Robust Alginate-Catechol@Polydopamine Free-Standing Membranes

Feb 15, 2017 - The use of either small molecules (urea, pyrocatechol) or polymers paves the way to understand which kind of compounds can be used for ...
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Robust alginate-catechol@polydopamine free-standing mem-branes obtained from the water/air interface Florian Ponzio, Vincent Le Houérou, Spyridon Zafeiratos, Christian GAUTHIER, Tony Garnier, Loic Jierry, and Vincent BALL Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.6b04435 • Publication Date (Web): 15 Feb 2017 Downloaded from http://pubs.acs.org on February 19, 2017

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Robust alginate-catechol@polydopamine free-standing membranes obtained from the water/air interface Florian Ponzio 1, Vincent Le Houerou 2, Spyridon Zafeiratos3, Christian Gauthier2,, Tony Garnier2 Loic Jierry 2, Vincent Ball1,4,* 1: Institut National de la Santé et de la Recherche Médicale, Unité MIxte de Recherche 1121 11 rue Humann, 67085 Strasbourg Cedex, France. 2. Université de Strasbourg, Institut Charles Sadron, Centre National de la Recherche Scientifique, Unité Propre 22 23 rue du Loess, 67034 Strasbourg Cedex 2, France. 3. Institut de Chimie des Procédés pour l’Energie, l’Environnement et la Santé(ICPEES) ECPM, University of Strasbourg, 25 rue Becquerel Cedex 2, 67087 Strasbourg, France 4: Université de Strasbourg, Faculté de Chirurgie Dentaire, 8 rue Sainte Elizabeth, 67000 Strasbourg, France.

*Corresponding author: [email protected]

KEYWORDS:. Free standing membranes, alginate-catechol, stimuli responsiveness, adhesion, polydopamine.

ABSTRACT: The formation of polydopamine composite membranes at the water/air interface using different chemical strategies is reported. The use of either small molecules (urea, pyrocatechol) or polymers paves the way to understand which kind of compounds can be used for the formation of PDA-composite free-standing membranes produced at the water/air interface. Based on these screening results, we have found that alginate grafted with catechol groups allows the formation of robust free-standing films with asymmetric composition, stimuli-responsive and self-healing properties. The stickiness of these membranes depends on the relative humidity and its adhesion behavior on PDMS was characterized using the JKR method. Thus, alginate-catechol polydopamine films appear as a new class of PDA composites, mechanically robust through covalent crosslinking and based on fully biocompatible constituting partners. These results open the door to potential applications in the biomedical field.

Introduction Inspired by mussels and their unique way to attach to all kinds of materials under wet conditions, polydopamine and more generally catecholamine based films have been widely used in various areas of research1-4 One main reason for this spectacular success is the possibility to form thin films on the surface of all kind of materials, even on Teflon, by using a simple dip coating method in a slightly alkaline dopamine solution5. This procedure presents some drawbacks like the low thicknesses of the resulting films, their brittle nature and a time consuming synthesis (several hours). Currently, improvements of the preparation method of PDA films are intensively investigated6-8. A second important reason explaining this enthusiasm stays in the different ways to get PDA films from solid/liquid but also liquid/liquid interfaces.

Currently, PDA films are widely used for their biocompatibility9, for energy conversion, environmental applications11 and mostly as a support layer for postfunctionalizations12-14. In addition, PDA can also be obtained as grains from the centrifugation of the dopamine solutions having undergone oxidation. Those grains have found applications as catalysts15-16 or as adsorbents for the selective removal of copper(II)17. Finally PDA was also used to produce hollow capsules from the solid/liquid interface18 by using sacrificial silica templates or from the liquid/liquid interface with oil emulsion in water19 for drug delivery.20 However, the water/air interface has so far been little studied to get PDA based films. Our team has demonstrated that the PDA film formation at the water/air interface arises from a heterogeneous nucleation process21 where amphiphilic species are created from the oxidation of dopamine which is a polar highly water soluble molecule. Those PDA films produced at the water/air interface

