Cell wall-anchored surface proteins of Staphylococcus aureus: Many proteins, multiple functions

Current Topics in Microbiology and Immunology

Volumn 409, Issue , 2017, Pages 95-120

  Geoghegan, Joan A ^a   Foster, Timothy J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CELL MEMBRANE PROTEIN; CELL SURFACE PROTEIN; FIBRIN; FIBRINOGEN; FIBRONECTIN BINDING PROTEIN; LECTIN; NUCLEOTIDASE; PEPTIDOGLYCAN; PROTEIN DOCK; PROTEIN LATCH; PROTEIN LOCK; PROTEIN MSCRAMM; PROTEIN SASG; UNCLASSIFIED DRUG; VIRULENCE FACTOR; MEMBRANE PROTEIN;

BACTERIAL CELL WALL; BACTERIAL COLONIZATION; CELL ADHESION; CELL INVASION; CELL PROLIFERATION; CELL SURFACE DISPLAY; CELL SURVIVAL; COMMENSAL; EPITHELIUM CELL; HOST CELL; HUMAN; INNATE IMMUNITY; LIGAND BINDING; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TARGETING; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; TRIPLE HELIX; BACTERIUM ADHERENCE; CELL WALL;

BACTERIAL ADHESION; BACTERIAL PROTEINS; CELL WALL; MEMBRANE PROTEINS; STAPHYLOCOCCUS AUREUS;

EID: 85041292207     PISSN: 0070217X     EISSN: 21969965     Source Type: Book Series    
DOI: 10.1007/82_2015_5002     Document Type: Chapter

References (130)

1. Antikainen J, Kuparinen V, Lahteenmaki K, Korhonen TK (2007) Enolases from Gram-positive bacterial pathogens and commensal lactobacilli share functional similarity in virulence-associated traits. FEMS Immunol Med Microbiol 51:526–534
2. Arrecubieta C et al (2006) The role of Staphylococcus aureus adhesins in the pathogenesis of ventricular assist device-related infections. J Infect Dis 193:1109–1119
3. Barbu EM et al (2010) beta-Neurexin is a ligand for the Staphylococcus aureus MSCRAMM SdrC. PLoS Pathog 6:e1000726
4. Barbu EM, Mackenzie C, Foster TJ, Hook M (2014) SdrC induces staphylococcal biofilm formation through a homophilic interaction. Mol Microbiol 94:172–185
5. Becker S, Frankel MB, Schneewind O, Missiakas D (2014) Release of protein A from the cell wall of Staphylococcus aureus. Proc Natl Acad Sci U S A 111:1574–1579
6. Berends ET, Horswill AR, Haste NM, Monestier M, Nizet V, von Kockritz-Blickwede M (2010) Nuclease expression by Staphylococcus aureus facilitates escape from neutrophil extracellular traps. J Innate Immun 2:576–586
7. Brouillette E, Grondin G, Shkreta L, Lacasse P, Talbot BG (2003) In vivo and in vitro demonstration that Staphylococcus aureus is an intracellular pathogen in the presence or absence of fibronectin-binding proteins. Microb Pathog 35:159–168
8. Burke FM, Di Poto A, Speziale P, Foster TJ (2011) The A domain of fibronectin-binding protein B of Staphylococcus aureus contains a novel fibronectin binding site. FEBS J 278:2359–2371
9. Burman JD et al (2008) Interaction of human complement with Sbi, a staphylococcal immunoglobulin-binding protein: indications of a novel mechanism of complement evasion by Staphylococcus aureus. J Biol Chem 283:17579–17593
10. Cassat JE, Skaar EP (2012) Metal ion acquisition in Staphylococcus aureus: overcoming nutritional immunity. Semin Immunopathol 34:215–235
11. Cheng AG, Kim HK, Burts ML, Krausz T, Schneewind O, Missiakas DM (2009) Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. FASEB J 23:3393–3404
12. Clarke SR et al (2006) Identification of in vivo-expressed antigens of Staphylococcus aureus and their use in vaccinations for protection against nasal carriage. J Infect Dis 193:1098–1108
