Cation–π interactions and their contribution to mussel underwater

To date, more than 20 types of mfps have been discovered, and studies on their ... complex coacervates at the beginning of the 20th century.35 Complex...
0 downloads 0 Views 1MB Size
Subscriber access provided by Université de Strasbourg - Service Commun de la Documentation

Biological and Environmental Phenomena at the Interface

Cation–# interactions and their contribution to mussel underwater adhesion studied using a surface forces apparatus: A mini-review Sohee Park, Sangsik Kim, YongSeok Jho, and Dong Soo Hwang Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.9b01976 • Publication Date (Web): 17 Aug 2019 Downloaded from pubs.acs.org on August 21, 2019

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 46 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Langmuir

Cation–π interactions and their contribution to mussel underwater adhesion studied using a surface forces apparatus: A mini-review Sohee Park,† Sangsik Kim,†, § YongSeok Jho,*, || and Dong Soo Hwang*, †, §



Division of Environmental Science and Engineering, Pohang University of Science

and Technology (POSTECH), 77 Chengam-ro, Nam-gu, Pohang 37673, Republic of Korea

§ Division

of Integrative Biosciences and Biotechnology, Pohang University of

Science and Technology (POSTECH), 77 Chengam-ro, Nam-gu, Pohang 37673, Republic of Korea

|| Department

of Physics and Research Institute of Natural Science, Gyeongsang

National University, Jinju 52828, Republic of Korea

ACS Paragon Plus Environment

Langmuir 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

KEYWORDS: cation- interaction, mussel adhesive protein, mussel foot protein, complex coacervate, surface forces apparatus (SFA)

ABSTRACT Mussel underwater adhesion is a model phenomenon important for the understanding of broader biological adhesion and the development of biomimetic wet adhesives. The catechol moiety of 3,4-dihydroxyphenyl-L-alanine (DOPA) is known to be actively involved in the mechanism of mussel underwater adhesion; however, other underwater adhesion mechanisms are also crucial. The surface forces apparatus (SFA) has often been used to explore the contributions of other mechanisms to mussel underwater adhesion, e.g., recent SFA-based nanomechanical studies have revealed that cation- interactions, one of the strongest intermolecular interactions in water, are the pivotal interactions of adhesive proteins involved in underwater mussel adhesion. This review surveys recent research on cation- interactions and their contributions to strong mussel underwater adhesion, shedding light on some biological processes and facilitating the development of biomedical adhesives.

1. Introduction

ACS Paragon Plus Environment

Page 2 of 46

Page 3 of 46 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Langmuir

Mussels effectively engage in underwater adhesion to wet substrates by secreting a proteinaceous thread-like structure called byssus.1-2 Proteins involved in this adhesion are termed mussel foot proteins (mfps), as byssus is mainly produced in the mussel foot, and have been extensively studied to model adhesion in water.3-6 The various mfps discovered during the 40-year research on mussel adhesion often contain 3,4-dihydroxy-L-phenylalanine (DOPA), a post-translationally modified amino acid derived from tyrosine (Tyr).7 DOPA has been proven to be the most important moiety for mussel underwater adhesion by a variety of scientific methods, and the catecholic moiety of DOPA has been used to generate numerous mussel-inspired polymers as wet adhesives or universal coatings for a variety of applications.8-16 However, DOPA easily loses its adhesion ability at neutral to basic pH or in the presence of oxygen, while the catechol moiety of DOPA is poorly stable under conditions relevant to seawater.17-18 Therefore, work to elucidate other mechanisms of mussel underwater adhesion has been continued, and recent biochemical, nanomechanical, and spectroscopic studies suggest complex coacervation involved in the liquid-liquid phase separation (LLPS) of mfps,19-24 thiol-based redox chemistry

ACS Paragon Plus Environment

Langmuir 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

for controlling the oxidation of DOPA in cross-linking,18, 25-26 and cation- interactions in mfps20, 23-24, 27-28 as known possible contributors to adhesion. To date, more than 20 types of mfps have been discovered, and studies on their localization and functions in byssus are ongoing.16, 29 As most mfps contain DOPA and are rich in cationic and aromatic amino acids (Figure 1), they have been termed polyphenolic basic proteins, with most of them being cationic polyelectrolytes at neutral and basic pH.

