Magnetically Navigated CoreâShell Polymer Capsules as

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Applications of Polymer, Composite, and Coating Materials

Magnetically navigated core-shell polymer capsules as nanoreactors loadable at the oil/water interface Joanna Odrobi#ska, El#bieta Gumieniczek-Ch#opek, Micha# Szuwarzy#ski, Agnieszka Radziszewska, Sylwia Fiejdasz, Tomasz Str#czek, Czes#aw Kapusta, and Szczepan Zapotoczny ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.8b22690 • Publication Date (Web): 27 Feb 2019 Downloaded from http://pubs.acs.org on February 28, 2019

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ACS Applied Materials & Interfaces

Magnetically navigated core-shell polymer capsules as nanoreactors loadable at the oil/water interface Joanna Odrobińska,† Elżbieta Gumieniczek-Chłopek,‡,† Michał Szuwarzyński,# Agnieszka Radziszewska,≠ Sylwia Fiejdasz,‡ Tomasz Strączek,‡ Czesław Kapusta,‡ Szczepan Zapotoczny†*

†

Faculty of Chemistry, Jagiellonian University, Gronostajowa 2, 30-387, Krakow, Poland

‡

Faculty of Physics and Applied Computer Science, AGH University of Science and

Technology, A. Mickiewicza Ave. 30, Poland, 30-059 Krakow, Poland #

AGH University of Science and Technology, Academic Centre for Materials and

Nanotechnology, al. A. Mickiewicza 30, 30-059 Krakow, Poland ≠ Faculty

of Metals Engineering and Industrial Computer Science, AGH University of Science

and Technology, A. Mickiewicza Av. 30, 30-059 Krakow, Poland

KEYWORDS: polymer nanocapsules, magnetic nanoparticles, core-shell capsules, amphiphilic polymers, oil water interface

ACS Paragon Plus Environment

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ABSTRACT Polymer core-shell nanocapsules with magnetic nanoparticles embedded in their oil cores were fabricated and applied as nano(photo)reactors. Superparamagnetic iron oxide nanoparticles (SPIONs) coated with oleic acid were first synthesized, characterized structurally and their magnetic properties were determined. The capsules with chitosan-based shells were then formed in a one-step process by sonication-assisted mixing of (1) an aqueous solution of the hydrophobically derivatized chitosan and (2) oleic acid containing the dispersed SPIONs. In such a way magnetic capsules with diameter of ca. 500-600 nm containing encapsulated SPIONs with an average diameter of ca. 20-30 nm were formed as revealed by dynamic light scattering and scanning transmission electron microscopy measurements. The composition and magnetic properties of the formed capsules were also followed using e.g., dynamic light scattering, electron microscopies and magnetic force microscopy. The water-dispersible capsules, thanks to their magnetic properties, were then navigated in a static magnetic field gradient and transferred between the water and oil phases, as evidenced using fluorescent microscopy. In such a way the capsules could be loaded in a controlled way with a hydrophobic reactant, perylen, which was later photooxidized upon transferring the capsules to the aqueous phase. The capsules were shown to serve as robust reloadable nanoreactors/nanocontainers that via magnetic navigation can be transferred between immiscible phases without disruption. These features make them promising reusable systems not only for loading and carrying lipophilic actives, conducting useful reactions in the confined environment of the capsules but also for e.g. magnetic separation and guiding of the encapsulated active molecules to the site of action.


