Molecular architecture of Streptococcus pneumoniae TIGR4 pili

EMBO Journal

Volumn 28, Issue 24, 2009, Pages 3921-3930

  Hilleringmann, Markus ^a   Ringler, Philippe ^b   Müller, Shirley A ^b   De Angelis, Gabriella ^a   Rappuoli, Rino ^a   Ferlenghi, Ilaria ^a   Engel, Andreas ^b  

^a NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Gram positive bacteria; Mass measurement; Pilus; STEM; Streptococcus pneumoniae

Indexed keywords

PROTEIN RRGA; PROTEIN RRGB; PROTEIN RRGC; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM PILUS; MORBIDITY; MORTALITY; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; STREPTOCOCCUS PNEUMONIAE; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BLOTTING, WESTERN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; FIMBRIAE, BACTERIAL; MICE; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; STREPTOCOCCUS PNEUMONIAE;

POSIBACTERIA; STREPTOCOCCUS PNEUMONIAE;

EID: 72449126072     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.360     Document Type: Article

References (44)

1. Abbot EL, Smith WD, Siou GP, Chiriboga C, Smith RJ, Wilson JA, Hirst BH, Kehoe MA (2007) Pili mediate specific adhesion of Streptococcus pyogenes to human tonsil and skin. Cell Microbiol 9: 1822-1833
2. Bagnoli F, Moschioni M, Donati C, Dimitrovska V, Ferlenghi I, Facciotti C, Muzzi A, Giusti F, Emolo C, Sinisi A, Hilleringmann M, Pansegrau W, Censini S, Rappuoli R, Covacci A, Masignani V, Barocchi MA (2008) A second pilus type in Streptococcus pneu-moniae is prevalent in emerging serotypes and mediates adhesion to host cells. J Bacteriol 190: 5480-5492
3. Barocchi MA, Ries J, Zogaj X, Hemsley C, Albiger B, Kanth A, Dahlberg S, Fernebro J, Moschioni M, Masignani V, Hultenby K, Taddei AR, Beiter K, Wartha F, von Euler A, Covacci A, Holden DW, Normark S, Rappuoli R, Henriques-Normark B (2006) A pneumococcal pilus influences virulence and host inflammatory responses. Proc Natl Acad Sci USA 103: 2857-2862
4. Broz P, Mueller CA, Muller SA, Philippsen A, Sorg I, Engel A, Cornelis GR (2007) Function and molecular architecture of the Yersinia injectisome tip complex. Mol Microbiol 65: 1311-1320
5. Budzik JM, Marraffini LA, Schneewind O (2007) Assembly of pili on the surface of Bacillus cereus vegetative cells. Mol Microbiol 66: 495-510
6. Budzik JM, Oh SY, Schneewind O (2008) Cell wall anchor structure of BcpA pili in Bacillus anthracis. J Biol Chem 283: 36676-36686
7. Dramsi S, Caliot E, Bonne I, Guadagnini S, Prevost MC, Kojadinovic M, Lalioui L, Poyart C, Trieu-Cuot P (2006) Assembly and role of pili in group B streptococci. Mol Microbiol 60: 1401-1413
8. Fälker S, Nelson AL, Morfeldt E, Jonas K, Hultenby K, Ries J, Melefors Ö, Normark S, Henriques-Normark B (2008) Sortase-mediated assembly and surface topology of adhesive pneumo-coccal pili. Mol Microbiol 70: 595-607
9. Fronzes R, Remaut H, Waksman G (2008) Architectures and biogenesis of non-flagellar protein appendages in Gram-negative bacteria. EMBO J 27: 2271-2280
10. Hava DL, Camilli A (2002) Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol Microbiol 45: 1389-1406
11. Hilleringmann M, Giusti F, Baudner Barbara C, Masignani V, Covacci A, Rappuoli R, Barocchi Michele A, Ferlenghi I (2008) Pneumococcal pili are composed of protofilaments exposing adhesive clusters of Rrg A. PLoS Pathog 4: e1000026
12. Kang HJ, Baker EN (2009) Intramolecular isopeptide bonds give thermodynamic and proteolytic stability to the major pilin protein of Streptococcus pyogenes. J Biol Chem 284: 20729-20737
13. Kang HJ, Coulibaly F, Clow F, Proft T, Baker EN (2007) Stabilizing isopeptide bonds revealed in Gram-positive bacterial pilus structure. Science (Washington, DC, USA) 318: 1625-1628
14. Krishnan V, Gaspar AH, Ye N, Mandlik A, Ton-That H, Narayana SVL (2007) An IgG-like domain in the minor pilin GBS52 of Streptococcus agalactiae mediates lung epithelial cell adhesion. Structure (Cambridge, MA, USA) 15: 893-903
15. Krzyžáneka V, Müller SA, Engel A, Reichelt R (2009) MASDET-a fast and user-friendly multiplatform software for mass determination by dark-field electron microscopy. J Struct Biol 165: 78-87
16. Lauer P, Rinaudo CD, Soriani M, Margarit I, Maione D, Rosini R, Taddei AR, Mora M, Rappuoli R, Grandi G, Telford JL (2005) Genome analysis reveals pili in group B Streptococcus. Science 309: 105
17. LeMieux J, Hava DL, Basset A, Camilli A (2006) RrgA and RrgB are components of a multisubunit pilus encoded by the Streptococcus pneumoniae rlrA pathogenicity islet. Infect Immun 74: 2453-2456
18. LeMieux J, Woody S, Camilli A (2008) Roles of the sortases of Streptococcus pneumoniae in assembly of the RlrA pilus. J Bacteriol 190: 6002-6013
