Bond-Strengthening in Staphylococcal Adhesion to Hydrophilic and Hydrophobic Surfaces Using Atomic Force Microscopy

Boks, Niels P.; Busscher, Henk J.; Mei, Henny C. van der; Norde, Willem

doi:10.1021/la801824c

Cited by 90 publications

(91 citation statements)

References 23 publications

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“…Adhesion forces increased with increasing the contact time to 1 s (280 ± 113 pN; Fig. 2 C and D), indicating that cell-cell bonds strengthen with the duration of adhesion (19,26). Force profiles showed multiple ruptures, unlike the 100-ms curves, which we believe result from the sequential rupture of multiple bonds.…”

Section: Resultsmentioning

confidence: 86%

Molecular interactions and inhibition of the staphylococcal biofilm-forming protein SdrC

Feuillie

Formosa-Dague

Hays

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Staphylococcus aureus forms biofilms on indwelling medical devices using a variety of cell-surface proteins. There is growing evidence that specific homophilic interactions between these proteins represent an important mechanism of cell accumulation during biofilm formation, but the underlying molecular mechanisms are still not well-understood. Here we report the direct measurement of homophilic binding forces by the serine-aspartate repeat protein SdrC and their inhibition by a peptide. Using single-cell and single-molecule force measurements, we find that SdrC is engaged in low-affinity homophilic bonds that promote cell-cell adhesion. Low-affinity intercellular adhesion may play a role in favoring biofilm dynamics. We show that SdrC also mediates strong cellular interactions with hydrophobic surfaces, which are likely to be involved in the initial attachment to biomaterials, the first stage of biofilm formation. Furthermore, we demonstrate that a peptide derived from β-neurexin is a powerful competitive inhibitor capable of efficiently blocking surface attachment, homophilic adhesion, and biofilm accumulation. Molecular modeling suggests that this blocking activity may originate from binding of the peptide to a sequence of SdrC involved in homophilic interactions. Our study opens up avenues for understanding the role of homophilic interactions in staphylococcal adhesion, and for the design of new molecules to prevent biofilm formation during infection.Staphylococcus aureus | SdrC | adhesion | biofilms | inhibition T he nosocomial pathogen Staphylococcus aureus is a major cause of superficial and invasive infections. A remarkable trait of this bacterium is its ability to form biofilms on implanted devices, thereby triggering infections that are difficult to treat with antibiotics (1, 2). Biofilm formation is initiated by attachment of the bacteria to abiotic surfaces, protein-coated materials, and host cells, and followed by cell-cell adhesion and multiplication leading to a mature biofilm (1, 2). A variety of cell-surface components are involved in intercellular interactions (2, 3). Although the polycationic polysaccharide intercellular adhesin has long been thought to be the main component promoting intercellular adhesion (4, 5), there is now a compelling body of evidence that cell wall-anchored (CWA) proteins are also involved (2, 3). Several recombinant CWA proteins have been shown to form dimers in solution (6-9). In some cases (i.e., Aap), crystallographic studies have provided insights into the mechanism of dimer formation (9, 10). Although very useful, in vitro methods provide information on purified molecules that are removed from their cellular context. Clearly, elucidating the molecular mechanisms by which CWA proteins self-associate in vivo is key to enhancing our understanding of biofilm accumulation.The increase of multidrug-resistant strains has created an urgent need for new therapeutics for bacterial infections. Biofilm inhibitors, where bacteria are prevented from forming biofilms rather than...

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Section: Resultsmentioning

confidence: 86%

Molecular interactions and inhibition of the staphylococcal biofilm-forming protein SdrC

Feuillie

Formosa-Dague

Hays

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Figure 1a shows an AFM force-distance curve for Staphylococcus epidermidis on glass with multiple peaks in the retraction curve. Considering each adhesion peak as an individual detachment event (2,5,8,10,26,27), each peak provides a specific adhesion force (F) according to equation 1, and the only variable for a given combination of bacterial strain and substratum is the number of short-range bonds (k). It should be noted that it is a tedious task to identify the minor peaks, since it is not clear a priori when a peak should be taken as an individual detachment event.…”

Section: Theoretical Background Of Poisson Analysis Of Adhesion Forcesmentioning

confidence: 99%

“…AFM spectroscopy reveals the distance dependence of the adhesion force, and measured force-distance curves can be compared with theoretical models (3,7,8,13), which are usually based on the Derjaguin-Landau-Verwey-Overbeek (DLVO) theory (12, 39). The extended DLVO theory (36) includes not only long-range LW and EDL interactions, as does the classical DLVO theory, but also short-range AB interactions.…”

