We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Skip to main content
SpringerLink
Log in

Physical properties of the specific PapG–galabiose binding in E. coli P pili-mediated adhesion

  • Original Paper
  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

Detailed analyses of the mechanisms that mediate binding of the uropathogenic Escherichia coli to host cells are essential, as attachment is a prerequisite for the subsequent infection process. We explore, by means of force measuring optical tweezers, the interaction between the galabiose receptor and the adhesin PapG expressed by P pili on single bacterial cells. Two variants of dynamic force spectroscopy were applied based on constant and non-linear loading force. The specific PapG–galabiose binding showed typical slip-bond behaviour in the force interval (30–100 pN) set by the pilus intrinsic biomechanical properties. Moreover, it was found that the bond has a thermodynamic off-rate and a bond length of 2.6 × 10−3 s−1 and 5.0 Å, respectively. Consequently, the PapG–galabiose complex is significantly stronger than the internal bonds in the P pilus structure that stabilizes the helical chain-like macromolecule. This finding suggests that the specific binding is strong enough to enable the P pili rod to unfold when subjected to strong shear forces in the urinary tract. The unfolding process of the P pili rod promotes the formation of strong multipili interaction, which is important for the bacterium to maintain attachment to the host cells.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

UPEC:

Uropathogenic Escherichia coli

UTI:

Urinary tract infection

FMOT:

Force measuring optical tweezers

AFM:

Atomic force microscopy

DFS:

Dynamic force spectroscopy

MSE:

Mean square error

References

  • Andersson M, Fällman E, Uhlin BE, Axner O (2006a) Dynamic force spectroscopy of the unfolding of P pili. Biophys J 91:2717–2725. doi:10.1529/biophysj.106.087429

    Article  PubMed  CAS  Google Scholar 

  • Andersson M, Fällman E, Uhlin BE, Axner O (2006b) Force measuring optical tweezers system for long time measurements of Pili stability. SPIE 6088:286–295

    Google Scholar 

  • Andersson M, Fällman E, Uhlin BE, Axner O (2006c) A sticky chain model of the elongation of Escherichia coli P pili under strain. Biophys J 90:1521–1534. doi:10.1529/biophysj.105.074674

    Article  PubMed  CAS  Google Scholar 

  • Andersson M, Uhlin BE, Fallman E (2007) The biomechanical properties of E. coli Pili for urinary tract attachment reflect the host environment. Biophys J 93:3008–3014. doi:10.1529/biophysj.107.110643

    Article  PubMed  CAS  Google Scholar 

  • Barsegov V, Thirumalai D (2005) Dynamics of unbinding of cell adhesion molecules: transition from catch to slip bonds. Proc Natl Acad Sci USA 102:1835–1839. doi:10.1073/pnas.0406938102

    Article  PubMed  CAS  Google Scholar 

  • Bell MG (1978) Models for the specific adhesion of cells to cells. Science 200:618–627. doi:10.1126/science.347575

    Article  PubMed  CAS  Google Scholar 

  • Björnham O, Axner O, Andersson M (2008) Modeling of the elongation and retraction of Escherichia coli P pili under strain by Monte Carlo simulations. Eur Biophys J Biophys Lett 37:381–391

    Google Scholar 

  • Dembo M, Torney DC, Saxman K, Hammer D (1988) The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc R Soc Lond B Biol Sci 234:55–83

    PubMed  CAS  Google Scholar 

  • Enami M, Nakasone N, Honma Y, Kakinohana S, Kudaka J, Iwanaga M (1999) Expression of type I pili is abolished in verotoxin-producing Escherichia coli O157. FEMS Microbiol Lett 179:467–472. doi:10.1111/j.1574-6968.1999.tb08764.x

    Article  PubMed  CAS  Google Scholar 

  • Evans E (2001) Probing the relation between force—lifetime—and chemistry in single molecular bonds. Annu Rev Biophys Biomol Struct 30:105–128. doi:10.1146/annurev.biophys.30.1.105