13. Clarke SR et al (2007) The Staphylococcus aureus surface protein IsdA mediates resistance to innate defenses of human skin. Cell Host Microbe 1:199–212
14. Clarke SR, Andre G, Walsh EJ, Dufrene YF, Foster TJ, Foster SJ (2009) Iron-regulated surface determinant protein A mediates adhesion of Staphylococcus aureus to human corneocyte envelope proteins. Infect Immun 77:2408–2416
15. Clarke SR, Foster SJ (2008) IsdA protects Staphylococcus aureus against the bactericidal protease activity of apolactoferrin. Infect Immun 76:1518–1526
16. Clarke SR, Wiltshire MD, Foster SJ (2004) IsdA of Staphylococcus aureus is a broad spectrum, iron-regulated adhesin. Mol Microbiol 51:1509–1519
17. Conrady DG, Wilson JJ, Herr AB (2013) Structural basis for Zn2+-dependent intercellular adhesion in staphylococcal biofilms. Proc Natl Acad Sci U S A 110:E202–E211
18. Corrigan RM, Miajlovic H, Foster TJ (2009) Surface proteins that promote adherence of Staphylococcus aureus to human desquamated nasal epithelial cells. BMC Microbiol 9:22
19. Corrigan RM, Rigby D, Handley P, Foster TJ (2007) The role of Staphylococcus aureus surface protein SasG in adherence and biofilm formation. Microbiology 153:2435–2446
20. Cregg KM, Wilding I, Black MT (1996) Molecular cloning and expression of the spsB gene encoding an essential type I signal peptidase from Staphylococcus aureus. J Bacteriol 178:5712–5718
21. Dastgheyb S, Parvizi J, Shapiro IM, Hickok NJ, Otto M (2015) Effect of biofilms on recalcitrance of staphylococcal joint infection to antibiotic treatment. J Infect Dis 211:641–650
22. DeDent A, Bae T, Missiakas DM, Schneewind O (2008) Signal peptides direct surface proteins to two distinct envelope locations of Staphylococcus aureus. EMBO J 27:2656–2668
23. Deis LN et al (2015) Suppression of conformational heterogeneity at a protein-protein interface. Proc Natl Acad Sci U S A 112:9028–9033
24. Deivanayagam CC et al (2000) Novel fold and assembly of the repetitive B region of the Staphylococcus aureus collagen-binding surface protein. Structure 8:67–78
25. Deivanayagam CC et al (2002) A novel variant of the immunoglobulin fold in surface adhesins of Staphylococcus aureus: crystal structure of the fibrinogen-binding MSCRAMM, clumping factor A. EMBO J 21:6660–6672
26. Dziewanowska K, Patti JM, Deobald CF, Bayles KW, Trumble WR, Bohach GA (1999) Fibronectin binding protein and host cell tyrosine kinase are required for internalization of Staphylococcus aureus by epithelial cells. Infect Immun 67:4673–4678
27. Entenza JM, Foster TJ, Ni Eidhin D, Vaudaux P, Francioli P, Moreillon P (2000) Contribution of clumping factor B to pathogenesis of experimental endocarditis due to Staphylococcus aureus. Infect Immun 68:5443–5446
28. Flick MJ et al (2013) Genetic elimination of the binding motif on fibrinogen for the S. aureus virulence factor ClfA improves host survival in septicemia. Blood 121:1783–1794
29. Foster TJ, Geoghegan JA, Ganesh VK, Hook M (2014) Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 12:49–62
30. Ganesh VK et al (2008) A structural model of the Staphylococcus aureus ClfA-fibrinogen interaction opens new avenues for the design of anti-staphylococcal therapeutics. PLoS Pathog 4:e1000226
31. Ganesh VK et al (2011) Structural and biochemical characterization of Staphylococcus aureus clumping factor B/ligand interactions. J Biol Chem 286:25963–25972
32. Geoghegan JA et al (2010) Role of surface protein SasG in biofilm formation by Staphylococcus aureus. J Bacteriol 192:5663–5673
