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Pilus Assembly in Gram-Positive Bacteria

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Protein and Sugar Export and Assembly in Gram-positive Bacteria

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 404))

Abstract

Pili of Gram-positive bacteria are unique structures on the bacterial surface, assembled from covalently linked polypeptide subunits. Pilus assembly proceeds by transpeptidation reactions catalyzed by sortases, followed by covalent anchoring of the filament in the peptidoglycan layer. Another distinctive property is the presence of intramolecular isopeptide bonds, conferring extraordinary chemical and mechanical stability to these elongated structures. Besides their function in cell adhesion and biofilm formation, this section discusses possible application of pilus constituents as vaccine components against Gram-positive pathogens.

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Abbreviations

BP:

Backbone protein

AP:

Ancillary protein

CWSS:

Cell wall sorting signal

m-Dap:

Meso-2,6-diaminopimelic acid

GAS:

Group A streptococcus (S. pyogenes)

GBS:

Group B streptococcus (S. agalactiae)

MIDAS:

Metal ion-dependent adhesion site

MSCRAMMs:

Microbial surface components recognizing adhesive matrix molecules

PI:

Pilus islet

vWFA:

von Willebrand factor type A domain

References

  • Abbot EL, Smith WD, Siou GPS, Chiriboga C, Smith RJ, Wilson JA et al (2007) Pili mediate specific adhesion of Streptococcus pyogenes to human tonsil and skin. Cell Microbiol 9:1822–1833

    Article  CAS  PubMed  Google Scholar 

  • Alegre-Cebollada J, Badilla CL, Fernández JM (2010) Isopeptide bonds block the mechanical extension of pili in pathogenic Streptococcus pyogenes. J Biol Chem 285:11235–11242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arias CA, Murray BE (2008) Emergence and management of drug-resistant enterococcal infections. Expert Rev Anti Infect Ther 6:637–655

    Article  CAS  PubMed  Google Scholar 

  • Bagnoli F, Moschioni M, Donati C, Dimitrovska V, Ferlenghi I, Facciotti C et al (2008) A second pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. J Bacteriol 190:5480–5492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barocchi MA, Ries J, Zogaj X, Hemsley C, Albiger B, Kanth A et al (2006) A pneumococcal pilus influences virulence and host inflammatory responses. Proc Natl Acad Sci USA 103:2857–2862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barocchi MA, Censini S, Rappuoli R (2007) Vaccines in the era of genomics: the pneumococcal challenge. Vaccine 25:2963–2973

    Article  CAS  PubMed  Google Scholar 

  • Basset A, Zhang F, Benes C, Sayeed S, Herd M, Thompson C et al (2013) Toll-like receptor (TLR) 2 mediates inflammatory responses to oligomerized RrgA pneumococcal pilus type 1 protein. J Biol Chem 288:2665–2675

    Article  CAS  PubMed  Google Scholar 

  • Bienkowska J, Cruz M, Atiemo A, Handin R, Liddington R (1997) The von Willebrand factor A3 domain does not contain a metal ion-dependent adhesion site motif. J Biol Chem 272:25162–25167

    Article  CAS  PubMed  Google Scholar 

  • Bradshaw WJ, Davies AH, Chambers CJ, Roberts AK, Shone CC, Acharya KR (2015) Molecular features of the sortase enzyme family. FEBS J 282:2097–2114

    Article  CAS  PubMed  Google Scholar 

  • Buccato S, Maione D, Rinaudo CD, Volpini G, Taddei AR, Rosini R et al (2006) Use of Lactococcus lactis expressing pili from group B Streptococcus as a broad-coverage vaccine against streptococcal disease. J Infect Dis 194:331–340

    Article  CAS  PubMed  Google Scholar 

  • Budzik JM, Marraffini LA, Schneewind O (2007) Assembly of pili on the surface of Bacillus cereus vegetative cells. Mol Microbiol 66:495–510

