and temperature-responsive pesticide release platform through core

An NIR- and temperature-responsive pesticide release platform through core-shell .... To the best of our knowledge, until now no work has been ...... ...
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A Near-Infrared and Temperature-Responsive Pesticide Release Platform through Core−Shell Polydopamine@PNIPAm Nanocomposites Xiaohui Xu,† Bo Bai,*,‡ Honglun Wang,‡ and Yourui Suo‡ †

College of Environmental Science and Engineering, Chang’an University, Xi’an 710054, P. R. China State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining 810001, P. R. China

‡

S Supporting Information *

ABSTRACT: Controlled stimuli-responsive release systems are a feasible and effective way to increase the efficiency of pesticides and help improve environmental pollution issues. However, near-infrared (NIR)-responsive systems for encapsulation of pesticides for controlling release have not been reported because of high cost and load ability of conventional NIR absorbers as well as complicated preparation process. Herein, we proposed polydopamine (PDA) microspheres as a photothermal agent owing to their abundant active sites, satisfactory photothermal efficiency, low cost, and easy fabrication, followed by capping with a PNIPAm thermosensitive polymer shell. In this core−shell PDA@PNIPAm hybrid system, the PDA core provided excellent temperature and NIR-light sensitivity as well as high loading capacity, while the PNIPAm applied as both a thermosensitive gatekeeper and a pesticide reservoir. The structure of the PDA@PNIPAm nanocomposites was characterized by transmission electron microscopy, scanning electron microscopy, Fourier transform infrared spectroscopy, ultraviolet−visible spectroscopy, dynamic light scattering, and thermogravimetric analysis; the results showed that the nanocomposites had a well-defined core−shell configuration for efficient loading of small pesticide molecules. Moreover, the core−shell PDA@PNIPAm nanocomposites exhibited high loading capacity and temperature- or NIR-controlled release performance. Overall, this system has significant potential in controlled drug release and agriculture-related fields as a delivery system for pesticides with photothermal responsive behavior. KEYWORDS: near-infrared light, stimuli-responsive, polydopamine, thermoresponsive polymer, controlled release

1. INTRODUCTION Pesticides make a significant contribution to boost the yield and quality of agricultural production by protecting crops from pests, and approximately one-third of world’s food supplies may be reduced without pests and diseases control.1 However, up to 90% of the applied conventional pesticides never get to their target sites to produce effective performance and enter the environment via evaporation, degradation, and leaching, resulting in serious adverse effects such as surface/underground water pollution and resource waste.2,3 To overcome such limits, controlled stimuli-responsive release systems have gained considerable attention in virtue of their ability to regulate release of certain active ingredients at the desired site in a designated manner.4,5 These systems have been verified to efficiently increase the performance level of pesticides and save manpower and energy and reduce environment contamination in comparison to conventional formulations.6 In particular, external stimuli such as pH,7 temperature,8 microbe,9 γirradiation,10 and UV light11,12-responsive materials have been developed for triggered pesticides release in agriculture domain. Among the various stimuli-responsive systems, UV lightresponsive materials are particularly attractive and more © 2017 American Chemical Society

achievable in practical applications, because they can employ safe and abundant available sunlight (containing ∼4% UV light) as a triggering source for controlled release. Another newly emerged system, namely, near-infrared (NIR) light-responsive materials, has been intensively explored for indrug delivery owing to their greater tissue penetration abilities and negligible toxicity to the tissue.13 These materials commonly encapsulate gold-based nanomaterials such as gold nanorods, gold nanocages, and nanohexapods as photothermal agents into the thermal-responsive polymers matrix as the drug delivery carrier.14−16 When exposed to NIR light, the photothermal agents can readily absorb and convert photo energy into thermal energy producing heat, leading to the volume shrinkage of the polymer matrices, realizing the triggered release of entrapped drugs. Despite excellent drug release effect and the rich resource of NIR light, which occupies ∼52% of solar photons,17 NIR light-responsive systems have not been applied in the agriculture sector for controlling Received: November 30, 2016 Accepted: January 26, 2017 Published: January 26, 2017 6424