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confidence: 99%

“…As an alternative, a statistical method, called Poisson analysis, was first applied by Han, Williams, and Beebe (19,43) to determine the magnitude of individual LW bonds between an AFM tip and a gold surface, as well as the strength of an individual AB bond between an AFM tip and a mica surface. Soon afterwards, Poisson analysis of AFM adhe-sion forces was used to determine the nature of the interaction forces between single molecules (25,34,41,42) and the nature of the forces mediating bacterial adhesion to surfaces (2,5,8,10,26,27).…”

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confidence: 99%

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Statistical Analysis of Long- and Short-Range Forces Involved in Bacterial Adhesion to Substratum Surfaces as Measured Using Atomic Force Microscopy

Chen

Busscher

Mei

et al. 2011

Appl Environ Microbiol

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Surface thermodynamic analyses of microbial adhesion using measured contact angles on solid substrata and microbial cell surfaces are widely employed to determine the nature of the adhesion forces, i.e., the interplay between Lifshitz-van der Waals and acid-base forces. While surface thermodynamic analyses are often viewed critically, atomic force microscopy (AFM) can also provide information on the nature of the adhesion forces by means of Poisson analysis of the measured forces. This review first presents a description of Poisson analysis and its underlying assumptions. The data available from the literature for different combinations of bacterial strains and substrata are then summarized, leading to the conclusion that bacterial adhesion to surfaces is generally dominated by short-range, attractive acid-base interactions, in combination with long-range, weaker Lifshitz-van der Waals forces. This is in line with the findings of surface thermodynamic analyses of bacterial adhesion. Comparison with single-molecule ligand-receptor forces from the literature suggests that the short-range-force contribution from Poisson analysis involves a discrete adhesive bacterial cell surface site rather than a single molecular force. The adhesion force arising from these cell surface sites and the number of sites available may differ from strain to strain. Force spectroscopy, however, involves the tedious task of identifying the minor peaks in the AFM retraction force-distance curve. This step can be avoided by carrying out Poisson analysis on the work of adhesion, which can also be derived from retraction force-distance curves. This newly proposed way of performing Poisson analysis confirms that multiple molecular bonds, rather than a single molecular bond, contribute to a discrete adhesive bacterial cell surface site.Bacteria can adhere to various natural (33) and synthetic (11) surfaces, a phenomenon with widely different fields of application ranging from marine fouling, soil remediation, and food and drinking water processing to medicine and dentistry. In order to avoid the problems sometimes associated with bacterial adhesion, or to take advantage of it, better understanding of the mechanisms by which bacteria adhere to surfaces is required.Bacterial adhesion to surfaces can be approached by biochemical methods, by which the molecular structures mediating adhesion are unraveled (5, 18, 22, 31), or by physicochemical methods. Surface thermodynamic analyses of bacterial cell and substratum surfaces using measured contact angles with liquids have not only indicated when thermodynamic conditions are favorable or unfavorable for adhesion (1, 37) but can also be employed in combination with measured zeta potentials of the interacting surfaces to determine the nature of the adhesion forces that mediate initial adhesion, i.e., the interplay among long-range (Lifshitz-van der Waals [LW] and electrical double-layer [EDL]) and short-range (Lewis acid-base [AB]) interaction forces (35). Surface thermodynamic analyses of bacterial ad...

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“…21,23,26 Boks et al reported that bond strengthening for four strains of S. epidermidis on a hydrophobic surface was fast and limited to a minor increase, while strengthening of the bonds on a hydrophilic surface increases significantly with contact time. 33 As water molecules adjacent to a hydrophobic surface are not able to form hydrogen bonds with that surface (hydrophobic effect), bacterial adhesion to a hydrophobic specimen is brought about by an entropically favorable release of water molecules. The results of this research indicated that the amount of bacteria that adhered to the more hydrophobic Co-Cr-Mo surface was significantly less than that for the rather hydrophilic CP-Ti surface.…”

Section: Discussionmentioning

confidence: 99%

Adherence ability of Staphylococcus epidermidis on prosthetic biomaterials: an in vitro study

Shida

Koseki²,

Yoda³

et al. 2013

IJN

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Bond-Strengthening in Staphylococcal Adhesion to Hydrophilic and Hydrophobic Surfaces Using Atomic Force Microscopy

Cited by 90 publications

References 23 publications

Molecular interactions and inhibition of the staphylococcal biofilm-forming protein SdrC

Molecular interactions and inhibition of the staphylococcal biofilm-forming protein SdrC

Statistical Analysis of Long- and Short-Range Forces Involved in Bacterial Adhesion to Substratum Surfaces as Measured Using Atomic Force Microscopy

Adherence ability of Staphylococcus epidermidis on prosthetic biomaterials: an in vitro study

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