    Article  CAS  PubMed  Google Scholar 

  • Budzik JM, Oh SY, Schneewind O (2008) Cell wall anchor structure of BcpA pili in Bacillus anthracis. J Biol Chem 283:36676–36686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Budzik JM, Oh SY, Schneewind O (2009a) Sortase D forms the covalent bond that links BcpB to the tip of Bacillus cereus pili. J Biol Chem 284:12989–12997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Budzik JM, Poor CB, Faull KF, Whitelegge JP, He C, Schneewind O (2009b) Intramolecular amide bonds stabilize pili on the surface of bacilli. Proc Natl Acad Sci USA 106:19992–19997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Comfort D, Clubb RT (2004) A comparative genome analysis identifies distinct sorting pathways in gram-positive bacteria. Infect Immun 72:2710–2722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cozzi R, Prigozhin D, Rosini R, Abate F, Bottomley MJ, Grandi G et al (2012) Structural basis for group B streptococcus pilus 1 sortases C regulation and specificity. PLoS ONE 7:e49048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cozzi R, Zerbini F, Assfalg M, D’Onofrio M, Biagini M, Martinelli M et al (2013) Group B streptococcus pilus sortase regulation: a single mutation in the lid region induces pilin protein polymerization in vitro. FASEB J 27:3144–3154

    Article  CAS  PubMed  Google Scholar 

  • Cozzi R, Malito E, Lazzarin M, Nuccitelli A, Castagnetti A, Bottomley MJ et al (2015) Structure and assembly of group B streptococcus pilus 2b backbone protein. PLoS ONE 10:e0125875

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cruz MA, Yuan H, Lee JR, Wise RJ, Handin RI (1995) 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

    Article  CAS  PubMed  Google Scholar 

  • Danne C, Dubrac S, Trieu-Cuot P, Dramsi S (2014) Single cell stochastic regulation of pilus phase variation by an attenuation-like mechanism. PLoS Pathog 10:e1003860

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Angelis G, Moschioni M, Muzzi A, Pezzicoli A, Censini S, Delany I et al (2011) The Streptococcus pneumoniae pilus-1 displays a biphasic expression pattern. PLoS ONE 6:e21269

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deivanayagam CC, Wann ER, Chen W, Carson M, Rajashankar KR, Hook 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Dramsi S, Caliot E, Bonne I, Guadagnini SP, Prévost MC, Kojadinovic M. et al (2006) Assembly and role of pili in group B streptococci. Mol Microbiol 60:1401–1413

    Google Scholar 

  • Dutton RJ, Boyd D, Berkmen M, Beckwith J (2008) Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proc Natl Acad Sci USA 105:11933–11938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El Mortaji L, Contreras-Martel C, Moschioni M, Ferlenghi I, Manzano C, Vernet T et al (2012a) The full-length Streptococcus pneumoniae major pilin RrgB crystallizes in a fibre-like structure, which presents the D1 isopeptide bond and provides details on the mechanism of pilus polymerization. Biochem J 441:833–841

    Article  PubMed  CAS  Google Scholar 

  • El Mortaji L, Fenel D, Vernet T, Di G (2012b) Association of RrgA and RrgC into the Streptococcus pneumoniae pilus by sortases C-2 and C-3. Biochemistry 51:342–352

    Article  PubMed  CAS  Google Scholar 

  • Fälker S, Nelson AL, Morfeldt E, Jonas K, Hultenby K, Ries J et al (2008) Sortase-mediated assembly and surface topology of adhesive pneumococcal pili. Mol Microbiol 70:595–607

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Falugi F, Zingaretti C, Pinto V, Mariani M, Amodeo L, Manetti AGO et al (2008) Sequence variation in group A streptococcus pili and association of pilus backbone types with lancefield T serotypes. J Infect Dis 198:1834–1841

    Article  CAS  PubMed  Google Scholar 

  • Flores-Mireles AL, Pinkner JS, Caparon MG, Hultgren SJ (2014) EbpA vaccine antibodies block binding of Enterococcus faecalis to fibrinogen to prevent catheter-associated bladder infection in mice. Sci Transl Med 6:254ra127