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sulfate (SDS), and ammonium persufate (APS) were supplied by Tianjin Chemical Reagent Factory (Tianjin, China). Imidacloprid (95%) was purchased from a local agrochemical supplier (Shaanxi, China) and used without further purification. 2.2. Preparation of Polydopamine Microspheres. Polydopamine microspheres were synthesized by using a previously reported method with minor modification.8 Typically, 28−30% NH4OH (1 mL), ethanol (20 mL), and deionized water (45 mL) were added into a 100 mL beaker under mild magnetic stirring. Then deionized water (5 mL) containing dopamine hydrochloride (0.3 g) was slowly injected into the above solution and reacted for 12 h. Subsequently, PDA nanoparticles were collected by centrifugation (4000 rpm, 10 min) and washed with deionized water (10 mL, three times). 2.3. Preparation of the Core−Shell PDA@PNIPAm Nanocomposites. PDA@PNIPAm core−shell nanocomposites were prepared via seeded precipitation polymerization as follows:32 an aqueous solution of NIPAm and the as-prepared PDA microspheres with various amounts of 100 mM NIPAm (6.0, 10, 14 mL) and PDA (2 mg), MBA (1.2 mL 50 mM), and SDS (100 μL 100 mM) was added to a flask, and the mixture was stirred at 70 °C for 30 min with air-purging of Ar. Then APS (1.0 mL 10 mM) was injected to initiate the polymerization reaction. To form the nanoscaled cross-linked network matrix, the polymerization was allowed to proceed for an additional 3 h in dark at 70 °C. Then the resulting core−shell particles were centrifuged and washed with distilled water and methanol to eliminate unreacted monomer and other low molecules. 2.4. Measurement of Photothermal Performance. For measuring the photothermal conversion performance of the core− shell nanocomposites, 1 mL of PDA@PNIPAm aqueous solutions with various concentrations (0−100 μg/mL) were placed into several quartz cuvettes and then irradiated with an 808 nm NIR laser for 10 min, respectively. Temperature variation of the core−shell PDA@ PNIPAm nanocomposites solution was measured by using an infrared thermometer at each time interval. Simultaneously, 1 mL of distilled water served as blank control group, and its temperature was evaluated at the same condition. 2.5. Pesticide Loading Content. IMI was dissolved in deionized water with a concentration of 0.1 mg/mL, and 60 mg PDA@PNIPAm nanocomposites with various ratios of NIPAm and PDA were dispersed in 25 mL of IMI aqueous solution under magnetic stirring at room temperature. After 12 h of incubation, the mixed IMI/PDA@ PNIPAm solution was collected by centrifugation at 4000 rpm for 5 min, and then 2 mL of the suspension was collected for UV−vis spectro-photometer measurement at 271 nm to determine the loaded amount of IMI. 2.6. Temperature and Light-Responsive Pesticide Releasing Test. To evaluate thermoresponsive IMI release, pesticide-loaded IMI/PDA@PNIPAm nanocomposites were suspended in deionized water and agitated at 15, 25, and 40 °C for 20 h. At different time intervals, the suspension was centrifuged (4000 rpm, 5 min) and collected for the IMI quantification, then refilled with the same volume of fresh buffers and resuspended. Next, pesticide-loaded PNIPAm polymer and IMI/PDA@PNIPAm nanocomposites with various ratios between PNIPAm and PDA were placed in the heating bath set to the temperature at 15 °C for 10 h, and then the temperature of the heating bath was set at 40 °C for another 15 h. The amount of pesticide released into the medium was measured at each time interval. For NIR-trigged IMI release, 5 mL of IMI/PDA@PNIPAm suspension at a concentration of 60 μg/mL was exposed to the 808 nm NIR light (2 W/cm−2) for 30 min at different time points (1, 2.5, 5, 7.5, and 10 h). One milliliter of the supernatants was collected at predetermined time to analyze IMI absorbance at 271 nm, and the samples were then redispersed for further irradiation. The suspension incubated in dark condition was used as a negative control. The cumulative amount of IMI released from the nanocomposites was calculated according to the following equation:

