Eliminating Diffusion Limitations at the Solid–Liquid Interface for Rapid

Letter pubs.acs.org/journal/abseba

Eliminating Diffusion Limitations at the Solid−Liquid Interface for Rapid Polymer Deposition Mei-Xia Zhao,†,‡ Junwei Li,† and Xiaohu Gao*,† †

Department of Bioengineering, University of Washington, Seattle, Washington 98195, United States Key Laboratory of Natural Medicine and Immune-Engineering of Henan Province, Henan University, Kaifeng 475004, China

‡

S Supporting Information *

ABSTRACT: Polydopamine (PDA), a bioinspired polymer, has found diverse applications including biotechnology and energy research due to its unique properties for surface modification. In recent years, the reaction conditions for dopamine polymerization and thin film growth have been thoroughly examined and optimized. The fundamental problem of diffusion limitation at the solid−liquid interface that slows down PDA deposition, however, remains to be addressed. Here, we present a physical methodology that can be added onto virtually all the current chemical conditions for rapid deposition of polymers on surface. The concept of this general technology can potentially impact other research areas dealing with solid−liquid interfaces, such as biosensing and catalysis. KEYWORDS: surface coating, diffusion limitation, polymer, polydopamine, wettability

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can increase the PDA polymerization rate by approximately 20fold compared to the classic dip-coating procedure reported by Messersmith and co-workers, enabling fast surface deposition of PDA.16 Despite these advances in the polymerization chemistry, a fundamental issue remain to be addressed is how to efficiently transfer PDA polymer chains and aggregates onto surfaces, a mass transfer problem seen at virtually all solid/ liquid interfaces. The speed of PDA surface coating is largely determined by two processes, attachment of preformed PDA polymers and their aggregates onto the surface and polymerization occurring on the surface. Although it is difficult to quantitatively delineate the contribution of each process (even the PDA polymerization chemistry is not entirely understood at this time),17 both processes at the solid−liquid interface are affected by diffusion. The mass transfer limitation becomes a rate-limiting problem when the kinetics of PDA coating (regardless of adsorption of preformed polymer in solution or polymerization on surface) greatly exceed the rate of polymer and monomer diffusion from bulk solution to the surface, which creates a depletion layer near the surface (substantially reduced concentration of the coating materials).18 This is expected since preformed PDA aggregates and active dopamine monomers (or dopamine and oxygen together) need to travel through the bulk solution and reach the solid-support surface. In direct contrast to chemical reactions and binding events in solution where simple mixing (e.g., mechanical stirring) effectively promotes mass transfer,

recise control of surface properties is of crucial importance to the development of functional materials and devices. Among different surface treatment strategies, polymer coating has become increasingly popular because of the broad availability of polymers with various degrees of wettability, anticorrosive capability, degradation rate, and antifouling capability, and with various reactive chemical groups. Depending on the application (e.g., tissue engineering, controlled drug release, solar cells, and implants), a polymer or polymer combination can be grafted onto the surface of a device to enhance its performance.1−4 Indeed, a number of robust coating methods have been developed in recent years such as surface-initiated polymerization, layer-by-layer deposition, and self-assembled monolayers.5−7 In this context, a polymer of particular interest is polydopamine, because it can attach to virtually any surface and react with compounds containing primary amine or thiol groups.8 PDA has been proven useful in a broad spectrum of biomedical research, ranging from drug delivery to modulation of cell adhesion and biosensing.9,10 Since the initial report of an incredibly simple dip-coating procedure from Dr. Messersmith and co-workers,11 significant research efforts have been invested to understand the polymerization chemistry and optimize the reaction conditions to improve the smoothness of the coating, the reaction rate, and the coating thickness. For example, Park, Zhao, and Ruth have investigated the effects of oxidants and buffers on the formation rate and smoothness of PDA films,12−14 whereas Levkin and co-workers have developed a UV-triggered polymerization method to control PDA surface coating with high temporal and spatial resolution.15 Most recently, Xu et al. discovered that addition of CuSO4 and H2O2 © XXXX American Chemical Society

Received: December 27, 2016 Accepted: April 14, 2017

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DOI: 10.1021/acsbiomaterials.6b00810 ACS Biomater. Sci. Eng. XXXX, XXX, XXX−XXX

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ACS Biomaterials Science & Engineering

Figure 1. Schematic illustration of the CDR technology for rapid coating of PDA on surface. (a) Conventional dip-coating method for PDA deposition on a substrate (the circle). Because fluid on surface is stationary, even with stirring, a PDA depletion layer is formed as PDA near the surface is consumed. (b) CDR method enabled rapid PDA coating. The reaction container is tilted back and forth, resulting in repeated draining and replenishing of the PDA solution on the substrate surface. This process effectively removes the depletion layer, rendering the substrate exposed to PDA in the bulk solution at all time.

