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Downloaded Via UNIV of CALIFORNIA MERCED on April 28, 2020 at 20:21:08 (UTC) UC Merced UC Merced Previously Published Works Title Impact of Molecular Architecture and Adsorption Density on Adhesion of Mussel-Inspired Surface Primers with Catechol-Cation Synergy. Permalink https://escholarship.org/uc/item/3138f8nm Journal Journal of the American Chemical Society, 141(47) ISSN 0002-7863 Authors Degen, George D Stow, Parker R Lewis, Robert B et al. Publication Date 2019-11-14 DOI 10.1021/jacs.9b04337 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Article Cite This: J. Am. Chem. Soc. 2019, 141, 18673−18681 pubs.acs.org/JACS Impact of Molecular Architecture and Adsorption Density on Adhesion of Mussel-Inspired Surface Primers with Catechol-Cation Synergy † ‡ ‡ † § George D. Degen, Parker R. Stow, Robert B. Lewis, Roberto C. Andresen Eguiluz, Eric Valois, † ‡ ⊥ † ∥ Kai Kristiansen, Alison Butler,*, and Jacob N. Israelachvili , , † ‡ § Department of Chemical Engineering, Department of Chemistry and Biochemistry, Biomolecular Science and Engineering, and ∥ Materials Department, University of California, Santa Barbara, California 93106, United States *S Supporting Information ABSTRACT: Marine mussels secrete proteins rich in residues containing catechols and cationic amines that displace hydration layers and adhere to charged surfaces under water via a cooperative binding effect known as catechol-cation synergy. Mussel-inspired adhesives containing paired catechol and cationic functionalities are a promising class of materials for biomedical applications, but few studies address the molecular adhesion mechanism(s) of these materials. To determine whether intramolecular adjacency of these functionalities is necessary for robust adhesion, a suite of siderophore analog surface primers was synthesized with systematic variations in intramolecular spacing between catechol and cationic functionalities. Adhesion measurements conducted with a surface forces apparatus (SFA) allow adhesive failure to be distinguished from cohesive failure and show that the failure mode depends critically on the siderophore analog adsorption density. The adhesion of these molecules to muscovite mica in an aqueous electrolyte solution demonstrates that direct intramolecular adjacency of catechol and cationic functionalities is not necessary for synergistic binding. However, we show that increasing the catechol-cation spacing by incorporating nonbinding domains results in decreased adhesion, which we attribute to a decrease in the density of catechol functionalities. A mechanism for catechol-cation synergy is proposed based on electrostatically driven adsorption and subsequent binding of catechol functionalities. This work should guide the design of new adhesives for binding to charged surfaces in saline environments. 1. INTRODUCTION catechol-poly(ethylenimine),14,15 among others.16,17 Molecules 18 Rational design of wet adhesives requires an understanding of containing Dopa and other catechols adhere to apatite and metal oxide19 surfaces found in bone and implant materials, the intermolecular interactions between adhesives and 20 substrates in saline environments such as seawater or body and have been shown to be biocompatible, making them Downloaded via UNIV OF CALIFORNIA MERCED on April 28, 2020 at 20:21:08 (UTC). fl attractive alternatives to existing medical adhesives, many of uids. Designing adhesives for use in these environments is ff 21,22 23−25 See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles. fi which are ine ective or cytotoxic. challenging for example, van der Waals forces are signi - fi cantly reduced under water, and ions in solution compete with Despite widespread scienti c and applications-based re- search on materials containing catechol functionalities,20 adhesives for binding sites on charged surfaces. Despite these fi challenges, marine mussels adhere to many inorganic and speci c adhesion mechanisms of these materials have only − 26 organic surfaces,1 3 typically by relying on adhesive proteins recently begun to be explored. It has been demonstrated that rich in the catecholic amino acid 3,4-dihydroxyphenylalanine adhesives incorporating catechol and cationic amine function- (Dopa).4 Due to the large proportion of cationic residues, alities bind more strongly to muscovite mica in saline solutions most commonly lysine, paired with Dopa in the most adhesive than adhesives incorporating either catechols or cations 27 ff interfacial mussel protein (Mfp-5),1,5 it has been hypothesized alone, a cooperative e ect known as catechol-cation synergy. The adjacent pairing of Dopa and lysine in the Mfp-5 that both these residues are important for adhesion. 