pesticides release, since these systems are still confronted with some critical issues: (i) high production cost of gold nanomaterials; (ii) lack of drug loading capacity of the single gold nanomaterial due to the their relatively small surface area;18 (iii) complicated and lengthy fabrication process, followed by intensive washing to remove chemical surfactants and toxic organic solvents.19 As a family of novel functional nanomaterials, polydopamine (PDA) nanoparticles were demonstrated to possess a photothermal conversion efficiency of 40%, much higher than that of widely used gold nanorod (22%).20 As a desirable photothermal agent, PDA have been applied in photothermal therapy and NIR-controlled release systems.21−24 Moreover, PDA nanoparticles were completely composed of naturally occurring dopamine yet could be easily prepared through the self-polymerization of dopamine a weakly alkaline solution (i.e., pH = 8.5). Benefiting from the simpler and cost-effective synthesis strategy, the intriguing and natural adhesive PDA materials have been applied in farming fields for controlled release of pesticide8,25 and fertilizer.4 Most importantly, PDA materials contain plentiful chemically active amino groups, catechol groups, and aromatic rings on their surface, endowing them with relatively high loading or adsorbing capabilities toward chemical drugs26,27 or basic dyes28,29 via π−π stacking and hydrogen bonding. Therefore, PDA nanoparticles with satisfactory photothermal efficiency, low cost, easy fabrication, and high loading capability can potentially act as an alternative to gold-based nanoparticles,30 thereby showing bright prospect in constructing a NIR lightresponsive formulation for controlling pesticide release. Herein, we fabricated novel core−shell polydopamine@ PNIPAm nanocomposites (PDA@PNIPAm) that can be used as an NIR light-controlled release targeted system for pesticide. At the core of our innovation is NIR-responsive PDA microsphere that is surrounded by a poly(N-isopropylacrylamide) polymer shell (PNIPAm), which was used as both the medium of the pesticide and the photothermally sensitive gatekeeper. To the best of our knowledge, until now no work has been reported on stable colloidal PDA microspheres modified with PNIPAm shells. Imidacloprid (IMI), accounting for 11−15% of the total insecticide market, was chosen as a model pesticide encapsulated in the nanocarrier because of its worldwide and heavy application in agriculture (for over 140 agricultural crops).31 Meanwhile, the positive relationship between IMI pesticide effect and surrounding temperature provides a good reason for using the core−shell PDA@ PNIPAm nanocomposites, which could simultaneously deliver IMI and increase the pesticide temperature when exposed to sunlight, thereby enhancing the efficacy of killing insect. The structure of the PDA@PNIPAm core−shell nanocomposites was characterized by transmission electron microscopy (TEM), scanning electron microscopy (SEM), Fourier transform infrared (FT-IR) spectroscopy, ultraviolet−visible (UV−vis) spectroscopy, dynamic light scattering (DLS), and thermogravimetric analysis (TGA). The core−shell PDA@PNIPAm nanocomposites were primarily assessed for their photothermal effect and pesticide loading capacity, and then the stimuliresponsive IMI release from the IMI-loaded PDA@PNIPAm (IMI/PDA@PNIPAm) was evaluated with the application of stimuli including NIR light and temperature.

2. EXPERIMENTAL SECTION 2.1. Materials. Dopamine hydrochloride, N-isopropylacrylamide (NIPAm), N,N′-methylenebis(acrylamide) (MBA), sodium dodecyl

pesticide release efficiency(%) = 6425

Wr × 100 We

(1)

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ACS Applied Materials & Interfaces Scheme 1. Proposed Mechanism for the Formation of Core−Shell PDA@PNIPAm Nanocomposites

Figure 1. SEM images of the PDA microspheres (a−c) and PDA@PNIPAm nanocomposites (d−f) and TEM images of the PDA microspheres (g, h) and PDA@PNIPAm nanocomposites (i). where We and Wr are the mass of pesticide entrapped in the obtained nanocomposites at equilibrium state and released from pesticideloaded nanocomposites at time t during the release process, respectively. 2.7. Sample Analysis. The functional groups of the products were confirmed using a PerkinElmer FTIR System 2000 in 600−4000 cm−1 range via KBr pellet. The hydrodynamic diameters of PDA

microspheres and PDA@PNIPAm nanocomposites were determined by DLS (ZetaSizer ZS90, Malvern). A Hitachi S-4800 SEM and Tecnai G2−20 TEM were used to observe their surface morphologies. UV− vis−NIR spectra were obtained using a Tecan Infinite M200 spectrophotometer. The concentrations of IMI in the adsorption and release experiments were determined by Shimadzu-18A UV−vis spectrophotometer. The NIR light was produced by an NIR laser (808 nm, 2 6426

