Architects at the bacterial surface-sortases and the assembly of pili with isopeptide bonds

Nature Reviews Microbiology

Volumn 9, Issue 3, 2011, Pages 166-176

  Hendrickx, Antoni P A ^a   Budzik, Jonathan M ^a   Oh, So Young ^a   Schneewind, Olaf ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; HEME; PILIN; SORTASE;

ACTINOMYCES NAESLUNDII; BACTERIAL CELL WALL; CELL DIVISION; CORYNEBACTERIUM DIPHTHERIAE; CYTOARCHITECTURE; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; GRAM POSITIVE BACTERIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN STRUCTURE; REVIEW; STAPHYLOCOCCUS INTERMEDIUS; STREPTOCOCCUS; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS GALLOLYTICUS; STREPTOCOCCUS PNEUMONIAE; STREPTOCOCCUS PYOGENES;

AMINOACYLTRANSFERASES; BACTERIAL PROTEINS; BACTERIAL VACCINES; CYSTEINE ENDOPEPTIDASES; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GRAM-POSITIVE BACTERIA; PROTEIN SORTING SIGNALS;

BACTERIA (MICROORGANISMS); POSIBACTERIA;

EID: 79951816315     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2520     Document Type: Review

References (134)

1. Brinton, C. C. Jr. Non-flagellar appendages of bacteria. Nature 183, 782-786 (1959.
2. Houwink, A. L. Flagella, gas vacuoles and cell-wall structure in Halobacterium halobium; an electron microscope study. J. Gen. Microbiol. 15, 146-150 (1956.
3. Mudd, S., Polevitzky, K., Anderson, T. F. & Chambers, L. A. Bacterial morphology as shown by the electron microscope: II. The bacterial cell-wall in the genus Bacillus. J. Bacteriol. 42, 251-264 (1941.
4. Swanson, J., Hsu, K. C. & Gotschlich, E. C. Electron microscopic studies on streptococci. I. M antigen. J. Exp. Med. 130, 1063-1091 (1969.
5. Yanagawa, R., Otsuki, K. & Tokui, T. Electron microscopy of fine structure of Corynebacterium renale with special reference to pili. Jpn. J. Vet. Res. 16, 31-37 (1968).
6. Yanagawa, R. & Honda, E. Presence of pili in species of human and animal parasites and pathogens of the genus Corynebacterium. Infect. Immun. 13, 1293-1295 (1976.
7. Mazmanian, S. K., Liu, G., Ton-That, H. & Schneewind, O. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285, 760-763 (1999).
8. Ton-That, H. & Schneewind, O. Assembly of pili on the surface of Corynebacterium diphtheriae. Mol. Microbiol. 50, 1429-1438 (2003). (Pubitemid 37475871)
9. Schneewind, O., Fowler, A. & Faull, K. F. Structure of the cell wall anchor of surface proteins in Staphylococcus aureus. Science 268, 103-106 (1995.
10. Ton-That, H., Liu, G., Mazmanian, S. K., Faull, K. F. & Schneewind, O. Purification and characterization of sortase, the transpeptidase that cleaves surface proteins of Staphylococcus aureus at the LPXTG motif. Proc. Natl Acad. Sci. USA 96, 12424-12429 (1999. (Pubitemid 29513518)
11. Marraffini, L. A., Dedent, A. C. & Schneewind, O. Sortases and the art of anchoring proteins to the envelopes of gram-positive bacteria. Microbiol. Mol. Biol. Rev. 70, 192-221 (2006.
12. Clancy, K. W., Melvin, J. A. & McCafferty, D. G. Sortase transpeptidases: insights into mechanism, substrate specificity, and inhibition. Biopolymers 94, 385-396 (2010.
13. Ilangovan, U., Ton-That, H., Iwahara, J., Schneewind, O. & Clubb, R. T. Structure of sortase, the transpeptidase that anchors proteins to the cell wall of Staphylococcus aureus. Proc. Natl Acad. Sci. USA 98, 6056-6061 (2001. (Pubitemid 32488192)
14. Manzano, C. et al. Sortase-mediated pilus fiber biogenesis in Streptococcus pneumoniae. Structure 16 1838-1848 (2008).
15. Neiers, F. et al. Two crystal structures of pneumococcal pilus sortase C provide novel insights into catalysis and substrate specificity. J. Mol. Biol. 393, 704-716 (2009.