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INTRODUCTION Magnetic remote navigation and drug targeting towards the intended pathology sites as well as magnetically controlled release of biologically active compounds are the current challenges in the development of smart multifunctional drug delivery systems.1 Micro(nano)encapsulation techniques like emulsion polymerization, interfacial polymerization, emulsification or salting out that have gained interest in biomedical applications2–4 may be used for that purpose. Encapsulation of the cargo molecules provides advantages such as enhanced bioavailability of lipophilic drugs, isolation and protection of active sensitive compounds like vitamins and carotenoids from aggressive biological environment, better therapeutic efficacy, limitation of the side effects and altering the release of the actives in a controlled manner.5,6 Such nano and microcarriers can be loaded not only with chemotherapeutic drugs but also with corrosion inhibitors,7 quantum dots8 or magnetic nanoparticles that may enable magnetic navigation of the carriers to the desired site of action.9 They can also be used for local heating in hyperthermal anticancer therapy or magnetically-triggered release of active compounds10-12 as well as labeling of organs to enhance the contrast in Magnetic Resonance Imaging.13 Theranostic approach – combining therapeutic functionality (e.g., drug carriers) and diagnostics (e.g., MRI imaging) is of particular interest for such systems.14,15 Magnetic containers may be also used in tissue engineering guiding cells to a desired site of action and simultaneously delivering bioactive molecules,16 as well as for magnetic field-enhanced cell seeding.17,18 Among a number of magnetically responsive systems like liposomes,19-21 microspheres,22,23 magnetomicelles,24 core-shell nanoparticles,25 polymerosomes,26,27 the magnetic capsules gain increasing interest as they provide numerous advantages, such as long term stability during storage, high loading capacity, physical and chemical versatilities of the capsule’s shells that can be


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engineered for specific applications. Generally, magnetic nanoparticles can be incorporated in the capsules’ cores28–31 or shells.11,32–37 A versatile technique for preparation of the capsules with magnetic shell is the layer-by-layer (LbL) assembly technique,38,39 which involves the alternating deposition of various materials (e.g. polyelectrolytes, proteins, nucleic acids, lipids, inorganic nanoparticles), assembled through complementary interactions (e.g., electrostatics, H-bonding) onto colloidal templates such as calcium carbonate, polystyrene or silica,40–42 followed by decomposition of the template leaving hollow capsules (aqueous core). Although there are some recent reports on mechanical enhancement of such capsules43 they commonly suffer from limited mechanical stability and require a separate step for loading them with desired active substance. Incorporating magnetic nanoparticles inside the capsules’ cores can be achieved by e.g., pHinduced precipitation of inorganic salts in the capsules interior44 or depositing polyelectrolytes on stabilized oil droplets containing magnetic nanoparticles.31 Formation of such systems via LbL assembly is also a multistep time-consuming procedure and the formed oil cores require stabilization by low molecular weight surfactants that can upon dilution or addition of some organic solvents partially diffuse from the oil/water interface decreasing the stabilization. To overcome those limitations we proposed application of amphiphilic graft polyelectrolytes45–48 as exclusive stabilizers of the oil-core nanocapsules that can be formed in a simple one-step procedure. The hydrophobic arms of that polymers anchor into the oil droplets at the water-oil interfaces ensuring long term stabilization of the nanocapsules without the need of additional surfactants. Such hydrophobic cores may serve as an environment for hydrophobically modified magnetic nanoparticles and/or hydrophobic drugs while the hydrophilic shell ensures the stabilization of the capsules in an aqueous medium. For biomedical applications biocompatible


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natural polysaccharides like chitosan, dextran, alginate, cellulose, and hyaluronic acid and their amphiphilic derivatives are highly attractive as their properties can be easily adjusted. Controlled (un)loading of the oil-core microcapsules dispersed in water is also a challenge for their applications as micro(nano)reactors.49,50 Although they may provide a confined environment for the reactions proceeding in hydrophobic solvents after completing the reaction they should typically be disintegrated to release the products and the system cannot be used for the subsequent cycles.51 Magnetic core of the capsules in combination with the semi-permeable walls would allow us to carry out chemical reactions inside the capsules in a cyclic manner by sequential magnetically-driven transferring them between two immiscible phases (loading reactants – reaction - unloading products). Such reusable nanoreactors possess great potential for carrying out chemical reactions in a controlled and highly efficient way49 but they can be also utilized in e.g. environmental protection for effective removal of organic pollutants from the wastewater.52, 53 Moreover, the magnetic cores of the capsules allows for the magnetic separation that is a powerful method for the purification of biomolecules. The magnetic separation is also an attractive alternative to filtration or centrifugation providing also opportunity for sorbent regeneration and recovery of loaded species.54 Herein, we report a facile one-step method for the formation of the magnetic capsules in which hydrophobic molecules may be also encapsulated so they might serve for magnetically guided delivery of therapeutic or diagnostic agents. The studies focus on their applications as nano(photo)reactors that via remote navigation with magnetic field could be transferred between two immiscible phases enabling their loading with reactants and conducting reactions in a cyclic manner.