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Figure 2. (a) TGA curves of pristine PDA, PNIPAm, and PDA@PNIPAm in nitrogen atmosphere. (b) FT-IR spectrometry analysis. (c) UV−vis spectra of dopamine, PDA, and IMI/PDA@PNIPAm. (inset) Photograph of aqueous solutions of dopamine and PDA. (d) Hydrodynamic diameter change of the PDA microsphere and PDA@PNIPAm nanocomposites at various temperatures.

polymerization to form PDA microspheres.35 This procedure was coupled with a color change of the solution from pale brown to dark brown. Subsequently, the obtained PDA microspheres were introduced into N-isopropylacrylamide solution containing the cross-linker MBA and the APS freeradical initiator. The PDA microspheres can easily capture Nisopropylacrylamide monomer and act as active sites for the polymerization reaction, since PDA is rich in amine and catechol functional groups on its surface. As a result, a crosslinked poly(N-isopropylacrylamide) polymer layer was coated onto the surface of PDA microsphere by seeded precipitation polymerization, forming a well-defined core−shell structure for efficient loading of small pesticide molecules. In the process of pesticide loading, the entrapped IMI may possibly undergo two distinct major interactions with PDA@PNIPAm to be encapsulated into the as-prepared nanocomposite. One resulted from π−π stacking and hydrogen interaction existing between IMI molecules and the primary amino and catechol groups in the PDA cores.36 These interactions of poorly soluble molecules and PDA could enable a high IMI payload within the as-prepared nanocomposite and endow the nanocomposite with NIR-sensitive property, which has gained extensive interests in previous study.37 The second interaction was the physical entrapment of IMI inside the polymer matrix, since the cross-linked network structure of the PNIPAm matrix can promote pesticide encapsulation and finally endow the core− shell nanocomposites with temperature-sensitive property.38 To verify the successfully synthesized PDA microspheres and PDA@PNIPAm nanocomposites, SEM and TEM images were employed to characterize the core−shell structures of the final products, as displayed in Figure 1. SEM observation of the above-obtained PDA microspheres indicated that PDA micro-

W/cm2), and the temperature variation of PDA@PNIPAm nanocomposites aqueous solution was monitored using a noncontact infrared thermometer (WH380, WHDZ).

3. RESULTS AND DISCUSSION 3.1. Synthesis and Characterization of the Core−Shell PDA@PNIPAm Nanocomposites. In this study, we devised an NIR light and temperature remote-triggered pesticide delivery system based on the photothermal PDA dispersed in cross-linked PNIPAm matrix, which undergoes a reversible phase transition in water from an extended random coil to a dense globular conformation when the temperature is greater than 32 °C.33,34 Such design combines synergistically photothermal properties and thermoresponsive properties in a single nanoplatform; the PDA embedded inside the PNIPAm matrix could serve as an antenna to absorb the light and convert it to heat, which will induce shrinkage of the PNIPAm matrix and facilitate the release IMI from the interior of polymer matrix. The application of PDA microspheres embedding immobilized approach is advantageous compared to other photothermal nanoparticles such as gold nanoparticles owing to easy fabrication and scale-up, low cost, and high loading, since the introduced PDA microspheres not only exhibit strong photothermal effect but also provide additional active surface for IMI immobilization. As depicted in Scheme 1, the preparation of the core−shell nanocomposites was started from synthesis of PDA microspheres according to a well-developed method.8 In mix of water, ethanol, and ammonia, dopamine monomer was first oxidized and cyclized to dopaminechrome, followed by rearrangement to produce an intermediate named 5,6dihydroxyindole, which further suffered from intermolecular 6427

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was larger due to the swelling of the PNIPAm shell in aqueous solution, as shown in Supporting Information. The size variation of PDA@PNIPAm nanocomposites at various temperatures is possibly owing to the dehydration of PNIPAm polymer chains and the collapse of the hydrophilic segments.44 Benefiting from the smart swollen/shrunken feature, the pesticide-loaded PDA@PNIPAm nanocomposites were supposed to gradually squeeze out the pesticide at a moderately high environmental temperature and finally achieve the desired pesticide effect. 3.2. Photothermal Effect of the Core−Shell PDA@ PNIPAm Nanocomposites. Prior to construction of the multifunctional pesticide release system, the photothermal conversion capability of core−shell PDA@PNIPAm nanocomposites under irradiation needs to be evaluated to validate their potential as NIR-responsive materials. In this section, to examine whether the amount of generated heat depends on the concentration of nanocomposites, we investigated the changes in the temperature of aqueous PDA@PNIPAm with different concentrations ranging from 20 to 100 μg/mL under NIR light irradiation with an 808 nm laser at 2 W/cm 2 for 10 min. As seen in Figure 3, the temperature of all the mediums containing