5 Furthermore, other compounds containing catechol and sequence has prompted speculation that intramolecular cationic functionalities have been shown to adhere to many proximity of catechol and cationic functionalities may be ff surfaces. Polydopamine, formed from the polymerization and necessary for adhesion, and that an intramolecular cuto − self-assembly of oxidized dopamine,6 9 adheres to a wide distance may exist beyond which catechol-cation synergy no variety of materials and has been proposed for many applications.10 Other adhesives containing catechol and Received: April 22, 2019 − cationic functionalities include catechol-chitosan11 13 and Published: November 14, 2019 © 2019 American Chemical Society 18673 DOI: 10.1021/jacs.9b04337 J. Am. Chem. Soc. 2019, 141, 18673−18681 Journal of the American Chemical Society Article longer operates.28 A recent study showed that the order of catechol and cationic functionalities impacts the single- molecule pull-off force,29 supporting the hypothesis that direct adjacency of catechol and cationic functionalities may be enhance adhesion. However, until now no study has directly explored the impact of intramolecular spacing on catechol- cation synergy. Here, we present adhesion measurements of siderophore analog surface primers with systematically varying intra- molecular spacing between catechol and cationic amine functionalities. We show that the pull-off force mediated by the siderophore analogs depends critically on the adsorption density and confirm that catechol-cation synergy enables adhesion. Surprisingly, the results demonstrate that direct intramolecular adjacency between catechol and cationic functionalities is not necessary for catechol-cation synergy and suggest that no intramolecular cutoff distance between these functionalities exists for which catechol-cation synergy will be abolished. To explain the results, we propose a mechanism for catechol-cation synergy based on electrostati- cally driven adsorption and support this mechanism with a qualitative model. 2. EXPERIMENTAL SECTION We synthesized a suite of seven siderophore analogs, synthetic mimics of bacterial iron chelators called siderophores.30 Each analog has a central tris(2-aminoethyl)amine (Tren) scaffold with three identical peptide arms. Here, each peptide arm contained glycine (G) and lysine (K) and were capped with either the catechol 2,3- dihydroxybenzoyl (2,3-DHBA) or benzoyl functionality (Figure 1). The intramolecular spacing between 2,3-DHBA and lysine in the peptide arms was varied by changing the peptide sequence. Three of the analogs were isomers: Tren(GGK-Cat)3, Tren(GKG-Cat)3, and Tren(KGG-Cat) . Siderophore analogs with even greater catechol- Figure 1. Suite of siderophore analogs investigated. (A) Tris(2- 3 ff − cation spacing (Tren(KGGG-Cat)3 and Tren(KGGGGGG-Cat)3), aminoethyl)amine (Tren) sca old. R-groups are shown in (B H). cationic amines but without catechols (Tren(GGK-Benz)3), and only The intramolecular distance between 2,3-DHBA and lysine is varied catechols (Tren(GGG-Cat)3) were also synthesized. Additional in (B) Tren(GGK-Cat)3, (C) Tren(GKG-Cat)3, (D) Tren(KGG- details on materials, synthesis, and molecular characterization are Cat)3, (E) Tren(KGGGGGG-Cat)3, and (F) Tren(KGGG-Cat)3. included in the Supporting Information, SI, (S1 and S2). Analogs Analogs containing lysine without 2,3-DHBA, (G) Tren(GGK- were dissolved at 1 mM in an aqueous salt solution (50 mM acetic Benz)3, and 2,3-DHBA without lysine, (H) Tren(GGG-Cat)3 were acid, 150 mM KNO3, pH = 3.3), chosen to mimic physiological ionic also synthesized. strengths but avoid catechol oxidation by maintaining an acidic pH. Adhesion measurements were performed using a surface forces apparatus (SFA) model SFA2000 (SurForce, LLC), described in 31 detail in the SI (S3) and elsewhere. In the SFA, freshly cleaved during separation corresponding to the most negative force measured muscovite mica surfaces were arranged in a crossed cylinder geometry. during separation. Pull-off force did not depend on separation velocity All experiments were performed at a constant temperature. Side- (V =2−10 nm/s) (Figure S32) nor maximum compression (F/R = rophore analogs were deposited via adsorption from solution into out 9−108 mN/m). We use the term “pull-off” instead of “adhesion” films on either one (asymmetric deposition) or both (symmetric μ because the force required to separate the mica surfaces can deposition) mica surfaces. For asymmetric deposition, 50 L of 400 fi − μM siderophore analog solution was injected onto one of the mica correspond to adhesive failure at the lm mica interface, cohesive fi −fi surfaces and incubated for at least 60 min. The surface was then failure at the lm lm interface, or a combination of the two failure rinsed before adhesion measurements. For symmetric deposition, modes.
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