Figure 2. PP and PVDF membranes coated with PDA. (a) Photographs of PP membranes coated with of PDA. (b) Darkness of the PP membrane measured by ImageJ. (c, d) The same experiments performed on PVDF membranes. Error bars showing standard deviations from four separate measurements.

acknowledge that its effect is the most prominent on systems dealing with coating and binding materials of low concentration (longer average diffusion distance) and large size (e.g., polymers, nanoparticles, and macrobiomolecules). In contrast, small molecules of high concentration are less constrained by the diffusion limitation. Because of its aforementioned versatility, we have selected PDA to demonstrate the concept of CDR-aided rapid surface coating. Besides the functionalities, an additional benefit of PDA is its inherent dark color, allowing the coating process to be readily monitored. As shown in Figure 1b, a substrate is placed on one side of a container that rocks side-to-side, where the incubation solution comes in contact with the substrate in a similar fashion as ocean waves washing the beach. Through this process, the substrate goes through incubation and drainage

reaction and adsorption at interfaces are generally limited by diffusion limitation. The classic fluid dynamics theories can help explain it. For example, using the model of flow profile in a tube, the flow rate decreases to zero at the boundary regardless of the overall volumetric flow rate in a tube. Therefore, even with vigorous stirring, the fluid on surface is stationary, resulting in slow mass transfer dominated by diffusion (Figure 1a). Recently, we reported an innovative approach (cyclic draining−replenishing, CDR) to bypass the diffusion limitation, and demonstrated its use in rapid cell staining without affecting the imaging sensitivity and specificity.18 Here, we show that the same concept can be extended to surface modification with polymers. Although the general concept of CDR applies to virtually all events occurring at the liquid/solid interfaces, we B

DOI: 10.1021/acsbiomaterials.6b00810 ACS Biomater. Sci. Eng. XXXX, XXX, XXX−XXX

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ACS Biomaterials Science & Engineering

within 3 h. In comparison, a similar course of wettability change was observed for static incubation as well, except taking significantly longer time (WCA dropped to 56.3° in 6 h and the droplet disappeared after 12 h PDA coating). Because material wettability is not only affected by the coating material chemical composition, but also the morphology, we studied the microstructure of the PDA-coated PVDF membrane via two independent methods, scanning electron microscopy (SEM), and atomic force microscopy (AFM). As shown in the SEM images (Figure 4a), no obvious morphology changes were

cycles repeatedly (CDR process), which is completely different from the classic dip-coating procedure where the substrate is soaked in the dopamine solution continuously. In the incubation phase, the coating material mixture including dopamine monomers, oligomers, and polymers binds with the substrate surface and creates a depletion layer near the surface, whereas in the drainage phase, the depletion layer is completely eliminated while some dopamine monomers and oligomers on the substrate are fully exposed to oxygen in air and quickly polymerize into the PDA network. Repeating this process in multiple cycles leads to deposition of PDA at a significantly improved rate. To demonstrate the concept, we tested two types of filtration membranes (polypropylene and polyvinylidene fluoride, PP and PVDF) commonly used in chemistry laboratories for PDA coating under either the conventional dip-coating condition or the CDR condition. As shown in Figure 2a, the PP membrane turned brown-black, a color indicator of PDA coating, within minutes under the CDR condition, whereas similar degree of deposition took several hours under static incubation. The darkness of the membrane was measured using the free publicdomain Java image processing software, ImageJ, developed at the National Institutes of Health. Semiquantitative comparison reveals that the darkness of membranes coated with the CDR process for 20 min reaches the same level as membranes continuously incubated for 12 h, significantly shortening processing time (Figure 2b). Similar results were also found in the PVDF membrane (Figure 2c, d) as well as a variety of other porous and nonporous materials (Figure S1). Note that the CDR rocking speed (frequency of drain-replenish cycling) was probed and optimized by testing a number of settings. As shown in Figure S2, at a rocking speed between 2 to 4 rpm, the CDR process is most effective in increasing PDA coating rate for the PVDF membrane. Next, we applied the CDR-aided rapid PDA-coating technology to tune the wettability of the hydrophobic PVDF membranes. As shown in Figure 3, the PVDF membranes are

Figure 4. Morphology and thickness of PDA coated on surfaces. (a) SEM micrographs of PVDF membranes before PDA coating (untreated), and coated with PDA using the conventional dip-coating protocol (static) or the CDR process. No significant morphological changes are observed for the three samples. High-magnification scale bar, 2 μm; low-magnification scale bar, 5 μm. (b) AFM imaging of PDA-coated flat silicon wafer. PDA deposition using CDR is significantly faster.

