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Conjugation of Hyaluronic Acid onto Surfaces via the Interfacial Polymerization of Dopamine to Prevent Protein Adsorption Renliang Huang, Xia Liu, Huijun Ye, Rongxin Su, Wei Qi, Libing Wang, and Zhimin He Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.5b02320 • Publication Date (Web): 21 Oct 2015 Downloaded from http://pubs.acs.org on October 26, 2015

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Conjugation of Hyaluronic Acid onto Surfaces via the Interfacial Polymerization of Dopamine to Prevent Protein Adsorption Renliang Huang,†, ǁ Xia Liu, ‡, ǁ Huijun Ye,‡ Rongxin Su,*, ‡, §, # Wei Qi, ‡, §, # Libing Wang, ‡ and Zhimin He‡ †

Tianjin Key Laboratory of Indoor Air Environmental Quality Control, School of Environmental

Science and Engineering, Tianjin University, Tianjin 300072, P. R. China ‡

State Key Laboratory of Chemical Engineering, School of Chemical Engineering and

Technology, Tianjin University, Tianjin 300072, P. R. China §

Collaborative Innovation Center of Chemical Science and Engineering (Tianjin), Tianjin

300072, P. R. China #

Tianjin Key Laboratory of Membrane Science and Desalination Technology, Tianjin University,

Tianjin 300072, P. R. China

ACS Paragon Plus Environment

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ABSTRACT: A versatile, convenient, and cost-effective method that can be used for grafting antifouling materials onto different surfaces is highly desirable in many applications. Here, we report the one-step fabrication of antifouling surfaces via the polymerization of dopamine and the simultaneous deposition of anionic hyaluronic acid (HA) on Au substrates. The water contact angle of the Au surfaces decreased from 84.9° to 24.8° after the attachment of a highly uniform polydopamine (PDA)/HA hybrid film. The results of surface plasmon resonance analysis showed that the Au-PDA/HA surfaces adsorbed proteins from solutions of bovine serum albumin, lysozyme, β-lactoglobulin, fibrinogen, and soybean milk in ultralow or low amounts (4.8−31.7 ng/cm2). The hydrophilicity and good antifouling performance of the PDA/HA surfaces is attributable to the HA chains that probably attached onto their upper surface via hydrogen bonding between PDA and HA. At the same time, the electrostatic repulsion between PDA and HA probably prevents the aggregation of PDA, resulting in the formation of a highly uniform PDA/HA hybrid film with the HA chains (with a stretched structure) on the upper surface. We also developed a simple method for removing this PDA/HA film and recycling the Au substrates by using an aqueous solution of NaOH as the hydrolyzing agent. The Au surface remained undamaged, and a PDA/HA film could be redeposited on the surface, with the surface exhibiting good antifouling performance even after ten such cycles. Finally, it was found that this grafting method is applicable to other substrates, including epoxy resins, polystyrene, glass, and steel, owing to the strong adhesion of PDA with these substrates.


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INTRODUCTION Surface plasmon resonance (SPR) spectroscopy is a label-free analytical technique that allows for noninvasive, time-resolved measurements of the small changes in the refractive index of materials. It has received great attention owing to its potential for use in sensing applications and has come to be employed widely in the fields of pharmaceutics, diagnostics, food safety, and environmental monitoring.1-7 Since SPR is highly sensitive to the refractive index at a depth of approximately 200 nm from the metallic surface, any molecular binding or migration in this region will cause a change in the SPR response.8 This exquisite sensitivity, along with the nearsurface selectivity of SPR spectroscopy, makes it an ideal technique for detecting different types of molecules. However, the surface fouling of sensor chips by single proteins or complex natural media (e.g., blood and milk) during SPR detection is a ubiquitous and problematic phenomenon that can mask the analytic signal and greatly reduce the accuracy of the obtained results. To address the issue of surface fouling, various fouling-resistant materials have been developed over the past few decades,9-15 such as zwitterionic polymers,16-17 hydrophilic polymers,18 saccharides,19 and peptides/proteins.8, 20-21 Owing to the complexity of the antifouling behaviors of these materials and given the diversity of pollutants, the design of new antifouling materials and their efficient attachment to diverse surfaces has attracted significant academic and commercial interest in recent years. Two basic strategies, termed “graft to” and “graft from,” are currently used for fabricating antifouling surfaces.22 The first one involves the binding of a presynthesized molecule with a chemical anchoring group on the desired surface. This strategy involves reactions such as the thiol-gold, thiol-ene, and hydroxyl-epoxy reactions. For example, Lin et al.23 fabricated a very thin layer of nonfouling zwitterionic cysteine though Au-S binding between Au and cysteine