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EXPERIMENTAL SECTION Materials Superparamagnetic iron oxide nanoparticles hydrophobically modified with oleic acid were prepared according to the method described earlier,55 vacuum-dried at 60˚C, and dispersed in oleic acid. Amphiphilic chitosan derivative (CChit-C12) containing both, quaternary ammonium (with degree of substitution DS = 67.5 %) and N-dodecyl groups (DS = 2.0 %) was synthesized according to the previously described procedure.56 The degree of deacetylation of chitosan was determined by elemental analysis to be equal to 78 %. Ferrous sulfate hexahydrate ( ≥99.0%, Aldrich), ferric chloride hexahydrate (98%, Aldrich), ammonia water (25%, POCH Gliwice), toluene (p.a., Chempur), sodium chloride (NaCl, p.a., Lachner), oleic acid (OA, PhEur, Aldrich), n-octadecane (p.a., Polyscience Corp.), perylene (Pe, gold label, 99.9 %, Aldrich), Rubrene powder (Aldrich), hydrogen peroxide (30 % solution, p.a., Avantor Performance Material Poland S.A., Poland), sulfuric acid (H2SO4, 96 %, Chempur) were used as received. Deionized water was used to prepare all the solutions.

Apparatus Magnetic properties of nanoparticles and their suspensions were measured with a Vibrating Sample Magnetometer of the Quantum Desing Physical Property Measurement System. Magnetization measurements were performed in the function of applied magnetic field at 4 - 300 K temperature range. The Field Cooled (FC) and Zero Field Cooled (ZFC) susceptibility curves were taken in this temperature range at a 100 Oe magnetic field strength for at least three batches of SPION. Before the measurement the sample was cooled without magnetic field from room temperature to 4 K, then it was heated to 360 K under 100 Oe magnetic field (ZFC measurement)


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and again cooled under 100 Oe magnetic field (FC measurement). 57Fe Mössbauer measurements were carried out with a constant acceleration spectrometer in the transmission mode. The 50 mCi 57Co/Rh source was used. The crystal structure of the prepared nanoparticles was characterized with a Siemens D5000 X-ray diffractometer with Cu Kα radiation using graphite monochromator at room temperature. FTIR spectra in attenuated total reflectance (ATR) mode (on diamond) were recorded using an ALPHA FT-IR spectrometer (Bruker). Malvern Zetasizer Nano ZS instrument working at 173° detection angle was used for dynamic light scattering (DLS) measurements. The measurements were performed at 22 °C and the reported data represent the averages from three series of measurements (10-100 runs each) and their standard deviations. General purpose mode was used as the distribution analysis algorithm. Zeta potential was determined also with Malvern Zetasizer Nano ZS apparatus using Laser Doppler Velocimetry (LDV). Confocal microphotographs were collected using an inverted microscope Nikon Ti-E with objective Plan Apo 100×/1.4 Oil. DIC and a confocal system Nikon A1. Steady-state fluorescence spectra were measured at room temperature using SLM Aminco 8100 spectrofluorimeter equipped with a 450 W xenon lamp as a source of light. Nova NanoSEM 450 (FEI, the Netherlands) scanning electron microscope (SEM) operating at 30 keV was used for imaging the surface morphology of the capsules The observations were carried out using scanning transmission electron microscope mode (STEM). Atomic Force Microscope (AFM) images were obtained with Dimension Icon microscope (Bruker, Santa Barbara, CA) working in the Tapping mode in air. Magnetic Force Microscope (MFM) images were acquired using the same microscope working in the Lift mode (lift height of 500 nm). In all the measurements magnetic Co/Cr covered standard silicon cantilevers of normal spring constant of 2 N/m were used. Before scanning the cantilevers were magnetized with a small magnet. A Rayonet photochemical reactor (model RPR-100) equipped


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with 6 lamps (λmax= 300 nm), was used to irradiate samples for the photooxidation studies. Total intensity of the light measured at 312 nm by VLX 3W radiometer was determined to be 4.7 mW/cm2.