16. Neiers, F. et al. Cloning, expression, purification, crystallization and preliminary X-ray analysis of the pilus-associated sortase C from Streptococcus pneumoniae. Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 65, 55-58 (2009.
17. Zong, Y., Mazmanian, S. K., Schneewind, O. & Narayana, S. V. The structure of sortase B, a cysteine transpeptidase that tethers surface protein to the Staphylococcus aureus cell wall. Structure 12, 105-112 (2004. (Pubitemid 38114810)
18. Zhang R. et al. Structures of sortase B from Staphylococcus aureus and Bacillus anthracis reveal catalytic amino acid triad in the active site. Structure 12. 1147-1156, 2004. (Pubitemid 38900757)
19. Race, P. R. et al. Crystal structure of Streptococcus pyogenes sortase A: implications for sortase mechanism. J. Biol. Chem. 284, 6924-6933 (2009.
20. Weiner, E. M., Robson, S., Marohn, M. & Clubb, R. T. The Sortase A enzyme that attaches proteins to the cell wall of Bacillus anthracis contains an unusual active site architecture. J. Biol. Chem. 285, 23433-23443 (2010.
21. Suree, N. et al. The structure of the Staphylococcus aureus sortase-substrate complex reveals how the universally conserved LPXTG sorting signal is recognized. J. Biol. Chem. 284, 24465-24477 (2009.
22. Hendrickx, A. P., Willems, R. J., Bonten, M. J. & van Schaik, W. LPXTG surface proteins of enterococci. Trends Microbiol. 17, 423-430 (2009.
23. Soriani, M. & Telford, J. L. Relevance of pili in pathogenic streptococci pathogenesis and vaccine development. Future. Microbiol. 5, 735-747 (2010.
24. Mandlik, A., Swierczynski, A., Das, A. & Ton-That, H. Pili in Gram-positive bacteria: assembly, involvement in colonization and biofilm development. Trends Microbiol. 16, 33-40 (2008.
25. Pallen, M. J., Lam, A. C., Antonio, M. & Dunbar, K. An embarrassment of sortases - a richness of substrates? Trends Microbiol. 9, 97-102 (2001.
26. Comfort, D. & Clubb, R. T. A comparative genome analysis identifies distinct sorting pathways in gram-positive bacteria. Infect. Immun. 72, 2710-2722 (2004. (Pubitemid 38542398)
27. Dramsi, S., Trieu-Cuot, P. & Bierne, H. Sorting sortases: a nomenclature proposal for the various sortases of Gram-positive bacteria. Res. Microbiol. 156, 289-297 (2005). (Pubitemid 40487449)
28. Perry, A. M., Ton-That, H., Mazmanian, S. K. & Schneewind, O. 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 (2002. (Pubitemid 34967912)
29. Patti, J. M., Allen, B. L., McGavin, M. J. & Hook, M. MSCRAMM-mediated adherence of microorganisms to host tissues. Annu. Rev. Microbiol. 48, 585-617 (1994.
30. Speziale, P. et al. Structural and functional role of Staphylococcus aureus surface components recognizing adhesive matrix molecules of the host. Future. Microbiol. 4, 1337-1352 (2009.
31. Bierne, H. et al. Sortase B, a new class of sortase in Listeria monocytogenes. J. Bacteriol. 186, 1972-1982 (2004. (Pubitemid 38381184)
32. Marraffini, L. A. & Schneewind, O. Anchor structure of staphylococcal surface proteins. V. Anchor structure of the sortase B substrate IsdC. J. Biol. Chem. 280, 16263-16271 (2005. (Pubitemid 40616753)
33. Maresso, A. W. & Schneewind, O. Iron acquisition and transport in Staphylococcus aureus. Biometals 19, 193-203 (2006). (Pubitemid 43794828)
34. Maresso, A. W., Chapa, T. J. & Schneewind, O. Surface protein IsdC and Sortase B are required for heme-iron scavenging of Bacillus anthracis. J. Bacteriol. 188, 8145-8152 (2006). (Pubitemid 44845685)
35. Budzik, J. M. et al. Amide bonds assemble pili on the surface of bacilli. Proc. Natl Acad. Sci. USA 105, 10215-10220 (2008).