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residues. The basic requirement for this approach is the modification of the substrate (e.g., Au) or the antifouling molecules (e.g., polyethylene glycol (PEG) and dextran). As a result, this strategy often suffers from significant limitations, including surface chemical specificity, the need for complicated and expensive protocols and, in some cases, difficulty in recycling. The other strategy involves of the in situ growth of a polymer on the surface to be modified via an initiator anchored onto the surface. For instance, Alswieleh et al.17 synthesized a new biofoulingresistant poly(cysteine methacrylate) brush, which was grown from the surface of a silicon wafer by atom-transfer radical polymerization. Liu et al.24 employed surface-initiated photoinifertermediated polymerization to graft zwitterionic poly(serine methacrylate) brushes on Au surfaces. These approaches allow one to synthesize antifouling layers with desirable surface densities and thicknesses, owing to the high density of the initiation sites and the growth of the chain ends. However, the anchoring of the initiator on the surface and the use of an appropriate catalyst are necessary for initiating the growth of the polymer bushes from the surface. In addition, the “graft from” strategy is also not suitable for immobilizing a few readily available antifouling materials,19-20, 25 such as natural polysaccharide and peptides. Therefore, it is highly desirable to develop a versatile, convenient, and cost-effective method for grafting antifouling materials onto different surfaces. Dopamine (DA) is a highly reactive molecule that polymerizes at alkaline pH values to form the adherent polydopamine (PDA), which can be used for coating different types of surfaces (e.g., metals, metal oxides, and glass).26-29 Various interactions, including covalent bonding (e.g., in the cases of amine and thiol groups), chelation bonding (e.g., in the case of TiO2), and hydrogen bonding (e.g., in the case of SiO2), are involved in the adhesion of DA or PDA to substrates, depending on the surface chemistry, which involves the catechol/quinone groups


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present.28, 30-31 By exploiting this fact, some antifouling materials have been attached onto surfaces through a PDA-assisted strategy.32-34 Instead of preventing the attachment of unwanted molecules on an antifouling surface, PDA can also be used to promote the binding of target molecules in biodetectors.35-37 For the PDA-assisted surface coating, a classic example is the use of a single DA residue to modify the end of a linear PEG chain that had been successfully immobilized on a Ti surface, such that the number of cells that adhered to this surface after 2 weeks in a culture was very low.38 Gao et al.39 synthesized a mimetic- and initiator-containing linker carrying two adhesive catechol groups for surface anchoring. Two zwitterionic poly(carboxybetaine) arms were grown from each initiator, resulting in strong binding on a Au surface; the surface packing density was also high. The second route involves a two-step attachment process, in which the PDA layer is formed and simultaneously bound onto the surface. An antifouling layer is subsequently generated on the PDA surface via an amine- or thiol- catechol/quinone reaction33, 40 or hydrogen bonding.41 For example, on a two-layered poly(ethylene oxide)-N(H)-PDA surface, the rate of protein adsorption from human blood plasma was only 7 ± 2 ng/cm2 at the maximal grafting density.33 The third strategy is to simply mix antifouling materials with a DA monomer solution and then codeposit them onto the surface to be coated via the polymerization of DA. In this case, a few nonionic macromolecules, such as polyvinyl alcohol (PVA)42 and dextran,34 have been successfully incorporated onto surfaces via DA-assisted codeposition. It is generally believed that the hydrogen bonds between such macromolecules (or hydroxyl groups) and PDA contribute to the formation of the hybrid films, which exhibit good antifouling properties. On the one hand, strong hydrogen-bond donor/acceptor ability should favor the codeposition of the hybrid film and enhance its surface density and stability. Therefore, common chemical groups such as the amide group (CO-NH) are


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potential alternatives to the hydroxyl group (OH), which was exploited in most previous studies. On the other hand, during the polymerization of DA, large, black aggregates (or precipitates) form generally, owing to the strong noncovalent interactions. The addition of nonionic macromolecules (e.g., dextran) can suppress the aggregation of the DA oxidative products; however, small aggregates (i.e., not large enough to precipitate) are still observed on the surface, especially at high dopamine loading rates.34, 43 Given that PDA exhibits a negative zeta potential at low alkaline pH values,44 anionic macromolecules are most likely to favor the formation of a uniform and smooth film, owing to the resulting electrostatic repulsion. This electrostatic interaction may also cause the macromolecules to be stretched to a greater degree on the surface, thus helping the deposited film retain its fouling resistance. In this study, we attempted to fabricate a protein-resistant SPR surface via the simple DA-assisted codeposition of anionic antifouling materials and PDA onto a Au substrate. Hyaluronic acid (HA) is a strongly hydrophilic anionic polysaccharide and contains a large number of amide (CO−NH) and carboxyl (COOH) groups, which provide hydrogen bond donors/acceptors and are negatively charged.19, 45 The antifouling property of HA with respect to protein adsorption and marine adhesion has been demonstrated well in previous studies.19, 25, 46-47 However, the protocols involved in the modification of the substrate or HA for fabricating such antifouling surfaces are complicated. For example, we recently proposed a grafting method that involved the formation of a self-assembled monolayer, the epoxy-activation of a Au surface, and a ring-opening reaction between epoxy and hydroxyl groups.19 Herein, we report a simple, onestep process for immobilizing HA molecules onto a Au surface via the interfacial polymerization of DA. The codeposition of PDA and HA was monitored by SPR spectroscopy, in order to ensure the successful attachment of the PDA/HA film on the Au surface. The Au-PDA and Au-