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could be transferred by the Langmuir-Schaeffer method on different substrates. Even if the film produced at the water/air interface can be transferred on solid substrates, some cracks appeared during the process and the film was not stable when the vessel was slightly shaken. To circumvent this mechanical fragility of PDA films obtained from the water/air interface, other groups have designed “composite” PDA based films. They added poly(ethylene imine) (PEI) in the subphase containing dopamine in order to chemically crosslink PDA during its formation at the water/air interface, leading thus to composite PDA based films. Xui’s group used low molecular weight PEI (600 g/mol)22 providing free-standing films with thickness ranging from 80 nm up to 1 µm depending both on the dopamine/PEI ratio used in solution and on the reaction time. Higher molecular weight PEI (750 kDa)23 allowed to produce a membrane with a thickness of up to 40 µm. Both membranes described were Janus-like, i.e. one face rich in PDA whereas the other face was PEI rich. Those films also displayed self-healing properties and stimuli responsivity to water after an initial drying step. However, these two studies showing the possibility to produce stable PDA polymer composite membranes at the water/air interface rely on the same polymer, namely PEI. Owing to the almost limitless possibilities of adding cross-linkers able to bind to PDA in the subphase, it is crucial to pave the way to a rationale method for the formation PDA-composite free standing membranes at the water/air interface. This implies to investigate a large repertoire of molecules able or not to interact with PDA. In this study we have investigated the influence of small molecules and of different polymers as possible crosslinkers during the PDA formation at the water/air interface in order to get a better idea on the optimal structure of robust PDA membranes at the water/air interface. Since PDA formation is based on different kinds of interactions (covalent bonds, hydrogen bonds, Π-stacking or metal coordination), the selection of potential crosslinkers interacting through hydrogen bonds, coordination bonds or covalent bonds between PDA particles have been tested. A selection among the chosen molecules led us to the use of alginate-catechol (Alg-CAT), i.e. sodium alginate grafted with catechol groups, as an efficient covalent cross-linker. Such a polymer has already been used to crosslink alginate based gels in the absence of calcium cations. 24 The measurement of the membrane thickness, its self-healing properties, and its stimuli responsiveness to water were studied and are reported herein. Materials and Methods Chemicals were used as received without further purification. Dopamine hydrochloride (Product No: H8502, CAS: 62-31-7), Pyrocatechol (Product No:C9510; CAS: 120-80-9), Poly(allylamine hydrochloride) (PAH, Product No: 283215-25g; CAS: 71550-12-4), poly(diallyldimethyl ammonium chloride) (PDADMAC, Product No: 409022-1L; CAS: 120-80-9), Copper sulfate (Product No: 61230, CAS: 7758-98-7), Alginic acid sodium salt from brown algae (Product No: A2033, CAS: 9005-38-

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3) and sodium periodate (Product No: 311448, CAS: 779028-5) were purchased from Sigma-Aldrich and used without further purification. Ammonium peroxodisulfate (Product No: 1257273, CAS: 7727-54-0) was purchased from Fluka. Tris(hydroxymethyl) aminomethane (Tris, Product No:200923-A, CAS: 77-86-1) was obtained from EURODEMEX. Anhydrous sodium acetate (Product No: 6268) and Urea (Product No: 0044631; CAS: 57-13-6) were purchased from Merck. Alginate catechol (Alg-CAT) was prepared according to the procedure reported elsewhere. 24,25 The degree of substitution of catechol groups on alginic acid was 10% as determined from NMR spectroscopy. Polydopamine films at the water/air interface Dopamine hydrochloride at 2 mg.mL-1 and PAH, PDADMAC, or urea at different concentrations were dissolved in Tris buffer at 50 mM, pH = 8.5 with oxygen as the oxidant. Dopamine and pyrocatechol at 2 mg.mL-1 were dissolved in sodium acetate buffer at 50 mM, pH = 5 with sodium copper sulfate 20 mM as the oxidant. The solutions were left unstirred for 24 hours of reaction. Sodium alginate and Alg-CAT were dissolved in Tris buffer 50 mM, pH = 8.5 and stirred for 3 h. During that time, the solutions became slightly brown due to a slow oxidation of the catechol groups on the polymer. Then dopamine hydrochloride (at 2 mg.mL-1) was added to the solution and left unstirred for 24 h. Once the membrane formed at the water/air interface it was detached from the vial with a scalpel blade and deposed on a PTFE plate for drying overnight at 37 °C. Description of the JKR technique and experiments The Johnson-Kendall-Roberts (JKR) adhesion test consists in detaching the contact between an elastomeric hemisphere and a planar substrate of interest deposited on a rigid slide. The force is continuously monitored along the test thanks to a sensor connected to the movable punt form on which the hemisphere sample is attached. The value of interest is the force needed to detach the contact, named pull-off force, and is given by the JKR theory 26 where W is the work of adhesion and R is the radius of the hemisphere. ଷ

ܲ௢௙௙ = − ߨܹܴ (1) ଶ

A scheme representing this specific setup is reported in Figure 1. Additional experimental details can be found elsewhere.27

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Langmuir from 0.1 to 0.4 V (Figure SI2) influence the measurement of the pull off force. We can observe an increase of the pull off force when the frequency increases (Figure SI1) which is similar to an increase of the viscosity of the material. In addition when the amplitude increases (Figure SI2) the pull off force increases which can indicate that the material is pressure sensitive. But most probably only the slope of the sinusoid increases with the increase in amplitude. To simplify we will take a low and constant amplitude and frequency for the rest of the measurements which gives the lowest standard deviation, respectively 0.1V and 0.2 Hz. Cross-sectional imaging of a membrane produced after 24 h in the presence of Alg-CAT at 20 mg.mL-1 was obtained after embedding the membrane between two epoxy resin layers using a Quanta 200 Field Effect Gun Scanning Electron Microscope (Philips-FEI).