Synthesis of magnetic nanoparticles The synthesis of oleic acid-coated superparamagnetic iron oxide nanoparticles (SPIONs) was carried out in an aqueous solution following the co-precipitation method described earlier.55 Briefly, the iron salts in molar ratio Fe(III) : Fe(II) = 2:1 (ferric chloride hexahydrate : ferrous sulfate heptahydrate), and 100 mL of deionized water were stirred for 15 min in a jacketed vessel under nitrogen flow. Ammonia aqueous solution (25%, 25 mL) was quickly added to the reaction mixture while stirring. The reaction mixture was turned black and the precipitate was formed. Oleic acid (1 mL) was slowly added to the reaction mixture over 1 h at 80ºC. The reaction mixture was then transferred to an extractor and the iron oxide nanoparticles were separated with 100 mL toluene. To aid layer separation, a small amount of sodium chloride solution was added. Magnetic chromatography was used to purify the surface-modified nanoparticles. Namely, a dispersion of the magnetic nanoparticles was passed through a column filled with steel wool that was placed in a strong magnetic field provided by neodymium magnets. The nanoparticles that sticked to the wool were then rinsed out of the column with a suitable solvent, without application of magnetic field, and collected. Finally, the nanoparticles were vacuum dried and dispersed in oleic acid.

Preparation of the capsules templated on liquid magnetic cores Chitosan-based nanocapsules were obtained in an ultrasound-assisted emulsification of CChit-C12 aqueous solution (1 g/L in 0.15 mol/L NaCl) and SPIONs (50 g/L) dispersed in oleic acid (100:1


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volume ratio) following previously published procedures for the formation of the oil core nanocapsules.48,57 The mixture was first homogenized using vortex shaker and then sonicated for 30 min at room temperature in the ultrasonic bath.

Preparation of the capsules with solid cores for STEM and AFM imaging The nanocapsules for STEM measurements were obtained using n-octadecane instead of oleic acid as the core oil. Sonication (ultrasonic bath - 540 W, Sonic-6, Polsonic) was performed at 32°C. After sonication the capsules with liquid n-octadecane cores were cooled down to room temperature that led to solidification of the cores. For AFM measurements the capsules obtained according to the procedure described above were deposited on a silicon wafer that was firstly cleaned carefully using “piranha” solution (a mixture of 96 % H2SO4 and 30 % H2O2 solutions with volume ratio of 1:1), rinsed with deionized water and dried in a stream of argon. A droplet of the emulsion containing the capsules was placed on such prepared silicon wafer surface and dried in a stream of argon. Then it was rinsed with deionized water in order to remove the non-adsorbed capsules and finally dried in a stream of argon.

Magnetic navigation of the capsules Magnetic navigation of the capsules was tracked with the use of Fluorescence Microscope Nikon TE2000 with high sensitivity Andor iXon Camera. The observations were carried out in a bright field mode as well as using fluorescence microscopy with appropriate filters: FL1 (UV-2A, Ex 330-380, DM 400, BA 420), FL2 (TRITC, Ex 540/25, DM 565, BA 605/55). The set of 7 neodymium permanent magnets with a magnetic flux density of 78mT (maximum flux density at the top of last magnet was estimated at 470mT) was used to produce magnetic field for the


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magnetic navigation experiments (Scheme S1 in Supplementary Information). The maximum of the magnetic flux density and its gradient were focused onto oleic acid phase near the region of phase boundary (10 mm from it). When necessary, the magnet assembly was positioned at another side of the system to transfer back the capsules to the aqueous phase. Loading of the capsules with perylene and its photooxidation The capsules with magnetic cores dispersed in water were magnetically guided to the oleic acid phase containing perylene (1g/L) (30 min) and then shifted back to the aqueous phase (30 min) (first cycle) using the procedure described above. Then, an aliquot (1 ml) of the aqueous dispersion of the perylene loaded capsules was placed in a quartz cuvette, saturated with oxygen and irradiated in a Rayonet photoreactor for 1h. The aqueous dispersion was then contacted with the oleic acid phase and the capsules were again magnetically transferred to the oleic phase for loading with perylene (second cycle). The perylene emission spectra were measured before and after each loading and photooxidation cycle.