    Google Scholar 

  • Frankel BA, Kruger RG, Robinson DE, Kelleher NL, McCafferty DG (2005) Staphylococcus aureus sortase transpeptidase SrtA: insight into the kinetic mechanism and evidence for a reverse protonation catalytic mechanism. Biochemistry 44:11188–11200

    Article  CAS  PubMed  Google Scholar 

  • Frankel BA, Tong Y, Bentley ML, Fitzgerald MC, McCafferty DG (2007) Mutational analysis of active site residues in the Staphylococcus aureus transpeptidase SrtA. Biochemistry 46:7269–7278

    Article  CAS  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Gentile MA, Melchiorre S, Emolo C, Moschioni M, Gianfaldoni C, Pancotto L et al (2011) Structural and functional characterization of the Streptococcus pneumoniae RrgB pilus backbone D1 domain. J Biol Chem 286:14588–14597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gianfaldoni C, Censini S, Hilleringmann M, Moschioni M, Facciotti C, Pansegrau W et al (2007) Streptococcus pneumoniae pilus subunits protect mice against lethal challenge. Infect Immun 75:1059–1062

    Article  CAS  PubMed  Google Scholar 

  • Harfouche C, Filippini S, Gianfaldoni C, Ruggiero P, Moschioni M, Maccari S et al (2012) RrgB321, a fusion protein of the three variants of the pneumococcal pilus backbone RrgB, is protective in vivo and elicits opsonic antibodies. Infect Immun 80:451–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hava DL, Hemsley CJ, Camilli A (2003) Transcriptional regulation in the Streptococcus pneumoniae rlrA pathogenicity islet by RlrA. J Bacteriol 185:413–421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Helgstrand C, Wikoff WR, Duda RL, Hendrix RW, Johnson JE, Liljas L (2003) The refined structure of a protein catenane: the HK97 bacteriophage capsid at 3.44 Å resolution. J Mol Biol 334:885–899

    Article  CAS  PubMed  Google Scholar 

  • Heras B, Shouldice SR, Totsika M, Scanlon MJ, Schembri MA, Martin JL (2009) DSB proteins and bacterial pathogenicity. Nat Rev Microbiol 7:215–225

    Article  CAS  PubMed  Google Scholar 

  • Hilleringmann M, Giusti F, Baudner BC, Masignani V, Covacci A, Rappuoli R et al (2008) Pneumococcal pili are composed of protofilaments exposing adhesive clusters of Rrg A. PLoS Pathog 4:e1000026

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Izoré T, Contreras-Martel C, El ML, Manzano C, Terrasse R, Vernet T et al (2010) Structural basis of host cell recognition by the pilus adhesin from Streptococcus pneumoniae. Structure 18:106–115

    Article  PubMed  CAS  Google Scholar 

  • Kalkum M, Eisenbrandt R, Lurz R, Lanka E (2002) Tying rings for sex. Trends Microbiol 10:382–387

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang HJ, Baker EN (2011) Intramolecular isopeptide bonds: protein crosslinks built for stress? Trends Biochem Sci 36:229–237

    Article  CAS  PubMed  Google Scholar 

  • Kang HJ, Baker EN (2012) Structure and assembly of Gram-positive bacterial pili: unique covalent polymers. Curr Opin Struct Biol 22:200–207

    Article  CAS  PubMed  Google Scholar 

  • Kang HJ, Coulibaly Fl, Clow F, Proft T, Baker EN (2007) Stabilizing isopeptide bonds revealed in gram-positive bacterial pilus structure. Science 318:1625–1628

    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  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang HJ, Coulibaly F, Proft T, Baker EN (2011) Crystal structure of Spy0129, a Streptococcus pyogenes class B sortase involved in pilus assembly. PLoS ONE 6:e15969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang HJ, Paterson NG, Kim CU, Middleditch M, Chang C, Ton-That H, Baker EN (2014) A slow-forming isopeptide bond in the structure of the major pilin SpaD from Corynebacterium diphtheriae has implications for pilus assembly. Acta Crystallogr D Biol Crystallogr 70:1190–1201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kankainen M, Paulin L, Tynkkynen S, von Ossowski I, Reunanen J, Partanen P et al (2009) Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human- mucus binding protein. Proc Natl Acad Sci USA 106:17193–17198