Figure 1: Schematic representation of the experimental “dynamic JKR” device used to perform pull-off tests.

After application of an initial force, the setup records the evolution of the oscillating load ΔP as a response to the imposed oscillating displacement of the hemisphere. The stability of the cycles is systematically checked over 4 cycles. The main drawback of this technique is that the results, in terms of work of separation, do not permit to assess the surface energy as defined in the Young-Dupré equation (see eq. 2) since this latter is valid for an ideal reversible equilibrium test and exceeds it when dissipation processes occur. ܹ = ߛଵ ൅ ߛଶ − ߛଵଶ

(2)

where ߛଵ and ߛଶ are the material/ air surface tensions of both materials 1 and 2 respectively and ߛଵଶ is the surface tension of the 1-2 interface. However, the pull-off technique may be a convenient test in order to distinguish the contact performances of soft matter surfaces. Indeed, while using the same hemisphere as a probe, it allows comparing the adhesion performance of a specimen depending on test conditions (imposed frequency, loading amplitude, environmental moisture, etc) or to discriminate different planar samples as demonstrated by Moreno-Couranjou et al.28 on patterned surfaces. The radius of the hemisphere used here is equal to 12.5 mm. First we tested which parameters (frequency, amplitude) were the best for our system at a fixed relative humidity of 30% at room temperature where the membrane remain in a dry state. We investigated how the frequency ranging from 0.02 to 2 Hz (Figure SI1) and the amplitude ranging

The X-ray photoelectron spectroscopy (XPS) measurements were carried out in an ultrahigh vacuum (UHV) spectrometer equipped with a VSW Class WA hemispherical electron analyzer. A monochromatic Al Kα X-ray source (1486.6 eV) was used as incident radiation. Survey and high resolution spectra were recorded in constant pass energy mode (90 and 44 eV, respectively). The C 1s

peak at 285 eV was used as an internal reference of the binding energy scale. The infrared spectra of both sides of a 80 µm thick membrane were measured in the ATR mode with a Spectrum Two spectrophotometer (Perkin Elmer) at a resolution of 2 cm-1. Results and discussion In all the experiments, dopamine (2 mg.mL-1) was dissolved in 50 mM Tris buffer at pH = 8.5 with oxygen as the oxidant, except when we dissolved dopamine and pyrocatechol (both at 2 mg.mL-1). In this later case, the experiments are performed in a 50 mM sodium acetate buffer at pH = 5.0 with copper sulfate (40mM) as the oxidant. As reported previously, without the addition of an oxidative reagent in solution, no PDA film is formed at the water/air interface.21 The chemical structure, molecular weight, and the concentration range of the species added to the dopamine solutions (called “subphase”) are given in Table 1. A picture showing the state of the solutions after 24 h of oxidation is also given in Table 1. The following adjuvents to PDA have been used: (i) small molecules such as urea and pyrocatechol, (ii) polyelectrolytes such as poly(allylamine hydrochloride) (PAH), poly(diallyldimethylammonium chloride) (PDADMAC), sodium alginate and sodium alginate modified with catechol groups.24,25 Urea has four hydrogen bond donors and two acceptor groups, explaining is high solubility in water (1080 g.L-1 at 20°C). Hence, it was anticipated that urea could form hydrogen bonds with catechol and quinone groups during the formation of PDA in solution as well as at the water/air interface. An increase in urea concentration (up to

