Skip to main content
SpringerLink
Log in

Protein Folding in Bacterial Adhesion: Secretion and Folding of Classical Monomeric Autotransporters

  • Chapter
  • First Online:
Bacterial Adhesion

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

Abstract

Bacterial adhesins mediate the attachment of bacteria to their niches, such as the tissue of an infected host. Adhesins have to be transported across the cell envelope to become active and during this secretion process they fold into their final conformation. This chapter focuses on the biogenesis of the classical monomeric autotransporter proteins, which are the most ubiquitous class of secreted proteins in Gram-negative bacteria. They may function as adhesins, but other functions are also known. Autotransporter proteins have a modular structure and consist of an N-terminal signal peptide and a C-terminal translocator domain with in between the secreted passenger domain that harbours the functions. The signal peptide directs the transport across the inner membrane to the periplasm via the Sec machinery. The translocator domain inserts into the outer membrane and facilitates the transport of the passenger to the cell surface. In this chapter, I will review our current knowledge of the secretion of classical monomeric autotransporters and the methods that have been used to assess their folding during the translocation, both in vitro and in vivo.

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

  • Barnard TJ, Dautin N, Lukacik P, Bernstein HD, Buchanan SK (2007) Autotransporter structure reveals intra-barrel cleavage followed by conformational changes. Nat Struct Mol Biol 14:1214–1220

    Article  PubMed  CAS  Google Scholar 

  • Benz I, Schmidt MA (1992) Isolation and serologic characterization of AIDA-I, the adhesin mediating the diffuse adherence phenotype of the diarrhea-associated Escherichia coli strain 2787, O126-H27. Infect Immun 60:13–18

    PubMed  CAS  Google Scholar 

  • Benz I, Schmidt MA (2001) Glycosylation with heptose residues mediated by the aah gene product is essential for adherence of the AIDA-I adhesin. Mol Microbiol 40:1403–1413

    Article  PubMed  CAS  Google Scholar 

  • Bos MP, Robert V, Tommassen J (2007) Biogenesis of the Gram-negative bacterial outer membrane. Annu Rev Microbiol 61:191–214

    Article  PubMed  CAS  Google Scholar 

  • Brandon LD, Goldberg MB (2001) Periplasmic transit and disulfide bond formation of the autotransported Shigella protein IcsA. J Bacteriol 183:951–958

    Article  PubMed  CAS  Google Scholar 

  • Brandon LD, Goehring N, Janakiraman A, Yan AW, Wu T, Beckwith J, Goldberg MB (2003) IcsA, a polarly localized autotransporter with an atypical signal peptide, uses the sec apparatus for secretion, although the sec apparatus is circumferentially distributed. Mol Microbiol 50:45–60

    Article  PubMed  CAS  Google Scholar 

  • Buchanan SK (1999) β-barrel proteins from bacterial outer membranes: structure, function and refolding. Curr Opin Struct Biol 9:455–461

    Article  PubMed  CAS  Google Scholar 

  • Burgess NK, Dao TP, Stanley AM, Fleming KG (2008) β-barrel proteins that reside in the Escherichia coli outer membrane in vivo demonstrate varied folding behavior in vitro. J Biol Chem 283:26748–26758

    Article  PubMed  CAS  Google Scholar 

  • Charbonneau ME, Berthiaume F, Mourez M (2006) Proteolytic processing is not essential for multiple functions of the Escherichia coli autotransporter adhesin involved in diffuse adherence, AIDA-I. J Bacteriol 188:8504–8512

    Article  PubMed  CAS  Google Scholar 

  • Charbonneau ME, Janvore J, Mourez M (2009) Autoprocessing of the Escherichia coli AIDA-I autotransporter a new mechanism involving acidic residues in the junction region. J Biol Chem 284:17340–17351

    Article  PubMed  CAS  Google Scholar 

  • Charbonneau ME, Mourez M (2008) The Escherichia coli AIDA-I autotransporter undergoes cytoplasmic glycosylation independently of export. Res Microbiol 159:537–544

    Article  PubMed  CAS  Google Scholar 

  • Coutte L, Alonso S, Reveneau N, Willery E, Quatannens B, Locht C, Jacob-Dubisson F (2003) Role of adhesin release for mucosal colonization by a bacterial pathogen. J Exp Med 197:735–742