spheres possess perfect and regular spherical structure with an average size of ∼250 nm (Figure 1a,b) and showed good dispersibility and smooth surfaces (Figure 1c). By contrast, the PDA@PNIPAm nanocomposites were narrowly dispersed spherical microparticles with an increased particle size (∼300 nm, Figure 1d,e) as well as relatively coarser surface (Figure 1f). The change of surface morphology is due to the successful coverage of PNIPAm polymer shell on the surface of PDA substrate, which is consistent with previous study.39 Moreover, the regular spherical structure of the PDA microspheres (Figure 1d,e) and a typical core−shell structure of PDA@PNIPAm with PDA microspheres as the core and PNIPAm polymer as the outer shell was vividly displayed by the TEM image (Figure 1f). As can be observed, the PNIPAm polymer shell with a thickness of ∼30 nm was in a doughnut shape that surrounded the PDA microspheres well, further demonstrating the existence of PNIPAm thin layer on the surface of virgin PDA scaffold. The outer PNIPAm shell could act as a container to hold the active agents in the pesticide-loading process and as a gatekeeper to control the release speed of the loaded active ingredients into the surrounding medium. The presence of PNIPAm polymer shell on the PDA surface was further verified by TGA (Figure 2a). Pristine PNIPAm exhibited drastic thermal decomposition between 200 and 500 °C due to the decomposition of the PNIPAm polymer, and the weight left was found to be ∼6.7%. For the PDA microspheres, the residue mass was found to be up to ∼58.6%, which derives from their high residual rate during pyrolysis.40 Compared with PDA microspheres, PDA@PNIPAm nanoparticles showed ∼40.6% weight loss within the same temperature frame, which suggests that the PDA microsphere was successfully capped by a PNIPAm polymer layer. Furthermore, the chemical compositions of pristine dopamine, PDA, PNIPAm, PDA@ PNIPAm, and IMI/PDA@PNIPAm were characterized by FTIR spectrometry (Figure 2b). For the FT-IR curve of PDA, the absorption bands at 1520, 1615, and 3420 cm−1 corresponded to the shearing vibration of N−H in the amide group, aromatic rings, and the −OH groups in catechol, respectively, suggesting the successful polymerization of dopamine.41 The PDA@ PNIPAm had a similar FT-IR absorbance as to the pristine PNIPAm, and the absorbance peaks at 1660 and 1550 cm−1 were attributed to the C−O stretching and the secondary amide N−H deformation vibration of PNIPAm,42 further confirming the presence of PNIPAm in the PDA@PNIPAm. In the UV−vis spectra (Figure 2c), unlike dopamine monomer, PDA showed a pronounced absorption ranging from UV to NIR wavelengths due to the oxidation of dopamine into dopachrome and dopaindole and their subsequent selfpolymerization process,43 in which a color change of the solution was detected from colorless to deep brown (the inset image of Figure 2c). Compared with PDA, PDA@PNIPAm displayed a broad NIR plasmon absorption peak after coating with temperature-responsive polymer, indicating PNIPAm coating does not impede their capability to convert NIR light into heat. As for the DLS analysis (Figure 2d), the size change of PDA microsphere is negligible observed, while the hydrodynamic diameter of the PDA@PNIPAm nanocomposites start to decrease when the temperature is elevated to 32 °C, implying that the core−shell PDA@PNIPAm nanocomposites are temperature-dependent. In comparison with the data observed by SEM and TEM, the hydrodynamic diameter of PDA particles (254.5 nm) remained unchanged, while the size of polydopamine@PNIPAm (326.2 nm) at 25 °C

Figure 3. Temperature changes of pure water and various concentration of PDA@PNIPAm aqueous under irradiation with NIR light (808 nm, 2 W/cm2).