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600 mg.mL-1) allowed to stabilize a PDA based colloidal suspension, whereas PDA precipitates out from the solution in the presence of urea at 100 and 200 mg.mL-1 (Table 1, entry 1). In all cases, urea impedes the formation of a PDA film at the water/air interface. It is not a good adjuvant to form more robust PDA based membranes. Pyrocatechol (Table 1, Entry 2) is expected to strengthen the structure of PDA not only through hydrogen bonds but also through π-staking interactions as well as aryl-aryl coupling. In addition, the presence of metallic cations in solution such as Cu2+ can also contribute to the PDA membrane stability through coordination bonds with catechol groups of PDA, playing the role of ligands. 29 The combination of pyrocatechol and dopamine (both at 2 mg.mL-1) with 40 mM copper sulfate in acetate buffer at pH = 5 led to the formation of a completely different membrane than the one obtained with dopamine alone (in Tris buffer at pH = 8.5): In addition the oxidized dopamine solution is brown in Tris buffer whereas the pyrocatechol/dopamine solution is deep dark blue in the sodium acetate buffer (Figures 2a and 2b). The appearance of the membranes formed at the water/air interface differ in both cases: the membranes formed from dopamine alone are shiny whereas the membranes formed from the pyrocatechol/dopamine mixture are rough and dark (Figures 2c and 2d). The pyrocatechol-dopamine membranes can withstand solution stirring up to 500 rpm without apparent rupture whereas those produced from a solution containing only dopamine crack already at 300 rpm (Figures 2e and 2f). Moreover, waves on the pyrocatechol-dopamine membrane are observed during the stirring process. Hence, the addition of pyrocatechol to dopamine solutions increases the mechanical resistance of the membranes with respect to shear stresses. However, even by changing the pyrocatechol/dopamine molar ratio from 1/3 to 3/1, and by using different oxidants (sodium periodate, ammonium persulfate instead of Cu(II)), the resulting PDA membranes are too fragile to be transferred onto a solid substrate.

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Table 1: Chemical structure and molecular weight of the different adjuvents co-dissolved with dopamine at 2 mg.mL-1. Last column: pictures of the different dopamine+ adjuvant solutions after 24h of reaction.

Figure 2: Pictures of the (a) dopamine solution and (b) pyrocatechol/dopamine solution when the PDA membrane is formed at the water/air interface after 24h of reaction. Pictures of the PDA membrane formed at the water/air interface from (c) dopamine solution and (d) pyrocatechol/dopamine solution at rest and after stirring, (e) and (f), respectively.

We then tested the influence of two different polycations with two different kinds of amino groups (Table 1, Entries 3 and 4): namely PAH bearing primary amines and PDADMAC carrying quaternary ammonium groups. As mentioned above, PEI has been already successfully used to get PDA membranes from water/air interface. 22,23 We expected that PAH could also stabilize the PDA membranes because polyamines can form covalent bonds with PDA through Michael addition or Schiff base (imine) formation.12 In addition, the pKa of 1,2-catechol units is 9.25,30 meaning that when PDA is formed at pH 8.5, some phenolate groups are generated and the PDA films is negatively charged.31 Therefore, the positive charges of PAH could also contribute for attractive electrostatic interactions with the PDA membrane. Surprisingly, when the concentration of PAH in the dopamine solution is increased from 1 to 10 and then to 20 mg.mL-1, a fading of the brown color of the solution is observed and no membranes are formed, even after 24h. We already found that PAH allows to form PDA nanoparticles with decreasing size when the PAH/dopamine ratio increases, with a simultaneous inhibition of PDA deposition at the solid/water

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interface. 32 Hence these PDA@PAH nanoparticles do not self-assemble at the water/air interface. In the case where PDADMAC is added in the dopamine solution, whatever its concentration from 10 to 100 mg.mL-1, the resulting solution becomes dark indicating the formation of PDA but no membrane formation is noticed at the water/air interface. We postulate that the PDA particles are capped with PDADMAC or PAH 32 impeding their subsequent self-assembly through electrostatic repulsion. It must be noted that PAH and PDADMAC are both linear polymers compared to the branched PEI used in previous works.22,23 In conclusion of this screening process of potent PDA stabilizers at the water/air interface, it appears that pyrocatechol is the most promising chemical entity to get a PDA membrane at the water/air interface, whereas urea and the two investigated polycations do not allow to form a membrane at all. To improve the mechanical stability of the membranes formed at the water/air interface, we assume that pyrocatechol moieties would be more efficient as a crosslinker if they would be linked to a polymer chain in order to create covalent bridges between isolated PDA clusters. Recently, alginate has been covalently modified with pyrocatechol groups 24,25, providing an alginate-catechol polymer (Alg-CAT). This modified biopolymer has been successfully used for biomedical applications.33 Alg-CAT was mixed with dopamine at 2 mg.mL-1 in a Tris buffer at pH = 8.5 and the resulting film was compared with the one obtained using unmodified sodium alginate (Figure 3a and 3b). NaIO4 was not used as an oxidant of dopamine-Alg-CAT mixtures or natural sodium alginate because this strong oxidant may oxidize or damage the polymer, rich in hydroxyl groups able to be oxidized in aldehydes. For both alginate and Alg-CAT, we observed an increase of the dark color close to the water/air interface (Figures 3c and 3d). However, only the membranes formed with Alg-CAT stick strongly to the vial and are able to withstand the weight of the subphase when the vial is turned upside down (Figure 3f). In the presence of unmodified sodium alginate, the films formed at the water/air interface are not robust enough to withstand the weight of the solution meaning that unmodified alginate is unable to strengthen the PDA based membranes (Figure 3e). The UV-visible spectra of the subphase with dopamine and Alg-CAT are homothetic of those of the AlgCAT solution (Figure 3g). Finally, only the addition of Alg-CAT to the dopamine solution allows the formation of a free standing membrane. The most mechanically stable and easy to handle membrane is obtained for a concentration of 20 mg.mL-1 in Alg-CAT. Below this value, the PDA@Alg-CAT membrane is really sticky and very difficult to handle and above a concentration of 30 mg.mL-1 a hydrogel is formed in the whole vial containing Alg-CAT and the dopamine solution. This finding is in agreement with the gelation ability of catechol modified polymers. 24,33

