Skip to main content
SpringerLink
Log in

Crystallography of Gram-Positive Bacterial Adhesins

  • Chapter
  • First Online:
Bacterial Adhesion

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 715))

Abstract

Both Gram-negative and Gram-positive pathogens display a multitude of proteins and protein assemblies (pili or fimbriae) on their cell surfaces, which are often used for adherence and initiate colonization and pathogenesis. Adhesive proteins known as MSCRAMMs (microbial surface components recognizing adhesive matrix molecules), anchored by a specific enzyme called sortase in Gram-positive bacteria, target the host’s extracellular matrix proteins (ECM) like collagen, fibrinogen and fibronectin. In the past decade, structural analysis by X-ray crystallography has enhanced our understanding of the interactions between MSCRAMMs and the host ECM by revealing several novel structural features that dictate surface protein assembly and the mode of their adhesion to host tissue. The latest focus is on the recently discovered Gram-positive bacterial pili, assembly of which is assisted by yet another specific sortase. Novel features like inter- and intra-molecular isopeptide bonds that facilitate the stability of the pilins, and intra-molecular donor strand complementation to stabilize the adhesin-target interactions are specific to Gram-positive bacteria. This chapter describes and discusses the common structural details between surface proteins and pilins of Gram-positive bacteria and biological implications emanating from these structures.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 179.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 229.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Baker C, Edward M (2001) Group B streptococcal infections. In: Remington JS, Klein JO (eds) Infectious diseases of the fetus and newborn infant. WB Saunders, Philadelphia: PA, pp 1091–1156

    Google Scholar 

  • 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 USA 105:12254–12258

    Article  PubMed  CAS  Google Scholar 

  • Bork P, Holm L, Sander C (1994) The immunoglobulin fold. Structural classification, sequence patterns and common core. J Mol Biol 242:309–320

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 β3 subunit: cation displacement is involved in ligand binding. Cell 79: 659–667

    Article  PubMed  Google Scholar 

  • Emsley J, Knight CG, Farndale RW, Barnes MJ (2004) Structure of the integrin α2β1-binding collagen peptide. J Mol Biol 335:1019–1028

    Article  PubMed  CAS  Google Scholar 

  • Emsley J, Knight CG, Farndale RW, Barnes MJ, Liddington RC (2000) Structural basis of collagen recognition by integrin α2β1. Cell 101:47–56

    Article  PubMed  CAS  Google Scholar 

  • Flock JI, Froman G, Jonsson K, Guss B, Signas C, Nilsson B, Raucci G, Höök M, Wadstrom T, Lindberg M (1987) Cloning and expression of the gene for a fibronectin-binding protein from Staphylococcus aureus. EMBO J 6:2351–2357

    PubMed  CAS  Google Scholar 

  • Froman G, Switalski LM, Speziale P, Höök M (1987) Isolation and characterization of a fibronectin receptor from Staphylococcus aureus. J Biol Chem 262:6564–6571

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Gaspar AH, Ton-That H (2006) Assembly of distinct pilus structures on the surface of Corynebacterium diphtheriae. J Bacteriol 188:1526–1533

    Article  PubMed  CAS  Google Scholar 

  • Greenberg CS, Birckbichler PJ, Rice RH (1991) Transglutaminases: multifunctional cross-linking enzymes that stabilize tissues. FASEB J 5:3071–3077

    PubMed  CAS  Google Scholar 

  • Hahn E, Wild P, Hermanns U, Sebbel P, Glockshuber R, Häner M, Taschner N, Burkhard P, Aebi U, Müller SA (2002) Exploring the 3D molecular architecture of Escherichia coli type 1 pili. J Mol Biol 323:845–857

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Herrick S, Blanc-Brude O, Gray A, Laurent G (1999) Fibrinogen. Int J Biochem Cell Biol 31: 741–746

    Article  PubMed  CAS  Google Scholar 

  • Hilleringmann M, Ringler P, Müller SA, De Angelis G, Rappuoli R, Ferlenghi I, Engel A (2009) Molecular architecture of Streptococcus pneumoniae TIGR4 pili. EMBO J 28:3921–3930

    Article  PubMed  CAS  Google Scholar 

  • House-Pompeo K, Boles JO, Höök M (1994) Characterization of bacterial adhesin interactions with extracellular matrix components utilizing biosensor technology. Methods: Companion Method Enzymol 6:134–142

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Jonsson K, Signas C, Müller 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kehrel B (1995) Platelet-collagen interactions. Semin Thromb Hemost 21:123–129

    Article  PubMed  CAS  Google Scholar 

  • 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 γ chain. Biochemistry 23:1767–1774

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kuusela P (1978) Fibronectin binds to Staphylococcus aureus. Nature 276:718–720

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Ponnuraj K, Xu Y, Ganesh VK, Sillanpää 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

    Article  PubMed  CAS  Google Scholar 

  • Mandlik A, Swierczynski A, Das A, Ton-That H (2007) Corynebacterium diphtheriae employs specific minor pilins to target human pharyngeal epithelial cells. Mol Microbiol 64:111–124