RESULTS AND DISCUSSION Hydrophobically modified SPIONs The obtained iron oxide nanoparticles coated with oleic acid were shown to have an average diameter equal to 24 ± 4 nm as determined using STEM (Figure 1A). The nanoparticles were also extracted to toluene for DLS measurements that revealed their relatively small average hydrodynamic diameter of 27 nm (Figure 1B) indicating a lack of aggregation of the particles in the toluene medium.


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Figure 1. STEM image of the vacuum-dried magnetic nanoparticles (A) and Hydrodynamic diameters of the magnetic nanoparticles coated with oleic acid and dispersed in toluene as measured via dynamic light scattering method (B).

FT-IR analysis was performed to determine the surface composition of the OA-modified magnetic nanoparticles. The bands at 2917 cm−1 and 2851 cm−1 in the spectrum of OA-modified iron oxide nanoparticles (Figure S1) can be assigned to the asymmetric and symmetric CH2 stretching in OA molecules, respectively. Instead of C=O stretching band of the carboxyl group (1711 cm−1) that is typical of pure OA, two new bands appeared at 1629 cm−1 and 1410 cm−1. They are characteristic bands of the asymmetric and symmetric -COO− stretching, respectively. It indicates that OA was chemisorbed as a carboxylate onto the surface of iron oxide nanoparticles.58,59 The results of XRD analysis (Figure S2) of the obtained materials compared to microcrystalline magnetite pattern indicate the inverse spinel structure of the nanoparticles. The shift of the diffraction peaks towards higher angles, well visible at higher angles for (422), (511) and (440) peaks, corresponds to a smaller lattice constant. It indicates the presence of cationic vacancies in their structure, corresponding to the oxidized form of magnetite, i.e. maghemite.60 To determine


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the size of the crystallites the Williamson-Hall method was used. A small angle of inclination of the fitted line indicates a small content of defects in the structure and the size of crystallites determined from intersection with the vertical coordinate axis was determined to be ca. 12.5 nm.61 The magnetization measurements were performed in the function of applied magnetic field in the 4-300 K temperature range (Figure 2). The values of the remanence and coercivity field decreased with increasing temperature up to 100 K. The curves captured at 200 K and 300 K showed the collapsed hysteresis loops with vanishing coercive field and remanent magnetization that are characteristic of superparamagnetic materials.62 Temperature dependences of magnetic susceptibility for cooling at zero magnetic field (ZFC) and for cooling at 100 Oe field (FC) are shown in Figure S3. Each size fraction of the nanoparticles exhibits different anisotropy energy barrier to be overcome by thermal fluctuations of the particle magnetic moment that results in a distribution of their blocking temperatures (TB).63 The average TB of the synthesized magnetic nanoparticles was estimated from the maximum of the ZFC curve (Figure S3) to be equal to 170 K. Thus, above this temperature the nanoparticles demonstrate superparamagnetic behavior64 that is in line with the results of the magnetization measurements.


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Figure 2. Magnetization vs. magnetic field curves for nanoparticles studied

at different

temperatures.

Mössbauer spectra of the nanoparticles coated with oleic acid were measured in order to further characterize their iron oxide core structure. The spectrum measured at liquid helium temperature (4.2K) showed a symmetrical sextet (Figure S4 A) with the isomer shift of 0.375 mm/s that is characteristic of magnetically ordered state of maghemite (-Fe2O3).65 The spectrum measured at room temperature exhibited significant broadening that was reduced for the spectrum collected in the magnetic field applied in the sample plane, i.e. perpendicularly to the propagation vector of gamma rays (Figure S4 C and D). The spectra could be fitted with two sextets corresponding to iron in tetrahedral and octahedral environments in the inverse spinel structure.66 The overall conclusions from the Mössbauer spectra measurements confirmed the presence of the maghemite phase in the nanoparticles and their superparamagnetic properties. More detailed discussion on those results together with the hyperfine parameters obtained from the fits of the spectra (Table S1) are presented in SI.


