Structural Basis of Host Cell Recognition by the Pilus Adhesin from Streptococcus pneumoniae

Structure

Volumn 18, Issue 1, 2010, Pages 106-115

  Izoré, Thierry ^a   Contreras Martel, Carlos ^a   El Mortaji, Lamya ^a   Manzano, Clothilde ^a   Terrasse, Rémy ^a   Vernet, Thierry ^a   Di Guilmi, Anne Marie ^a   Dessen, Andréa ^a  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

MICROBIO; PROTEINS

Indexed keywords

ADHESIN; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM PILUS; CONTROLLED STUDY; CRYSTAL STRUCTURE; EXTRACELLULAR MATRIX; GRAM POSITIVE BACTERIUM; HOST CELL; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; MACROMOLECULE; MASS SPECTROMETRY; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; STREPTOCOCCUS PNEUMONIAE;

ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; EXTRACELLULAR MATRIX; FIMBRIAE, BACTERIAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; STREPTOCOCCUS PNEUMONIAE;

ANIMALIA; BACTERIA (MICROORGANISMS); EUKARYOTA; POSIBACTERIA; PROKARYOTA; STREPTOCOCCUS PNEUMONIAE;

EID: 73449128661     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2009.10.019     Document Type: Article

References (53)

1. Abbot E.L., Smith W.D., Siou G.P.S., Chiriboga C., Smith R.J., Wilson J.A., Hirst B.H., and Kehoe M.A. Pili mediate specific adhesion of Streptococcus pyogenes to human tonsil and skin. Cell. Microbiol. 9 (2007) 1822-1833
2. Barocchi M.A., Ries J., Zogaj X., Hemsley C., Albiger B., Kanth A., Dahlberg S., Fernebro J., Moschioni M., Masignani V., et al. A pneumococcal pilus influences virulence and host inflammatory responses. Proc. Natl. Acad. Sci. USA 103 (2006) 2857-2862
3. Bienkowska J., Cruz M., Atiemo A., Handin R., and Liddington R. The von Willebrand Factor A3 domain does not contain a metal ion-dependent adhesion site motif. J. Biol. Chem. 272 (1997) 25162-25167
4. Bricogne G., Vonrhein C., Flensburg C., Schiltz M., and Paciorek W. Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr. D Biol. Crystallogr. 59 (2003) 2023-2030
5. Bronzwaer S.L., Cars O., Buchholz U., Molstad S., Goettsch W., Veldhuijzen I.K., Kool J.L., Sprenger M.J.W., and Degener J.E. A European study on the relationship between antimicrobial use and antimicrobial resistance. Emerg. Infect. Dis. 8 (2002) 278-282
6. Budzik J.M., Marraffini L.A., Souda P., Whitelegge J.P., Faull K.F., and Schneewind O. Amide bonds assemble pili on the surface of bacilli. Proc. Natl. Acad. Sci. USA 105 (2008) 10215-10220
7. Cruz M.A., Yuan H., Lee J.R., Wise R.J., and Handin R.I. Interaction of the von Willebrand factor (vWF) with collagen. J. Biol. Chem. 270 (1995) 10822-10827
8. de la Fortelle E., and Bricogne G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276 (1997) 472-494
9. Deivanayagam C.C.S., Rich R.L., Carson M., Owens R.T., Danthuluri S., Bice T.W., Hook M., and Narayana S.V.L. Novel fold and assembly of the repetitive B region of the Staphylococcus aureus collagen-binding surface protein. Structure 8 (2000) 67-78
10. Dodson K.W., Pinkner J.S., Rose T., Magnusson G., Hultgren S.J., and Waksman G. Structural basis of the interaction of the pyelonephritic E. coli adhesin to its human kidney receptor. Cell 105 (2001) 733-743
11. Dormitzer P.R., Ulmer J.B., and Rappuoli R. Structure-based antigen design: a strategy for next generation vaccines. Trends Biotechnol. 26 (2008) 659-667
12. Dramsi S., Caliot E., Bonne I., Guadagnini S., Prevost M.-C., Kojadinovic M., Lalioui L., Poyart C., and Trieu-Cout P. Assembly and role of pili in group B streptococci. Mol. Microbiol. 60 (2006) 1401-1413