Figure 1. Amino acid compositions of mfps isolated from Mytilus californianus.6, 29-32

Cationic polyelectrolyte proteins are highly water-soluble and appear to be a counterproductive choice for adhesion in aqueous media, as they are dispersed and diffused away at the moment of their secretion into seawater.33-34 So, how can mussels achieve successful underwater adhesion using these proteins? Some relevant clues can be found in the works of Bungenberg de Jong, who discovered and studied complex coacervates at the beginning of the 20th century.35 Complex coacervation is

ACS Paragon Plus Environment

Page 4 of 46

Page 5 of 46 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Langmuir

an LLPS phenomenon that occurs when oppositely charged polyelectrolytes are dissolved in water at a specific pH and ionic strength (Figure 2). During complex coacervation, most participating polyelectrolytes assemble into dense polyelectrolyterich droplets, the so-called complex coacervates, while the droplet exterior becomes depleted in polyelectrolytes. The concentration of polyelectrolytes in the dense coacervate phase ranges from about 200 to 4000 mg/mL.36-39 In addition, as complex coacervate droplets generally have a very fragile interface (interfacial energy between 3 mN/m and 1 m/m),22-23,

36, 40-44

their collisions afford the droplets to grew from

micro- to mesodroplets, eventually resulting in bulk macrophase separation (Figure 2).

Figure 2. Schematics of complex coacervation of positively charged polyelectrolytes (poly-Llysine) and negatively charged polyelectrolytes (hyaluronic acid). Yellow color comes from additionally added fluorescein.

ACS Paragon Plus Environment

Langmuir 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

The complex coacervate concept can be used to explain the secretion of mfps. That is, the spontaneous occurrence of coacervation prevents cationic polyelectrolyte mfps from dispersing and disappearing in seawater upon secretion, with the concentration of mfps in the coacervate phase reaching values of ~2000 mg/mL. In addition, the low interfacial energy of the coacervate assists wetting and the infiltration of the coacervated adhesive into rough target surfaces while enhancing the area of contact to facilitate adhesion. Finally, the DOPA residues of mfps form chemical cross-links with neighboring chemical functional groups at seawater pH (~8.2) or engage in DOPA-metal coordination to solidify the adhesive and realize successful underwater adhesion for mussel attachment. Most mussel adhesive proteins characterized so far are cationic polyelectrolytes, whereas anionic polyelectrolytes have not yet been discovered in mussel adhesive plaque, which poses the question of whether the complex coacervation principle is applicable to the phase separation of mussel adhesive proteins.29 The abundance of aromatic residues in the primary structure of mfps suggests one clue to answer this question. Dougherty and colleagues suggested cation- interactions as one of the

ACS Paragon Plus Environment

Page 6 of 46

Page 7 of 46 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Langmuir

strongest intermolecular interactions in aqueous media and demonstrated their contributions in biomolecules.45-51 Recently, the surfaces forces apparatus (SFA) has been used to demonstrate the high strength of cation- interactions and their reversible formation in water.27-28, 52-54 In this review, we briefly summarize the current knowledge on cation- interactions and SFA use for the characterization of cation- interactions in aqueous media and for probing the contribution of these interactions to mussel underwater adhesion.

2. Cation- interactions 2.1. Theoretical background

Figure 3. Cation- interaction between benzene and cation. Cation- interactions are non-covalent interactions occurring between the face of an electron-rich -system (e.g., benzene, indole, or phenol) and a cation (Li+, Na+, K+,

ACS Paragon Plus Environment

Langmuir 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

NH4+) (Figure 3). Kebarle’s group found that in the gas phase, K+ ions prefer bonding to benzene than to water55 and showed that the largest contributions to binding energy are ion-induced dipole and ion-quadrupole attractions, with other contributions such as those of dispersion and electronic repulsion being minor. Subsequent studies verified that the above trend holds not only for K+, but also for other ions such as Li+ and Na+,56-57 revealing that smaller ions with a large charge density have larger gasphase binding energies, which decrease in the order of Li+ > Na+ > K+ and Be2+ > Mg2+ > Ca2+, while the reverse order is observed for monovalent cations in water. Dougherty termed this interaction “cation-” interaction to distinguish it from the already known “-” interaction.58-59 Cation- interactions exhibit extraordinary properties in aqueous environments. In general, molecules can be classified as either hydrophilic or hydrophobic; in the latter case, the surface hydrogen bond network of water is different from that in the bulk. Cations feature a strongly held hydration shell which prevents the overly close approach of other polar molecules,60 and the distance between a given cation and other polar particles is limited by the thickness of the hydration shell unless the