33. Geoghegan JA, Monk IR, O’Gara JP, Foster TJ (2013) Subdomains N2N3 of fibronectin binding protein A mediate Staphylococcus aureus biofilm formation and adherence to fibrinogen using distinct mechanisms. J Bacteriol 195:2675–2683
34. Gomez MI et al (2004) Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nat Med 10:842–848
35. Gomez MI, O’Seaghdha M, Magargee M, Foster TJ, Prince AS (2006) Staphylococcus aureus protein A activates TNFR1 signaling through conserved IgG binding domains. J Biol Chem 281:20190–20196
36. Graille M et al (2000) Crystal structure of a Staphylococcus aureus protein A domain complexed with the Fab fragment of a human IgM antibody: structural basis for recognition of B-cell receptors and superantigen activity. Proc Natl Acad Sci U S A 97:5399–5404
37. Grigg JC, Ukpabi G, Gaudin CF, Murphy ME (2010) Structural biology of heme binding in the Staphylococcus aureus Isd system. J Inorg Biochem 104:341–348
38. Grundmeier M, Hussain M, Becker P, Heilmann C, Peters G, Sinha B (2004) Truncation of fibronectin-binding proteins in Staphylococcus aureus strain Newman leads to deficient adherence and host cell invasion due to loss of the cell wall anchor function. Infect Immun 72:7155–7163
39. Gruszka DT et al (2012) Staphylococcal biofilm-forming protein has a contiguous rod-like structure. Proc Natl Acad Sci U S A 109:E1011–E1018
40. Gruszka DT et al (2015) Cooperative folding of intrinsically disordered domains drives assembly of a strong elongated protein. Nat Commun 6:7271
41. Hair PS et al (2010) Clumping factor A interaction with complement factor I increases C3b cleavage on the bacterial surface of Staphylococcus aureus and decreases complement-mediated phagocytosis. Infect Immun 78:1717–1727
42. Hair PS, Ward MD, Semmes OJ, Foster TJ, Cunnion KM (2008) Staphylococcus aureus clumping factor A binds to complement regulator factor I and increases factor I cleavage of C3b. J Infect Dis 198:125–133
43. Hammer ND, Skaar EP (2011) Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu Rev Microbiol 65:129–147
44. Hazenbos WL et al (2013) Novel staphylococcal glycosyltransferases SdgA and SdgB mediate immunogenicity and protection of virulence-associated cell wall proteins. PLoS Pathog 9: e1003653
45. Herman-Bausier P, El-Kirat-Chatel S, Foster TJ, Geoghegan JA, Dufrene YF (2015) Staphylococcus aureus Fibronectin-Binding Protein A Mediates Cell-Cell Adhesion through Low-Affinity Homophilic Bonds. MBio 6:e00413–e00415
46. Higgins J, Loughman A, van Kessel KP, van Strijp JA, Foster TJ (2006) Clumping factor A of Staphylococcus aureus inhibits phagocytosis by human polymorphonuclear leucocytes. FEMS Microbiol Lett 258:290–296
47. Josefsson E et al (1998a) Three new members of the serine-aspartate repeat protein multigene family of Staphylococcus aureus. Microbiology 144:3387–3395
48. Josefsson E, O’Connell D, Foster TJ, Durussel I, Cox JA (1998b) The binding of calcium to the B-repeat segment of SdrD, a cell surface protein of Staphylococcus aureus. J Biol Chem 273:31145–31152
49. Josefsson E, Hartford O, O’Brien L, Patti JM, Foster T (2001) Protection against experimental Staphylococcus aureus arthritis by vaccination with clumping factor A, a novel virulence determinant. J Infect Dis 184:1572–1580
50. Josefsson E, Higgins J, Foster TJ, Tarkowski A (2008) Fibrinogen binding sites P336 and Y338 of clumping factor A are crucial for Staphylococcus aureus virulence. PLoS ONE 3:e2206
