Dual-Responsive Capsules with Tunable Low Critical Solution

Apr 29, 2013 - Biomimetic Adhesives and Coatings Based on Mussel Adhesive Proteins. Yuan Liu , Hao Meng , Phillip B. Messersmith , Bruce P. Lee , Jeff...
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Dual-Responsive Capsules with Tunable Low Critical Solution Temperatures and Their Loading and Release Behavior Zhiyuan Ma,† Xin Jia,*,† Jiamei Hu,† Guoxiang Zhang,† Feng Zhou,‡ Zhiyong Liu,† and Heyun Wang† †

School of Chemistry and Chemical Engineering/Key Laboratory for Green Processing of Chemical Engineering of Xinjiang Bingtuan, Key Laboratory for Chemical Materials of Xinjiang Uygur Autonomous Region, Shihezi University, Shihezi 832003, PR China ‡ State Key Laboratory of Solid Lubrication, Lanzhou Institute of Chemical Physics, Chinese Academy of Sciences, Lanzhou 730000, PR China S Supporting Information *

ABSTRACT: Dual-responsive capsules sensitive to pH and temperature changes were successfully prepared by grafting random copolymer brushes of 2-(2-methoxyethoxy)ethyl methacrylate (MEO2MA) and oligo(ethylene glycol) methacrylate (OEGMA) from polydopamine (Pdop)-coated SiO2 via a surfaceinitiated atom-transfer radical polymerization (SI-ATRP) method with subsequent removal of the SiO2 core. The uptake and release properties of the resulting capsules are highly affected by changes in the pH values and temperature of the solution. The capsules can take up cationic dye rhodamine 6G (Rh6G) at high pH and T < LCST but not at low pH and T > LCST. In contrast, the capsules can release Rh6G at pH < 7 and temperature below the LCST, but release is less efficient under the opposite conditions. This dualresponsive property was also observed for the anionic dye methyl orange.

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useful in controlled-release systems and drug delivery.34−36 In particular, poly(N-isopropylacrylamide) (PNIPAM) has been the most studied thermoresponsive polymer, which exhibits a LCST of around 32 °C in water.37−40 Recently, Lutz and coworkers indicated that random copolymers of 2-(2methoxyethoxy)ethyl methacrylate (MEO2MA) and oligo(ethylene glycol) methacrylate (OEGMA) exhibiting LCST values between 26 and 90 °C are an attractive alternative to poly(N-isopropylacrylamide) (PNIPAM), and the ATRP technique has been successfully applied to this monomer system.41−43 The LCST of these copolymers could be accurately tuned by adjusting the fraction of OEGMA units in the copolymer chains.44,45 Such chemistry features could be used for feasibly designing multisensitive Pdop-based capsules with tunable LCST. In this work, we demonstrate novel dual pH-responsive and thermoresponsive capsules by grafting P(MEO 2 MA-coOEGMA) from a Pdop-coated SiO2 template via SI-ATRP and subsequent removal of the SiO2 cores with HF. These capsules are composed of a pH-responsive polydopamine inner layer and a thermosensitive P(MEO2MA-co-OEGMA) outer shell. The loading and release behaviors of these capsules were studied in detail using rhodamine 6G (Rh6G) as the test molecule. These capsules show different LCSTs depending on the structure of water-soluble polymer and also exhibit stimuli-

INTRODUCTION Stimuli-responsive and “smart” materials are widely used in controlled-release systems.1−5 For example, these materials may change their water affinity so that interior channels will open or close in response to an external stimulus such as temperature or pH change. Responsive polymeric capsules have numerous applications in biomedical materials6−8 (e.g., as drug-delivery vehicles 9,10 ). The development of a low-cost capsule production and encapsulation approach is still needed. Dopamine and its equivalent compounds11,12 can self-polymerize to form polydopamine (Pdop) on virtually any substrate surface,13−15 providing a novel possibility to produce capsules.16,17 It was also reported that polydopamine showed excellent biocompatibility and low cytotoxicity, making it a versatile platform for bioapplications.18−21 Pdop layers exhibit pH-switchable permselectivity for both cationic and anionic small molecules and have been used to take up and release charged molecules selectively.22 Most importantly, the Pdop layer has been found to be an extremely flexible platform for atom-transfer radical polymerization, which allows for tailoring the surface functionalities of Pdop by grafting polymer brushes.23−26 It was reported that varied types of polymer brushes were grafted from the Pdop platform.27,28 However, mussel-inspired Pdop capsules with multi-stimuli-responsive surface-grafted polymer brushes have rarely been investigated and afford an alternative structure for specific applications. Thermoresponsive materials have been widely investigated in nano/biotechnology.29−33 Water-soluble polymers exhibiting a lower critical solution temperature (LCST) are potentially © XXXX American Chemical Society