    Article  PubMed  CAS  Google Scholar 

  • de Jonge MI, Bos MP, Hamstra HJ, Jiskoot W, van Ulsen P, Tommassen J, van Alphen L, van der Ley P (2002) Conformational analysis of opacity proteins from Neisseria meningitidis. Eur J Biochem 269:5215–5223

    Article  PubMed  Google Scholar 

  • Dé E, Saint N, Glinel K, Meli AC, Lévy D, Jacob-Dubuisson F (2008) Influence of the passenger domain of a model autotransporter on the properties of its translocator domain. Mol Membr Biol 25:192–U14

    Article  PubMed  Google Scholar 

  • Desvaux M, Cooper LM, Filenko NA, Scott-Tucker A, Turner SM, Cole JA, Henderson IR (2006) The unusual extended signal peptide region of the type V secretion system is phylogenetically restricted. FEMS Microbiol Lett 264:22–30

    Article  PubMed  CAS  Google Scholar 

  • Edwards JA, Groathouse NA, Boitano S (2005) Bordetella bronchiseptica adherence to cilia is mediated by multiple adhesin factors and blocked by surfactant protein A. Infect Immun 73:3618–3626

    Article  PubMed  CAS  Google Scholar 

  • Emsley P, Charles IG, Fairweather NF, Isaacs NW (1996) Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 381:90–92

    Article  PubMed  CAS  Google Scholar 

  • Eslava C, Navarro-Garcia F, Czeczulin JR, Henderson IR, Cravioto A, Nataro JP (1998) Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect Immun 66:3155–3163

    PubMed  CAS  Google Scholar 

  • Fexby S, Bjarnsholt T, Jensen PO, Roos V, Høiby N, Givskov M, Klemm P (2007) Biological trojan horse: antigen 43 provides specific bacterial uptake and survival in human neutrophils. Infect Immun 75:30–34

    Article  PubMed  CAS  Google Scholar 

  • Fink DL, Cope LD, Hansen EJ, St. Geme JW III (2001) The Hemophilus influenzae Hap autotransporter is a chymotrypsin clan serine protease and undergoes autoproteolysis via an intermolecular mechanism. J Biol Chem 276:39492–39500

    Article  PubMed  CAS  Google Scholar 

  • Fink DL, Green BA, St Geme JW III (2002) The Haemophilus influenzae Hap autotransporter binds to fibronectin, laminin, and collagen IV. Infect Immun 70:4902–4907

    Article  PubMed  CAS  Google Scholar 

  • Fukuda I, Suzuki T, Munakata H, Hayashi N, Katayama E, Yoshikawa M, Sasakawa C (1995) Cleavage of Shigella surface protein VirG occurs at a specific site, but the secretion is not essential for intracellular spreading. J Bacteriol 177:1719–1726

    PubMed  CAS  Google Scholar 

  • Gangwer KA, Mushrush DJ, Stauff DL, Spiller B, McClain MS, Cover TL, Lacy DB (2007) Crystal structure of the Helicobacter pylori vacuolating toxin p55 domain. Proc Natl Acad Sci USA 104:16293–16298

    Article  PubMed  CAS  Google Scholar 

  • Hauck CR, Meyer TF (1997) The lysosomal/phagosomal membrane protein h-Lamp-1 is a target of the IgA1 protease of Neisseria gonorrhoeae. FEBS Lett 405:86–90

    Article  PubMed  CAS  Google Scholar 

  • Henderson IR, Czeczulin J, Eslava C, Noriega F, Nataro JP (1999) Characterization of pic, a secreted protease of shigella flexneri and enteroaggregative Escherichia coli. Infect Immun 67:5587–5596

    PubMed  CAS  Google Scholar 

  • Henderson IR, Navarro-Garcia F, Nataro JP (1998) The great escape: structure and function of the autotransporter proteins. Trends Microbiol 6:370–378

    Article  PubMed  CAS  Google Scholar 

  • Hendrixson DR, St Geme IIIJW (1998) The Haemophilus influenzae Hap serine protease promotes adherence and microcolony formation, potentiated by a soluble host protein. Mol Cell 2:841–850