51. Kang M et al (2013) Collagen-binding Microbial Surface Components Recognizing Adhesive Matrix Molecule (MSCRAMM) of Gram-positive Bacteria Inhibit Complement Activation via the Classical Pathway. J Biol Chem 288:20520–20531
52. Keane FM, Loughman A, Valtulina V, Brennan M, Speziale P, Foster TJ (2007) Fibrinogen and elastin bind to the same region within the A domain of fibronectin binding protein A, an MSCRAMM of Staphylococcus aureus. Mol Microbiol 63:711–723
53. Kenny JG et al (2009) The Staphylococcus aureus response to unsaturated long chain free fatty acids: survival mechanisms and virulence implications. PLoS ONE 4:e4344
54. Ko YP et al (2013) Phagocytosis escape by a Staphylococcus aureus protein that connects complement and coagulation proteins at the bacterial surface. PLoS Pathog 9:e1003816
55. Ko YP, Liang X, Smith CW, Degen JL, Hook M (2011) Binding of Efb from Staphylococcus aureus to fibrinogen blocks neutrophil adherence. J Biol Chem 286:9865–9874
56. Koch TK et al (2012) Staphylococcus aureus proteins Sbi and Efb recruit human plasmin to degrade complement C3 and C3b. PLoS ONE 7:e47638
57. Kukita K et al (2013) Staphylococcus aureus SasA is responsible for binding to the salivary agglutinin gp340, derived from human saliva. Infect Immun 81:1870–1879
58. Kwiecinski J, Jin T, Josefsson E (2014) Surface proteins of Staphylococcus aureus play an important role in experimental skin infection. APMIS 122:1240–1250
59. Lambris JD, Ricklin D, Geisbrecht BV (2008) Complement evasion by human pathogens. Nat Rev Microbiol 6:132–142
60. Li M et al (2012) MRSA epidemic linked to a quickly spreading colonization and virulence determinant. Nat Med 18:816–819
61. Liu Q et al (2015) Targeting surface protein SasX by active and passive vaccination to reduce Staphylococcus aureus colonization and infection. Infect Immun 83:2168–2174
62. Lizcano A, Sanchez CJ, Orihuela CJ (2012) A role for glycosylated serine-rich repeat proteins in gram-positive bacterial pathogenesis. Mol Oral Microbiol 27:257–269
63. Lower SK et al (2011) Polymorphisms in fibronectin binding protein A of Staphylococcus aureus are associated with infection of cardiovascular devices. Proc Natl Acad Sci U S A 108:18372– 18377
64. Malachowa N, DeLeo FR (2010) Mobile genetic elements of Staphylococcus aureus. Cell Mol Life Sci 67:3057–3071
65. Marraffini LA, Schneewind O (2005) Anchor structure of staphylococcal surface proteins. V. Anchor structure of the sortase B substrate IsdC. J Biol Chem 280:16263–16271
66. Martin FJ et al (2009) Staphylococcus aureus activates type I IFN signaling in mice and humans through the Xr repeated sequences of protein A. J Clin Invest 119:1931–1939
67. Mazmanian SK, Liu G, Ton-That H, Schneewind O (1999) Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285:760–763
68. Mazmanian SK, Ton-That H, Schneewind O (2001) Sortase-catalysed anchoring of surface proteins to the cell wall of Staphylococcus aureus. Mol Microbiol 40:1049–1057
69. McAdow M, Kim HK, Dedent AC, Hendrickx AP, Schneewind O, Missiakas DM (2011) Preventing Staphylococcus aureus sepsis through the inhibition of its agglutination in blood. PLoS Pathog 7:e1002307
70. McAleese FM, Walsh EJ, Sieprawska M, Potempa J, Foster TJ (2001) Loss of clumping factor B fibrinogen binding activity by Staphylococcus aureus involves cessation of transcription, shedding and cleavage by metalloprotease. J Biol Chem 276:29969–29978
