevic V, Pooley HM, Karamata D (2002b) Characterization of a Bacillus subtilis thermosensitive teichoic acid-deficient mutant: gene mnaA (yvyH) encodes the UDP-N-acetylglucosamine 2-epimerase. J Bacteriol 184(15):4316–4320
168. Soulat D, Grangeasse C, Vaganay E, Cozzone AJ, Duclos B (2007) UDP-acetyl-mannosamine dehydrogenase is an endogenous protein substrate of Staphylococcus aureus protein-tyrosine kinase activity. J Mol Microbiol Biotechnol 13(1–3):45–54
169. Soulat D, Jault JM, Duclos B, Geourjon C, Cozzone AJ, Grangeasse C (2006) Staphylococcus aureus operates protein-tyrosine phosphorylation through a specific mechanism. J Biol Chem 281(20):14048–14056
170. Steinhuber A, Goerke C, Bayer MG, Doring G, Wolz C (2003) Molecular architecture of the regulatory locus sae of Staphylococcus aureus and its impact on expression of virulence factors. J Bacteriol 185(21):6278–6286
171. Sun F, Ji Q, Jones MB, Deng X, Liang H, Frank B, Telser J, Peterson SN, Bae T, He C (2012) AirSR, a [2Fe-2S] cluster-containing two-component system, mediates global oxygen sensing and redox signaling in Staphylococcus aureus. J Am Chem Soc 134(1):305–314
172. Sutcliffe IC (2012) Exposing a chink in the armor of methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci USA 109(46):18637–18638
173. Suzuki T, Campbell J, Swoboda JG, Walker S, Gilmore MS (2011a) Role of wall teichoic acids in Staphylococcus aureus endophthalmitis. Invest Ophthalmol Vis Sci 52(6):3187–3192
174. Suzuki T, Swoboda JG, Campbell J, Walker S, Gilmore MS (2011b) In vitro antimicrobial activity of wall teichoic acid biosynthesis inhibitors against Staphylococcus aureus isolates. Antimicrob Agents Chemother 55(2):767–774
175. Swoboda JG, Campbell J, Meredith TC, Walker S (2010) Wall teichoic acid function, biosynthesis, and inhibition. ChemBioChem 11(1):35–45
176. Swoboda JG, Meredith TC, Campbell J, Brown S, Suzuki T, Bollenbach T, Malhowski AJ, Kishony R, Gilmore MS, Walker S (2009) Discovery of a small molecule that blocks wall teichoic acid biosynthesis in Staphylococcus aureus. ACS Chem Biol 4(10):875–883
177. Takahashi K, Kurokawa K, Moyo P, Jung DJ, An JH, Chigweshe L, Paul E, Lee BL (2013) Intradermal immunization with wall teichoic acid (WTA) elicits and augments an anti-WTA IgG response that protects mice from methicillin-resistant Staphylococcus aureus infection independent of mannose-binding lectin status. PLoS ONE 8(8):e69739
178. Thakker M, Park J-S, 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
179. Thoendel M, Kavanaugh JS, Flack CE, Horswill AR (2011) Peptide signaling in the staphylococci. Chem Rev 111(1):117–151
180. Thomas KJ, Rice CV (2015) Equilibrium binding behavior of magnesium to wall teichoic acid. Biochim Biophys Acta 1848 (10 Pt A):1981–1987
181. Tu Quoc PH, Genevaux P, Pajunen M, Savilahti H, Georgopoulos C, Schrenzel J, Kelley WL (2007) Isolation and characterization of biofilm formation-defective mutants of Staphylococcus aureus. Infect Immun 75(3):1079–1088
182. Tuchscherr LP, Buzzola FR, Alvarez LP, Caccuri RL, Lee JC, Sordelli DO (2005) Capsule-negative Staphylococcus aureus induces chronic experimental mastitis in mice. Infect Immun 73(12):7932–7937
183. Tuchscherr LP, Buzzola FR, Alvarez LP, Lee JC, Sordelli DO (2008) Antibodies to capsular polysaccharide and clumping factor A prevent mastitis and the emergence of unencapsulated and small-colony variants of Staphylococcus aureus in mice. Infect Immun 76(12):5738–5744
184. Tzianabos AO, Wang JY, Lee JC (2001) Structural rationale for the modulation of abscess formation by Staphylococcus aureus capsular polysaccharides. Proc Natl Acad Sci USA 98 (16):9365–9370
185. Ubeda C, Maiques E, Knecht E, Lasa I, Novick RP, Penades JR (2005) Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol Microbiol 56(3):836–844
186. Valle J, Toledo-Arana A, Berasain C, Ghigo JM, Amorena B, Penades JR, Lasa I (2003) SarA and not sigmaB is essential for biofilm development by Staphylococcus aureus. Mol Microbiol 48 (4):1075–1087
187. Verdier I, Durand G, Bes M, Taylor KL, Lina G, Vandenesch F, Fattom AI, Etienne J (2007) Identification of the capsular polysaccharides in Staphylococcus aureus clinical isolates by PCR and agglutination tests. J Clin Microbiol 45(3):725–729