Received: January 4, 2013 Revised: April 18, 2013

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increase with the molar fraction of OEGMA in the copolymer. Thus, the LCST could be tuned to suitable temperatures by simply changing the molar fraction of the two monomers. The dotted lines corresponding to the differentiation of turbidity as a function of temperature show that the three kinds of capsules have LCSTs of 38, 47, and 56 °C, respectively, for capsules 1 to 3. TGA analysis verified that the random copolymer brushes were successfully grafted onto the Pdop-functionalized SiO2, as shown in Figure 2. The TGA of the SiO2 core had a 7.57%

responsive (pH and temperature) uptake and release behavior for test molecules. Such dual stimuli-responsive capsules are potentially useful for controlled release applications.

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EXPERIMENTAL SECTION

Details of the preparation of dual-responsive capsules using surfaceinitiated ATRP and their loading and release studies in different pH buffer solutions are given in the Supporting Information.

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RESULTS AND DISCUSSION The fabrication strategy is shown in Scheme 1. The stimuliresponsive capsules were successfully prepared by templateScheme 1. Procedures for the Fabrication of DualResponsive Capsules

Figure 2. TGA curves of the samples. For OEGMA1 to OEGMA3, the OEGMA contents are 10, 15, and 20 mol %, respectively.

weight loss at temperatures of up to 1000 °C. The Pdopmodified core had an 11.89% weight loss. After being decorated with the ATRP initiator, a 13.91% weight loss was measured. The difference between products corresponds to 0.164 mmol of initiator groups per gram of SiO2@Pdop-Br. After grafting polymerization, the weight loss values at different fraction of OEGMA units in stock solutions were as follows: 24.24% (10%), 24.55% (15%), and 26.04% (20%) at 1000 °C. Water absorption (the weight loss below 200 °C) was excluded from the calculation. The results of the grafting polymerization were further verified, as confirmed by the GPC (Figure 3), after an alkaline etching method (1 M NaOH).11,12 The GPC curve with a narrow molecular weight distribution (Mw/Mn < 1.5) confirmed the successful ATRP reaction. The result demonstrated that thermoresponsive brushes are grafted on the Pdop

mediated two-step polymerization. SiO2@Pdop was prepared by the spontaneous polymerization of dopamine on a SiO2 substrate. The bromoalkyl initiators were then immobilized on the Pdop coating. Subsequently, SI-ATRP was employed to graft P(MEO2MA-co-OEGMA) on the Pdop layer. Finally, the SiO2 substrate was removed by HF etching. Figure 1 shows the phase-transition scenario of three capsules grafted with P(MEO2MA-co-OEGMA) of different molar fractions. As previously reported,44,45 LCST values

Figure 1. Solid lines show turbidity as a function of temperature measured for aqueous solutions (1 mg mL−1) of three capsules with increasing OEGMA content: capsule 1 (10%), capsule 2 (15%), and capsule 3 (20%). Dotted lines show the first derivative of turbidity as a function of temperature for three samples.

Figure 3. GPC traces of P(MEO2MA-co-OEGMA) retrieved from dual-responsive capsules. B

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Figure 4. TEM photograph of (A) the SiO2 core and (B) Pdop-coated and (C) dual-responsive capsules.