Figure 3: Chemical structures of (a) sodium alginate and (b) AlgCAT. Pictures of (c) sodium alginate and (d) Alg-CAT solutions after 24 h of oxidation. Pictures of an alginate (e) and an AlgCAT (f) membrane sticky to the vial. (g): UV-Vis spectra of the solution containing both Alg-CAT and dopamine in the subphase and Alg-CAT solution alone after 24h of reaction. (h) Schematic representation of the covalent cross-links formed between AlgCAT and PDA aggregates.

We assume that the PDA@Alg-CAT membrane formed at the water/air interface acts as a barrier for oxygen explaining its exclusive formation there and the limitation of its growth in deeper parts of the solution. The diffusion of oxygen from the air to the subphase through the interface allows the oxidation of catechol groups, both from PDA and Alg-CAT, leading to a high local concentration of reactive quinone species in close vicinity to the interface. Thus PDA particles are formed and then aggregate to finally be crosslinked together with Alg-CAT through aryl-aryl coupling reactions. A schematic representation of this possible mechanism of the Alg-CAT membrane formation is given in Figure 3h. Once the composite membrane is formed, the diffusion of O2 in the deeper part of the solution may be slowed down and the growth of the film is stopped or slowed down. Similarly to the membranes obtained with PEI23, the PDA@Alg-CAT membranes display self-healing properties. When they are cut with a scalpel or torn, a complete self-healing of the cut or separated pieces of the PDA@Alg-CAT film is observed after 24h. Furthermore, once the PDA@Alg-CAT film is removed from the water/air interface, a new film identical to the first one is formed. This operation can be repeated, until there is no solution left in the reaction vessel. This finding strongly corroborates our assumption that the as formed membrane slows down the diffusion of O2 in deeper parts of the solution: as soon as the membrane is peeled off, the exposed solution is again exposed to ambient air, O2 is available at the maximal possible partial pressure 34 and the formation of the membrane is reinitiated. The dried composite membranes are stimuli-responsive to water: when put in contact with water they start to swell and begin to roll up to form a tube (Figure 4a). This may be an indication of an asymmetric membrane com-

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a distance of several times the penetration depth of the IR beam in the film, namely a few µm. It is hence not surprising that the IR spectra of both sides of the PDA@Alg CAT appear almost identical (Figure SI3) with two family of peaks. The first collection of peaks located between 1000 and 1300 cm-1 attributed mainly to C-O stretching vibrations in alginate and the second family of peaks between 1300 and 1700 cm-1 originating mainly from catechols and amides. It has to be noted however that the ATR-IR spectra of both sides of the membrane are markedly different from the reference spectra of PDA films obtained in the same conditions (Tris buffer at pH = 8.5, O2 as the oxidant). 35 The composition of PDA in PDA@Alg-CAT membranes may hence be different from that in pristine PDA films produced in the same conditions. This deserves further investigations. However the sampling depth of XPS spectroscopy is restricted to the outer 2-5 nm of the sample surface and allows to distinguish differences on the surface species. Deconvolution of the N1s XPS spectrum using 3 N 1s components 36, showed that the N-C=O/ pyrrolic peaks area ratios are 4.4 for the mat side and 1.8 for the shiny one. Hence, the shiny side of the membrane is significantly enriched with nitrogen atoms belonging to pyrrole groups which are characteristic to 5,6-dihydroxyindole structures formed upon the oxidation of dopamine. Simultaneously the shiny side of the membrane is relatively depleted in nitrogen atoms belonging to amide groups. These amide nitrogens originate from the Alg-CAT polymer (see Figure 3b).

NC =O

position resulting in a differential swelling on its two faces. During this process, the membrane became sticky at small hydration levels and could be glued on different materials but when the amount of water was progressively increased, they detached from the substrate and formed tubes. To quantify the adhesion of PDA@Alg-CAT membranes we used the Johnson-Kendall-Roberts (JKR) method 26 in a sealed chamber where the relative humidity could be varied (Figure 1). The JKR method allows to measure the pull-off force between our membrane and a PDMS semi-sphere at a controlled relative humidity.