36. Manzano, C., Izore, T., Job, V., Di Guilmi, A. M. & Dessen, A. Sortase activity is controlled by a flexible lid in the pilus biogenesis mechanism of Gram-positive pathogens. Biochemistry 48, 10549-10557 (2009).
37. Marraffini, L. A. & Schneewind, O. Targeting proteins to the cell wall of sporulating Bacillus anthracis. Mol. Microbiol. 62, 1402-1417 (2006). (Pubitemid 44707202)
38. Marraffini, L. A. & Schneewind, O. Sortase C?-mediated anchoring of BasI to the cell wall envelope of Bacillus anthracis. J. Bacteriol. 189, 6425-6436 (2007). (Pubitemid 47378651)
39. Ton-That, H., Faull, K. F. & Schneewind, O. Anchor structure of staphylococcal surface proteins. A branched peptide that links the carboxyl terminus of proteins to the cell wall. J. Biol. Chem. 272, 22285-22292 (1997. (Pubitemid 27382863)
40. Navarre, W. W., Ton-That, H., Faull, K. F. & Schneewind, O. Anchor structure of staphylococcal surface proteins. II. COOH-terminal structure of muramidase and amidase-solubilized surface protein. J. Biol. Chem. 273, 29135-29142 (1998). (Pubitemid 28507612)
41. Budzik, J. M., Oh, S.-Y. & Schneewind, O. Sortase D forms the covalent bond that links BcpB to the tip of Bacillus cereus pili. J. Biol. Chem. 284, 12989-12997 (2009.
42. Budzik, J. M., Marraffini, L. A. & Schneewind, O. Assembly of pili on the surface of Bacillus cereus vegetative cells. Mol. Microbiol. 66, 495-510 (2007). (Pubitemid 47482390)
43. Lauer, P. et al. Genome analysis reveals pili in Group B Streptococcus. Science 309 105 2005. (Pubitemid 40934983)
44. Mora, M. et al. Group A Streptococcus produce pilus-like structures containing protective antigens and Lancefield T antigens. Proc. Natl Acad. Sci. USA 102, 15641-15646 (2005. (Pubitemid 41528109)
45. Scheffers, D. J. & Pinho, M. G. Bacterial cell wall synthesis: new insights from localization studies. Microbiol. Mol. Biol. Rev. 69, 585-607 (2005. (Pubitemid 41798464)
46. Strominger, J. L. Penicillin-sensitive enzymatic reactions in bacterial cell wall synthesis. Harvey Lect. 64, 179-213 (1968).
47. Boneca, I. G., Huang, Z. H., Gage, D. A. & Tomasz, A. Characterization of Staphylococcus aureus cell wall glycan strands, evidence for a new beta-N-acetylglucosaminidase activity. J. Biol. Chem. 275, 9910-9918 (2000. (Pubitemid 30202035)
48. Dmitriev, B. A., Toukach, F. V., Holst, O., Rietschel, E. T. & Ehlers, S. Tertiary structure of Staphylococcus aureus cell wall murein. J. Bacteriol. 186, 7141-7148 (2004. (Pubitemid 39383098)
49. Cole, R. M. & Hahn, J. J. Cell wall replication in Streptococcus pyogenes. Science 135, 722-724 (1962.
50. Pooley, H. M. Turnover and spreading of old wall during surface growth of Bacillus subtilis. J. Bacteriol. 125, 1127-1138 (1976.
51. Ghuysen, J. M., Tipper, D. J. & Strominger, J. L. Structure of the cell wall of Staphylococcus aureus, strain Copenhagen. IV. The teichoic acid-glycopeptide complex. Biochemistry 4, 474-485 (1965.
52. Kline, K. A. et al. Mechanism for sortase localization and the role of sortase localization in efficient pilus assembly in Enterococcus faecalis. J. Bacteriol. 191, 3237-3247 (2009.
53. Budzik, J. M., Oh, S.-Y. & Schneewind, O. Cell wall anchor structure of BcpA pili in Bacillus anthracis. J. Biol. Chem. 283, 36676-36686 (2008.
54. Mandlik, A., Swierczynski, A., Das, A. & Ton-That, H. Corynebacterium diphtheriae employs specific minor pilins to target human pharyngeal epithelial cells. Mol. Microbiol. 64, 111-124 (2007. (Pubitemid 46435028)
55. Ton-That, H., Marraffini, L. A. & Schneewind, O. Sortases and pilin elements involved in pilus assembly of Corynebacterium diphtheriae. Mol. Microbiol. 53, 251-261 (2004. (Pubitemid 38901395)
56. Guttilla, I. K. et al. Acyl enzyme intermediates in sortase-catalyzed pilus morphogenesis in gram-positive bacteria. J. Bacteriol. 191, 5603-5612 (2009).