13. Dramsi S., Magnet S., Davison S., and Arthur M. Covalent attachment of proteins to peptidoglycan. FEMS Microbiol. Rev. 32 (2008) 307-320
14. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
15. Emsley J., Knight C.G., Farndale R.W., Barnes M.J., and Liddington R. Structural basis of collagen recognition by integrin α2β1. Cell 101 (2000) 47-56
16. Fälker S., Nelson A.L., Morfeldt E., Jonas K., Hultenby K., Ries J., Melefors O., Normark S., and Henriques-Normark B. Sortase-mediated assembly and surface topology of adhesive pneumococcal pili. Mol. Microbiol. 70 (2008) 595-607
17. Gianfaldoni C., Censini S., Hilleringmann M., Moschioni M., Facciotti C., Pansegrau W., Masignani V., Covacci A., Rappuoli R., Barocchi M.A., and Ruggiero P. Streptococcus pneumoniae pilus subunits protect mice against lethal challenge. Infect. Immun. 75 (2007) 1059-1062
18. Hilleringmann M., Giusti F., Baudner B.C., Masignani V., Covacci A., Rappuoli R., Barocchi M.A., and Ferlenghi I. Pneumococcal pili are composed of protofilaments exposing adhesive clusters of RrgA. PLoS Pathog. 4 (2008) e1000026
19. Huizinga E.G., van der Plas R.M., Kroon J., Sixma J.J., and Gros P. Crystal structure of the A3 domain of human von Willebrand factor: implications for collagen binding. Structure 5 (1997) 1147-1156
20. Imberty A., Lortat-Jacob H., and Perez S. Structural view of glycosaminoglycan-protein interactions. Carbohydr. Res. 342 (2007) 430-439
21. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26 (1993) 795-800
22. Kamata T., and Takada Y. Direct binding of collagen to the I domain of integrin α2β1 (VLA-2, CD49b/CD29) in a divalent cation-independent manner. J. Biol. Chem. 269 (1994) 26006-26010
23. Kang H.J., and Baker E.N. Intramolecular isopeptide bonds give thermodynamic and proteolytic stability to the major pilin protein of Streptococcus pyogenes. J. Biol. Chem. 284 (2009) 20729-20737
24. Kang H.J., Coulibaly F., Clow F., Proft T., and Baker E.N. Stabilizing isopeptide bonds revealed in Gram-positive bacterial pilus structure. Science 318 (2007) 1625-1628
25. Kreikemeyer B., Nakata M., Oehmcke S., Gschwendtner C., Normann J., and Podbielski A. Streptococcus pyogenes collagen type I-binding Cpa surface protein. Expression profile, binding characteristics, biological function, and potential clinical impact. J. Biol. Chem. 280 (2005) 33228-33239
26. Krishnan V., Gaspar A.H., Ye N., Mandlik A., Ton-That H., and Narayana S.V.L. An IgG-like domain in the minor pilin GBS52 of Streptococcus agalactiae mediates lung epithelial cell adhesion. Structure 15 (2007) 893-903
27. Lee J.-O., Bankston L.A., Arnaout M.A., and Liddington R.C. Two conformations of the integrin A-domain (I-domain): a pathway for activation?. Structure 3 (1995) 1333-1340
28. Lee J.-O., Rieu P., Arnaout M.A., and Liddington R. Crystal structure of the A domain from the α subunit of integrin CR3 (CD11b/CD18). Cell 80 (1995) 631-638
29. LeMieux J., Hava D.L., Basset A., and Camilli A. RrgA and RrgB are components of a multisubunit pilus encoded by the Streptococcus pneumoniae rlrA pathogenicity islet. Infect. Immun. 74 (2006) 2453-2456
30. Levine O.S., O'Brien K.L., Knoll M., Adegbola R.A., Black S., Cherian T., Dagan R., Goldblatt D., Grange A., Greenwood B.M., et al. Pneumococcal vaccination in developing countries. Lancet 367 (2006) 1880-1882
31. Maione D., Margarit I., Rinaudo C.D., Masignani V., Mora M., Scarselli M., Tettelin H., Brettoni C., Iacobini E.T., Rosini R., et al. Identification of a universal group B Streptococcus vaccine by multiple genome screen. Science 309 (2005) 148-150
32. Maisey H.C., Hensler M., Nizet V., and Doran K.S. Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. J. Bacteriol. 189 (2007) 1464-1467