    Google Scholar 

  • Khare B, Fu ZQ, Huang IH, Ton-That H, Narayana SV (2011) The crystal structure analysis of group B Streptococcus sortase C1: a model for the “lid” movement upon substrate binding. J Mol Biol 414:563–577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kreikemeyer B, Gamez G, Margarit I, Giard JC, Hammerschmidt S, Hartke A, Podbielski A (2011) Genomic organization, structure, regulation and pathogenic role of pilus constituents in major pathogenic Streptococci and Enterococci. Int J Med Microbiol 301:240–251

    Article  CAS  PubMed  Google Scholar 

  • Krishnan V, Dwivedi P, Kim BJ, Samal A, Macon K, Ma X et al (2013) Structure of Streptococcus agalactiae tip pilin GBS104: a model for GBS pili assembly and host interactions. Acta Crystallogr D Biol Crystallogr 69:1073–1089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumazawa N, Yanagawa R (1972) Chemical properties of the pili of Corynebacterium renale. Infect Immun 5:27–30

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lancefield RC (1940) Type-specific antigens, M and T, of matt and glossy variants of group a hemolytic streptococci. J Exp Med 71:521–537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lauer P, Rinaudo CD, Soriani M, Margarit I, Maione D, Rosini R et al (2005) Genome analysis reveals pili in group B Streptococcus. Science 309:105

    Article  CAS  PubMed  Google Scholar 

  • Law SK, Dodds AW (1997) The internal thioester and the covalent binding properties of the complement proteins C3 and C4. Protein Sci 6:263–274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le DT, Tran TL, Duviau MP, Meyrand M, Guerardel Y, Castelain M et al (2013) Unraveling the role of surface mucus-binding protein and pili in muco-adhesion of Lactococcus lactis. PLoS ONE 8:e79850

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Egelman EH, Craig L (2012) Structure of the Vibrio cholerae type IVb Pilus and stability comparison with the Neisseria gonorrhoeae type IVa pilus. J Mol Biol 418:47–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin FY, Weisman LE, Azimi PH, Philips JB III, Clark P, Regan J et al (2004) Level of maternal IgG anti-group B streptococcus type III antibody correlated with protection of neonates against early-onset disease caused by this pathogen. J Infect Dis 190:928–934

    Article  CAS  PubMed  Google Scholar 

  • Linke C, Young PG, Kang HJ, Bunker RD, Middleditch MJ, Caradoc-Davies TT et al (2010) Crystal structure of the minor pilin FctB reveals determinants of Group A streptococcal pilus anchoring. J Biol Chem 285:20381–20389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linke-Winnebeck C, Paterson NG, Young PG, Middleditch MJ, Greenwood DR, Witte G, Baker EN (2014) Structural model for covalent adhesion of the Streptococcus pyogenes pilus through a thioester bond. J Biol Chem 289:177–189

    Article  CAS  PubMed  Google Scholar 

  • Luo BH, Takagi J, Springer TA (2004) Locking the beta3 integrin I-like domain into high and low affinity conformations with disulfides. J Biol Chem 279:10215–10221

    Article  CAS  PubMed  Google Scholar 

  • Maione D, Margarit I, Rinaudo CD, Masignani V, Mora M, Scarselli M et al (2005) Identification of a universal group B streptococcus vaccine by multiple genome screen. Science 309:148–150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manetti AGO, Zingaretti C, Falugi F, Capo S, Bombaci M, Bagnoli F et al (2007) Streptococcus pyogenes pili promote pharyngeal cell adhesion and biofilm formation. Mol Microbiol 64:968–983

    Article  CAS  PubMed  Google Scholar 

  • Manzano C, Izore T, Job V, Di Guilmi AM, Dessen AA, Izoré T (2009) Sortase activity is controlled by a flexible lid in the pilus biogenesis mechanism of gram-positive pathogens. Biochemistry 48:10549–10557