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PDA/HA surfaces were further characterized using contact angle measurements and atomic force microscopy (AFM). We then employed SPR spectroscopy to measure the nonspecific protein adsorption of single proteins (lysozyme, bovine serum albumin (BSA), β-lactoglobulin (β-LG), and fibrinogen) and natural-protein-containing complexes (100% blood serum and soybean milk) as test samples. The polymerization time and weight ratio of HA to DA (denoted as mHA/DA) were optimized to maximize the antifouling performance. Furthermore, given that PDA undergoes depolymerization in strongly alkaline conditions, we investigated the recycling and reuse of the Au-PDA/HA surface and evaluated its recyclability by washing it with aqueous solution of NaOH; washing with a H2SO4/H2O2 solution was used as a control treatment for comparison. Finally, this one-step grafting approach was expanded to other substrates (an epoxy resin, polystyrene, glass, and steel), and its versatility with respect to these surfaces was assessed. EXPERIMENTAL Materials. HA (MW = 100 kDa) extracted from rooster comb, DA, BSA, lysozyme, β-LG, and fibrinogen were purchased from Sigma-Aldrich (Beijing, China) and used as received. Soybean milk was purchased from a local market, and its protein content was determined using a bicinchoninic acid (BCA) assay kit developed by the Beyotime Institute of Biotechnology (Jiangsu, China). Blood serum with a protein concentration of 52.4 mg/mL was obtained from BEST-Biotech, Inc. (Tianjin, China) and used without dilution. The water used in all the experiments was purified using a three-stage Millipore Milli-Q Plus 185 purification system (Millipore Corp., Bedford, MA). The pH values of all the solutions used were determined with a MP220 pH meter (Mettler-Toledo, Switzerland). All the solutions were filtered using syringe


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filters with 0.22-µm-diameter pores before use. All the other chemicals, such as NaOH, H2SO4, H2O2, and phosphate buffer saline (PBS), were obtained from commercial sources. Preparation of bare Au-coated chips. A BK7 glass substrate (1.5×1 cm2) was coated with a 2-nm-thick layer of chromium and then a 50-nm-thick layer of gold using an electron beam evaporator (Temescal, CA, USA) at a base pressure of 10-6 Torr. The deposition rates for the chromium and gold layers were 0.5 and 1 Å/s, respectively. The resulting bare Au-coated chip was cleaned with an ultraviolet (UV)/ozone cleaning device, rinsed with anhydrous ethanol and ultrapure water, and subsequently dried with high-purity nitrogen. The as-prepared Au chip was then stored in a container until further use. Fabrication of Au-PDA and Au-PDA/HA chips. In a typical experiment, first, DA was dissolved in a Tris buffer solution (10 mM, pH of 8.5) in a final concentration of 2 mg/mL. Next, an aqueous solution mixture of DA (2 mg/mL) and HA (2 mg/mL) was prepared in a Tris buffer (10 mM, pH of 8.5). Then, the cleaned bare Au chips were immersed in either the DA solution or the DA/HA solution and incubated in a rotary shaker at 100 rpm and 28°C for 120 min. These dipped chips, denoted as Au-PDA and Au-PDA/HA, respectively, were then rinsed thoroughly with ultrapure water, dried in a stream of nitrogen, and stored in a container until further use. To optimize the antifouling performance, a number of Au-PDA/HA chips were prepared following the above-mentioned procedure for incubation times of 60–180 min. In all these cases, the concentrations of DA and HA were held constant at 2 mg/mL. Furthermore, HA solutions with concentrations of 0–8 mg/mL were also used to prepare Au-PDA/HA chips. In these cases, the DA concentration was kept constant at 2 mg/mL and the incubation time at 120 min. The value of mHA/DA was maintained at 0–4 to describe the experimental conditions.