71. McCarthy AJ, Lindsay JA (2010) Genetic variation in Staphylococcus aureus surface and immune evasion genes is lineage associated: implications for vaccine design and host-pathogen interactions. BMC Microbiol 10:173
72. McCormack N, Foster TJ, Geoghegan JA (2014) A short sequence within subdomain N1 of region A of the Staphylococcus aureus MSCRAMM clumping factor A is required for export and surface display. Microbiology 160:659–670
73. McGavin MJ, Zahradka C, Rice K, Scott JE (1997) Modification of the Staphylococcus aureus fibronectin binding phenotype by V8 protease. Infect Immun 65:2621–2628
74. Miajlovic H, Zapotoczna M, Geoghegan JA, Kerrigan SW, Speziale P, Foster TJ (2010) Direct interaction of iron-regulated surface determinant IsdB of Staphylococcus aureus with the GPIIb/IIIa receptor on platelets. Microbiology 156:920–928
75. Molkanen T, Tyynela J, Helin J, Kalkkinen N, Kuusela P (2002) Enhanced activation of bound plasminogen on Staphylococcus aureus by staphylokinase. FEBS Lett 517:72–78
76. Monk IR, Foster TJ (2012) Genetic manipulation of Staphylococci-breaking through the barrier. Front Cell Infect Microbiol 2:49
77. Monk IR, Shah IM, Xu M, Tan MW, Foster TJ (2012) Transforming the untransformable: application of direct transformation to manipulate genetically Staphylococcus aureus and Staphylococcus epidermidis. MBio 3:e00277-11
78. Monk IR, Tree JJ, Howden BP, Stinear TP, Foster TJ (2015) Complete Bypass of Restriction Systems for Major Staphylococcus aureus Lineages. MBio 6:e00308–e00315
79. Moreillon P et al (1995) Role of Staphylococcus aureus coagulase and clumping factor in pathogenesis of experimental endocarditis. Infect Immun 63:4738–4743
80. Mulcahy ME et al (2012) Nasal colonisation by Staphylococcus aureus depends upon clumping factor B binding to the squamous epithelial cell envelope protein loricrin. PLoS Pathog 8: e1003092
81. Novick RP, Christie GE, Penades JR (2010) The phage-related chromosomal islands of Gram-positive bacteria. Nat Rev Microbiol 8:541–551
82. O’Brien LM, Walsh EJ, Massey RC, Peacock SJ, Foster TJ (2002) Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell Microbiol 4:759–770
83. O’Halloran DP, Wynne K, Geoghegan JA (2015) Protein A is released into the Staphylococcus aureus culture supernatant with an unprocessed sorting signal. Infect Immun 83:1598–1609
84. O’Seaghdha M et al (2006) Staphylococcus aureus protein A binding to von Willebrand factor A1 domain is mediated by conserved IgG binding regions. FEBS J 273:4831–4841
85. Palmqvist N, Foster T, Tarkowski A, Josefsson E (2002) Protein A is a virulence factor in Staphylococcus aureus arthritis and septic death. Microb Pathog 33:239–249
86. Patel AH, Nowlan P, Weavers ED, Foster T (1987) Virulence of protein A-deficient and alpha-toxin-deficient mutants of Staphylococcus aureus isolated by allele replacement. Infect Immun 55:3103–3110
87. Patti JM, Allen BL, McGavin MJ, Hook M (1994a) MSCRAMM-mediated adherence of microorganisms to host tissues. Annu Rev Microbiol 48:585–617
88. Patti JM et al (1994b) The Staphylococcus aureus collagen adhesin is a virulence determinant in experimental septic arthritis. Infect Immun 62:152–161
89. Peacock SJ, Foster TJ, Cameron BJ, Berendt AR (1999) Bacterial fibronectin-binding proteins and endothelial cell surface fibronectin mediate adherence of Staphylococcus aureus to resting human endothelial cells. Microbiology 145:3477–3486