Figure 5. (A) Effects of pH on Rh6G loading kinetics at T < LCST for capsule 1. Uptake efficiency by changing the buffer solution temperature between T < LCST and T > LCST for capsules (B) 1, (C) 2, and (D) 3.

an initial concentration of 10 μM after 48 h at pH 8.6. As the pH changed to 7.0, the uptake efficiency of Rh6G decreased to 62%, and less than 25% loading was observed at pH 4.8. Apparently, the loading capacity of dye is mainly affected by the pH values. The loading curve of capsule 1 at T > LCST has the same tendency (Figure S1). Other capsules show similar loading behavior (Figure S2). As discussed above, the Pdopbased shell plays a key role in controlling the guest molecules entering the capsules. The loading behaviors of three kinds of capsules at temperatures above or below the LCST were also studied in detail. The uptake rate of Rh6G was fast, but the OEGMAbased top layer clearly made a difference. It is found that the loading efficiency of Rh6G is significantly lower at T > LCST than at T < LCST. This difference should originate from the thermoresponsive layer. For example, the uptake behaviors of capsule 1 at pH 8.6 insinuate that the OEGMA-based coronas are in a collapsed state at 43 °C (T > LCST), which makes the Rh6G permeability of the random copolymer brushes low and obstructs the passage of dye molecules across the layer. However, at 34 °C (T < LCST), thermoresponsive chains are

substrate and the relative molecular weights of P(MEO2MA-coOEGMA) can be tuned by adjusting the molar fraction of the two monomers. Transmission electron microscope (TEM) images of the SiO2 core and Pdop-coated and dual-responsive capsules are shown in Figure 4. The capsules have an average diameter of about 360 nm. After polymer grafting, the wall thickness becomes larger as seen in Figure 4C. The shell thicknesses of Pdop and dual-responsive capsules are 25 and 36 nm, respectively. Dual-responsive capsules with a pH-switchable inner wall formed by Pdop and a thermoresponsive top layer exhibited dual-switchable permselectivity for dye molecules. A typical pH-induced loading experiment was performed as follows: the capsules were immersed in a guest solution at different pH values (10 μM) at room temperature. Figure 5A plots the changes in absorption intensity over time at three pH values, which are very close to those reported in previous studies.16,17 Clearly, the rhodamine 6G (Rh6G) uptake of capsule 1 was rapid for the first hour; thereafter, it proceeded at a slower rate and finally reached saturation. Nearly 83% Rh6G was loaded for C

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Figure 6. (A) Effects of pH value on the release kinetics at T < LCST for capsule 1. Temperature-dependent Rh6G release profiles recorded at either T < LCST or T > LCST for capsules (B) 1, (C) 2, and (D) 3.

ability of the Pdop layer allows for the controlled release of preloaded Rh6G from the capsules. Next, we studied the thermoswitchable release of Rh6G from the stimuli-responsive capsules by carrying out the same experiments as described above. The plots of the accumulated release amount as a function of release time are shown in Figure 6B−D. To investigate this, the release of dyes from capsules was monitored in acid-buffered solutions at a temperature above or below the LCST. These results clearly indicate that the delivery release system has a thermoresponsive character, with the release of the entrapped dye molecules decreasing by 10−20% above the LCST for all three capsules. This is consistent with our prediction that the collapse and swelling of the OEGMA-based outer layer can be used to adjust the permeability, as illustrated in Scheme 2. The probable dual-responsive loading and release procedure of Rh6G is shown in Scheme 2, where the polymer layer swells

soluble, which opens the channel of the brushes and favors the uptake of dye molecules (Figure 5B). The same rationale can be applied to the results for capsules 2 and 3 (Figures 5C,D). The dye release behaviors of dual-responsive capsules were also investigated. The capsules were preloaded by immersion in a dye solution (25 μM) at pH 8.6 and room temperature (below the LCST of the top OEGMA-based layer). After the impregnation of dye molecules reached a steady state, the capsules were taken out and dipped in water at a high temperature (above the LCST) to allow the top OEGMAbased brush layer to collapse and entrap the guest. Afterward, the dye-loaded capsules were rinsed with water at temperature above the LCST three times to remove dye molecules remaining on the polymer brush. For the release behavior of capsules, the Rh6G-encapsulated capsules were immersed in a solvent to study the effects of pH and temperature on the release kinetics. After that, the supernatant fluid obtained by centrifugation was removed and the UV−vis absorbance values were measured at regular intervals. Figure 6 shows the results obtained with Rh6G-loaded capsules as a plot of the absorption intensity normalized with respect to the highest value versus time. The release profile reveals a significant pH response at either T < LCST or T > LCST. First, we study the effects of pH on the release kinetics at temperature below the LCST; capsule 1 was employed as a model. Figure 6A shows the release examples of the data obtained at pH 4.6, 7.0, and 8.6. At low pH, the protonated Pdop film allowed more Rh6G to be released into the solution at a faster rate than the uncharged and deprotonated internal layer at pH 7.0 and 8.6. The release curve of capsule 1 at T > LCST has the same tendency (Figure S3), suggesting that the release of dye is mainly controlled by the Pdop inner film. The release data of capsules 2 and 3 also clearly demonstrate that the release of dyes is sensitive to the pH of the releasing solution (Figure S4). Therefore, the pH-dependent perme-