    Article  PubMed  CAS  Google Scholar 

  • Hritonenko V, Kostakioti M, Stathopoulos C (2006) Quaternary structure of a SPATE autotransporter protein. Mol Membr Biol 23:466–474

    Article  PubMed  CAS  Google Scholar 

  • Ieva R, Bernstein HD (2009) Interaction of an autotransporter passenger domain with bama during its translocation across the bacterial outer membrane. Proc Natl Acad Sci USA 106:19120–19125

    Article  PubMed  CAS  Google Scholar 

  • Ieva R, Skillman KM, Bernstein HD (2008) Incorporation of a polypeptide segment into the β-domain pore during the assembly of a bacterial autotransporter. Mol Microbiol 67:188–201

    Article  PubMed  CAS  Google Scholar 

  • Jacob-Dubuisson F, Fernandez R, Coutte L (2004) Protein secretion through autotransporter and two-partner pathways. Biochim Biophys Acta 1694:235–257

    Article  PubMed  CAS  Google Scholar 

  • Jain S, Goldberg MB (2007) Requirement for yaet in the outer membrane assembly of autotransporter proteins. J Bacteriol 189:5393–5398

    Article  PubMed  CAS  Google Scholar 

  • Johnson TA, Qiu JZ, Plaut AG, Holyoak T (2009) Active-site gating regulates substrate selectivity in a chymotrypsin-like serine protease: the structure of Haemophilus influenzae Immunoglobulin A1 protease. J Mol Biol 389:559–574

    Article  PubMed  CAS  Google Scholar 

  • Jong WSP, Luirink J (2008) The conserved extension of the Hbp autotransporter signal peptide does not determine targeting pathway specificity. Biochem Biophys Res Comm 368:522–527

    Article  PubMed  CAS  Google Scholar 

  • Jong WSP, ten Hagen-Jongman CM, den Blaauwen T, Slotboom DJ, Tame JRH, Wickström D, de Gier JW, Otto BR, Luirink J (2007) Limited tolerance towards folded elements during secretion of the autotransporter Hbp. Mol Microbiol 63:1524–1536

    Article  PubMed  CAS  Google Scholar 

  • Junker M, Besingi RN, Clark PL (2009) Vectorial transport and folding of an autotransporter virulence protein during outer membrane secretion. Mol Microbiol 71:1323–1332

    Article  PubMed  CAS  Google Scholar 

  • Junker M, Clark PL (2010) Slow formation of aggregation-resistant β-sheet folding intermediates. Proteins 78:812–824

    Article  PubMed  CAS  Google Scholar 

  • Junker M, Schuster CC, McDonnell AV, Sorg KA, Finn MC, Berger B, Clark PL (2006) Pertactin β-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc Natl Acad Sci USA 103:4918–4923

    Article  PubMed  CAS  Google Scholar 

  • Kajava AV, Steven AC (2006) The turn of the screw: variations of the abundant β-solenoid motif in passenger domains of type V secretory proteins. J Struct Biol 155:306–315

    Article  PubMed  CAS  Google Scholar 

  • Khalid S, Sansom MSP (2006) Molecular dynamics simulations of a bacterial autotransporter: NalP from Neisseria meningitidis. Mol Membr Biol 23:499–508

    Article  PubMed  CAS  Google Scholar 

  • Klauser T, Pohlner J, Meyer TF (1990) Extracellular transport of cholera-toxin B-subunit using Neisseria IgA protease β-domain – conformation-dependent outer-membrane translocation. EMBO J 9:1991–1999

    PubMed  CAS  Google Scholar 

  • Klemm P, Hjerrild L, Gjermansen M, Schembri MA (2004) Structure-function analysis of the self-recognizing antigen 43 autotransporter protein from Escherichia coli. Mol Microbiol 51:283–296

    Article  PubMed  CAS  Google Scholar 

  • Konieczny MPJ, Benz I, Hollinderbäumer B, Beinke C, Niederweis M, Schmidt MA (2001) Modular organization of the AIDA autotransporter translocator: the N-terminal β(1)-domain is surface-exposed and stabilizes the transmembrane β(2)-domain. Antonie Van Leeuwenhoek 80:19–34