PDA@PNIPAm nanocomposites increased gradually with exposure time, while pure water showed negligible temperature change under identical irradiation conditions. This phenomenon indicates that the PDA@PNIPAm efficiently converts the photo energy into thermal energy by absorbing light and produces enough heat to cause a substantial temperature enhancement, confirming that the photothermal conversion of PDA@PNIPAm could be induced by sunlight as well as by NIR light. In addition, the amount of PDA@PNIPAm nanocomposites exerted a great influence on the temperature of the surrounding medium, and the temperature increased monotonically with the stepwise increase in the nanocomposite concentration. For the PDA@PNIPAm nanocomposites aqueous solution at concentrations ranging from 20 to 100 μg mL−1 irradiated for 10 min, the temperature increment varied from 10.2 to 24.2 °C (Figure S2). These results imply that the concentration and exposure time dominate the degree of temperature increase and can be tailored for specific application. For example, even though the environment 6428

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surrounding medium.45 Consequently, lower IMI loading was observed for the PDA@PNIPAm nanocomposite with higher amount of NIPAm. For further exploring the potential mechanism behind the slow adsorption rate of IMI on PDA@PNIPAm, the experimental data were then fitted to the following pseudofirst-order equation, pseudo-second-order model, and intraparticle diffusion model, respectively.46

temperature is below the melting point of the PNIPAm nanoparticles, the switching temperature can be easily achieved by increasing the concentration of PDA@PNIPAm nanocomposites. Therefore, it can be expected from the results that PDA@PNIPAm nanocomposites have significant potential as a light-responsive release system to trigger the release of the loaded pesticide with the utilization of polydopamine photothermal agent and a thermosensitive matirx. 3.3. Enhanced Pesticide Loading of the Core−Shell PDA@PNIPAm Nanocomposites. For pesticide delivery systems, the high agrochemicals loading capacity is one of the most important performance evaluation criteria. In this section, the IMI adsorption kinetics and isotherm of PDA@PNIPAm with various NIPAm and PDA ratios were depicted in Figure 4,

ln(qe − qt) = ln qe − k1t

(2)

t 1 t = + qt qe k 2·qe 2

(3)

qt = K idt 1/2 + C

(4)

where qe and qt (μg/mg) represent the adsorption capacities at equilibrium and at any time (min), separately. k1 (min−1), k2 (μg/mg·min), and kid (μg/mg·min1/2) are the rate constants, and C (μg/mg) is the intercept. The calculated relevant parameters were tabulated in Table S1. From Figure 4 and the obtained correlation coefficients (R2) of Table S1, it is evident that the adsorption of IMI onto PDA@PNIPAm nanocomposites could be best described by the pseudo-secondorder model, while the IMI loading behavior of PNIPAm followed the pseudo-first-order. It signifies that the IMI loading process onto PDA@PNIPAm nanocomposites is controlled by a relatively strong chemical adsorption process instead of a common physisorption one, and the IMI adsorption of PNIPAm is mainly a physical adsorption process. Consequently, in the core−shell PDA@PNIPAm formulation, the PDA microspheres presumably provide a more compatible “molecular glue” environment for the ring structure of IMI, and the PNIPAm shell can also act as a medium for loading IMI. Moreover, the regression of qt versus t1/2 for the intraparticle diffusion model is found to be linear, and the linear plots do not pass through the origin point (Figure S3). This phenomenon demonstrates that the pore diffusion was also a rate-controlling step during the pesticide loading process. 3.4. Temperature-Responsive Pesticide Release from the Core−Shell PDA@PNIPAm Nanocomposites. Since the driving force for pesticide release is temperature-induced shrinking process of the PNIPAm polymer with a low lower critical solution temperature (LCST) of 32−33 °C, thermalsensitive release profiles were exploited at various temperatures to assess the temperature stimuli responsiveness of pesticideloaded nanocomposites. Several representative pesticide release profiles from IMI/PDA@PNIPAm nanocomposites at 15, 25, and 40 °C are shown in Figure 5a, where the percent of IMI escaped is plotted against time at the designated temperature. As shown in Figure 5a, the amount of IMI released was essentially negligible at 15 °C, and there was a slight increase (∼20.5% within 5 h) at 25 °C, although the shrinking point of PNIPAm was still slightly higher than this temperature. In comparison, at 40 °C, the fastest drug release behavior was observed, and up to 64.3% of the encapsulated IMI was continuously released over the same period of time. The reason for the temperature-induced variation of the release rate is that the overall physicochemical property of the IMI/PDA@ PNIPAm core−shell nanocomposites has strong temperature dependence.47 At low temperature the IMI/PDA@PNIPAm nanocomposites network was fully swollen, and the pesticide was entrapped inside the PNIPAM shell, leading to a dramatic