First we investigated how the different sides of the membrane affect the pull-off force at constant relative humidity of 30%.(Figure 4d). The PDA rich side (which is shiny in the dry state), the face previously exposed to air, of the membranes display a pull-off force almost two times higher than the Alg-CAT rich side (which appears as mat in the dry state) of the membrane: respectively 0.022 N and 0.012 N (Figure 4d). Our results are in agreement with those obtained using PEI23 where a PDA rich layer is preferably formed at the water/air interface at the first stage of the reaction. Another proof of the membrane asymmetry is obtained from the SEM cross-sectional image of a dry membrane (Figure 4b): two different domains can be observed on an approximately 80 µm thick membrane. This membrane anisotropy is also confirmed on the compositional level by means of XPS spectroscopy (Figure 5) but not by means of ATR-IR spectroscopy (Figure SI3). ATR-IR spectroscopy probes the membrane over

N -O

Figure 4: (a) Pictures representing the responsivity of the PDA@Alg-CAT membranes to the addition of water. (b) SEM images of the dry membrane obtained from an Alg-CAT solution at 20 mg.mL-1 and (c) its UV-visible spectrum. Pull off data of (d) PDA@Alg-CAT membrane at different concentrations in AlgCAT depending on the side of the membrane (30% relative humidity) and (e) pull off data as a function of the relative humidity.

py rr ol ic

A

XPS I ntensity (a.u.)

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mat

B

shiny 406

404

402

400

398

396

Binding Energy (eV)

Figure 5: High resolution N1s XPS spectra of both sides of a PDA@Alg-CAT membrane. A: mat side (AlgCAT rich side), B: shiny side (PDA rich side).

Even if a possible mechanism of membrane formation has been proposed23, the mechanism of membrane formation at the water/air interface is still elusive. Indeed, the only noticeable feature on the UV-vis spectra of the PDA@Alg-CAT membranes is a broad peak at around 500 nm (Figure 4c). Interestingly the spectrum of

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the PDA@Alg-CAT membrane is similar to the one measured on a membrane obtained with high molecular weight PEI. 23 The chemical moieties at the origin of such a brood peak are not yet identified at the moment. Finally we varied the relative humidity (RH) from 30% to 80% which is the maximum that can be reached without damaging the setup. Upon this increase in RH, the pull-off forces doubles from 0.022 N to 0.046 N (Figure 4e). Only at higher RH, does the membrane detach again from its support. These results show that a high amount of water is needed to obtain the membrane to start to roll up. Conclusions Through an exploratory study leading to the use of AlgCAT as a crosslinker of PDA, we have designed a new kind of self-standing membrane. The covalent crosslinking between Alg-CAT and PDA aggregates occurs most probably through aryl-aryl coupling reactions. This PDA@Alg-CAT membrane is self-healing, stimuli responsive to water and Janus like (as seen on the basis of differential adhesion and compositional differences on its both sides). Investigation of the adhesion of the membrane when varying the relative humidity content showed that the adhesion increased by a factor 2 when the RH increased from 30% to 80% and that the PDA rich side (close to the water/air interface) of the membrane is stickier than the Alg-CAT side (in the aqueous solution), of the membrane. Hence, this easy to prepare and easy to handle self-standing membrane is prepared only from dopamine, Alg-CAT, water and oxygen from the air providing a possible fully biocompatible system.

Supporting Information. Optimization of the JKR experiments and ATR-IR spectra of both sides of a PDA@AlgCAT membrane. “This material is available free of charge via the Internet at http://pubs.acs.org.” For instructions on what should be included in the Supporting Information as well as how to prepare this material for publication, refer to the journal’s Instructions for Authors. AUTHOR INFORMATION Corresponding Author * Prof. Vincent Ball. Université de Strasbourg. Faculté de Chirurgie Dentaire, Université de Strasbourg. France.

Email : [email protected] Present Addresses †If an author’s address is different than the one given in the affiliation line, this information may be included here.

ACKNOWLEDGMENT Dr. Hicham Ibn El Ahrach, Luxembourguish Institute for Science and Technology, is acknowledged for the SEM images

ABBREVIATIONS PDA: polydopamine.

JKR: Johnson-Kendall-Roberts.