57. Mandlik, A., Das, A. & Ton-That, H. The molecular switch that activates the cell wall anchoring step of pilus assembly in gram-positive bacteria. Proc. Natl Acad. Sci. USA 105, 14147-14152 (2008.
58. Swierczynski, A. & Ton-That, H. Type III pilus of corynebacteria: Pilus length is determined by the level of its major pilin subunit. J. Bacteriol. 188, 6318-6325 (2006. (Pubitemid 44448574)
59. Swaminathan, A. et al. Housekeeping sortase facilitates the cell wall anchoring of pilus polymers in Corynebacterium diphtheriae. Mol. Microbiol. 66, 961-974 (2007. (Pubitemid 350050422)
60. Krishnan, V. et al. An IgG-like domain in the minor pilin GBS52 of Streptococcus agalactiae mediates lung epithelial cell adhesion. Structure 15 893-903 2007. (Pubitemid 47212752)
61. Kang, H. J., Coulibaly, F., Clow, F., Proft, T. & Baker, E. N. Stabilizing isopeptide bonds revealed in Gram-positive bacterial pilus structure. Science 318, 1625-1628 (2007). (Pubitemid 350233661)
62. Deivanayagam, C. C. et al. Novel fold and assembly of the repetitive B region of the Staphylococcus aureus collagen-binding surface protein. Structure 8, 67-78 (2000. (Pubitemid 30051343)
63. Linke, C. et al. Crystal structure of the minor pilin FctB reveals determinants of Group A streptococcal pilus anchoring. J. Biol. Chem. 285, 20381-20389 (2010.
64. Kang, H. J. & Baker, E. N. Intramolecular isopeptide bonds give thermodynamic and proteolytic stability to the major pilin protein of Streptococcus pyogenes. J. Biol. Chem. 284, 20729-20737 (2009.
65. Alegre-Cebollada, J., Badilla, C. L. & Fernandez, J. M. Isopeptide bonds block the mechanical extension of pili in pathogenic Streptococcus pyogenes. J. Biol. Chem. 285, 11235-11242 (2010.
66. Smith, W. D. et al. Roles of minor pilin subunits Spy0125 and Spy0130 in the serotype M1 Streptococcus pyogenes strain SF370. J. Bacteriol. 192, 4651-4659 (2010.
67. Manetti, A. G. et al. Streptococcus pyogenes pili promote pharyngeal cell adhesion and biofilm formation. Mol. Microbiol. 64, 968-983 (2007. (Pubitemid 46743959)
68. Pointon, J. A. et al. A highly unusual thioester bond in a pilus adhesin is required for efficient host cell interaction. J. Biol. Chem. 285, 33858-33866 (2010.
69. Law, S. K. & Dodds, A. W. The internal thioester and the covalent binding properties of the complement proteins C3 and C4. Protein Sci. 6, 263-274 (1997). (Pubitemid 27079917)
70. Cherry, S. & Silverman, N. Host-pathogen interactions in drosophila: new tricks from an old friend. Nature Immunol. 7, 911-917 (2006. (Pubitemid 44263904)
71. Linke, C., Young, P. G., Kang, H. J., Proft, T. & Baker, E. N. Purification, crystallization and preliminary crystallographic analysis of the minor pilin FctB from Streptococcus pyogenes. Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 66, 177-179 (2010.
72. Kang, H. J. & Baker, E. N. Intramolecular isopeptide bonds: protein crosslinks built for stress? Trends Biochem. Sci. 4 Nov 2010 (doi:10.1016/j.tibs.2010.09.007.
73. Hendrickx, A. P. et al. Differential PilA pilus assembly by a hospital-acquired and a community-derived Enterococcus faecium isolate. Microbiology 156, 2649-2659 (2010.
74. Budzik, J. M. et al. Intramolecular amide bonds stabilize pili on the surface of bacilli. Proc. Natl Acad. Sci. USA 106, 19992-19997 (2009.