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Surface coatings. DA (2 mg/mL) and HA/DA (mHA/DA=1) solutions were prepared as described above. Pieces of epoxy resin (2×1 cm2), polystyrene (2×1 cm2), glass (2×1.5 cm2), and steel (2×2 cm2) were each cleaned with a UV/ozone cleaning device for 15 min at room temperature. Then, each of the cleaned substrates was immersed in either the DA solution or the HA/DA solution and incubated in a rotary shaker at 100 rpm and 28°C for 120 min. The substrates were then rinsed with ultrapure water, dried in a stream of nitrogen, and stored in a container until further use. Surface characterization. To monitor the attachment of the PDA and PDA/HA films onto the Au surfaces, the SPR angles of the surfaces, including the bare Au, Au-PDA, and Au-PDA/HA surfaces, were measured using a SPR spectrometer operated in the angle-scanning mode. A PBS solution was used as the running buffer in all these experiments. The static contact angles of the bare, PDA-coated, and PDA/HA-coated surfaces were measured using an OCA15EC optical contact-angle-measuring instrument (DataPhysics Instruments, Germany) equipped with the software SCA 202. In all the experiments, a 1 µL droplet of water was deposited on the tested surfaces at room temperature. The contact angle was calculated by numerically fitting the profile of the droplet from the three-phase interface of the image captured by a charge-coupled device camera. The given values are the averages of four separate measurements performed at different areas on each substrate. The topographies of the bare Au, Au-PDA, and Au-PDA/HA surfaces were characterized using an Agilent 5500 AFM system (Agilent, USA) in the contact mode; the system was equipped with the software N9797 AU-1FP Pico. Silicon nitride AFM tips (NP-S, Bruker AFM Probes, USA) with an elastic modulus of 0.58 N/m were used for the imaging experiments.


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Measuring nonspecific protein adsorption using SPR. To evaluate the protein resistances of the Au-PDA/HA surfaces, six different protein solutions, including four single-protein solutions and two natural complex media, were used as the test samples. Specifically, lysozyme, BSA, βLG, and fibrinogen were individually dissolved in a PBS solution in a final concentration of 1 mg/mL. The soybean milk and blood serum samples were centrifuged at 5000 rpm (Sigma 318K, Germany) for 20 min and subsequently filtered through a 0.22 µm filter (Millex-GP, Millipore, USA). Using a BCA protein assay, the protein concentrations in these samples were found to be 7.6 mg/mL and 52.4 mg/mL, respectively. A time-resolved SPR (TR-SPR) spectrometer (DyneChem HiTech Ltd., Changchun, China) equipped with a 650 nm laser as the light source was used to observe the real-time adsorption of the proteins onto the Au-PDA/HA surfaces. A baseline signal was established by making a PBS buffer solution flow over the Au-PDA/HA surfaces at a flow rate of 50 µL/min for approximately 30 min. The protein-containing solution was injected into the flow cell at a flow rate of 10 µL/min for 10 min. This was followed by cleaning with a PBS solution at 10 µL/min for 10 min. During this process, the shift in the SPR angle was recorded as the ∆θ value, which was used to quantify the amount of protein adsorbed. In the case of the TR-SPR system used, a shift in the SPR angle of 0.12° corresponded to a surface coverage of 100 ng/cm2.19 The detection limit for the TR-SPR system was 0.0015°, which corresponded to a surface coverage of 1.25 ng/cm2. Recycling and reuse of Au-PDA/HA chips. The Au-PDA/HA chip was immersed in an aqueous solution (pH of 13) of NaOH, sonicated for 30 min, and then washed with ultrapure water twice. This operation was repeated thrice to ensure the complete removal of the PDA/HA film. As a control, a Au-PDA/HA chip was immersed in a solution mixture of H2SO4 and H2O2


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(7:3 v/v mixture of concentrated H2SO4 and 30% H2O2) for 3 h. To confirm that the PDA/HA film had been removed completely, the SPR angle of the washed Au surface was measured by SPR spectroscopy in the angle-scanning mode. In order to reuse the washed Au chip, we immersed the chip in a solution mixture of DA and HA (mHA/DA= 1) as per the above-described procedure. The as-prepared Au-PDA/HA chip was then exposed to a protein solution for the antifouling assay, as described above. In this study, ten cycles of recycling and redeposition were performed, in order to assess the recyclability of the Au-PDA/HA chips. RESULTS AND DISCUSSION Fabrication and characterization of Au-PDA/HA Chips. In this study, we attempted to immobilize an anionic polysaccharide, namely, HA, on a Au surface via the interfacial polymerization of DA. Scheme 1 illustrates the strategy for the codeposition of PDA and HA onto the Au substrate via hydrogen bonding. In the proposed method, a bare Au substrate is immersed in a solution mixture of HA and DA and incubated at 25°C for 2 h. During this process, the DA monomers self-polymerize at a pH of 8.5; thus, both PDA and HA are spontaneously codeposited onto the Au surface, resulting in the formation of a PDA/HA hybrid film (Au-PDA/HA). Given that HA contains a large number of amide, hydroxyl, and carboxyl groups, which can act as hydrogen bond donors and acceptors, it is likely that the strong hydrogen bonding between PDA and HA contributes to their codeposition onto the Au surface. Scheme 1. Schematic illustration of the preparation and recycling of the Au-PDA/HA chips


