Structural biology of Gram-positive bacterial adhesins

Protein Science

Volumn 20, Issue 5, 2011, Pages 759-772

  Vengadesan, Krishnan ^a   Narayana, Sthanam V L ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Bacterial adhesions; Gram positive pili; Pilins; Protein structure

Indexed keywords

ADHESIN; BACTERIAL ADHESIN; BACTERIAL PROTEIN; COLLAGEN; FIBRINOGEN; FIBRONECTIN; IMMUNOGLOBULIN; MEMBRANE PROTEIN; PILIN; UNCLASSIFIED DRUG;

BACILLUS ANTHRACIS; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM PILUS; CELL WALL; CORYNEBACTERIUM DIPHTHERIAE; CYTOPLASM; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; INTRACELLULAR TRANSPORT; LIGAND BINDING; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS PNEUMONIAE; STREPTOCOCCUS PYOGENES; STRESS;

ADHESINS, BACTERIAL; EXTRACELLULAR MATRIX PROTEINS; FIMBRIAE, BACTERIAL; GRAM-POSITIVE BACTERIA; GRAM-POSITIVE BACTERIAL INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, MOLECULAR; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA;

EID: 79954455133     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.613     Document Type: Review

References (69)

1. Kline KA, Dodson KW, Caparon MG, Hultgren SJ (2010) A tale of two pili: assembly and function of pili in bacteria. Trends Microbiol 18:224-232.
2. Sauer FG, Mulvey MA, Schilling JD, Martinez JJ, Hultgren SJ (2000) Bacterial pili: molecular mechanisms of pathogenesis. Curr Opin Microbiol 3:65-72. (Pubitemid 30094266)
3. Waksman G, Hultgren SJ (2009) Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat Rev Microbiol 7:765-774.
4. Choudhury D, Thompson A, Stojanoff V, Langermann S, Pinkner J, Hultgren SJ, Knight SD (1999) X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 285: 1061-1066.
5. Scott JR, Zahner D (2006) Pili with strong attachments: Gram-positive bacteria do it differently. Mol Microbiol 62:320-330. (Pubitemid 44477224)
6. Telford JL, Barocchi MA, Margarit I, Rappuoli R, Grandi G (2006) Pili in Gram-positive pathogens. Nat Rev Microbiol 4:509-519. (Pubitemid 43905610)
7. Ton-That H, Schneewind O (2004) Assembly of pili in Gram-positive bacteria. Trends Microbiol 12:228-234. (Pubitemid 38534627)
8. Ton-That H, Schneewind O (2003) Assembly of pili on the surface of Corynebacterium diphtheriae. Mol Microbiol 50:1429-1438. (Pubitemid 37475871)
9. Cossart P, Jonquieres R ( 2000) Sortase, a universal target for therapeutic agents against Gram-positive bacteria? Proc Natl Acad Sci USA 97:5013-5015. (Pubitemid 30313659)
10. Patti JM, Allen BL, McGavin MJ, Höök M (1994) MSCRAMM-mediated adherence of microorganisms to host tissues. Annu Rev Microbiol 48:585-617.
11. Hawiger J, Timmons S, Strong DD, Cottrell BA, Riley M, Doolittle RF (1982) Identification of a region of human fibrinogen interacting with staphylococcal clumping factor. Biochemistry 21:1407-1413. (Pubitemid 12153090)
12. Kuusela P (1978) Fibronectin binds to Staphylococcus aureus. Nature 276:718-720. (Pubitemid 9073530)
13. Speziale P, Raucci G, Visai L, Switalski LM, Timpl R, Höök M (1986) Binding of collagen to Staphylococcus aureus Cowan 1 J Bacteriol 167:77-81. (Pubitemid 16067047)
14. Schneewind O, Model P, Fischetti VA (1992) Sorting of protein A to the staphylococcal cell wall. Cell 70:267-281.
15. Krishnan V, Gaspar AH, Ye N, Mandlik A, Ton-That H, Narayana SV (2007) An IgG-like domain in the minor pilin GBS52 of Streptococcus agalactiae mediates lung epithelial cell adhesion. Structure 15:893-903. (Pubitemid 47212752)