    Article  PubMed  CAS  Google Scholar 

  • Kostakioti M, Stathopoulos C (2006) Role of the α-helical linker of the C-terminal translocator in the biogenesis of the serine protease subfamily of autotransporters. Infect Immun 74:4961–4969

    Article  PubMed  CAS  Google Scholar 

  • Leininger E, Roberts M, Kenimer JG, Charles IG, Fairweather N, Novotny P, Brennan MJ (1991) Pertactin, an arg-gly-asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc Natl Acad Sci USA 88:345–349

    Article  PubMed  CAS  Google Scholar 

  • Lin L, Ayala P, Larson J, Mulks M, Fukuda M, Carlsson SR, Enns C, So M (1997) The Neisseria type-2 IgA1 protease cleaves lamp1 and promotes survival of bacteria within epithelial cells. Mol Microbiol 24:1083–1094

    Article  PubMed  CAS  Google Scholar 

  • Lindenthal C, Elsinghorst EA (2001) Enterotoxigenic Escherichia coli TibA glycoprotein adheres to human intestine epithelial cells. Infect Immun 69:52–57

    Article  PubMed  CAS  Google Scholar 

  • Lipski SL, Akimana C, Timpe JM, Wooten RM, Lafontaine ER (2007) The Moraxella catarrhalis autotransporter McaP is a conserved surface protein that mediates adherence to human epithelial cells through its N-terminal passenger domain. Infect Immun 75:314–324

    Article  PubMed  CAS  Google Scholar 

  • Loveless BJ, Saier MH (1997) A novel family of channel-forming, autotransporting, bacterial virulence factors. Mol Membr Biol 14:113–123

    Article  PubMed  CAS  Google Scholar 

  • Meng GY, Surana NK, St Geme IIIJW, Waksman G (2006) Structure of the outer membrane translocator domain of the Haemophilus influenzae Hia trimeric autotransporter. EMBO J 25:2297–2304

    Article  PubMed  CAS  Google Scholar 

  • Ohnishi Y, Nishiyama M, Horinouchi S, Beppu T (1994) Involvement of the COOH-terminal pro-sequence of Serratia marcescens serine-protease in the folding of the mature enzyme. J Biol Chem 269:32800–32806

    PubMed  CAS  Google Scholar 

  • Oliver DC, Huang G, Nodel E, Pleasance S, Fernandez RC (2003) A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol Microbiol 47:1367–1383

    Article  PubMed  CAS  Google Scholar 

  • Oomen CJ, van Ulsen P, Van Gelder P, Feijen M, Tommassen J, Gros P (2004) Structure of the translocator domain of a bacterial autotransporter. EMBO J 23:1257–1266

    Article  PubMed  CAS  Google Scholar 

  • Otto BR, Sijbrandi R, Luirink J, Oudega B, Heddle JG, Mizutani K, Park SY, Tame JRH (2005) Crystal structure of hemoglobin protease, a heme binding autotransporter protein from pathogenic Escherichia coli. J Biol Chem 280:17339–17345

    Article  PubMed  CAS  Google Scholar 

  • Peterson JH, Szabady RL, Bernstein HD (2006) An unusual signal peptide extension inhibits the binding of bacterial presecretory proteins to the signal recognition particle, trigger factor, and the SecYEG complex. J Biol Chem 281:9038–9048

    Article  PubMed  CAS  Google Scholar 

  • Plaut AG, Gilbert JV, Artenstein MS, Capra JD (1975) Neisseria gonorrhoeae and Neisseria meningitidis extracellular enzyme cleaves human Immunoglobulin A. Science 190:1103–1105

    Article  PubMed  CAS  Google Scholar 

  • Pohlner J, Halter R, Beyreuther K, Meyer TF (1987) Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325:458–462

    Article  PubMed  CAS  Google Scholar 

  • Purdy GE, Fisher CR, Payne SM (2007) Icsa surface presentation in Shigella flexneri requires the periplasmic chaperones DegP, Skp, and SurA. J Bacteriol 189:5566–5573