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To confirm the surface attachment of the PDA/HA film, we employed SPR spectroscopy to measure the change in the SPR angle, as it is highly sensitive to variations in the refractive index at a depth of approximately 200 nm from the Au surface. As shown in Figure 1, the SPR angle of a bare Au surface is 62.13°. This changes to 63.74° and 63.94° after the attachment of the PDA and PDA/HA films, respectively. The increase in the SPR angle confirmed that PDA or PDA/HA films were attached successfully onto the Au surfaces. The shift in the angle in the case of the PDA/HA film (1.81°) is much higher than that reported previously for a covalently grafted layer of HA (0.39°).19 This probably suggests that the weight and/or density of the PDA/HA film is higher than that of the HA layer. As shown in Figure S1, XPS data shows that the photoelectron signals of the Au substrates (Au4f7) decreased after PDA or PDA/HA modification, indicative of the successful surface coverage. Additionally, the C/O atomic ratio of Au-PDA/HA surface is lower than that of Au-PDA surface and is also close to the value of HA powder (Figure S2), which provides strong evidence for the formation of PDA/HA hybrid layer. Moreover, it is worth noting that the Au-PDA/HA chip exhibited a lower peak width at half height than did the bare Au and Au-PDA chips; this can be attributed to the uniform architecture of the PDA/HA film. In


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particular, in the absence of HA, a brown-black precipitate was observed during the polymerization of DA alone (Figure S3), indicating that the aggregation of the DA oxidative products via noncovalent interactions had occurred.48 As expected, the addition of HA significantly suppressed the aggregation process, as evidenced by the fact that the solution mixture turned black, indicating the formation of PDA, and no aggregates were observed even after centrifugation. Similar results have been observed in the presence of dextran in a previous study,34 in which the authors claimed that the hydrogen bonding between dextran and the oxidative products, as well as the steric hindrance resulting from the dextran macromolecule, inhibited the formation of large aggregates. In addition to these two factors, in the present case, electrostatic repulsion between HA and PDA probably also contributed to the suppression of the aggregation process, because both the HA and the PDA chains have negatively charged surfaces.44, 49 a)

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Figure 1. (a) Curves for the angle scans of the bare Au, Au-PDA, and Au-PDA/HA chips and (b) shifts in the SPR angle of the different chips. To characterize the wettabilities of the Au-PDA and Au-PDA/HA surfaces, the static water contact angles of the bare Au, Au-PDA, and Au-PDA/HA surfaces were measured. As shown in Figure 2, the bare Au surface was weakly hydrophilic and had a water contact angle of 84.9°,


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which decreased to 42.5° upon the deposition of the PDA film, presumably owing to the presence of hydrophilic chemical groups (e.g., OH). The attachment of the PDA/HA hybrid film decreased the water contact angle further, to 24.8°, and the coated surface exhibited extreme hydrophilicity, which could be attributed to a large number of HA chains being attached on the surface. Owing to the adhesion, the polymerization of DA initiated quickly on the Au surface, resulting in the formation of a thin and strongly adhering PDA layer on the surface. As the polymerization process proceeded, the codeposition of PDA and HA onto the initial PDA layer occurred, owing to the strong hydrogen bonding between the two, resulting in the formation of a PDA/HA hybrid layer. Later, a HA layer likely containing a few PDA molecules was generated from the hybrid layer, because of the electrostatic repulsion between HA and PDA and owing to steric hindrance (Scheme 1).

Figure 2. Contact angles of the bare Au, Au-PDA, and Au-PDA/HA surfaces. The insets show the corresponding images of the water droplets. The surface morphologies of the attached PDA and PDA/HA films were observed directly using AFM. Figure 3 shows typical AFM images of the Au surfaces before and after the deposition of the PDA and PDA/HA films. It is found that the bare Au and Au-PDA chips


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exhibited root mean square (rms) roughness of 5.2 and 5.6, respectively. Large aggregates were also observed on the PDA surface, in keeping with a precious report.43 As shown in Figures 3e,f, the Au-PDA/HA chip had a smooth surface with an rms roughness of 2.2 nm. The rms roughness value for the PDA/HA film was lower than that for a PDA/dextran film (4.89).34 As expected, no large aggregates were observed on the surface of the PDA/HA film, probably because HA inhibited the aggregation process.

Figure 3. Flattened and topographic AFM images of the (a-b)Au, (c-d) Au-PDA, and (e-f) AuPDA/HA surfaces.