Scheme 2. Loading and Release Behaviors of DualResponsive Capsules

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Figure 7. Effects of pH on MO (A) loading and (B) release recorded at T < LCST.

at T < LCST and favors the uptake and release. In contrast, the layer collapsed at T > LCST, contracting the polymer chains and thereby restraining the loaded transportation of molecules. For the Pdop film, the layer has a net negative charge at high pH, which excludes anions but lets cations pass; at low pH, it is positively charged and excludes cations but passes anions. Interestingly, we found the capsules take up guest molecules at high pH and T < LCST, but it is hard to load Rh6G at low pH and T > LCST. In contrast, they could release Rh6G at pH < 7 and temperature below the LCST, but it is difficult to release under the reverse condition. In another experiment, the pH-dependent loading and release properties of capsule 2 with an anionic dye, methyl orange, was studied. The uptake and release curves show a contrary pH-responsive trend as compared to that for Rh6G. It is noted that the loading efficiency of MO decreases with the increasing pH value, which directly contrasts with the effect of pH on the loading of positively charged Rh6G. For instance, the uptake efficiency is no more than 20 and 65% at pH 8.6 and 7.0 for the initial concentration of 10 × 10−6 M (Figure 7A), respectively. However, as high as 90% MO was loaded after 6 h at pH 4.6, and the effects of the contact time on the uptake efficiency are similar to that of Rh6G in pH 8.6 solution; that is, the uptake of MO is rapid for the first few hours, and thereafter it continues at a slower rate before reaching equilibrium. For the release experiment, the results for different pH values of solutions are shown in Figure 7B. Only 43.5% release is observed at pH 4.6, but this increases to 63.7% at pH 7.0 and to 100% at pH 8.5. As shown in Figures S5 and S6, the temperature dependence of the uptake and release kinetics for the anionic MO is similar to that of the cationic Rh6G, demonstrating that similar forces control the permeability of the capsules, namely, the swelling and collapse of the outer OEGMA layer with temperature for the two different dyes. Therefore, dual-responsive capsules formed by an inner Pdop layer and an outer P(MEO2MA-co-OEGMA) corona can take up and release charged small molecules depending on the pH and have similar temperature dependences for release.

Rh6G (MO) depending on the temperature and pH. The dualsensitive Pdop-based capsules have the potential for biomedical applications where the permeability needs to be finely tuned.45,46−48

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ASSOCIATED CONTENT

S Supporting Information *

Dual-responsive capsule preparation details. Details of loading and release studies in different pH buffer solutions. This material is available free of charge via the Internet at http:// pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the Natural Science Foundation of China (21264013). ABBREVIATIONS Pdop, polydopamine; MEO2MA, 2-(2-methoxyethoxy)ethyl methacrylate; OEGMA, oligo(ethylene glycol)methacrylate; Rh6G, rhodamine 6G

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REFERENCES

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CONCLUSIONS The present work reports a novel dual-responsive capsule design that is readily obtained by grafting P(ME2OMA-coOEGMA) brushes onto Pdop-modified SiO2 spheres via the SIATRP method and subsequent removal of the SiO2 core. The dual-responsive capsules are robust and stable in different pH buffers. Most importantly, the stimuli-responsive capsules exhibited controllable loading and release with respect to E

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