    Google Scholar 

  • Margarit I, Rinaudo CD, Galeotti CL, Maione D, Ghezzo C, Buttazzoni E et al (2009) Preventing bacterial infections with pilus-based vaccines: the group B streptococcus paradigm. J Infect Dis 199:108–115

    Article  PubMed  Google Scholar 

  • Marraffini LA, Schneewind O (2006) Targeting proteins to the cell wall of sporulating Bacillus anthracis. Mol Microbiol 62:1402–1417

    Article  CAS  PubMed  Google Scholar 

  • Marraffini LA, Schneewind O (2007) Sortase C-mediated anchoring of BasI to the cell wall envelope of Bacillus anthracis. J Bacteriol 189:6425–6436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, Jelenska J et al (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299:906–909

    Article  CAS  PubMed  Google Scholar 

  • Meyrand M, Guillot A, Goin M, Furlan S, Armalyte J, Kulakauskas S et al (2013) Surface proteome analysis of a natural isolate of Lactococcus lactis reveals the presence of pili able to bind human intestinal epithelial cells. Mol Cell Proteomics 12:3935–3947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mora M, Bensi G, Capo S, Falugi F, Zingaretti C, Manetti AG et al (2005) Group A Streptococcus produce pilus-like structures containing protective antigens and Lancefield T antigens. Proc Natl Acad Sci USA 102:15641–15646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moschioni M, Donati C, Muzzi A, Masignani V, Censini S, Hanage WP et al (2008) Streptococcus pneumoniae contains 3 rlrA pilus variants that are clonally related. J Infect Dis 197:888–896

    Article  CAS  PubMed  Google Scholar 

  • Moschioni M, De Angelis G, Harfouche C, Bizzarri E, Filippini S, Mori E et al (2012) Immunization with the RrgB321 fusion protein protects mice against both high and low pilus-expressing Streptococcus pneumoniae populations. Vaccine 30:1349–1356

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Necchi F, Nardi-Dei V, Biagini M, Assfalg M, Nuccitelli A, Cozzi R et al (2011) Sortase a substrate specificity in GBS pilus 2a cell wall anchoring. PLoS ONE 6:e25300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neiers F, Madhurantakam C, Fälker S, Manzano C, Dessen A, Normark S et al (2009) Two crystal structures of pneumococcal pilus sortase C provide novel insights into catalysis and substrate specificity. J Mol Biol 393:704–716

    Article  CAS  PubMed  Google Scholar 

  • Nelson AL, Ries J, Bagnoli F, Dahlberg S, Fälker S, Rounioja S et al (2007) RrgA is a pilus-associated adhesin in Streptococcus pneumoniae. Mol Microbiol 66:329–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nielsen HV, Guiton PS, Kline KA, Port GC, Pinkner JS, Neiers F et al (2012) The metal ion-dependent adhesion site motif of the Enterococcus faecalis EbpA pilin mediates pilus function in catheter-associated urinary tract infection. MBio 3:e00177–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nielsen HV, Flores-Mireles AL, Kau AL, Kline K, Pinkner JS, Neiers F et al (2013) Pilin and sortase residues critical for endocarditis-and biofilm-associated pilus biogenesis in Enterococcus faecalis. J Bacteriol 195:4484–4495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nuccitelli A, Cozzi R, Gourlay LJ, Donnarumma D, Necchi F, Norais N et al (2011) Structure-based approach to rationally design a chimeric protein for an effective vaccine against group B Streptococcus infections. Proc Natl Acad Sci USA 108:10278–10283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orrskog S, Rounioja S, Spadafina T, Gallotta M, Norman M, Hentrich K et al (2012) Pilus adhesin RrgA interacts with complement receptor 3, thereby affecting macrophage function and systemic pneumococcal disease. MBio 4:e00535–12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oxaran V, Ledue-Clier F, Dieye Y, Herry JM, Pechoux C, Meylheuc T et al (2012) Pilus biogenesis in Lactococcus lactis: molecular characterization and role in aggregation and biofilm formation. PLoS ONE 7:e50989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pancotto L, De AG, Bizzarri E, Barocchi MA, Del GG, Moschioni M, Ruggiero P (2013) Expression of the Streptococcus pneumoniae pilus-1 undergoes on and off switching during colonization in mice. Sci Rep 3:2040