16. Kang HJ, Paterson NG, Gaspar AH, Ton-That H, Baker EN (2009) 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.
17. Izoré T, Contreras-Martel C, El Mortaji L, Manzano C, Terrasse R, Vernet T, Di Guilmi AM, Dessen A (2010) Structural basis of host cell recognition by the pilus adhesin from Streptococcus pneumoniae. Structure 18: 106-115.
18. Budzik JM, Poor CB, Faull KF, Whitelegge JP, He C, Schneewind O (2009) Intramolecular amide bonds stabilize pili on the surface of bacilli. Proc Natl Acad Sci USA 106:19992-19997.
19. Bork P, Holm L, Sander C (1994) The immunoglobulin fold. Structural classification, sequence patterns and common core. J Mol Biol 242:309-320.
20. Harpaz Y, Chothia C (1994) Many of the immunoglobulin superfamily domains in cell adhesion molecules and surface receptors belong to a new structural set which is close to that containing variable domains. J Mol Biol 238:528-539. (Pubitemid 24160280)
21. Symersky J, Patti JM, Carson M, House-Pompeo K, Teale M, Moore D, Jin L, Schneider A, DeLucas LJ, Höök M, Narayana SV (1997) Structure of the collagen-binding domain from a Staphylococcus aureus adhesin. Nat Struct Biol 4:833-838. (Pubitemid 27435349)
22. Deivanayagam CC, Rich RL, Carson M, Owens RT, Danthuluri S, Bice T, Höök M, Narayana SV (2000) Novel fold and assembly of the repetitive B region of the Staphylococcus aureus collagen-binding surface protein. Structure 8:67-78. (Pubitemid 30051343)
23. Yanagawa R, Otsuki K, Tokui T (1968) Electron microscopy of fine structure of Corynebacterium renale with special reference to pili. Jpn J Vet Res 16:31-37.
24. Mandlik A, Swierczynski A, Das A, Ton-That H (2008) Pili in Gram-positive bacteria: assembly, involvement in colonization and biofilm development. Trends Microbiol 16:33-40.
25. 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.
26. Kang HJ, Coulibaly F, Clow F, Proft T, Baker EN (2007) Stabilizing isopeptide bonds revealed in Gram-positive bacterial pilus structure. Science 318:1625-1628. (Pubitemid 350233661)
27. 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.
28. Pickart CM (2001) Mechanisms underlying ubiquitination. Annu Rev Biochem 70:503-533. (Pubitemid 32663902)
29. Greenberg CS, Birckbichler PJ, Rice RH (1991) Transglutaminases: multifunctional cross-linking enzymes that stabilize tissues. FASEB J 5:3071-3077. (Pubitemid 21892867)
30. Linke C, Young PG, Kang HJ, Bunker RD, Middleditch MJ, Caradoc-Davies TT, Proft T, Baker EN (2010) Crystal structure of the minor pilin FctB reveals determinants of Group A streptococcal pilus anchoring. J Biol Chem 285:20381-20389.
31. Mandlik A, Das A, Ton-That H (2008) 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.
32. Emsley J, Knight CG, Farndale RW, Barnes MJ, Liddington RC (2000) Structural basis of collagen recognition by integrin a2b1 Cell 101:47-56.
33. Krishnan V, Xu Y, Macon K, Volanakis JE, Narayana SV (2007) The crystal structure of C2a, the catalytic fragment of classical pathway C3 and C5 convertase of human complement. J Mol Biol 367:224-233. (Pubitemid 46274711)
34. Ponnuraj K, Xu Y, Macon K, Moore D, Volanakis JE, Narayana SV (2004) Structural analysis of engineered Bb fragment of complement factor B: insights into the activation mechanism of the alternative pathway C3-convertase. Mol Cell 14:17-28. (Pubitemid 38469906)
