Adaptive hydrophobic and hydrophilic interactions of mussel foot proteins with organic thin films

Abstract

The adhesion of mussel foot proteins (Mfps) to a variety of specially engineered mineral and metal oxide surfaces has previously been investigated extensively, but the relevance of these studies to adhesion in biological environments remains unknown. Most solid surfaces exposed to seawater or physiological fluids become fouled by organic conditioning films and biofilms within minutes. Understanding the binding mechanisms of Mfps to organic films with known chemical and physical properties therefore is of considerable theoretical and practical interest. Using selfassembled monolayers (SAMs) on atomically smooth gold substrates and the surface forces apparatus, we explored the forcedistance profiles and adhesion energies of three different Mfps, Mfp-1, Mfp-3, and Mfp-5, on (i) hydrophobic methyl (CH 3 )-and (ii) hydrophilic alcohol (OH)-terminated SAM surfaces between pH 3 and pH 7.5. At acidic pH, all three Mfps adhered strongly to the CH 3 -terminated SAM surfaces via hydrophobic interactions (range of adhesive interaction energy = −4 to −9 mJ/m 2 ) but only weakly to the OH-terminated SAM surfaces through H-bonding (adhesive interaction energy ≤ −0.5 mJ/m 2 ). 3, 4-Dihydroxyphenylalanine (Dopa) residues in Mfps mediate binding to both SAM surface types but do so through different interactions: typical bidentate H-bonding by Dopa is frustrated by the longer spacing of OHSAMs; in contrast, on CH 3 -SAMs, Dopa in synergy with other nonpolar residues partitions to the hydrophobic surface. Asymmetry in the distribution of hydrophobic residues in intrinsically unstructured proteins, the distortion of bond geometry between H-bonding surfaces, and the manipulation of physisorbed binding lifetimes represent important concepts for the design of adhesive and nonfouling surfaces. M arine mussels are experts at wet adhesion, achieving strong and durable attachments to a variety of surfaces in their chemically heterogeneous habitat. Adhesion is mediated by a byssus, which is essentially a bundle of leathery threads that emerge from the living mussel tissue at one end and are tipped by flat adhesive plaques at the other. Byssal plaques consist of a complex array of proteins (mostly mussel foot proteins, Mfps), each of which has a distinct localization and function in the structure, but all share the unusual modified amino acid 3, 4-dihydroxyphenylalanine (Dopa) (Fig. 1).Of the dozen or so known mussel foot proteins, Mfp-1, Mfp-3, and Mfp-5 have been shown to exhibit remarkable binding to mineral surfaces such as mica and TiO 2 (1). The versatility of mussel adhesion to surfaces with wide-ranging chemical and physical properties has inspired much research dedicated to understanding the mechanism of mussel adhesion and to developing biomimetic coatings and adhesives for wide-ranging industrial and biomedical applications, the latter including paints for coronary arteries (2), fetal membrane sealants (3), cell encapsulants (4), bone glues (5), and for securing transplants for diabetics (6).The catecholic moiety of Dopa (Fig. 1) ...

Surface-initiated self-healing of polymers in aqueous media

“…The Bell theory predicts that a bidentate hydrogen bond, such as that between a catechol donor and a surface acceptor, has a binding lifetime that is 10 6 times longer than the monodentate hydrogen-bond 20 ; experiment confirms that the catechol-mediated bidentate hydrogen bond is stronger than the monodentate hydrogen bond (that is, E bidentate ∼ 2E monodentate , or τ bidentate ∼ 10 6 τ monodentate ) (refs 13,20). In addition, previous studies of the intermolecular hydrogen bonds between phenolic hydroxyls 21 24 , concur that closely stacked catechols at surfaces provide strong intermolecular hydrogen bonds when brought into contact.…”

Resolving Non‐Specific and Specific Adhesive Interactions of Catechols at Solid/Liquid Interfaces at the Molecular Scale

“…The strongest binding energy of 29  k B T is measured for the interaction between Dopa and a titania‐coated tip. This is not unexpected since it has been pointed out previously that bidentate H‐bonding and metal coordination leads to strong adhesion between catechols and metal‐oxide surfaces 3a, 5. While our approach only provides equilibrated interaction free energies, insight into the exact binding mechanism is not possible.…”

“…Moreover, it is interesting that the interaction energy of Dopa with SAMs via H‐bonding is half the interaction energy of Dopa interacting with titania. Recently, Yu et al 3a. measured similar effects in SFA using proteins containing Dopa that bridge mica and an OH‐SAM coated surface.…”

“…Both surface forces apparatus (SFA)2b, 3 and single‐molecule force spectroscopy (SM‐AFM)4 experiments indicated that Dopa adheres well to metal‐oxide surfaces by bidentate H‐bonding and metal coordination 3a, 5. In particular, Lee et al 4a.…”

“…Using Bell–Evans theory,6 an approximate binding energy of 37  k B T per Dopa was estimated. Moreover Yu et al 3a. demonstrated that natural surfaces are usually covered with organic films, which will alter the interaction type and energy of Dopa binding to those surfaces.…”