33. Mandlik A., Swierczynski A., Das A., and Ton-that H. Corynebacterium diphtheriae employs specific minor pilins to target human pharyngeal epithelial cells. Mol. Microbiol. 64 (2007) 111-124
34. Mandlik A., Das A., and 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 (2008) 14147-14152
35. Mandlik A., Swierczynski A., Das A., and Ton-That H. Pili in Gram-positive bacteria: assembly, involvement in colonization and biofilm development. Trends Microbiol. 16 (2008) 33-40
36. Manzano C., Contreras-Martel C., El Mortaji L., Izore T., Fenel D., Vernet T., Schoehn G., Di Guilmi A.M., and Dessen A. Sortase-mediated pilus fiber biogenesis in Streptococcus pneumoniae. Structure 16 (2008) 1838-1848
37. Manzano C., Izoré T., Di Guilmi A.M., and Dessen A. Sortase activity is controlled by a flexible lid in the pilus biogenesis mechanism of Gram-positive pathogens. Biochemistry 48 (2009) 10549-10557
38. Mora M., Bensi G., Capo S., Falugi F., Zingaretti C., Manetti A.G.O., Maggi T., Taddei A.R., Grandi G., and Telford J.L. Group A Streptococcus produce pilus-like structures containing protective antigens and Lancefield T antigens. Proc. Natl. Acad. Sci. USA 102 (2005) 15641-15646
39. Murshudov G., Vagin A., and Dodson E. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53 (1997) 240-255
40. Nallapareddy S.R., Singh K.V., Sillanpaa J., Garsin D.A., Hook M., Erlandsen S.L., and Murray B.E. Endocarditis and biofilm-associated pili of Enterococcus faecalis. J. Clin. Invest. 116 (2006) 2799-2807
41. Neiers F., Madhurantakam C., Fälker S., Manzano C., Dessen A., Normark S., Henriques-Normark B., and Achour A. Two crystal structures of pneumococcal pilus sortase C provide novel insights into catalysis and substrate specificity. J. Mol. Biol. 393 (2009) 704-716
42. Nelson A.L., Ries J., Bagnoli F., Dahlberg S., Falkner S., Rounioja S., Tschop J., Morfeldt E., Ferlenghi I., Hilleringmann M., et al. RrgA is a pilus-associated adhesin in Streptococcus pneumoniae. Mol. Microbiol. 66 (2007) 329-340
43. Perrakis A., Morris R.M., and Lamzin V.S. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6 (1999) 458-463
44. Proft T., and Baker E.N. Pili in Gram-negative and Gram-positive bacteria-structure, assembly, and their role in disease. Cell. Mol. Life Sci. 66 (2009) 613-635
45. Qu A., and Leahy D.J. Crystal structure of the I-domain from the CD11a/CD18 (LFA-1, αLβ2) integrin. Proc. Natl. Acad. Sci. USA 92 (1995) 10277-10281
46. Scott J.R., and Zahner D. Pili with strong attachments: Gram-positive bacteria do it differently. Mol. Microbiol. 62 (2006) 320-330
47. Soto G.E., and Hultgren S.J. Bacterial adhesins: common themes and variations in architecture and assembly. J. Bacteriol. 181 (1999) 1059-1071
48. Springer T.A. Complement and multifaceted functions of VWA and integrin I domains. Structure 14 (2006) 1611-1616
49. Storoni L.C., McCoy A.J., and Read R.J. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 432-438
50. Telford J.L., Barocchi M.A., Margarit I., Rappuoli R., and Grandi G. Pili in Gram-positive pathogens. Nat. Rev. Microbiol. 4 (2006) 509-519
51. Ton-That H., and Schneewind O. Assembly of pili in Gram-positive bacteria. Trends Microbiol. 12 (2004) 228-234
52. Tuckwell D., Calderwood D.A., Green L.J., and Humphries M.J. Integrin α2 I-domain is a binding site for collagens. J. Cell Sci. 108 (1995) 1629-1637
53. Vorup-Jensen T., Ostermeier C., Shimaoka M., Hommel U., and Springer T. Structure and allosteric regulation of the αxβ2 integrin I domain. Proc. Natl. Acad. Sci. USA 100 (2003) 1873-1878