90. Perry AM, Ton-That H, Mazmanian SK, Schneewind O (2002) Anchoring of surface proteins to the cell wall of Staphylococcus aureus. III. Lipid II is an in vivo peptidoglycan substrate for sortase-catalyzed surface protein anchoring. J Biol Chem 277:16241–16248
91. Pilpa RM, Robson SA, Villareal VA, Wong ML, Phillips M, Clubb RT (2009) Functionally distinct NEAT (NEAr Transporter) domains within the Staphylococcus aureus IsdH/HarA protein extract heme from methemoglobin. J Biol Chem 284:1166–1176
92. Pishchany G et al (2010) Specificity for human hemoglobin enhances Staphylococcus aureus infection. Cell Host Microbe 8:544–550
93. Ponnuraj K et al (2003) A “dock, lock, and latch” structural model for a staphylococcal adhesin binding to fibrinogen. Cell 115:217–228
94. Que YA et al (2005) Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis. J Exp Med 201:1627–1635
95. Rhem MN et al (2000) The collagen-binding adhesin is a virulence factor in Staphylococcus aureus keratitis. Infect Immun 68:3776–3779
96. Roche FM, Meehan M, Foster TJ (2003) The Staphylococcus aureus surface protein SasG and its homologues promote bacterial adherence to human desquamated nasal epithelial cells. Microbiology 149:2759–2767
97. Rohde H et al (2005) Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol Microbiol 55:1883–1895
98. Salazar N et al (2014) Staphylococcus aureus manganese transport protein C (MntC) is an extracellular matrix- and plasminogen-binding protein. PLoS ONE 9:e112730
99. Schaffer AC et al (2006) Immunization with Staphylococcus aureus clumping factor B, a major determinant in nasal carriage, reduces nasal colonization in a murine model. Infect Immun 74:2145–2153
100. Schneewind O, Mihaylova-Petkov D, Model P (1993) Cell wall sorting signals in surface proteins of gram-positive bacteria. EMBO J 12:4803–4811
101. Schneewind O, Model P, Fischetti VA (1992) Sorting of protein A to the staphylococcal cell wall. Cell 70:267–281
102. Schroeder K et al (2009) Molecular characterization of a novel Staphylococcus aureus surface protein (SasC) involved in cell aggregation and biofilm accumulation. PLoS ONE 4:e7567
103. Schwarz-Linek U et al (2003) Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423:177–181
104. Schwarz-Linek U, Hook M, Potts JR (2004) The molecular basis of fibronectin-mediated bacterial adherence to host cells. Mol Microbiol 52:631–641
105. Schwarz-Linek U, Hook M, Potts JR (2006) Fibronectin-binding proteins of gram-positive cocci. Microbes Infect 8:2291–2298
106. Sharp JA et al (2012) Staphylococcus aureus surface protein SdrE binds complement regulator factor H as an immune evasion tactic. PLoS ONE 7:e38407
107. Siboo IR, Chaffin DO, Rubens CE, Sullam PM (2008) Characterization of the accessory Sec system of Staphylococcus aureus. J Bacteriol 190:6188–6196
108. Siboo IR, Chambers HF, Sullam PM (2005) Role of SraP, a Serine-Rich Surface Protein of Staphylococcus aureus, in binding to human platelets. Infect Immun 73:2273–2280
109. Silverman GJ, Goodyear CS (2006) Confounding B-cell defences: lessons from a staphylococcal superantigen. Nat Rev Immunol 6:465–475
110. Sinha B et al (1999) Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell Microbiol 1:101–117
111. Sinha B et al (2000) Heterologously expressed Staphylococcus aureus fibronectin-binding proteins are sufficient for invasion of host cells. Infect Immun 68:6871–6878
