The binding force of the staphylococcal adhesin SdrG is remarkably strong

Molecular Microbiology

Volumn 93, Issue 2, 2014, Pages 356-368

  Herman, Philippe ^a   El Kirat Chatel, Sofiane ^a   Beaussart, Audrey ^a   Geoghegan, Joan A ^b   Foster, Timothy J ^b   Dufrêne, Yves F ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; FIBRINOGEN; SDRG PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CARRIER PROTEIN; FBE PROTEIN, BACTERIA; LIGAND; PROTEIN BINDING;

ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIUM ADHERENCE; BINDING AFFINITY; CELL ADHESION; CELL SURFACE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; COVALENT BOND; DISSOCIATION; NONHUMAN; PRIORITY JOURNAL; SINGLE MOLECULE FORCE SPECTROSCOPY; SPECTROSCOPY; STAPHYLOCOCCUS EPIDERMIDIS; CHEMISTRY; METABOLISM; PHYSIOLOGY; SINGLE CELL ANALYSIS;

RUMEX; STAPHYLOCOCCUS EPIDERMIDIS;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL PROTEINS; CARRIER PROTEINS; FIBRINOGEN; LIGANDS; MICROSCOPY, ATOMIC FORCE; PROTEIN BINDING; SINGLE-CELL ANALYSIS; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 84904043538     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12663     Document Type: Article

References (43)