75. Kang, H. J., Paterson, N. G., Gaspar, A. H., Ton-That, H. & Baker, E. N. The Corynebacterium diphtheriae shaft pilin SpaA is built of tandem Ig-like modules with stabilizing isopeptide and disulfide bonds. Proc. Natl Acad. Sci. USA 106, 16967-16971 (2009).
76. Sarvas, M., Harwood, C. R., Bron, S. & van Dijl, J. M. Post-translocational folding of secretory proteins in Gram-positive bacteria. Biochim. Biophys. Acta 1694, 311-327 (2004. (Pubitemid 39535077)
77. Spraggon, G. et al. Supramolecular organization of the repetitive backbone unit of the Streptococcus pneumoniae pilus. PLoS ONE 5, e10919 2010.
78. Izore, T. et al. Structural basis of host cell recognition by the pilus adhesin from Streptococcus pneumoniae. Structure 18. 106-115 2010.
79. Bienkowska, J., Cruz, M., Atiemo, A., Handin, R. & Liddington, R. The von willebrand factor A3 domain does not contain a metal ion-dependent adhesion site motif. J. Biol. Chem. 272, 25162-25167 (1997. (Pubitemid 27415701)
80. Cruz, M. A., Yuan, H., Lee, J. R., Wise, R. J. & Handin, R. I. Interaction of the von Willebrand factor (vWF) with collagen. Localization of the primary collagen-binding site by analysis of recombinant vWF a domain polypeptides. J. Biol. Chem. 270, 10822-10827 (1995.
81. Springer, T. A. Complement and the multifaceted functions of VWA and integrin I domains. Structure 14, 1611-1616 (2006. (Pubitemid 46107278)
82. Ton-That, H. & Schneewind, O. Assembly of pili in Gram-positive bacteria. Trends Microbiol. 12, 228-234 (2004. (Pubitemid 38534627)
83. Yeung, M. K., Chassy, B. M. & Cisar, J. O. Cloning and expression of a type 1 fimbrial subunit of Actinomyces viscosus T14V. J. Bacteriol. 169, 1678-1683 (1987. (Pubitemid 17063500)
84. Yeung, M. K. & Cisar, J. O. Cloning and nucleotide sequence of a gene for Actinomyces naeslundii WVU45 type 2 fimbriae. J. Bacteriol. 170, 3803-3809 (1988.
85. Nallapareddy, S. R. et al. Endocarditis and biofilm-associated pili of Enterococcus faecalis. J. Clin. Invest 116, 2799-2807 (2006. (Pubitemid 44511643)
86. Hendrickx, A. P. et al. Expression of two distinct types of pili by a hospital-acquired Enterococcus faecium isolate. Microbiology 154, 3212-3223 (2008.
87. Barocchi, M. A. et al. A pneumococcal pilus influences virulence and host inflammatory responses. Proc. Natl Acad. Sci. USA 103, 2857-2862 (2006.
88. Dramsi, S. et al. Assembly and role of pili in group B streptococci. Mol. Microbiol. 60, 1401-1413 (2006. (Pubitemid 43801433)
89. El, M. L., Terrasse, R., Dessen, A., Vernet, T. & Di Guilmi, A. M. Stability and assembly of pilus subunits of Streptococcus pneumoniae. J. Biol. Chem. 285, 12405-12415 (2010.
90. Falker, S. et al. Sortase-mediated assembly and surface topology of adhesive pneumococcal pili. Mol. Microbiol. 70, 595-607 (2008.
91. Kemp, K. D., Singh, K. V., Nallapareddy, S. R. & Murray, B. E. Relative contributions of Enterococcus faecalis OG1RF sortase-encoding genes, srtA and bps (srtC), to biofilm formation and a murine model of urinary tract infection. Infect. Immun. 75, 5399-5404 (2007. (Pubitemid 350033628)
92. Lemieux, J., Woody, S. & Camilli, A. Roles of the sortases of Streptococcus pneumoniae in assembly of the RlrA pilus. J. Bacteriol. 190, 6002-6013 (2008.
93. Hedenstrom, M. et al. NMR studies of interactions between periplasmic chaperones from uropathogenic E. coli and pilicides that interfere with chaperone function and pilus assembly. Org. Biomol. Chem. 3, 4193-4200 (2005. (Pubitemid 41801590)
94. Remaut, H. et al. Fiber formation across the bacterial outer membrane by the chaperone/usher pathway. Cell 133 640-652 2008. (Pubitemid 351636304)
95. Nishiyama, M. & Glockshuber, R. The outer membrane usher guarantees the formation of functional pili by selectively catalyzing donor-strand exchange between subunits that are adjacent in the mature pilus. J. Mol. Biol. 396, 1-8 (2010.