19. Lode HM (2009) Clinical impact of antibiotic-resistant Gram-positive pathogens. Clin Microbiol Infect 15: 212-217
20. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: semiautomated software for high-resolution single-particle reconstitutions. J Struct Biol 128: 82-97H
21. Maisey HC, Hensler M, Nizet V, Doran KS (2007) Group B strepto-coccal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. J Bacteriol 189: 1464-1467
22. Mandlik A, Das A, Ton-That H (2008a) 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
23. Mandlik A, Swierczynski A, Das A, Ton-That H (2008b) Pili in Gram-positive bacteria: assembly, involvement in colonization and biofilm development. Trends Microbiol 16: 33-40
24. Manzano C, Contreras-Martel C, El Mortaji L, Izore T, Fenel D, Vernet T, Schoehn G, Di Guilmi AM, Dessen A (2008) Sortase-mediated pilus fiber biogenesis in Streptococcus pneumoniae. Structure 16: 1838-1848
25. Marraffini LA, Dedent AC, Schneewind O (2006) Sortases and the art of anchoring proteins to the envelopes of Gram-positive bacteria. Microbiol Mol Biol Rev 70: 192-221
26. Mora M, Bensi G, Capo S, Falugi F, Zingaretti C, Manetti AG, Maggi T, Taddei AR, Grandi G, Telford JL (2005) Group A Streptococcus produce pilus-like structures containing protective antigens and Lancefield T antigens. Proc Natl Acad Sci USA 102: 15641-15646
27. Mueller CA, Broz P, Müller SA, Ringler P, Erne-Brand F, Sorg I, Kuhn M, Engel A, Cornelis GR (2005) The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. Science 310: 674-676
28. Müller SA, Engel A (2001) Structure and mass analysis by scanning transmission electron microscopy. Micron 32: 21-31
29. Müller SA, Engel A (2006) Biological scanning transmission electron microscopy: imaging and single molecule mass determination. CHIMIA 60: 749-753
30. Nallapareddy SR, Singh KV, Sillanpaa J, Garsin DA, Hook M, Erlandsen SL, Murray BE (2006) Endocarditis and biofilm-associated pili of Enterococcus faecalis. J Clin Invest 116: 2799-2807
31. Neiers F, Madhurantakam C, Fälker S, Manzano C, Dessen A, Normark S, Henriques-Normark B, Achour A (2009) Two crystal structures of pneumococcal pilus sortase C provide novel insights into catalysis and substrate specificity. J Mol Biol 393: 704-716
32. Nelson AL, Ries J, Bagnoli F, Dahlberg S, Faelker S, Rounioja S, Tschoep J, Morfeldt E, Ferlenghi I, Hilleringmann M, Holden DW, Rappuoli R, Normark S, Barocchi MA, Henriques-Normark B (2007) RrgA is a pilus-associated adhesin in Streptococcus pneumoniae. Mol Microbiol 66: 329-340
33. Nobbs AH, Rosini R, Rinaudo CD, Maione D, Grandi G, Telford JL (2008) Sortase A utilizes an ancillary protein anchor for efficient cell wall anchoring of pili in Streptococcus agalactiae. Infect Immun 76: 3550-3560
34. Osaki M, Takamatsu D, Shimoji Y, Sekizaki T (2002) Characterization of Streptococcus suis genes encoding proteins homologous to sortase of gram-positive bacteria. J Bacteriol 184: 971-982
35. Proft T, Baker EN (2009) Pili in Gram-negative and Gram-positive bacteria-structure, assembly and their role in disease. Cell Mol Life Sci 66: 613-635
36. Rosch JW, Mann B, Thornton J, Sublett J, Tuomanen E (2008) Convergence of regulatory networks on the pilus locus of Streptococcus pneumoniae. Infect Immun 76: 3187-3196
37. Swaminathan A, Mandlik A, Swierczynski A, Gaspar A, Das A, Ton-That H (2007) Housekeeping sortase facilitates the cell wall anchoring of pilus polymers in Corynebacterium diphtheriae. Mol Microbiol 66: 961-974
38. Telford JL, Barocchi MA, Margarit I, Rappuoli R, Grandi G (2006) Pili in Gram-positive pathogens. Nat Rev Microbiol 4: 509-519
39. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD, Peterson S, Heidelberg J, DeBoy RT, Haft DH, Dodson RJ, Durkin AS, Gwinn M, Kolonay JF, Nelson WC, Peterson JD, Umayam LA, White O, Salzberg SL, Lewis MR, Radune D et al (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293: 498-506
40. Ton-That H, Marraffini LA, Schneewind O (2004) Sortases and pilin elements involved in pilus assembly of Corynebacterium diphtheriae. Mol Microbiol 53: 251-261
41. Ton-That H, Schneewind O (2003) Assembly of pili on the surface of Corynebacterium diphtheriae. Mol Microbiol 50: 1429-1438
42. Ton-That H, Schneewind O (2004) Assembly of pili in Gram-positive bacteria. Trends Microbiol 12: 228-234
43. Wu H, Fives-Taylor PM (2001) Molecular strategies for fimbrial expression and assembly. Crit Rev Oral Biol Med 12: 101-115
44. Xu P, Alves JM, Kitten T, Brown A, Chen Z, Ozaki LS, Manque P, Ge X, Serrano MG, Puiu D, Hendricks S, Wang Y, Chaplin MD, Akan D, Paik S, Peterson DL, Macrina FL, Buck GA (2007) Genome of the opportunistic pathogen Streptococcus sanguinis. J Bacteriol 189: 3166-3175