1. Alsteens, D., Garcia, M.C., Lipke, P.N., and Dufrene, Y.F. (2010) Force-induced formation and propagation of adhesion nanodomains in living fungal cells. Proc Natl Acad Sci USA 107: 20744-20749.
2. Andre, G., Kulakauskas, S., Chapot-Chartier, M.P., Navet, B., Deghorain, M., Bernard, E., etal. (2010) Imaging the nanoscale organization of peptidoglycan in living Lactococcus lactis cells. Nat Commun 1: 27.
3. Baumgartner, W., Hinterdorfer, P., Ness, W., Raab, A., Vestweber, D., Schindler, H., and Drenckhahn, D. (2000) Cadherin interaction probed by atomic force microscopy. Proc Natl Acad Sci USA 97: 4005-4010.
4. Beaussart, A., El-Kirat-Chatel, S., Herman, P., Alsteens, D., Mahillon, J., Hols, P., and Dufrene, Y.F. (2013a) Single-cell force spectroscopy of probiotic bacteria. Biophys J 104: 1886-1892.
5. Beaussart, A., Herman, P., El-Kirat-Chatel, S., Lipke, P.N., Kucharikova, S., Van Dijck, P., and Dufrene, Y.F. (2013b) Single-cell force spectroscopy of the medically important Staphylococcus epidermidis-Candida albicans interaction. Nanoscale 5: 10894-10900.
6. Boks, N.P., Busscher, H.J., van der Mei, H.C., and Norde, W. (2008) Bond-strengthening in staphylococcal adhesion to hydrophilic and hydrophobic surfaces using atomic force microscopy. Langmuir 24: 12990-12994.
7. Bowden, M.G., Heuck, A.P., Ponnuraj, K., Kolosova, E., Choe, D., Gurusiddappa, S., etal. (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.
8. Buck, A.W., Fowler, V.G., Jr, Yongsunthon, R., Liu, J., DiBartola, A.C., Que, Y.A., etal. (2010) Bonds between fibronectin and fibronectin-binding proteins on Staphylococcus aureus and Lactococcus lactis. Langmuir 26: 10764-10770.
9. Casillas-Ituarte, N.N., Lower, B.H., Lamlertthon, S., Fowler, V.G., Jr, and Lower, S.K. (2012) Dissociation rate constants of human fibronectin binding to fibronectin-binding proteins on living Staphylococcus aureus isolated from clinical patients. J Biol Chem 287: 6693-6701.
10. Dufrene, Y.F., Boonaert, C.J., Gerin, P.A., Asther, M., and Rouxhet, P.G. (1999) Direct probing of the surface ultrastructure and molecular interactions of dormant and germinating spores of Phanerochaete chrysosporium. J Bacteriol 181: 5350-5354.
11. Dupres, V., Menozzi, F.D., Locht, C., Clare, B.H., Abbott, N.L., Cuenot, S., etal. (2005) Nanoscale mapping and functional analysis of individual adhesins on living bacteria. Nat Methods 2: 515-520.
12. Dupres, V., Verbelen, C., Raze, D., Lafont, F., and Dufrene, Y.F. (2009) Force spectroscopy of the interaction between mycobacterial adhesins and heparan sulphate proteoglycan receptors. Chemphyschem 10: 1672-1675.
13. Ebner, A., Wildling, L., Kamruzzahan, A.S., Rankl, C., Wruss, J., Hahn, C.D., etal. (2007) A new, simple method for linking of antibodies to atomic force microscopy tips. Bioconjug Chem 18: 1176-1184.
14. El-Kirat-Chatel, S., Boyd, C.D., O'Toole, G.A., and Dufrene, Y.F. (2014) Single-molecule analysis of Pseudomonas fluorescens footprints. ACS Nano 8: 1690-1698.
15. Emerson, R.J., 4th, Bergstrom, T.S., Liu, Y., Soto, E.R., Brown, C.A., McGimpsey, W.G., and Camesano, T.A. (2006) Microscale correlation between surface chemistry, texture, and the adhesive strength of Staphylococcus epidermidis. Langmuir 22: 11311-11321.
16. Foster, T.J., Geoghegan, J.A., Ganesh, V.K., and Hook, M. (2014) Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 12: 49-62.
17. Fritz, J., Katopodis, A.G., Kolbinger, F., and 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.
18. Geoghegan, J.A., Ganesh, V.K., Smeds, E., Liang, X., Höök, M., and Foster, T.J. (2010) Molecular characterization of the interaction of Staphylococcal microbial surface components recognizing adhesive matrix molecules (MSCRAMM) ClfA and Fbl with fibrinogen. J Biol Chem 285: 6208-6216.
19. Grandbois, M., Beyer, M., Rief, M., Clausen-Schaumann, H., and Gaub, H.E. (1999) How strong is a covalent bond? Science 283: 1727-1730.
20. Hartford, O., O'Brien, L., Schofield, K., Wells, J., and Foster, T.J. (2001) The Fbe (SdrG) protein of Staphylococcus epidermidis HB promotes bacterial adherence to fibrinogen. Microbiology 147: 2545-2552.
21. Helenius, J., Heisenberg, C.P., Gaub, H.E., and Muller, D.J. (2008) Single-cell force spectroscopy. J Cell Sci 121: 1785-1791.