    Article  PubMed  CAS  Google Scholar 

  • Evans E, Ritchie K (1997) Dynamic strength of molecular adhesion bonds. Biophys J 72:1541–1555

    Article  PubMed  CAS  Google Scholar 

  • Evans E, Leung A, Hammer D, Simon S (2001) Chemically distinct transition states govern rapid dissociation of single L-selectin bonds under force. Proc Natl Acad Sci USA 98:3784–3789. doi:10.1073/pnas.061324998

    Article  PubMed  CAS  Google Scholar 

  • Evans E, Leung A, Heinrich V, Zhu CCh (2004) Mechanical switching and coupling between two dissociation pathways in a P-selectin adhesion bond. Proc Natl Acad Sci USA 101:11281–11286

    Article  PubMed  CAS  Google Scholar 

  • Fällman E, Schedin S, Jass J, Andersson M, Uhlin BE, Axner O (2004) Optical tweezers based force measurement system for quantitating binding interactions: system design and application for the study of bacterial adhesion. Biosens Bioelectron 19:1429–1437. doi:10.1016/j.bios.2003.12.029

    Article  PubMed  CAS  Google Scholar 

  • Forero M, Thomas WE, Bland C, Nilsson LM, Sokurenko EV, Vogel V (2004) A catch-bond based nanoadhesive sensitive to shear stress. Nano Lett 4:1593–1597. doi:10.1021/nl049329z

    Article  CAS  Google Scholar 

  • Foxman B, Brown P (2003) Epidemiology of urinary tract infections—transmission and risk factors, incidence, and costs. Infect Dis Clin North Am 17:227–241. doi:10.1016/S0891-5520(03)00005-9

    Article  PubMed  Google Scholar 

  • Fritz J, Katopodis AG, Kolbinger F, Anselmetti D (1998) Force-mediated kinetics of single P-selectin ligand complexes observed by atomic force microscopy. Proc Natl Acad Sci USA 95:12283–12288. doi:10.1073/pnas.95.21.12283

    Article  PubMed  CAS  Google Scholar 

  • Goldman AJ, Cox RG, Brenner H (1967) Slow viscous motion of a sphere parallel to a plane wall. II. Couette flow. Chem Eng Sci 22:653–660. doi:10.1016/0009-2509(67)80048-4

    Article  CAS  Google Scholar 

  • Guo B, Guilford WH (2006) Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. Proc Natl Acad Sci USA 103:9844–9849. doi:10.1073/pnas.0601255103

    Article  PubMed  CAS  Google Scholar 

  • Jass J, Schedin S, Fällman E, Ohlsson J, Nilsson U, Uhlin BE, Axner O (2004) Physical properties of Escherichia coli P pili measured by optical tweezers. Biophys J 87:4271–4283. doi:10.1529/biophysj.104.044867

    Article  PubMed  CAS  Google Scholar 

  • Larsson A, Ohlsson J, Dodson KW, Hultgren SJ, Nilsson U, Kihlberg J (2003) Quantitative studies of the binding of the class II PapG adhesin from uropathogenic Escherichia coli to oligosaccharides. Bioorg Med Chem 11:2255–2261. doi:10.1016/S0968-0896(03)00114-7

    Article  PubMed  CAS  Google Scholar 

  • Liang MN, Smith SP, Metallo SJ, Choi IS, Prentiss M, Whitesides GM (2000) Measuring the forces involved in polyvalent adhesion of uropathogenic Escherichia coli to mannose-presenting surfaces. Proc Natl Acad Sci USA 97:13092–13096. doi:10.1073/pnas.230451697

    Article  PubMed  CAS  Google Scholar 

  • Lindberg FP, Lund B, Normark S (1984) Genes of pyelonephritogenic E. coli required for digalactosidespecific agglutination of human cells. EMBO J 3:1167–1173