35. Konto-Ghiorghi Y, Mairey E, Mallet A, Dumenil G, Caliot E, Trieu-Cuot P, Dramsi S ( 2009) Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae. PLoS Pathog 5: e1000422.
36. 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. (Pubitemid 40934983)
37. 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. (Pubitemid 43801433)
38. Rosini R, Rinaudo CD, Soriani M, Lauer P, Mora M, Maione D, Taddei A, Santi I, Ghezzo C, Brettoni C, Buccato S, Margarit I, Grandi G, Telford JL (2006) Identification of novel genomic islands coding for antigenic pilus-like structures in Streptococcus agalactiae. Mol Microbiol 61:126-141.
39. Vengadesan K, Ma X, Dwivedi P, Ton-That H, Narayana SV (2010) Purification, crystallization and halide phasing of a Streptococcus agalactiae backbone pilin GBS80 fragment. Acta Crystallogr Sect F Struct Biol Cryst Commun 66:1666-1669.
40. Spraggon G, Koesema E, Scarselli M, Malito E, Biagini M, Norais N, Emolo C, Barocchi MA, Giusti F, Hilleringmann M, Rappuoli R, Lesley S, Covacci A, Masignani V, Ferlenghi I ( 2010) Supramolecular organization of the repetitive backbone unit of the Streptococcus pneumoniae pilus. PLoS One 5:e10919.
41. Budzik JM, Oh SY, Schneewind O (2009) Sortase D forms the covalent bond that links BcpB to the tip of Bacillus cereus pili. J Biol Chem 284:12989-12997.
42. Swierczynski A, Ton-That H (2006) Type III pilus of corynebacteria: Pilus length is determined by the level of its major pilin subunit. J Bacteriol 188:6318-6325. (Pubitemid 44448574)
43. Gaspar AH, Ton-That H (2006) Assembly of distinct pilus structures on the surface of Corynebacterium diphtheriae. J Bacteriol 188:1526-1533. (Pubitemid 43228686)
44. Mishra A, Das A, Cisar JO, Ton-That H (2007) Sortasecatalyzed assembly of distinct heteromeric fimbriae in Actinomyces naeslundii. J Bacteriol 189:3156-3165. (Pubitemid 46697406)
45. Shoulders MD, Raines RT (2009) Collagen structure and stability. Annu Rev Biochem 78:929-958.
46. House-Pompeo K, Boles JO, Höök M ( 1994) Characterization of bacterial adhesin interactions with extracellular matrix components utilizing biosensor technology. Methods: A Companion to Meth Enzymol 6:134-142.
47. Patti JM, House-Pompeo K, Boles JO, Garza N, Gurusiddappa S, Höök M (1995) Critical residues in the ligand-binding site of the Staphylococcus aureus collagen-binding adhesin (MSCRAMM). J Biol Chem 270: 12005-12011.
48. Ponnuraj K, Narayana SV (2007) Crystal structure of ACE19, the collagen binding subdomain of Enterococus faecalis surface protein ACE. Proteins 69:199-203. (Pubitemid 47339150)
49. Liu Q, Ponnuraj K, Xu Y, Ganesh VK, Sillanpaa J, Murray BE, Narayana SV, Höök M (2007) The Enterococcus faecalis MSCRAMM ACE binds its ligand by the Collagen Hug model. J Biol Chem 282:19629-19637. (Pubitemid 47100065)
50. Zong Y, Xu Y, Liang X, Keene DR, Höök A, Gurusiddappa S, Höök M, Narayana SV (2005) A 'Collagen Hug' model for Staphylococcus aureus CNA binding to collagen. EMBO J 24:4224-4236. (Pubitemid 41828898)
51. Deivanayagam CC, Wann ER, Chen W, Carson M, Rajashankar KR, Höök M, Narayana SV (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. (Pubitemid 36014538)
52. Emsley J, Knight CG, Farndale RW, Barnes MJ (2004) Structure of the integrin a2b1-binding collagen peptide. J Mol Biol 335:1019-1028. (Pubitemid 38091607)