ACS Paragon Plus Environment

Page 8 of 46

Page 9 of 46 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Langmuir

concentration of these particles is too high. Beyond this distance, water molecules weaken electrostatic energy, which significantly reduces the overall electrostatic interaction. Typical hydrophobic molecules are non-polar and therefore undergo selfaggregation but do not interact with ions. However, the hydrophobic but weakly polar -electron cloud is a quadrupole and can therefore form an induced dipole in response to the approach of cations.61 As a result, cation- interactions are negligibly weak at distances exceeding several hydration shell thicknesses but become very strong at smaller separations. The short-distance electrostatic attraction, which is significantly enhanced by the hydrophobicity of the -electron cloud, is the main cause of cation- interactions. Therefore, quantum mechanical simulations were applied to accurately calculate the strength of such interactions, and the obtained results were found not to depend on the level of theory but only on the nature of the cation and the -system.62 Cation-π interactions are strongly affected by both substituents on the aromatic ring and its constituents.63-64 Dougherty et al. compared the effects of substituents on πsystem–Na+ interactions,46 showing that the strength of these interactions depends on

ACS Paragon Plus Environment

Langmuir 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

electrostatic potential in an almost linear way. This implies that despite the importance of dispersion and induced dipole effects, cation- interactions are mainly governed by electrostatics, in agreement with Kebarle’s findings.55 However, the experimental cation- interaction strengths are always slightly higher than those predicted by electrostatic potential (ESP).65 It means substituents effect is still important, as nature utilizes modifications as the driving force in various chemical and biological systems.66 The effect of cations is just as important as that of -species. Remarkably, the trend observed for ion binding strength in the aqueous phase is opposite to that in the gaseous phase for monovalent cation. The strength of such bonds decreases in the order of K+ > Na+ > Li+ which agrees well with the order in Hofmeister series.59, 67 The origin of this specific ion-dependent effect in water is still unclear; however, there is a consensus that large monovalent cations in water form fragile hydration shells. For this reason, larger cations are easier to make a bond with π-species to overcome resistance from their first hydration shell. Nevertheless, the trend observed for divalent cations does not significantly change, as in this case, the electrostatics is dominant

ACS Paragon Plus Environment

Page 10 of 46

Page 11 of 46 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Langmuir

and hence the strength of cation-π bond is much stronger than that of monovalent one. Although quantum mechanical approaches are more accurate, they are very computationally expensive and hence, are not suitable for the simulation of large systems. Fortunately, as electrostatic interactions are the main contributor to cation- interactions, even non-polarizable classical force fields work quite reasonably. Sussman et al. showed that cation- interactions in a trimethylammonium-benzene system can be moderately reproduced without polarizable terms and with little modification of the atomic charges of cations in existing force fields.68 However, Orozco et al. claimed that the polarization effect is essential for reflecting the properties of the aromatic core65 and performed quantification to a generalized molecular interaction potential with polarization that may alternate molecular electrostatic potential.69 Later on Kollman, Lamoureux, Khan and others improved the classical force field models to better describe the cation- interactions.70-72 Although these classical models allow one to deal with larger systems, they are still not suited for the simulation of phase transitions such as the coacervation of positively

ACS Paragon Plus Environment

Langmuir 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 12 of 46

charged mussel adhesive proteins (so called like-charged proteins), as the phase transition itself is defined in the thermodynamic limit and the corresponding energy barrier is very difficult to overcome. Kim and his colleagues combined theoretical analysis and simulation to explain the cation- interaction– induced phase separation of like-charged proteins.23 In particular, they developed a Landau Wilson–type coarsegrained field theory in terms of the order parameter to reflect the system phase and used short-range attraction and long-range repulsion for model potentials. A DebyeHückel screening potential was adopted as the repulsion part. To obtain short-range attraction that integrates cation- interactions, hydrophobic attraction, etc., they performed quantum simulations, and approximation was performed using well-known functions that can be handled analytically. As a result, they found that macroscopic phase separation can be induced either by increasing the attractive strength or by reducing the repulsion decay length. Experimentally, one can increase attraction by introducing

poly(2-methacryloxyethyltrimethylammonium

chloride)