    Article  PubMed  CAS  Google Scholar 

  • Qu J, Mayer C, Behrens S, Holst O, Kleinschmidt JH (2007) The trimeric periplasmic chaperone Skp of Escherichia coli forms 1:1 complexes with outer membrane proteins via hydrophobic and electrostatic interactions. J Mol Biol 374:91–105

    Article  PubMed  CAS  Google Scholar 

  • Renn JP, Clark PL (2008) A conserved stable core structure in the passenger domain α-helix of autotransporter virulence proteins. Biopolymers 89:420–427

    Article  PubMed  CAS  Google Scholar 

  • Roussel-Jazédé V, Van Gelder P, Sijbrandi R, Rutten L, Otto BR, Luirink J, Gros P, Tommassen J, van Ulsen P (2011) Channel properties of the translocator domain of the autotransporter Hbp of Escherichia coli. Mol Membr Biol in press, doi:10.3109/09687688.2010.550328, appeared online 14 Feb 2011

    Google Scholar 

  • Ruiz-Pérez F, Henderson IR, Leyton DL, Rossiter AE, Zhang YH, Nataro JP (2009) Roles of periplasmic chaperone proteins in the biogenesis of serine protease autotransporters of Enterobacteriaceae. J Bacteriol 191:6571–6583

    Article  PubMed  Google Scholar 

  • Salacha R, Kovačić F, Brochier-Armanet C, Wilhelm S, Tommassen J, Filloux A, Voulhoux R, Bleves S (2010) The Pseudomonas aeruginosa patatin-like protein PlpD is the archetype of a novel type V secretion system. Environ Microbiol 12:1498–1512

    PubMed  CAS  Google Scholar 

  • Sauri A, Soprova Z, Wickström D, de Gier JW, Van der Schors RC, Smit AB, Jong WSP, Luirink J (2009) The Bam, Omp85, complex is involved in secretion of the autotransporter haemoglobin protease. Microbiology 155:3982–3991

    Article  PubMed  CAS  Google Scholar 

  • Serruto D, Adu-Bobie J, Scarselli M, Veggi D, Pizza M, Rappuoli R, Aricò B (2003) Neisseria meningitidis App, a new adhesin with autocatalytic serine protease activity. Mol Microbiol 48:323–334

    Article  PubMed  CAS  Google Scholar 

  • Sherlock O, Schembri MA, Reisner A, Klemm P (2004) Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: cell aggregation and biofilm formation. J Bacteriol 186:8058–8065

    Article  PubMed  CAS  Google Scholar 

  • Sijbrandi R, Urbanus ML, ten Hagen-Jongman CM, Bernstein HD, Oudega B, Otto BR, Luirink J (2003) Signal recognition particle (SRP)-mediated targeting and sec-dependent translocation of an extracellular Escherichia coli protein. J Biol Chem 278:4654–4659

    Article  PubMed  CAS  Google Scholar 

  • Skillman KM, Barnard TJ, Peterson JH, Ghirlando R, Bernstein HD (2005) Efficient secretion of a folded protein domain by a monomeric bacterial autotransporter. Mol Microbiol 58:945–958

    Article  PubMed  CAS  Google Scholar 

  • Sklar JG, Wu T, Kahne D, Silhavy TJ (2007) Defining the roles of the periplasmic chaperones SurA, Skp and DegP in Escherichia coli. Genes Dev 21:2473–2484

    Article  PubMed  CAS  Google Scholar 

  • Stathopoulos C, Provence DL, Curtiss R (1999) Characterization of the avian pathogenic Escherichia coli hemagglutinin Tsh, a member of the immunoglobulin A protease-type family of autotransporters. Infect Immun 67:772–781

    PubMed  CAS  Google Scholar 

  • Szabady RL, Peterson JH, Skillman KM, Bernstein HD (2005) An unusual signal peptide facilitates late steps in the biogenesis of a bacterial autotransporter. Proc Natl Acad Sci USA 102:221–226

    Article  PubMed  CAS  Google Scholar 

  • Tajima N, Kawai F, Park SY, Tame JRH (2010) A novel Intein-like autoproteolytic mechanism in autotransporter proteins. J Mol Biol 402:645–656