detected before and after PDA coating, suggesting the wettability change is largely a result of the surface chemical properties rather than structural properties. Furthermore, the PDA coating thickness can be directly measured by coating PDA on a silicon wafer (AFM measurements require smooth surfaces). Although the silicon wafer does not resemble the PVDF membrane in smoothness, porosity, chemical composition, and surface properties, the CDR rocking speed optimized for the PVDF membrane still shows significantly faster PDA deposition on the silicon wafer compared to static incubaton (approximately doubles the thickness at all four time points studied, Figure 4b). These observations show that hydrophobicity/hydrophilicity of a surface can be quickly and continuously tuned by combining the CDR approach with the unique features of PDA. Besides the rapid coating kinetics, a key feature of CDRaided polymerization is the green process, where no additional chemicals are added. It has been shown that the PDA polymerization and coating rate can be enhanced by adding CuSO4 as a catalyst.16 This chemically enhanced reaction kinetics often leaves trace amount of heavy metal behind that may interfere with downstream applications. We probed this issue by growing E. coli on PDA-coated PVDF membranes prepared using three conditions: slow dip-coating approach without additional chemicals, rapid CDR approach without additional chemicals, and the CuSO4-catalyzed approach, because excessive Cu2+ ion is known to inhibit the growth of

Figure 3. Comparison of PVDF water contact angle evolvement during PDA coating. (a) Visual observation and (b) quantitative WCA measurements show that PDA coating under the CDR condition is significantly faster in changing PVDF’s WCA, compared to the dipcoating process. Error bars showing standard deviations from four separate measurements.

highly hydrophobic with an initial water contact angle (WCA) of 132.5°. Coating them with PDA can convert the hydrophobic membranes to hydrophilic.19 When PDA were coated onto the PVDF membrane using the CDR approach for various durations, the WCA of the membrane quickly decreased to 36.4° within 1 h and the water droplet completely disappeared C

DOI: 10.1021/acsbiomaterials.6b00810 ACS Biomater. Sci. Eng. XXXX, XXX, XXX−XXX

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ACS Biomaterials Science & Engineering aerobic bacteria.20 Figure 5 shows that in comparison with membranes treated by static incubation and the CDR approach,

ORCID

Xiaohu Gao: 0000-0002-6054-0530 Funding

The Howard Hughes Medical Institute The National Institute of Health, Grant R21CA192985; and The Ministry of Education of China, Scholarship file number 201408410251 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported in part by NIH (R21CA192985) and the Department of Bioengineering at the University of Washington. J.L. thanks the Howard Hughes Medical Institute for a student fellowship, and M.X.Z. thanks the Ministry of Education of China for a CSC scholarship and the National Natural Science Foundation of China (21501044).

■ Figure 5. Viability of E. coli incubated with PDA-coated PVDF membrane prepared via different methods. The membranes prepared via (a) static incubation and (b) CDR show higher colony counts than (c) the CuSO4/H2O2 method, which contains Cu2+ as a catalyst. Error bars showing standard deviations from three separate measurements.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsbiomaterials.6b00810. Detailed methods, Figure S1 showing deposition of PDA on various substrates, and Figure S2 showing the rocking rate effect of CDR (PDF)

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REFERENCES

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membranes exposed to Cu2+ ion result in ∼54% lower colony counts. It is also worth mentioning that because CDR uses a physical mechanism to enhance the kinetics of reactions and interactions occurring at boundaries, it can be potentially combined with other chemical approaches. To conclude, polymer coating has been a popular approach to precisely control surface properties, but polymer deposition at the solid/liquid interface is a slow process because of the mass transfer limitation. In this work, we have developed a physical methodology that can reduce or avoid diffusion limitation. We show that PDA coating on membrane surfaces can be significantly enhanced under the same chemical reaction conditions. This method is low-cost, easy to implement, green, and has broad applications in fields requiring surface treatment such as diagnosis, tissue engineering, medical implants, and photovoltaics. Furthermore, we envision that it may inspire other chemical processes that occurring at the interface, such as catalysis.

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ABBREVIATIONS PDA, polydopamine CDR, cyclic draining-replenishing PP, polypropylene PVDF, polyvinylidene fluoride SEM, scanning electron microscopy AFM, atomic force microscopy WCA, water contact angle

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected].

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DOI: 10.1021/acsbiomaterials.6b00810 ACS Biomater. Sci. Eng. XXXX, XXX, XXX−XXX

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DOI: 10.1021/acsbiomaterials.6b00810 ACS Biomater. Sci. Eng. XXXX, XXX, XXX−XXX