Figure 4. Kinetics showing the adsorption of IMI by PDA@PNIPAm and PNIPAm with various PDA: NIPAm mass-to-volume ratios.

in which pristine PNIPAm also served as a reference in the assessment of pesticide loading property. As shown, the adsorption of IMI onto PDA@PNIPAm took place immediately and underwent an increase at a rapid rate during the first 5 h, followed by a much slower second step until this increment stopped after 12 h, suggesting the IMI adsorption is already saturated. By contrast, the IMI loading amount for PNIPAm is an especially faster process, and only 6 h was needed to reach the equilibrium state. And the loading capacity at equilibrium of PDA@PNIPAm for the concentration of 1 mg/mL can reach up to 46.7, 62.9, 54.2 μg/mg, corresponding to mass-to-volume ratios of 1:3, 1:5, and 1:7 between PDA and NIPAm, which are considerably higher than that of the virgin PNIPAm (36.4 μg/ mg). Obviously, the PNIPAm coating capped onto PDA microspheres significantly affected IMI’s absorbing efficiency, that is, the loading efficiency of IMI increased after embedding PDA in PNIPAm matrix, yet decreased with increasing the adding amount of NIPAm monomers. The enhanced loading capacity may be due to the imbedding of PDA microspheres into the network of PNIPAm matrix, because PDA microspheres are rich in phenyl, amino, and hydroxyl functional groups on their surface. These groups could afford numerous active sites for binding IMI molecules via π−π stacking and hydrogen-bond interaction, endowing PDA@PNIPAm the superior capability to load agricultural chemicals. With adding excessive N-isopropylacrylamide monomers, however, more homopolymerization of N-isopropylacrylamide occurred, and the movement of free radicals and NIPAm monomers was simultaneously hindered due to the enhanced viscosity of the 6429

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comparison with PNIPAm nanoparticles, nanocomposite embedded with PDA nanoparticles not only represents a burst-release mode by taking advantage of the immediate shrinking of PNIPAm matrix but also possesses a sustained release based on the pesticide diffusion from PDA surface under the same simulated conditions. 3.5. Near-Infrared Light-Responsive Pesticide Release from the Core−Shell PDA@PNIPAm Nanocomposites. In addition to the temperature-sensitive property, the NIR lightdependent characteristic of PDA was also harnessed to endow core−shell PDA@PNIPAm nanocomposites with NIR-responsive property. To further confirm the ability of external stimulus (NIR light) to trigger the IMI release, the IMI/PDA@PNIPAm nanocomposites were exposed to NIR-light irradiation, and the cumulative IMI release was evaluated by monitoring the absorbance at 271 nm using a UV−vis spectro-photometer, as plotted in Figure 6a. In the absence of NIR irradiation, the

Figure 5. (a) Release profiles of IMI from the IMI/PDA@PNIPAm nanocomposites under direct heating to various temperatures (15, 25, and 40 °C) for different periods of time. (b) Release profiles from the particles in a buffer solution with various NIPAm and PDA ratio.

decrease of the release rate of the IMI molecules. At high temperature above the LCST of PNIPAm, the PDA@PNIPAm core−shell nanocomposite was in a collapsed, hydrophobic state, strongly facilitating the IMI molecules to quickly diffuse into the surrounding medium. The obtained results demonstrate that the pesticide carrier indeed holds a thermosensitive releasing capability owing to the thermoresponsive property of PNIPAm, and the release behavior could be easily managed via controlling the environment temperature. Figure 5b shows the release profiles of IMI from the PDA@ PNIPAm nanocomposites with different ratios of NIPAm to PDA at different temperatures (15 and 40 °C). In all cases, there were no significant differences in the release rate of IMI at 15 °C, and only a small amount of IMI was escaped from the tested samples. At 40 °C, IMI was obviously released, and the accumulation releasing curve depended on the weight ratio of PNIPAm to PDA. The IMI release rate of the PDA@PNIPAm nanocomposites was decreased with the increasing of NIPAm, and the fastest release was obtained for the sample with a ratio of 1:7 between PDA and NIPAm, which consisted of more PNIPAm polymer and fewer PDA microspheres. It means that the existence of PDA microspheres inside the nanocomposite further slows pesticide release. This is because during the IMI release process, the certain amount of pesticide that is attached onto the PDA surface via hydrogen-bonding or π−π stacking interactions with a higher loading strength must first escape from the PDA surface into the cross-linked matrix of PNIPAm and subsequently diffuse into the surrounding media.37,48 In