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Piatek R, Bruzdziak P, Wojciechowski M, Zalewska-Piatek B, Kur J (2010) The noncanonical disulfide bond as the important stabilizing element of the immunoglobulin fold of the Dr fimbrial DraE subunit. Biochemistry 49:1460–1468

    Article  CAS  PubMed  Google Scholar 

  • Pointon JA, Smith WD, Saalbach G, Crow A, Kehoe MA, Banfield MJ (2010) A highly unusual thioester bond in a pilus adhesin is required for efficient host cell interaction. J Biol Chem 285:33858–33866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quigley BR, Zähner D, Hatkoff M, Thanassi DG, Scott JR, Zähner D (2009) Linkage of T3 and Cpa pilins in the Streptococcus pyogenes M3 pilus. Mol Microbiol 72:1379–1394

    Article  CAS  PubMed  Google Scholar 

  • Quigley BR, Hatkoff M, Thanassi DG, Ouattara M, Eichenbaum Z, Scott JR (2010) A foreign protein incorporated on the Tip of T3 pili in Lactococcus lactis elicits systemic and mucosal immunity. Infect Immun 78:1294–1303

    Article  CAS  PubMed  Google Scholar 

  • Reunanen J, von Ossowski I, Hendrickx AP, Palva A, de Vos WM (2012) Characterization of the SpaCBA pilus fibers in the probiotic Lactobacillus rhamnosus GG. Appl Environ Microbiol 78:2337–2344

    Google Scholar 

  • Rintahaka J, Yu X, Kant R, Palva A, von Ossowski I (2014) Phenotypical analysis of the Lactobacillus rhamnosus GG fimbrial spaFED operon: surface expression and functional characterization of recombinant SpaFED pili in Lactococcus lactis. PLoS ONE 9:e113922

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rosini R, Margarit I (2015) Biofilm formation by Streptococcus agalactiae: influence of environmental conditions and implicated virulence factors. Front Cell Infect Microbiol 5:6

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosini R, Rinaudo CD, Soriani M, Lauer P, Mora M, Maione D et al (2006) Identification of novel genomic islands coding for antigenic pilus-like structures in Streptococcus agalactiae. Mol Microbiol 61:126–141

    Article  CAS  PubMed  Google Scholar 

  • Schneewind O, Missiakas D (2014) Sec-secretion and sortase-mediated anchoring of proteins in gram-positive bacteria. Biochim Biophys Acta 1843:1687–1697

    Article  CAS  PubMed  Google Scholar 

  • Schuchat A (1998) Epidemiology of group B streptococcal disease in the United States: shifting paradigms. Clin Microbiol Rev 11:497–513

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shaik MM, Maccagni A, Tourcier G, Di Guilmi AM, Dessen AA (2014) Structural basis of pilus anchoring by the ancillary pilin RrgC of Streptococcus pneumoniae. J Biol Chem 289:16988–16997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sillanpää J, Chang C, Singh KV, Montealegre MC, Nallapareddy SR, Harvey BR et al (2013) Contribution of individual Ebp Pilus subunits of Enterococcus faecalis OG1RF to pilus biogenesis, biofilm formation and urinary tract infection. PLoS ONE 8:e68813

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smeesters PR, McMillan DJ, Sriprakash KS (2010) The streptococcal M protein: a highly versatile molecule. Trends Microbiol 18:275–282

    Article  CAS  PubMed  Google Scholar 

  • Smith WD, Pointon J, Abbot E, Kang HJ, Baker EN, Hirst BH et al (2010) Roles of minor pilin subunits Spy0125 and Spy0130 in the serotype M1 Streptococcus pyogenes strain SF370. J Bacteriol 192:4651–4659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solovyova AS, Pointon JA, Race PR, Smith WD, Kehoe MA, Banfield MJ (2010) Solution structure of the major (Spy0128) and minor (Spy0125 and Spy0130) pili subunits from Streptococcus pyogenes. Eur Biophys J EBJ 39:469–480