22. Hinterdorfer, P., and Dufrêne, Y.F. (2006) Detection and localization of single molecular recognition events using atomic force microscopy. Nat Methods 3: 347-355.
23. Josefsson, E., McCrea, K.W., Ni Eidhin, D., O'Connell, D., Cox, J., Hook, M., and Foster, T.J. (1998) Three new members of the serine-aspartate repeat protein multigene family of Staphylococcus aureus. Microbiology 144: 3387-3395.
24. Litvinov, R.I., Mekler, A., Shuman, H., Bennett, J.S., Barsegov, V., and Weisel, J.W. (2012) Resolving two-dimensional kinetics of the integrin alphaIIbbeta3-fibrinogen interactions using binding-unbinding correlation spectroscopy. J Biol Chem 287: 35275-35285.
25. Liu, Y., Strauss, J., and Camesano, T.A. (2008) Adhesion forces between Staphylococcus epidermidis and surfaces bearing self-assembled monolayers in the presence of model proteins. Biomaterials 29: 4374-4382.
26. Lower, S.K., Yongsunthon, R., Casillas-Ituarte, N.N., Taylor, E.S., DiBartola, A.C., Lower, B.H., etal. (2010) A tactile response in Staphylococcus aureus. Biophys J 99: 2803-2811.
27. Lower, S.K., Lamlertthon, S., Casillas-Ituarte, N.N., Lins, R.D., Yongsunthon, R., Taylor, E.S., etal. (2011) Polymorphisms in fibronectin binding protein A of Staphylococcus aureus are associated with infection of cardiovascular devices. Proc Natl Acad Sci USA 108: 18372-18377.
28. McCrea, K.W., Hartford, O., Davis, S., Eidhin, D.N., Lina, G., Speziale, P., etal. (2000) The serine-aspartate repeat (Sdr) protein family in Staphylococcus epidermidis. Microbiology 146: 1535-1546.
29. Mack, D. (1999) Molecular mechanisms of Staphylococcus epidermidis biofilm formation. J Hosp Infect 43 (Suppl.): S113-S125.
30. Merkel, R., Nassoy, P., Leung, A., Ritchie, K., and Evans, E. (1999) Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 397: 50-53.
31. Muller, D.J., Helenius, J., Alsteens, D., and Dufrene, Y.F. (2009) Force probing surfaces of living cells to molecular resolution. Nat Chem Biol 5: 383-390.
32. Nilsson, M., Frykberg, L., Flock, J.I., Pei, L., Lindberg, M., and Guss, B. (1998) A fibrinogen-binding protein of Staphylococcus epidermidis. Infect Immun 66: 2666-2673.
33. Oberhauser, A.F., Marszalek, P.E., Erickson, H.P., and Fernandez, J.M. (1998) The molecular elasticity of the extracellular matrix protein tenascin. Nature 393: 181-185.
34. Otto, M. (2009) Staphylococcus epidermidis - the 'accidental' pathogen. Nat Rev Microbiol 7: 555-567.
35. Ponnuraj, K., Bowden, M.G., Davis, S., Gurusiddappa, S., Moore, D., Choe, D., etal. (2003) A 'dock, lock, and latch' structural model for a staphylococcal adhesin binding to fibrinogen. Cell 115: 217-228.
36. Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J.M., and Gaub, H.E. (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276: 1109-1112.
37. Rief, M., Pascual, J., Saraste, M., and Gaub, H.E. (1999) Single molecule force spectroscopy of spectrin repeats: low unfolding forces in helix bundles. J Mol Biol 286: 553-561.
38. Simpson, K.H., Bowden, G., Hook, M., and Anvari, B. (2003) Measurement of adhesive forces between individual Staphylococcus aureus MSCRAMMs and protein-coated surfaces by use of optical tweezers. J Bacteriol 185: 2031-2035.
39. Sullan, R.M., Beaussart, A., Tripathi, P., Derclaye, S., El-Kirat-Chatel, S., Li, J.K., etal. (2013) Single-cell force spectroscopy of pili-mediated adhesion. Nanoscale 6: 1134-1143.
40. Tsang, P.H., Li, G., Brun, Y.V., Freund, L.B., and Tang, J.X. (2006) Adhesion of single bacterial cells in the micronewton range. Proc Natl Acad Sci USA 103: 5764-5768.
41. Xu, C.P., Boks, N.P., de Vries, J., Kaper, H.J., Norde, W., Busscher, H.J., and van der Mei, H.C. (2008) Staphylococcus aureus-fibronectin interactions with and without fibronectin-binding proteins and their role in adhesion and desorption. Appl Environ Microbiol 74: 7522-7528.
42. Yongsunthon, R., Fowler, V.G., Jr, Lower, B.H., Vellano, F.P., Alexander, E., Reller, L.B., etal. (2007) Correlation between fundamental binding forces and clinical prognosis of Staphylococcus aureus infections of medical implants. Langmuir 23: 2289-2292.
43. Zhmurov, A., Brown, A.E., Litvinov, R.I., Dima, R.I., Weisel, J.W., and Barsegov, V. (2011) Mechanism of fibrin(ogen) forced unfolding. Structure 19: 1615-1624.