Figure 6. (a) Cumulative release profiles of IMI from IMI/PDA@ PNIPAm nanocomposites with and without NIR-light irradiation (808 nm, 2 W/cm2). (b) Calculated IMI release rate from IMI/PDA@ PNIPAm nanocomposites for repeated on−off cycles.

release profile of IMI presents a rising tendency over time, indicating that IMI molecules diffuse from the PDA@PNIPAm nanocomposites into the surrounding media slowly and continuously. For the first 1 h, only 5.2% of IMI was released, and finally the IMI release was reaching an equilibrium value of 35.4% within 13 h. When the PDA@PNIPAm nanocomposites were under irradiation with NIR light, the IMI release was 6430

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ACS Applied Materials & Interfaces Notes

greatly enhanced and significantly reduced when the external trigger (NIR light) was turned off over the next 0.5 h of incubation. For instance, the cumulative release of IMI was measured by 15.7% after 30 min of NIR irradiation, which was almost threefold higher than that without light (5.2%). The NIR light-triggered IMI release is probably due to PDA microspheres dispersed in the cross-linked network of PNIPAm matrix, which can readily absorb and convert the NIR light into heat energy. The generated heat has the ability to dissociate the electrostatic interactions between IMI and the polymer matrix,32 increase the temperature above the LCST, rapidly shrink the volume size of the nanocomposites, and finally squeeze out the loaded IMI into the external media.49 More importantly, the release rates of IMI were tightly related to volume change of the polymer matrix with NIR-dependent swollen/shrunken behavior, as plotted in Figure 6b. The release rate was measured by 21.5% h −1 under first irradiation, quickly reducing to below 6.4% h −1 after 2 h of incubation in the dark, while increasing again to 16.6% h −1 during the second treatment cycle and significantly decreasing again under the shading condition. This IMI release pattern was observed periodically and for entire time of experiment, suggesting that the core−shell PDA@PNIPAm nanocomposites possess the continuous photothermal-responsive capacity and that the release rate of IMI can be controlled by switching NIR-light irradiation.

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by Shaanxi Provincial Natural Science Foundation of China (No. 2015JM2071), National Natural Science Foundation of China (No.21176031), Fundamental Research Funds for the Central Universities (Nos. 310829172201, 310829172202, 310829175001, and 310829165027) and State Key Laboratory of Plateau Ecology and Agriculture (Qinghai Univ.).

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4. CONCLUSIONS In summary, we fabricated novel core−shell PDA@PNIPAm nanocomposites that can be used as an NIR light-controlled release-targeted system for pesticide. The core PDA microspheres, which provided additional active sites for pesticide, can be proposed as alternative to conventional gold-based nanoparticles because of their excellent NIR sensitivity, low cost, and easy fabrication. The poly(N-isopropylacrylamide) thermosensitive polymer shell functioned as both the medium of the pesticide and the photothermally sensitive gatekeeper. The environment temperature and external NIR irradiation have an obvious influence in photothermal-responsive release property, that is, the release of the entrapped IMI molecules from the core−shell PDA@PNIPAm nanocomposites was enhanced by increasing temperature and more greatly under NIR-light irradiation. Therefore, this system with photothermal-responsive behavior has very broad applicability as a pesticide or drug delivery system in the fields of agriculture and pharmaceuticals.

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.6b15393. Detailed information including kinetic parameters, size distribution, temperature change, intraparticle diffusion plots of the PDA particles, and core−shell PDA@ PNIPAm nanocomposites (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Fax: +86 298 233 9961. Phone: +86 298 233 0952. ORCID

Bo Bai: 0000-0002-3958-9874 6431

DOI: 10.1021/acsami.6b15393 ACS Appl. Mater. Interfaces 2017, 9, 6424−6432

Research Article

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DOI: 10.1021/acsami.6b15393 ACS Appl. Mater. Interfaces 2017, 9, 6424−6432