REFERENCES (1) Liu, Y.; Ai, K.; Lu, L. Polydopamine and its Derivative Materials : Synthesis and Promising Applications in Energy, Environmental, and Biomedical Fields Chem. Rev. 2014, 114, 5067-5115. (2) Ball, V.; Del Frari, D.; Michel, M.; Buehler, M.J.; Toniazzo, V.; Singh, M.K., Gracio, J.; Ruch, D. Deposition Mechanism and Properties of Thin Polydopamine Films for High Added Value Applications in Surface Science at the Nanoscale. BioNanoSci 2012, 2, 16-34. (3) Sedó, J., Saiz‐Poseu, J., Busqué, F., Ruiz‐Molina, D. CatecholBased Biomimetic Functional Materials Adv. Mater. 2013, 25, 653701. (4) Yang, H. C., Luo, J., Lv, Y., Shen, P., Xu, Z. K. Surface Engineering of Polymer Membranes via Mussel-Inspired Chemistry. J. Memb. Sci. 2015, 483, 42-59. (5) Lee, H., Dellatore, S. M., Miller, W. M., Messersmith, MusselInspired Surface Chemistry for Multifunctional Coatings. Science 2007, 318, 426-430. (6) Hong S. H., Hong S., Ryou M.-H., Choi J. W., Kang S. M., Lee H. Sprayable Ultrafast Polydopamine Surface Modifications. Adv. Mater. Interfaces 2016, 3, DOI: 10.1002/admi.201500857. (7) Zhang, C., Ou, Y., Lei, W. X., Wan, L. S., Ji, J., Xu, Z. K. CuSO4/H2O2-Induced Rapid Deposition of Polydopamine Coatings with High Uniformity and Enhanced Stability. Angew. Chem. Int. Ed. 2016, 128, 3106-3109. (8) Ponzio, F.; Barthes, J.; Bour, J.; Michel, M.; Bertani, P.; Hemmerlé, J.; d’Ischia, M.; Ball, V. Oxidant Control of Polydopamine Surface Chemistry in Acids: A Mechanism-Based Entry to SuperhydrophilicSuperoleophobic Coatings. Chem. Mater 2016, 28, 4697-4705. (9) Lynge, M. E., van der Westen, R., Postma, A., Städler, B. Polydopamine-a nature-inspired polymer coating for biomedical science. Nanoscale 2011, 3, 4916-4928. (10) Ryou, M-H.; Lee, D.J.; Lee, J.-N.; Lee, Y.M.; Park, J.K.; Choi, J.W. Excellent Cycle Life of Lithium Metal Anodes in Lithium Ion Batteries with Mussel-Inspired Polydopamine–Coated Separators.Adv. Energy. Mater 2012, 2, 645-650. (11) Lee, M.; Rho, J.; Lee, D.-E.; Hong, S.; Choi, S.-J.; Messersmith, P.B.; Lee, H. Water Detoxification by a Substrate-Bound Catecholamine Adsorbent. ChemPlusChem. 2012, 77, 987-990. (12) Lee, H.; Rho, J.; Messersmith, P.B. Facile Conjugation of Biomolecules Onto Surfaces via Mussel Adhesive Protein Inspired Coatings Adv. Mater., 2009, 21, 431-434. (13) Ham, H.O.; Liu, Z.Q.; Lau, K.H.A.; Lee, H.; Messersmith, P.B. Facile DNA Immobilization of Surfaces Through a Catecholamine Polymer. Angew. Chem. Int. Ed. 2011 50, 732-736. (14) Bernsmann, F.; Frisch, B.; Ringwald, C.; Ball. V. Protein Adsorption on Dopamine-Melanin Films: Role of Electrostatic Interactions Inferred from ζ-Potential Measurements versus Chemisorption. J. Colloid Interf. Sci. 2010, 344, 54-60. (15) Mrówczyński, R., Bunge, A., Liebscher, J. Polydopamine-An Organocatalyst Rather than an Innocent Polymer. Chem– Eur J. 2014, 20, 8647-8653. (16) Ai, K.L., Liu, Y.L., Ruan, C.P., Lu, L.H, Lu, G. Q. Sp2 CDominant N-Doped Carbon Sub-micrometer Spheres with a Tunable Size: A Versatile Platform for Highly Efficient Oxygen-Reduction Catalysts Adv. Mater., 2013, 25, 998-1003. (17) Farnad, N.; Farhadi, K.; Voelcker, N.H. Polydopamine Nanoparticles as a New and Highly Selective Biosorbent for the Removal of Copper (II) Ions from Aqueous Solutions. Water Air Soil Pollut. 2012, 223, 3535-3544. (18) Postma, A., Yan, Y., Wang, Y., Zelikin, A. N., Tjipto, E., Caruso, F. Self-Polymerization of Dopamine as a Versatile and Robust Technique to Prepare Polymer Capsules. Chem Mater. 2009, 21, 3042-3044. (19) Xu, L; Liu, X., Wang, D. Interfacial Basicity-Guided Formation of Polydopamine Hollow Capsules in Pristine O/W Emulsions-