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Nonspecific protein adsorption on Au-PDA/HA surfaces. To assess the antifouling ability of the Au-PDA/HA chip, SPR spectroscopy was employed to measure nonspecific protein adsorption on its surface. The SPR chip was exposed to a PBS solution, which was used as a running buffer, in order to establish a baseline. Then, 100 µL of a protein solution was injected and made to flow over the surface of the chip at a flow rate of 10 µL/min. The chip was then cleaned with a PBS buffer at the same flow rate for 10 min. To ensure good antifouling performance, we investigated the effects of the polymerization time on the degree of protein adsorption, while using BSA as the test sample. Figure 4a shows the real-time SPR signal (denoted in terms of the shift in angle, ∆θ) corresponding to protein adsorption and desorption. When the polymerization time was 60 min, the SPR angle increased immediately after the injection of BSA. After the chip had been washed with PBS, a shift in the angle of 0.022° was observed; this corresponded to an adsorption rate of ~18 ng/cm2. As shown in Figure 4b, with an increase in the polymerization time from 60 min to 120 min, the degree of nonspecific protein adsorption decreased significantly. For a polymerization time of 120 min, an ultralow BSA adsorption rate of 4.8 ng/cm2 was observed; this is comparable to that of the covalently grafted Au-HA chip mentioned previously19 and lower than the commonly accepted ultralow fouling criterion of 5 ng/cm2. However, further increases in the polymerization time lowered the protein resistance. The rate of protein adsorption increased to more than 15 ng/cm2 after 180 min. On the one hand, the density and thickness of the PDA/HA film increased gradually as the polymerization process proceeded. On the other hand, the rates of deposition of PDA and HA changed dynamically, owing to the interactions between the Au surface, PDA, and HA. Therefore, this change in the degree of protein adsorption with the polymerization time may be attributed to the differences in the density, thickness, and compositions of the resulting PDA/HA


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films. The codeposition of PDA and HA is a complicated process, and the effects of these factors need further study.

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0.05

∆θ (degree)

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

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0.02 0.01

16 12 8 4

0.00

0 10

15

20

25

30

35

60

80

Time (min)

100

120

140

160

180

Time (min)

Figure 4. (a) SPR sensorgrams showing the rates of nonspecific protein adsorption onto AuPDA/HA chips prepared using different polymerization times and (b) the amount of protein adsorbed on a Au-PDA/HA surface. The weight ratio, mHA/DA, was held constant at 1. Each error bar represents the standard deviation from three independent experiments. We further investigated the effect of the weight ratio, mHA/DA, on protein adsorption. As shown in Figure 5, in the absence of HA (i.e., for mHA/DA=0), the Au-PDA surface exhibited an adsorption rate of 207.8 ng/cm2, which is close to the value for a bare Au surface, as reported previously.19 Although PDA exhibits a hydrophilic character and has a water contact angle of 42.5°, the binding of PDA with BSA via a reaction between the catechol/quinone and amino/thiol groups results in a high degree of protein adsorption. As expected, the incorporation of HA within the PDA coating effectively decreased the rate of BSA adsorption to less than 5 ng/cm2 at a mHA/DA value of 1. The amount of protein adsorbed on the PDA/HA hybrid film was only 2.3% of that adsorbed on the PDA film. The SPR results provided strong evidence to support the claim that a large amount of HA was attached on the top surface of the PDA/HA hybrid film. Using quartz crystal microbalance measurements, previous studies have also shown


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that the codeposition of PDA and nonionic macromolecules (e.g., PVA and dextran) inhibits protein adsorption; however, these studies did not report any quantitative data.34, 42 Compared to nonionic molecules, the attached HA probably exhibits a more stretched molecular conformation on the top surface, owing to the electrostatic repulsion between PDA and HA; this probably contributes to the protein resistance. However, further increases in the degree of HA loading led to increased protein adsorption (e.g., 70 ng/cm2 at mHA/DA = 4, see Figure 5 and Figure S4), presumably because the presence of a large amount of HA suppressed the aggregation of PDA on the surface, owing to the strong noncovalent interactions between the two in the bulk solution. Therefore, with respect to protein resistance, a polymerization time of 2 h and a weight ratio, mHA/DA, of 1 are ideal for the fabrication of optimized Au-PDA/HA chips. Further, these values

0.25 0.20 0.15

mHA/DA= 0 mHA/DA= 0.8 mHA/DA= 1 mHA/DA= 2 mHA/DA= 4

b)

240 200

2

a)

Adsorption (ng/cm )

were used in the experiments described below.

∆θ (degree)

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

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0.10 0.05

160 120 80 40

0.00

0 25

30

35

40

45

50

0

0.8

Time (min)

1

2

4

mHA/DA

Figure 5. (a) SPR sensorgrams showing nonspecific adsorption of proteins onto the AuPDA/HA chips prepared using different values of mHA/DA and (b) amount of protein adsorbed onto the Au-PDA/HA surface. The polymerization time was held constant at 2 h. Each error bar represents the standard deviation from three independent experiments.