96. Nelson, A. L. et al. RrgA is a pilus-associated adhesin in Streptococcus pneumoniae. Mol. Microbiol. 66, 329-340 (2007. (Pubitemid 47482375)
97. Abbot, E. L. et al. Pili mediate specific adhesion of Streptococcus pyogenes to human tonsil and skin. Cell. Microbiol. 9, 1822-1833 (2007. (Pubitemid 46958806)
98. Maisey, H. C., Hensler, M., Nizet, V. & Doran, K. S. Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. J. Bacteriol. 189, 1464-1467 (2007. (Pubitemid 46239769)
99. Konto-Ghiorghi Y. et al. Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae. PLoS Pathog. 5 e1000422 2009.
100. Maisey, H. C. et al. A group B streptococcal pilus protein promotes phagocyte resistance and systemic virulence. FASEB J. 22, 1715-1724 (2008. (Pubitemid 351811449)
101. Pezzicoli, A. et al. Pilus backbone contributes to group B Streptococcus paracellular translocation through epithelial cells. J. Infect. Dis. 198, 890-898 (2008.
102. Soriani, M. et al. Group B Streptococcus crosses human epithelial cells by a paracellular route. J. Infect. Dis. 193, 241-250 (2006. (Pubitemid 43113486)
103. Sillanpaa, J. et al. Characterization of the ebp pilus-encoding operon of Enterococcus faecium and its role in biofilm formation and virulence in a murine model of urinary tract infection. Virulence 1 236-246 2010.
104. Singh, K. V., Nallapareddy, S. R. & Murray, B. E. Importance of the ebp (endocarditis- and biofilm-associated pilus) locus in the pathogenesis of Enterococcus faecalis ascending urinary tract infection. J. Infect. Dis. 195, 1671-1677 (2007. (Pubitemid 46799225)
105. Hilleringmann, M. et al. Pneumococcal pili are composed of protofilaments exposing adhesive clusters of Rrg A. PLoS Pathog. 4, e1000026 (2008.
106. Sillanpaa, J. et al. A collagen-binding adhesin, Acb, and ten other putative MSCRAMM and pilus family proteins of Streptococcus gallolyticus subsp. gallolyticus (Streptococcus bovis group, biotype I). J. Bacteriol. 191 6643-6653 2009.
107. Bessen, D. E. & Kalia, A. Genomic localization of a T serotype locus to a recombinatorial zone encoding extracellular matrix-binding proteins in Streptococcus pyogenes. Infect. Immun. 70, 1159-1167 (2002. (Pubitemid 34163387)
108. Kreikemeyer, B. et al. Streptococcus pyogenes collagen type I-binding Cpa surface protein. Expression profile, binding characteristics, biological functions, and potential clinical impact. J. Biol. Chem. 280, 33228-33239 (2005. (Pubitemid 41397119)
109. Schneewind, O., Jones, K. F. & Fischetti, V. A. Sequence and structural characteristics of the trypsin-resistant T6 surface protein of group A streptococci. J. Bacteriol. 172, 3310-3317 (1990. (Pubitemid 20179789)
110. Murray, B. E. Vancomycin-resistant enterococcal infections. N. Engl. J. Med. 342, 710-721 (2000. (Pubitemid 30131425)
111. Werner, G. et al. Emergence and spread of vancomycin resistance among enterococci in Europe. Euro Surveill. 13, 19046 (2008.
112. Macleod, C. M., Hodges, R. G., Heidelberger, M. & Bernhard, W. G. Prevention of pneumococcal pneumonia by immunization with specific capsular polysaccharides. J. Exp. Med. 82, 445-465 (1945.
113. von Behring, E. & Kitasato, S. Über das zustandekommen der diphtherie-immunität und der tetanus-immunität bei Thieren. Dtsch. Med. Wochenschr. 16, 1113-1114 (1890) (in German.
114. Pletz, M. W., Maus, U., Krug, N., Welte, T. & Lode, H. Pneumococcal vaccines: mechanism of action, impact on epidemiology and adaption of the species. Int. J. Antimicrob. Agents 32, 199-206 (2008.