    PubMed  CAS  Google Scholar 

  • Lindberg F, Lund B, Johansson L, Normark S (1987) Localization of the receptor-binding protein adhesin at the tip of the bacterial pilus. Nature 328:84–87. doi:10.1038/328084a0

    Article  PubMed  CAS  Google Scholar 

  • Lugmaier RA, Schedin S, Kuhner F, Benoit M (2007) Dynamic restacking of Escherichia Coli P-pili. Eur Biophys J 37:111–120. doi:10.1007/s00249-007-0183-x

    Article  PubMed  CAS  Google Scholar 

  • Lund B, Lindberg F, Marklund BI, Normark S (1987) The PapG protein is the alpha-d-galactopyranosyl-(1–4)-beta-d-galactopyranose-binding adhesin of uropathogenic Escherichia Coli. Proc Natl Acad Sci USA 84:5898–5902. doi:10.1073/pnas.84.16.5898

    Article  PubMed  CAS  Google Scholar 

  • Maier B, Potter L, So M, Seifert HS, Sheetz MP (2002) Single pilus motor forces exceed 100 pN. Proc Natl Acad Sci USA 99:16012–16017. doi:10.1073/pnas.242523299

    Article  PubMed  CAS  Google Scholar 

  • Marshall BT, Long M, Piper JW, Yago T, McEver RP, Zhu C (2003) Direct observation of catch bonds involving cell-adhesion molecules. Nature 423:190–193. doi:10.1038/nature01605

    Article  PubMed  CAS  Google Scholar 

  • Miller E, Garcia TI, Hultgren S, Oberhauser A (2006) The mechanical properties of E. coli type 1 pili measured by atomic force microscopy techniques. Biophys J 91:3848–3856. doi:10.1529/biophysj.106.088989

    Article  PubMed  CAS  Google Scholar 

  • Morfill J, Blank K, Zahnd C, Luginbuhl B, Kuhner F, Gottschalk KE, Pluckthun A, Gaub HE (2007) Affinity-matured recombinant antibody fragments analyzed by single-molecule force spectroscopy. Biophys J 93:3583–3590. doi:10.1529/biophysj.107.112532

    Article  PubMed  CAS  Google Scholar 

  • Nilsson LM, Thomas WE, Trintchina E, Vogel V, Sokurenko EV (2006) Catch bond-mediated adhesion without a shear threshold—Trimannose versus monomannose interactions with the FimH adhesin of Escherichia coli. J Biol Chem 281:16656–16663. doi:10.1074/jbc.M511496200

    Article  PubMed  CAS  Google Scholar 

  • Odorico M, Teulon JM, Bessou T, Vidaud C, Bellanger L, Chen SWW, Quemeneur E, Parot P, Pellequer JL (2007) Energy landscape of chelated uranyl: antibody interactions by dynamic force spectroscopy. Biophys J 93:645–654. doi:10.1529/biophysj.106.098129

    Article  PubMed  CAS  Google Scholar 

  • Ohlsson J, Jass J, Uhlin BE, Kihlberg J, Nilsson UJ (2002) Discovery of potent inhibitors of PapG adhesins from uropathogenic Escherichia coli through synthesis and evaluation of galabiose derivatives. ChemBioChem 3:772–779. doi:10.1002/1439-7633(20020802)3:8<772::AID-CBIC772>3.0.CO;2-8

    Article  PubMed  CAS  Google Scholar 

  • Reid G, Sobel JD (1987) Bacterial adherence in the pathogenesis of urinary-tract infection: a review. Rev Infect Dis 9:470–487

    PubMed  CAS  Google Scholar 

  • Sandberg T, Kaijser B, Lidinjanson G, Lincoln K, Orskov F, Orskov I, Stokland E, Svanborgeden C (1988) Virulence of Escherichia Coli in relation to host factors in women with symptomatic urinary-tract infection. J Clin Microbiol 26:1471–1476