    Google Scholar 

  • Turner DPJ, Marietou AG, Johnston L, Ho KKL, Rogers AJ, Wooldridge KG, Ala’Aldeen DAA (2006) Characterization of MspA, an immunogenic autotransporter protein that mediates adhesion to epithelial and endothelial cells in Neisseria meningitidis. Infect Immun 74:2957–2964

    Article  PubMed  CAS  Google Scholar 

  • van den Berg B (2010) Crystal structure of a full-length autotransporter. J Mol Biol 396:627–633

    Article  PubMed  Google Scholar 

  • Van Gelder P, Dumas F, Winterhalter M (2000) Understanding the function of bacterial outer membrane channels by reconstitution into black lipid membranes. Biophys Chem 85:153–167

    Article  PubMed  Google Scholar 

  • van Ulsen P, Adler B, Fassler P, Gilbert M, van Schilfgaarde M, van der Ley P, van Alphen L, Tommassen J (2006a) A novel phase-variable autotransporter serine protease, AusI, of Neisseria meningitidis. Microbes Infect 8:2088–2097

    Article  PubMed  Google Scholar 

  • van Ulsen P, Gros P, Tommassen J (2006b) Structure and function of the translocator domain of bacterial autotransporters. In: Grisshammer R, Buchannan SK (eds) Structural biology of membrane proteins. Royal Society of Chemistry, Cambridge, pp 270–287

    Google Scholar 

  • van Ulsen P, Rutten L, Feller M, Tommassen J, van der Ende A (2008) Two-partner secretion systems of Neisseria meningitidis associated with invasive clonal complexes. Infect Immun 76:4649–4658

    Article  PubMed  Google Scholar 

  • van Ulsen P, van Alphen L, Hopman CTP, van der Ende A, Tommassen J (2001) In vivo expression of Neisseria meningitidis proteins homologous to the Haemophilus influenzae Hap and Hia autotransporters. FEMS Immunol Med Microbiol 32:53–64

    Article  PubMed  Google Scholar 

  • van Ulsen P, van Alphen L, ten Hove J, Fransen F, van der Ley P, Tommassen J (2003) A neisserial autotransporter NalP modulating the processing of other autotransporters. Mol Microbiol 50:1017–1030

    Article  PubMed  Google Scholar 

  • Veiga E, de Lorenzo V, Fernández LA (2004) Structural tolerance of bacterial autotransporters for folded passenger protein domains. Mol Microbiol 52:1069–1080

    Article  PubMed  CAS  Google Scholar 

  • Velarde JJ, Nataro JP (2004) Hydrophobic residues of the autotransporter EspP linker domain are important for outer membrane translocation of its passenger. J Biol Chem 279:31495–31504

    Article  PubMed  CAS  Google Scholar 

  • Virji M (2009) Pathogenic Neisseriae: surface modulation, pathogenesis and infection control. Nat Rev Microbiol 7:274–286

    Article  PubMed  CAS  Google Scholar 

  • Voulhoux R, Bos MP, Geurtsen J, Mols M, Tommassen J (2003) Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299:262–265

    Article  PubMed  CAS  Google Scholar 

  • Wagner JK, Heindl JE, Gray AN, Jain S, Goldberg MB (2009) Contribution of the periplasmic chaperone Skp to efficient presentation of the autotransporter icsa on the surface of Shigella flexneri. J Bacteriol 191:815–821

    Article  PubMed  CAS  Google Scholar 

  • Wilhelm S, Tommassen J, Jaeger KE (1999) A novel lipolytic enzyme located in the outer membrane of Pseudomonas aeruginosa. J Bacteriol 181:6977–6986

    PubMed  CAS  Google Scholar 

  • Zhang X, Rashid R, Wang K, Shan SO (2010) Sequential checkpoints govern substrate selection during cotranslational protein targeting. Science 328:757–760

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Section Molecular Microbiology, Department of Molecular Cell Biology, VU University Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands

    Peter van Ulsen

Authors
  1. Peter van Ulsen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter van Ulsen .

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

van Ulsen, P. (2011). Protein Folding in Bacterial Adhesion: Secretion and Folding of Classical Monomeric Autotransporters. 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_8

Download citation

Publish with us

Policies and ethics

Search

Navigation