    Article  PubMed  CAS  Google Scholar 

  • Navarre WW, Schneewind O (1999) Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63:174–229

    PubMed  CAS  Google Scholar 

  • Patti JM, Allen BL, McGavin MJ, Höök M (1994a) MSCRAMM-mediated adherence of microorganisms to host tissues. Annu Rev Microbiol 48:585–617

    Article  PubMed  CAS  Google Scholar 

  • Patti JM, Boles JO, Höök M (1993) Identification and biochemical characterization of the ligand binding domain of the collagen adhesin from Staphylococcus aureus. Biochemistry 32: 11428–11435

    Article  PubMed  CAS  Google Scholar 

  • Patti JM, Bremell T, Krajewska-Pietrasik D, Abdelnour A, Tarkowski A, Ryden C, Höök M (1994b) The Staphylococcus aureus collagen adhesin is a virulence determinant in experimental septic arthritis. Infect Immun 62:152–161

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pickart CM (2001) Mechanisms underlying ubiquitination. Annu Rev Biochem 70:503–533

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ponnuraj K, Narayana SV (2007) Crystal structure of ACE19, the collagen binding subdomain of Enterococus faecalis surface protein ACE. Proteins 69:199–203

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Remaut H, Rose RJ, Hannan TJ, Hultgren SJ, Radford SE, Ashcroft AE, Waksman G (2006) Donor-strand exchange in chaperone-assisted pilus assembly proceeds through a concerted β strand displacement mechanism. Mol Cell 22:831–842

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Richardson JS (1981) The anatomy and taxonomy of protein structure. Adv Prot Chem 34:167–399

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sauer FG, Knight SD, Waksman Gj, Hultgren SJ (2000a) PapD-like chaperones and pilus biogenesis. Semin Cell Dev Biol 11:27–34

    Article  PubMed  CAS  Google Scholar 

  • Sauer FG, Mulvey MA, Schilling JD, Martinez JJ, Hultgren SJ (2000b) Bacterial pili: molecular mechanisms of pathogenesis. Curr Opin Microbiol 3:65–72

    Article  PubMed  CAS  Google Scholar 

  • Schneewind O, Model P, Fischetti VA (1992) Sorting of protein A to the staphylococcal cell wall. Cell 70:267–281

    Article  PubMed  CAS  Google Scholar 

  • Schwarz-Linek U, Höök M, Potts JR (2006) Fibronectin-binding proteins of Gram-positive cocci. Microbes Infect 8:2291–2298

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 β-zipper. Nature 423:177–181

    Article  PubMed  CAS  Google Scholar 

  • Scott JR, Zahner D (2006) Pili with strong attachments: Gram-positive bacteria do it differently. Mol Microbiol 62:320–330

    Article  PubMed  CAS  Google Scholar 

  • Shoulders MD, Raines RT (2009) Collagen structure and stability. Annu Rev Biochem 78: 929–958

    Article  PubMed  CAS  Google Scholar 

  • Smith JW, Piotrowicz RS, Mathis D (1994) A mechanism for divalent cation regulation of β 3-integrins. J Biol Chem 269:960–967

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Telford JL, Barocchi MA, Margarit I, Rappuoli R, Grandi G (2006) Pili in Gram-positive pathogens. Nat Rev Microbiol 4:509–519

    Article  PubMed  CAS  Google Scholar 

  • Ton-That H, Schneewind O (2003) Assembly of pili on the surface of Corynebacterium diphtheriae. Mol Microbiol 50:1429–1438

    Article  PubMed  CAS  Google Scholar 

  • Ton-That H, Schneewind O (2004) Assembly of pili in Gram-positive bacteria. Trends Microbiol 12:228–234

    Article  PubMed  CAS  Google Scholar 

  • Waksman G, Hultgren SJ (2009) Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat Rev Microbiol 7:765–774

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Xu Y, Liang X, Chen Y, Koehler TM, Höök M (2004) Identification and biochemical characterization of two novel collagen binding MSCRAMMs of Bacillus anthracis. J Biol Chem 279:51760–51768

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Optometry and Center for Biophysical Sciences and Engineering, University of Alabama at Birmingham, Birmingham, AL, USA

    Vengadesan Krishnan

  2. Center for Biophysical Sciences and Engineering, University of Alabama at Birmingham, Birmingham, AL, 35294, USA

    Sthanam V.L. Narayana

Authors
  1. Vengadesan Krishnan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sthanam V.L. Narayana
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sthanam V.L. Narayana .

Editor information

Editors and Affiliations

  1. , Department I, Protein Evolution, Max-Planck Institute for Developmental B, Spemannstr. 35, Tübingen, 72076, Germany

    Dirk Linke

  2. , Institute of Biotechnology, University of Helsinki, Viikinkaari 1, Helsinki, FIN-00014, Finland

    Adrian Goldman

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Krishnan, V., Narayana, S.V. (2011). Crystallography of Gram-Positive Bacterial Adhesins. In: Linke, D., Goldman, A. (eds) Bacterial Adhesion. Advances in Experimental Medicine and Biology, vol 715. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0940-9_11

Download citation

Publish with us

Policies and ethics

Search

Navigation