(MADQUAT),

which engages in strong cation- interactions with lysine (Lys),23 while the decay length can be reduced by increasing salt concentration.24

ACS Paragon Plus Environment

Page 13 of 46 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Langmuir

2.2. Spectroscopic evidence of cation-π interactions in solution In the 1980s, i.e., before cation- interactions were recognized, Deakynet and MeotNer used high-pressure mass spectroscopy to show that cations strongly bind to simple aromatic molecules in the gas phase.73-74 In 1986, Perutz suggested the existence of an amino-aromatic interaction in a protein crystal structure based on the results of X-ray studies,75 while other crystal structure analyses demonstrated that aromatic residues prefer to be in close proximity to cationic residues.76-78 Since the term “cation- interaction” was coined, this non-covalent interaction has been considered to be highly important in biological systems. According to computer simulations, cation- interactions are expected to be about two times stronger than electrostatically attractive salt bridges in aqueous media48 and are therefore one of the most important non-covalent interactions modulating bio-specific binding. To better understand the role of cation- interactions, researchers used techniques such as Xray crystallography, NMR spectroscopy, UV-vis spectroscopy, Raman spectroscopy, and circular dichroism (CD) spectroscopy.

ACS Paragon Plus Environment

Langmuir 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Considering biological conditions, cation- interactions are expected to be significant in aqueous solutions, whereas the related experimental studies have mainly focused on gas and solid phases, as the identification of cation- interactions in aqueous media is not easy. For example, in addition to that of cation- interactions, molecular binding features the contributions of many other interactions such as hydrogen bonding and hydrophobic ones, which makes it difficult to single out a specific description of cation- interactions in solution. Moreover, the signals attributable to cation- interactions are relatively weak to be detected by routine spectroscopic techniques, as these interactions are affected by solvation in the aqueous phase. Given that molecules with -electron systems are often insoluble in aqueous media, another challenge is finding a proper cation- model system with a water-soluble -acceptor. In view of these difficulties, reports describing spectroscopic markers for characterizing cation- interactions in solution are very scarce, and some of these interactions have not been studied in aqueous solution. Pletneva et al. investigated a model peptide by 2D NMR spectroscopy, demonstrating the presence of cross-peaks

ACS Paragon Plus Environment

Page 14 of 46

Page 15 of 46 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Langmuir

between the protons of Lys and Tyr (or phenylalanine (Phe)),79 while Tsou et al. used 2D NMR to provide evidence of cation- interactions between a phenyl ring and an amine.80 Unlike the above researchers, who employed NMR spectroscopy to detect spatial proximity, Takeuchi et al. reported unusual intensity changes of the indole ring vibration in UV resonance Raman (UVRR) spectra, attributing these changes to interactions between K+ and the indole ring in the indole crown ether model and to those between His31 and Trp41 in M2-TMP ion channels.81 Several years later, UVRR spectroscopy was used to probe the indole crown ether model by Schlamadinger et al., who additionally observed that the vibrational modes of the indole ring, especially W18 and HOOP ones, were sensitized when the indole ring interacted with cations such as Na+, K+, or NH4+.82 Although UVRR markers for cation- interactions were suggested in the above work, the model system (indole crown ether) was still evaluated in an organic solvent. Another remarkable spectroscopic finding pertains to transition metal cation- interactions in aqueous solution. For example, Xue et al. revealed interactions

ACS Paragon Plus Environment

Langmuir 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

between a tryptophan residue of the CusF protein and Cu+/Ag+ based on wavelengthdependent intensity changes and vibrational mode frequency shifts in UVRR spectra,83 while Takeuchi et al. used CD spectroscopy to show that the cation-π interaction of Cu2+ with a tryptophan residue in a model peptide results in the appearance of a negative band at 223 nm.84

2.3. SFA-provided nanomechanical evidence of cation- interactions in solution To directly measure the forces involved in cation- interactions, Lu et al. employed the SFA,54 which is an ultrasensitive nanomechanical technique widely used to measure the normal or lateral force (F) between two opposing surfaces as a function of separation distance (D) in the presence of various media including gases and liquids. Moreover, a distance resolution of