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Toward Understanding of Emulsion Template Role. Chem. Mater. 2011, 23, 5105-5110. (20) Quignard, S., d'Ischia, M., Chen, Y., Fattaccioli, J. UltravioletInduced Fluorescence of Polydopamine-Coated Emulsion Droplets. ChemPlusChem, 2014, 79, 1254-1257. (21) Ponzio, F.; Payamyar, P.; Schneider, A.; Winterhalter, M.; Bour, J.; Addiego, F.; Krafft, M.-P.; Hemmerlé, J.; Ball, V. Polydopamine Films From the Forgotten Air/Water Interface. J. Phys. Chem. Lett. 2014, 5, 3436-3440. (22) Yang, H. C., Xu, W., Du, Y., Wu, J., Xu, Z. K. Composite FreeStanding Films of Polydopamine/Polyethyleneimine Grown at the Air/Water Interface. RSC Advances 2014, 4, 45415-45418. (23) Hong, S., Schaber, C. F., Dening, K., Appel, E., Gorb, S. N., Lee, H. Air/Water Interfacial Formation of Freestanding, StimuliResponsive, Self-Healing Catecholamine Janus-Faced Microfilms. Adv. Mater. 2014, 26, 7581-7587. (24) Lee, C.; Shin, J.; Lee, J.S.; Byun, E.; Ryu, J.H.; Um, S.H.; Kim, D.-I.; Lee, H.; Cho, S.W. Bioinspired, calcium free alginate hydrogels with tunable physical and mechanical properties and improved biocompatibility. Biomacromolecules 2013, 14, 2004-2013. (25) Mateescu, M.; Baixe, S.; Garnier, T.; Jierry, L. ; Ball, V. ; Haikel, Y. ; Metz-Boutigue, M.-H.; Nardin M.; Schaaf, P.; Lavalle, Ph. Antibacterial Peptide-Based Gel for Prevention of Medical Implanted-Device Infection. Plos One 2015, art e0145143. (26) Johnson, K. L., Kendall, K., Roberts, A. D. Surface Energy and the Contact of Elastic Solids. Proc.Royal Soc. London A: Mathematical, Physical and Engineering Sciences 1971, 324, 301-313. (27) Charrault, E., Gauthier, C., Marie, P., & Schirrer, R. Experimental and theoretical analysis of a dynamic JKR contact. Langmuir, 2009, 25, 5847-5854.

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(28) Moreno‐Couranjou, M., Blondiaux, N., Pugin, R., Le Houerou, V., Gauthier, C., Kroner, E., Choquet, P. Bio-Inspired Nanopatterned Polymer Adhesive: A Novel Elaboration Method and Performance Study. Plasma Processes and Polym., 2014, 11, 647-654. (29) Krogsgard, M.; Nue, V.; Birkedal, H. Mussel-Inspired Materials: Self-Healing through Coordination Chemistry. Chem. Eur. J. 2016, 22, 844-857. (30) Schweigert, N., Zehnder, A. J., Eggen, R. I. Chemical Properties of Catechols and their Molecular Modes of Toxic Action in Cells, From Microorganisms to Mammals. Environ. Microbiol. 2001, 3, 8191. (31) Ball, V. Impedance Spectroscopy and Zeta Potential Titration of Dopa-Melanin Films Produced by Oxidation of Dopamine. Colloids & Surf. A Physicochem. Eng. Aspects. 2010, 363, 92-97. (32) Mateescu, M., Metz-Boutigue, M.-H.; Bertani, Ph.; Ball, V. Polyelectrolytes to Produce Nanosized Functional Polydopamine. J. Colloid & Interf. Sci. 2016, 469, 184-190. (33) Lee, B. P., Dalsin, J. L., Messersmith, P. B. Synthesis and Gelation of DOPA-Modified Poly(ethylene glycol) Hydrogels. Biomacromolecules 2002, 3, 1038-1047. (34) Yang, H. C., Wu, Q. Y., Wan, L. S., Xu, Z. K. Polydopamine Gradients by Oxygen Diffusion Controlled Autoxidation. Chem. Comm. 2013, 49, 10522-10524. (35) Müller, M.; Keβler, B. Deposition from dopamine solutions at Ge substrates: an in-situ ATR-FTIR study. Langmuir 2011, 27, 12499-12505. (36) Lezanska, M.; Pietrzyk, P.; Sojka, Z. Investigations into the structure of nitrogen-containing CMK-3 and OCM-0.75 carbon replicas and the nature of surface functional groups by spectroscopic and sorption techniques. J. Phys. Chem. C 2010, 114, 1208-1216.

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