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Five solutions of proteins, including lysozyme, β-LG, fibrinogen, soybean milk, and undiluted blood serum, were chosen as the test samples to assess the antifouling performances of the fabricated chips. The molecular weights and isoelectric points (pI) of the single proteins are listed in Table S1. With the exception of lysozyme, the other single proteins are negatively charged at a pH of 7.4. As shown in Table S2, the bare Au surface had a high nonspecific adsorption from these protein media. However, the PDA/HA film resisted the adsorption of lysozyme, β-LG, and fibrinogen down to 6.5, 7.5, and 23.3 ng/cm2, respectively, indicating that the PDA/HA film exhibited good protein resistance. Surface hydration and steric repulsion, resulting from the flexible HA chains, probably act together to inhibit the adsorption of the proteins.13 Additionally, as shown in Table S2, the bare Au surface had a higher adsorption density for BSA (162.7 ng/cm2) and β-LG (152.9 ng/cm2) compared to that for lysozyme (63.9 ng/cm2), while the Au-PDA/HA surface had similar values of 4.8, 7.5 and 6.5 ng/cm2, respectively (Figure 6). In the running buffer (pH 7.4), the low pI value of BSA and β-LG allows them to be negatively charged. In these cases, the stong electrostatic repulsion between BSA/βLG and HA chain probably occurred due to the presence of carboxyl groups in HA molecules. Therefore, we expected that the electrostatic repulsion between proteins and HA plays an important role in the protein resistance. Moreover, the fact that fibrinogen was adsorbed in a large amount may be attributed to its fibrillar structure and large molecular weight. In the case of the natural protein complex media, the nonspecific adsorption rates for soybean milk and undiluted blood serum were 31.7 and 87.1 ng/cm2, respectively. The antifouling performance of the Au-PDA/HA surface was also comparable to that of the Au-HA surface.19 The results indicated that it is difficult for the HA-based surfaces to achieve low protein adsorption from


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blood serum, because a variety of protein (e.g., BSA, IgG, and apolipoprotein A-1) can be adsorbed to the antifouling surface, as demonstrated recently.50

Soybean milk Serum Fibrinogen

β -LG BSA Lysozyme 0

20

40

60

80

100

120

2

Adsorption (ng/cm ) Figure 6. Nonspecific adsorption of single proteins (lysozyme, BSA, β-LG, and fibrinogen; the concentration of all the solutions was 1 mg/mL) and natural complex media (100% blood serum, 52.4 mg/mL; soybean milk, 7.6 mg/mL) on Au-PDA/HA surfaces. Each error bar represents the standard deviation from three independent experiments. Recycling and reuse of Au-PDA/HA Chips. Generally, an antifouling surface adsorbs small amounts of proteins; however, long-term exposure to protein media during use can lead to the accumulation of proteins on the surface. This can cause the antifouling performance of the surface to deteriorate. In the case of SPR chips, the Au chip must be recycled once the surface starts exhibiting poor antifouling performance. Usually, the "piranha" solution (H2SO4 and H2O2 in a volume ratio of 7:3) is used to remove the organic layer. However, this damages the Au layer. As can be seen from Figure 7, after a chip was subjected to 5 cycles of PDA/HA codeposition and a H2SO4/H2O2 treatment, its Au layer was completely damaged. and no SPR peak was observed. It is known that PDA tends to undergo depolymerization in strongly alkaline


20

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solutions. In this study, an aqueous solution of NaOH (pH of 13) was used to remove the PDA/HA film under sonication. The SPR curve shows that the recovered Au chip had an SPR angle of 62.14°, which is very close to that of the bare Au chip (62.13°, as described before). Further, even after 5 codeposition cycles, the Au layer remained intact and undamaged.

Figure 7. Digital photographs and curves of SPR angle scans for bare Au chips recovered after 5 cycles using NaOH (blue) and H2SO4/H2O2 (orange). To assess the recyclability of the Au-PDA/HA chips, the extent of nonspecific protein adsorption on the PDA/HA surface after different numbers of cycles was measured using SPR spectroscopy. As shown in Figure 8, the amount of protein adsorbed on the redeposited PDA/HA surfaces was less than 10 ng/cm2 (less than 5 ng/cm2 in most cases) even after 10 cycles, indicating that they continued to exhibit good antifouling performance. We believe that this excellent recyclability under mild conditions along with the good antifouling performance make the fabricated Au-PDA/HA chips ideal for use as fouling-resistant SPR sensor chips.


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12 BSA 2

Adsorption (ng/cm )

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10 8 6 4 2 0 1

2

3

4

5

6

7

8

9

10

Number of cycles Figure 8. Amount of BSA adsorbed on the Au-PDA/HA surface after different numbers of cycles. Codeposition of PDA and HA onto other substrates. Given that PDA adheres strongly with diverse surfaces, we attempted to determine whether it is feasible to immobilize HA via the polymerization of DA on other substrates as well. Four different substrates, namely, an epoxy resin, polystyrene, glass, and steel, were chosen as the model surfaces. PDA and PDA/HA films were attached onto these surfaces following the same procedure as that used for the Au surfaces. The water contact angles of the bare and coated surfaces were measured to confirm whether the films had been deposited successfully. As can be seen from Table 1 and Figure S5, the water contact angles of the PDA surfaces were 40–45.5°, while those for the PDA/HA surfaces were 24.8–29.3°; this was regardless of the original values (14.6–91.7°), indicating that the surface coatings had been formed successfully. Thus, the method employed in this study can be used to fabricate different types of antifouling surfaces through a simple procedure.