115. Alonso, J. M. & Taha, M. K. [Meningococcal vaccines: present status and perspectives]. Therapie 60, 283-286 (2005) (in French.
116. Telford, J. L. Bacterial genome variability and its impact on vaccine design. Cell Host Microbe 3, 408-416 (2008. (Pubitemid 351773100)
117. Serino, L., Moriel, D. G., Rappuoli, R. & Pizza, M. Towards a vaccine against Escherichia coli-associated urinary tract infections. Future Microbiol. 5, 351-354 (2010.
118. Goluszko, P. et al. Vaccination with purified Dr Fimbriae reduces mortality associated with chronic urinary tract infection due to Escherichia coli bearing Dr adhesin. Infect. Immun. 73, 627-631 (2005. (Pubitemid 40041160)
119. Margarit, I. et al. Preventing bacterial infections with pilus-based vaccines: the group B streptococcus paradigm. J. Infect. Dis. 199, 108-115 (2009.
120. Falugi, F. et al. Sequence variation in group A Streptococcus pili and association of pilus backbone types with lancefield T serotypes. J. Infect. Dis. 198, 1834-1841 (2008.
121. Bagnoli, F. et al. A second pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. J. Bacteriol. 190, 5480-5492 (2008.
122. Gianfaldoni, C. et al. Streptococcus pneumoniae pilus subunits protect mice against lethal challenge. Infect. Immun. 75, 1059-1062 (2007. (Pubitemid 46203474)
123. Yamaguchi, T., Matsumoto, M., Sugimoto, Y., Soutome, S. & Oho, T. Gene cloning and characterization of Streptococcus intermedius fimbriae involved in saliva-mediated aggregation. Res. Microbiol. 160, 809-816 (2009.
124. Chen, P., Cisar, J. O., Hess, S., Ho, J. T. & Leung, K. P. Amended description of the genes for synthesis of Actinomyces naeslundii T14V type 1 fimbriae and associated adhesin. Infect. Immun. 75, 4181-4185 (2007. (Pubitemid 47206317)
125. Clark, W. B., Wheeler, T. T. & Cisar, J. O. Specific inhibition of adsorption of Actinomyces viscosus T14V to saliva-treated hydroxyapatite by antibody against type 1 fimbriae. Infect. Immun. 43, 497-501 (1984. (Pubitemid 14181591)
126. Gibbons, R. J. & Hay, D. I. Human salivary acidic proline-rich proteins and statherin promote the attachment of Actinomyces viscosus LY7 to apatitic surfaces. Infect. Immun. 56, 439-445 (1988. (Pubitemid 18040510)
127. Gibbons, R. J., Hay, D. I., Cisar, J. O. & Clark, W. B. Adsorbed salivary proline-rich protein 1 and statherin: receptors for type 1 fimbriae of Actinomyces viscosus T14V?-J1 on apatitic surfaces. Infect. Immun. 56, 2990-2993 (1988. (Pubitemid 18259960)
128. Revis, G. J., Vatter, A. E., Crowle, A. J. & Cisar, J. O. Antibodies against the Ag2 fimbriae of Actinomyces viscosus T14V inhibit lactose-sensitive bacterial adherence. Infect. Immun. 36, 1217-1222 (1982. (Pubitemid 12124843)
129. Kankainen, M. et al. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human- mucus binding protein. Proc. Natl Acad. Sci. USA 106, 17193-17198 (2009.
130. von Ossowski I. et al. Mucosal adhesion properties of the probiotic Lactobacillus rhamnosus GG SpaCBA and SpaFED pilin subunits. Appl. Environ. Microbiol. 76 2049-2057, 2010.
131. Rinaudo, C. D. et al. Specific involvement of pilus type 2a in biofilm formation in group B Streptococcus. PLoS ONE 5, e9216 (2010.
132. Edwards, A. M. et al. Scavenger receptor gp340 aggregates group A streptococci by binding pili. Mol. Microbiol. 68, 1378-1394 (2008. (Pubitemid 351725250)
133. Lizano, S., Luo, F. & Bessen, D. E. Role of streptococcal T antigens in superficial skin infection. J. Bacteriol. 189, 1426-1434 (2007. (Pubitemid 46239764)
134. Nakata, M. et al. Mode of expression and functional characterization of FCT-3 pilus region-encoded proteins in Streptococcus pyogenes serotype M49. Infect. Immun. 77, 32-44 (2009).