112. Thammavongsa V, Kern JW, Missiakas DM, Schneewind O (2009) Staphylococcus aureus synthesizes adenosine to escape host immune responses. J Exp Med 206:2417–2427
113. Thammavongsa V, Missiakas DM, Schneewind O (2013) Staphylococcus aureus degrades neutrophil extracellular traps to promote immune cell death. Science 342:863–866
114. Thammavongsa V, Schneewind O, Missiakas DM (2011) Enzymatic properties of Staphylococcus aureus adenosine synthase (AdsA). BMC Biochem 12:56
115. Vazquez V et al (2011) Fibrinogen is a ligand for the Staphylococcus aureus microbial surface components recognizing adhesive matrix molecules (MSCRAMM) bone sialoprotein-binding protein (Bbp). J Biol Chem 286:29797–29805
116. Vergara-Irigaray M et al (2009) Relevant role of fibronectin-binding proteins in Staphylococcus aureus biofilm-associated foreign-body infections. Infect Immun 77:3978–3991
117. Visai L et al (2009) Immune evasion by Staphylococcus aureus conferred by iron-regulated surface determinant protein IsdH. Microbiology 155:667–679
118. Walker JN et al (2013) The Staphylococcus aureus ArlRS two-component system is a novel regulator of agglutination and pathogenesis. PLoS Pathog 9:e1003819
119. Walker MJ et al (2014) Disease manifestations and pathogenic mechanisms of group a Streptococcus. Clin Microbiol Rev 27:264–301
120. Walsh EJ, Miajlovic H, Gorkun OV, Foster TJ (2008) Identification of the Staphylococcus aureus MSCRAMM clumping factor B (ClfB) binding site in the alphaC-domain of human fibrinogen. Microbiology 154:550–558
121. Walsh EJ, O’Brien LM, Liang X, Hook M, Foster TJ (2004) Clumping factor B, a fibrinogen-binding MSCRAMM (microbial surface components recognizing adhesive matrix molecules) adhesin of Staphylococcus aureus, also binds to the tail region of type I cytokeratin 10. J Biol Chem 279:50691–50699
122. Wang X, Ge J, Liu B, Hu Y, Yang M (2013) Structures of SdrD from Staphylococcus aureus reveal the molecular mechanism of how the cell surface receptors recognize their ligands. Protein Cell 4:277–285
123. Wann ER, Gurusiddappa S, Hook M (2000) The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J Biol Chem 275:13863–13871
124. Werbick C et al (2007) Staphylococcal chromosomal cassette mec type I, spa type, and expression of Pls are determinants of reduced cellular invasiveness of methicillin-resistant Staphylococcus aureus isolates. J Infect Dis 195:1678–1685
125. Wertheim HF et al (2008) Key role for clumping factor B in Staphylococcus aureus nasal colonization of humans. PLoS Med 5:e17
126. Xiang H et al (2012) Crystal structures reveal the multi-ligand binding mechanism of Staphylococcus aureus ClfB. PLoS Pathog 8:e1002751
127. Xu Y, Rivas JM, Brown EL, Liang X, Hook M (2004) Virulence potential of the staphylococcal adhesin CNA in experimental arthritis is determined by its affinity for collagen. J Infect Dis 189:2323–2333
128. Yang YH et al (2014) Structural insights into SraP-mediated Staphylococcus aureus adhesion to host cells. PLoS Pathog 10:e1004169
129. Zapotoczna M, Jevnikar Z, Miajlovic H, Kos J, Foster TJ (2013) Iron-regulated surface determinant B (IsdB) promotes Staphylococcus aureus adherence to and internalization by non-phagocytic human cells. Cell Microbiol 15:1026–1041
130. Zong Y et al (2005) A ‘Collagen Hug’ model for Staphylococcus aureus CNA binding to collagen. EMBO J 24:4224–4236