53. Rich RL, Demeler B, Ashby K, Deivanayagam CC, Petrich JW, Patti JM, Narayana SV, Höök M (1998) Domain structure of the Staphylococcus aureus collagen adhesin. Biochemistry 37:15423-15433. (Pubitemid 28516004)
54. Liotta LA, Tryggvason K, Garbisa S, Hart I, Foltz CM, Shafie S (1980) Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 284:67-68. (Pubitemid 10098769)
55. Kehrel B (1995) Platelet-collagen interactions. Semin Thromb Hemost 21:123-129.
56. Herrick S, Blanc-Brude O, Gray A, Laurent G (1999) Fibrinogen. Int J Biochem Cell Biol 31:741-746. (Pubitemid 29333117)
57. Kloczewiak M, Timmons S, Lukas TJ, Hawiger J (1984) Platelet receptor recognition site on human fibrinogen. Synthesis and structure-function relationship of peptides corresponding to the carboxy-terminal segment of the c chain. Biochemistry 23:1767-1774. (Pubitemid 14139817)
58. Smith JW, Piotrowicz RS, Mathis D (1994) A mechanism for divalent cation regulation of b3-integrins. J Biol Chem 269:960-967. (Pubitemid 24032470)
59. D'Souza SE, Haas TA, Piotrowicz RS, Byers-Ward V, McGrath DE, Soule HR, Cierniewski C, Plow EF, Smith JW (1994) Ligand and cation binding are dual functions of a discrete segment of the integrin b3 subunit: cation displacement is involved in ligand binding. Cell 79:659-667. (Pubitemid 24363809)
60. Ponnuraj K, Bowden MG, Davis S, Gurusiddappa S, Moore D, Choe D, Xu Y, Höök M, Narayana SV (2003) A ''dock, lock, and latch'' structural model for a staphylococcal adhesin binding to fibrinogen. Cell 115:217-228. (Pubitemid 37329585)
61. Ganesh VK, Rivera JJ, Smeds E, Ko YP, Bowden MG, Wann ER, Gurusiddappa S, Fitzgerald JR, Höök M, (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.
62. Schwarz-Linek U, Werner JM, Pickford AR, Gurusiddappa S, Kim JH, Pilka ES, Briggs JA, Gough TS, Höök M, Campbell ID, Potts JR (2003) Pathogenic bacteria attach to human fibronectin through a tandem bzipper. Nature 423:177-181. (Pubitemid 36569541)
63. Schwarz-Linek U, Pilka ES, Pickford AR, Kim JH, Höök M, Campbell ID, Potts JR (2004) High-affinity streptococcal binding to human fibronectin requires specific recognition of sequential F1 modules. J Biol Chem 279:39017-39025. (Pubitemid 39296063)
64. Schwarz-Linek U, Höök M, Potts JR (2006) Fibronectin-binding proteins of Gram-positive cocci. Microbes Infect 8:2291-2298. (Pubitemid 44311581)
65. Jonsson K, Signas C, Muller HP, Lindberg M (1991) Two different genes encode fibronectin binding proteins in Staphylococcus aureus. The complete nucleotide sequence and characterization of the second gene. Eur J Biochem 202:1041-1048.
66. Bingham RJ, Rudino-Pinera E, Meenan NA, Schwarz-Linek U, Turkenburg JP, Höök M, Garman EF, Potts JR (2008) Crystal structures of fibronectin-binding sites from Staphylococcus aureus FnBPA in complex with fibronectin domains. Proc Natl Acad Sci U S A 105:12254-12258.
67. Wann ER, Gurusiddappa S, Höök 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. (Pubitemid 30257461)
68. Bowden MG, Heuck AP, Ponnuraj K, Kolosova E, Choe D, Gurusiddappa S, Narayana SV, Johnson AE, Höök M (2008) Evidence for the ''dock, lock, and latch'' ligand binding mechanism of the staphylococcal microbial surface component recognizing adhesive matrix molecules (MSCRAMM) SdrG. J Biol Chem 283: 638-647.
69. Vengadesan K, Ma X, Dwivedi P, Ton-That H, Narayana SV (2011) A model for Group B Streptococcus pilus type 1: The structure of a 35-kDa C-terminal fragment of the major pilin GBS80 J Mol Biol 407: 731-743.