188. Vuong C, Kocianova S, Voyich JM, Yao Y, Fischer ER, DeLeo FR, Otto M (2004a) A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem 279(52):54881–54886
189. Vuong C, Kocianova S, Yao Y, Carmody AB, Otto M (2004b) Increased colonization of indwelling medical devices by quorum-sensing mutants of Staphylococcus epidermidis in vivo. J Infect Dis 190(8):1498–1505
190. Wacker M, Wang L, Kowarik M, Dowd M, Lipowsky G, Faridmoayer A, Shields K, Park S, Alaimo C, Kelley KA, Braun M, Quebatte J, Gambillara V, Carranza P, Steffen M, Lee JC (2014) Prevention of Staphylococcus aureus infections by glycoprotein vaccines synthesized in Escherichia coli. J Infect Dis 209(10):1551–1561
191. Wang H, Gill CJ, Lee SH, Mann P, Zuck P, Meredith TC, Murgolo N, She X, Kales S, Liang L, Liu J, Wu J, Santa Maria J, Su J, Pan J, Hailey J, McGuinness D, Tan CM, Flattery A, Walker S, Black T, Roemer T (2013) Discovery of wall teichoic acid inhibitors as potential anti-MRSA beta-lactam combination agents. Chem Biol 20(2):272–284
192. Watts A, Ke D, Wang Q, Pillay A, Nicholson-Weller A, Lee JC (2005) Staphylococcus aureus strains that express serotype 5 or serotype 8 capsular polysaccharides differ in virulence. Infect Immun 73(6):3502–3511
193. Wecke J, Perego M, Fischer W (1996) D-alanine deprivation of Bacillus subtilis teichoic acids is without effect on cell growth and morphology but affects the autolytic activity. Microb Drug Resist 2(1):123–129
194. Weidenmaier C, Goerke C, Wolz C (2012) Staphylococcus aureus determinants for nasal colonization. Trends Microbiol 20(5):243–250
195. Weidenmaier C, Kokai-Kun JF, Kristian SA, Chanturiya T, Kalbacher H, Gross M, Nicholson G, Neumeister B, Mond JJ, Peschel A (2004) Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 10(3):243–245
196. Weidenmaier C, McLoughlin RM, Lee JC (2010) The zwitterionic cell wall teichoic acid of Staphylococcus aureus provokes skin abscesses in mice by a novel CD4 + T-cell-dependent mechanism. PLoS ONE 5(10):e13227
197. Weidenmaier C, Peschel A (2008) Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 6(4):276–287
198. Weidenmaier C, Peschel A, Xiong YQ, Kristian SA, Dietz K, Yeaman MR, Bayer AS (2005) Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J Infect Dis 191 (10):1771–1777
199. Wickham JR, Halye JL, Kashtanov S, Khandogin J, Rice CV (2009) Revisiting magnesium chelation by teichoic acid with phosphorus solid-state NMR and theoretical calculations. J Phys Chem B 113(7):2177–2183
200. Wilkinson J (1958) The extracellular polysaccharides of bacteria. Bacteriol Rev 22:46–73
201. Winstel V, Kuhner P, Salomon F, Larsen J, Skov R, Hoffmann W, Peschel A, Weidenmaier C (2015) Wall teichoic acid glycosylation governs Staphylococcus aureus nasal colonization. mBio 6 (4):e00632
202. Winstel V, Liang C, Sanchez-Carballo P, Steglich M, Munar M, Broker BM, Penades JR, Nubel U, Holst O, Dandekar T, Peschel A, Xia G (2013) Wall teichoic acid structure governs horizontal gene transfer between major bacterial pathogens. Nat Commun 4:2345
203. Winstel V, Sanchez-Carballo P, Holst O, Xia G, Peschel A (2014a) Biosynthesis of the unique wall teichoic acid of Staphylococcus aureus lineage ST395. mBio 5 (2):e00869
204. Winstel V, Xia G, Peschel A (2014b) Pathways and roles of wall teichoic acid glycosylation in Staphylococcus aureus. Int J Med Microbiol 304(3-4):215-221
205. Xia G, Corrigan RM, Winstel V, Goerke C, Grundling A, Peschel A (2011) Wall teichoic acid-dependent adsorption of staphylococcal siphovirus and myovirus. J Bacteriol 193 (15):4006–4009
206. Xia G, Maier L, Sanchez-Carballo P, Li M, Otto M, Holst O, Peschel A (2010) Glycosylation of wall teichoic acid in Staphylococcus aureus by TarM. J Biol Chem 285(18):13405–13415
207. Xia G, Wolz C (2014) Phages of Staphylococcus aureus and their impact on host evolution. Infect Genet Evol 21:593–601
208. Zhang YH, Ginsberg C, Yuan Y, Walker S (2006) Acceptor substrate selectivity and kinetic mechanism of Bacillus subtilis TagA. Biochemistry 45(36):10895–10904