    Article  CAS  PubMed  Google Scholar 

  • Soriani M, Telford JL (2010) Relevance of pili in pathogenic streptococci pathogenesis and vaccine development. Future Microbiol 5:735–747

    Article  CAS  PubMed  Google Scholar 

  • Spirig T, Weiner EM, Clubb RT (2011) Sortase enzymes in gram-positive bacteria. Mol Microbiol 82:1044–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spraggon G, Koesema E, Scarselli M, Malito E, Biagini M, Norais N et al (2010) Supramolecular organization of the repetitive backbone unit of the Streptococcus pneumoniae pilus. PLoS ONE 5:e10919

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thanassi DG, Bliska JB, Christie PJ (2012) Surface organelles assembled by secretion systems of gram-negative bacteria: diversity in structure and function. FEMS Microbiol Rev 36:1046–1082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ton-That H, Mazmanian SK, Alksne L, Schneewind O (2002) Anchoring of surface proteins to the cell wall of Staphylococcus aureus. Cysteine 184 and histidine 120 of sortase form a thiolate-imidazolium ion pair for catalysis. J Biol Chem 277:7447–7452

    Article  CAS  PubMed  Google Scholar 

  • Ton-That H, Marraffini LA, Schneewind O (2004) Sortases and pilin elements involved in pilus assembly of Corynebacterium diphtheriae. Mol Microbiol 53:251–261

    Article  CAS  PubMed  Google Scholar 

  • Tripathi P, Beaussart A, Alsteens D, Dupres V, Claes I, von Ossowski I et al (2013) Adhesion and nanomechanics of pili from the probiotic Lactobacillus rhamnosus GG. ACS nano 7:3685–3697

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • von Ossowski I, Reunanen J, Satokari R, Vesterlund S, Kankainen M, Huhtinen H et al (2010) Mucosal adhesion properties of the probiotic Lactobacillus rhamnosus GG SpaCBA and SpaFED pilin subunits. Appl Environ Microbiol 76:2049–2057

    Article  CAS  Google Scholar 

  • von Ossowski I, Pietila TE, Rintahaka J, Nummenmaa E, Makinen VM, Reunanen J et al (2013) Using recombinant Lactococci as an approach to dissect the immunomodulating capacity of surface piliation in probiotic Lactobacillus rhamnosus GG. PloS one 8:e64416

    Article  CAS  Google Scholar 

  • Walden M, Crow A, Nelson MD, Banfield MJ (2014) Intramolecular isopeptide but not internal thioester bonds confer proteolytic and significant thermal stability to the S. pyogenes pilus adhesin Spy0125. Proteins 82:517–527

    Article  CAS  PubMed  Google Scholar 

  • Yanagawa R, Otsuki K (1970) Some properties of the pili of Corynebacterium renale. J Bacteriol 101:1063–1069

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Zähner D, Scott JR (2008) SipA is required for pilus formation in Streptococcus pyogenes serotype M3. J Bacteriol 190:527–535

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Liu JH, Yang W, Springer T, Shimaoka M, Wang JH (2009) Structural basis of activation-dependent binding of ligand-mimetic antibody AL-57 to integrin LFA-1. Proc Natl Acad Sci USA 106:18345–18350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors are grateful to Markus Hilleringmann for critical reading of the manuscript and numerous highly appreciated suggestions.

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Correspondence to Werner Pansegrau .

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Pansegrau, W., Bagnoli, F. (2015). Pilus Assembly in Gram-Positive Bacteria. In: Bagnoli, F., Rappuoli, R. (eds) Protein and Sugar Export and Assembly in Gram-positive Bacteria . Current Topics in Microbiology and Immunology, vol 404. Springer, Cham. https://doi.org/10.1007/82_2015_5016

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