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Table 1. Static water contact angles of different substrates before and after being coated with PDA and PDA/HA films Contact angle (°) Substrate Bare substrate

Substrate-PDA

Substrate-PDA/HA

Gold

84.9±0.1

42.5±0.4

24.8±0.1

Epoxy resin

58.6±0.9

41.5±1.1

29.3±1.8

Polystyrene

61.0±0.4

40.0±0.3

27.7+0.3

Glass

14.6±0.2

45.5±0.7

26.0±0.6

Steel

91.7±0.1

40.5±0.8

29.1±0.9

CONCLUSIONS In summary, a facile and versatile method for fabricating antifouling surfaces involving the one-step codeposition of PDA and HA onto different types of substrates (e.g., Au, polystyrene, and glass) was developed. In this method, HA was mixed with DA and then deposited onto the surface to be coated. This was accompanied by the polymerization of DA via the formation of hydrogen bonds between PDA and HA, resulting in the formation of highly uniform PDA/HA hybrid films. These films exhibited high hydrophilicity and good antifouling performances against the nonspecific adsorption of single proteins and natural protein complex media. This suggested that the upper surface of the PDA/HA film was mainly composed of stretched HA chains, presumably owing to the electrostatic repulsion between PDA and HA. The amount of protein adsorbed onto the Au-PDA/HA surfaces was ultralow (less than 5 ng/cm2) or low (less than 32 ng/cm2) when solutions containing BSA, lysozyme, β-LG, fibrinogen, and soybean milk were employed as the test samples. Moreover, a simple and practical method for recycling the Au substrates by washing the Au-PDA/HA chips in an aqueous solution of NaOH was also developed. This method allowed the PDA/HA film to be removed completely. The recovered Au


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surface could then be used again and exhibited excellent recyclability and antifouling performance even after ten recycling/redeposition cycles. Given that PDA adheres strongly to a number of different substrates and because of the simplicity of the one-step codeposition and substrate recycling processes, the methods developed in this study have great potential for use in the fabrication of recoverable antifouling surfaces for various applications. ASSOCIATED CONTENT Supporting Information. XPS survey spectra and the The C/O atomic ratio of bare Au, AuPDA, Au-PDA/HA and HA; photographs of PDA and PDA/HA solutions after being left to stand for 2 h; SPR sensorgrams showing nonspecific adsorption of proteins onto the AuPDA/HA chips prepared using different mHA/DA values and a polymerization time of 3 h; the amount of protein adsorbed onto the Au-PDA/HA surfaces; images showing the contact angles of the bare, PDA-coated, and PDA/HA coated-substrates; and properties of the proteins used for the adsorption assay; the nonspecific adsorption from single protein solutions and protein complexes-containing media on bare Au surface. This material is available free of charge via the Internet at http://pubs.acs.org/. AUTHOR INFORMATION Corresponding Author *

E-mail: [email protected] (R. S.).

Tel: +86 22 27407799. Fax: +86 22 27407599. Author Contributions ǁ

R.H. and X.L. contributed equally to this work.


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ACKNOWLEDGMENTS This work was supported by grants from the Ministry of Science and Technology of China (Nos. 2012YQ090194, 2012AA06A303, and 2012BAD29B05), the Natural Science Foundation of China (Nos. 21276192 and 21306134), and the Ministry of Education (Nos. NCET-11-0372 and 20130032120029). ABBREVIATIONS HA, hyaluronic acid; PDA, polydopamine; SPR, surface plasmon resonance; PEG, polyethylene glycol; DA, dopamine; PVA, polyvinyl alcohol; atomic force microscopy; BSA, bovine serum albumin; β-lactoglobulin, β-LG; BCA, bicinchoninic acid; PBS, phosphate buffer saline; UV, ultraviolet; TR, time-resolved; rms, root mean square. REFERENCES (1) Tokel, O.; Inci, F.; Demirci, U., Advances in Plasmonic Technologies for Point of Care Applications. Chem. Rev. 2014, 114, 5728-5752. (2) Zeng, S.; Baillargeat, D.; Ho, H.-P.; Yong, K.-T., Nanomaterials Enhanced Surface Plasmon Resonance for Biological and Chemical Sensing Applications. Chem. Soc. Rev. 2014, 43, 3426-3452. (3) Abadian, P. N.; Kelley, C. P.; Goluch, E. D., Cellular Analysis and Detection Using Surface Plasmon Resonance Techniques. Anal. Chem. 2014, 86, 2799-2812. (4) Fong, K. E.; Yung, L.-Y. L., Localized Surface Plasmon Resonance: A Unique Property of Plasmonic Nanoparticles for Nucleic Acid Detection. Nanoscale 2013, 5, 12043-12071. (5) Spoto, G.; Minunni, M., Surface Plasmon Resonance Imaging: What Next? J. Phys. Chem. Lett. 2012, 3, 2682-2691.


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TOC Graphic


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Conjugation of Hyaluronic Acid onto Surfaces via ... - ACS Publications

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