    PubMed  CAS  Google Scholar 

  • Stromberg N, Marklund BI, Lund B, Ilver D, Hamers A, Gaastra W, Karlsson KA, Normark S (1990) Host-specificity of uropathogenic Escherichia Coli depends on differences in binding specificity to gal-alpha 1–4gal-containing isoreceptors. EMBO J 9:2001–2010

    PubMed  CAS  Google Scholar 

  • Sundararaj S, Guo A, Habibi-Nazhad B, Rouani M, Stothard P, Ellison M, Wishart DS (2004) The CyberCell Database (CCDB): a comprehensive, self-updating, relational database to coordinate and facilitate in silico modeling of Escherichia coli. Nucleic Acids Res 32:D293–D295. doi:10.1093/nar/gkh108

    Article  PubMed  CAS  Google Scholar 

  • Thomas WE, Trintchina E, Forero M, Vogel V, Sokurenko EV (2002) Bacterial adhesion to target cells enhanced by shear force. Cell 109:913–923. doi:10.1016/S0092-8674(02)00796-1

    Article  PubMed  CAS  Google Scholar 

  • Thomas WE, Nilsson LM, Forero M, Sokurenko EV, Vogel V (2004) Shear-dependent ‘stick-and-roll’ adhesion of type 1 fimbriated Escherichia coli. Mol Microbiol 53:1545–1557. doi:10.1111/j.1365-2958.2004.04226.x

    Article  PubMed  CAS  Google Scholar 

  • Thomas W, Forero M, Yakovenko O, Nilsson L, Vicini P, Sokurenko E, Vogel V (2006) Catch-bond model derived from allostery explains force-activated bacterial adhesion. Biophys J 90:753–764. doi:10.1529/biophysj.105.066548

    Article  PubMed  CAS  Google Scholar 

  • Weissman SJ, Chattopadhyay S, Aprikian P, Obata-Yasuoka M, Yarova-Yarovaya Y, Stapleton A, Ba-Thein W, Dykhuizen D, Johnson JR, Sokurenko EV (2006) Clonal analysis reveals high rate of structural mutations in fimbrial adhesins of extraintestinal pathogenic Escherichia coli. Mol Microbiol 59:975–988. doi:10.1111/j.1365-2958.2005.04985.x

    Article  PubMed  CAS  Google Scholar 

  • Yang HY, Yu JP, Fu G, Shi XL, Xiao L, Chen YZ, Fang XH, He C (2007) Interaction between single molecules of Mac-1 and ICAM-1 in living cells: an atomic force microscopy study. Exp Cell Res 313:3497–3504. doi:10.1016/j.yexcr.2007.08.001

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We acknowledge Prof. Bernt-Eric Uhlin and Monica Persson, Department of Molecular Biology, Umeå University, Sweden, for providing the E. coli strains. We thank Dr. Erik Fällman for laboratorial assistance. We also thank Prof. Ulf J. Nilsson, Organic and Bioorganic Chemistry, Lund University, Sweden for providing the amino-galabiose coated beads. Economical support from the Magn. Bergvalls Foundation, Sweden, is also acknowledged.

Author information

Authors and Affiliations

  1. Department of Applied Physics and Electronics, Umeå University, 901 87, Umeå, Sweden

    Oscar Björnham, Håkan Nilsson & Staffan Schedin

  2. Department of Physics, Umeå University, 901 87, Umeå, Sweden

    Magnus Andersson

Authors
  1. Oscar Björnham
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Håkan Nilsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Magnus Andersson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Staffan Schedin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Staffan Schedin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Björnham, O., Nilsson, H., Andersson, M. et al. Physical properties of the specific PapG–galabiose binding in E. coli P pili-mediated adhesion. Eur Biophys J 38, 245–254 (2009). https://doi.org/10.1007/s00249-008-0376-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-008-0376-y

Keywords

Search

Navigation