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Capsules with magnetic properties Core-shell nanocapsules with magnetic cores and amphiphilic polymer coatings were prepared by mixing the aqueous solution of the ionic chitosan derivative grafted with dodecyl chains (CChitC12) with a hydrophobic solvent containing dispersed SPIONs (Scheme 1). The oil droplets formed during mixing and sonication can be stabilized in a aqueous medium without addition of any low molecular weight surfactant thanks to anchoring of the CChit-C12 hydrophobic side chains in the oil phase as we have only recently showed.48,57

Scheme 1. Step-by-step formation of the core-shell capsules composed of chitosan amphiphilic derivative (CChit-C12) shells and oleic acid cores containing magnetic nanoparticles.

Formation of the nanocapsules was followed using DLS measurements in water as well as STEM and AFM in a dry state. Oleic acid was typically used for the formation of the cores as SPIONs were coated with the same molecules in order to better stabilize their dispersion. The capsules for STEM and AFM measurements were formed using n-octadecane instead of oleic acid and the


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preparation was performed at the elevated temperature (32°C). The nanocapsules cores made of n-octadecane solidified at room temperature that enable imaging of the capsules both in air (AFM) and under vacuum (STEM). The results of DLS measurements (Figure 3) confirmed formation of the particles of initial average diameter equal to ca. 600 nm. Relatively high absolute values of zeta potential (ζ = + 21mV) measured for the capsules immediately after their preparation indicated high electrostatic contribution to stability of the formed nanoemulsion likely due to the presence of polymer quaternized ammonium groups in the capsules’ shell. The capsules with magnetic cores stored at 4°C showed long term stability as indicated by insignificant changes of the zeta potentials and average sizes even after ca. 2 months of storage (Figure 3 and Figure S5 in SI).

Figure 3. The changes in time of the number-averaged hydrodynamic diameters and zeta potential (ζ) values of the magnetic capsules stabilized by CChit-C12 during storage at 4˚C. The internal structure of the capsules was visualized by STEM (Figure 4A, and S6 in SI). It can be concluded that the SPIONs were successfully encapsulated in the liquid cores of the capsules. Unfortunately, the thin polymer shell of the capsule could not be clearly imaged here as such


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carbon-based materials produce much smaller contrast as compared to the iron-based nanoparticles. Some nanocapsules did not stay intact at the conditions required for STEM measurements and the released SPIONs could be also seen in the image (Figure 4A). AFM topography measurements of the surface deposited capsules (Figure 4B) showed their somehow distorted spherical shape due to the drying process. Nevertheless, magnetic force microscopy (MFM) confirmed magnetic properties of the obtained particles deposited from their aqueous suspension. The magnetic signal (Figure 4D) could be colocalized with the features present in the height and phase images that can be assigned to the capsules. The stronger magnetic signal was observed for larger capsules and/or their aggregates due to larger local concentration of the encapsulated SPIONs.

Figure 4. STEM image of the capsule with encapsulated SPIONs (dark spots) (A). Atomic force microscopy topography image (B), mechanical phase (C) and magnetic phase (D) images of the capsules with encapsulated magnetic nanoparticles (the arrows point to the same capsules in all three images).

Magnetic navigation Magnetically navigated transfer of the capsules between two immiscible phases (water and oleic acid) (Scheme 2, Scheme S1) was achieved thanks to the application of a static magnetic field with


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its gradient in the direction perpendicular to the oil-water interface. The process was monitored using fluorescence microscopy as the oil phase was labeled with rubrene and another fluorescent probe, perylene, was encapsulated inside the oil magnetic cores of the capsules. The fluorescence of both probes was monitored in the separate fluorescence channels of the microscope. The magnetically-driven pulling of the capsules from the water to oil phase was observed for 30 min and the respective images of the oil/water interface were captured before and after the pulling (Figure 5). One can easily notice accumulation of the capsules at the interface (Figure 5A, marked with red lines) while comparison with Figure 5B leads to the conclusion that the capsules were actually transported to the oil phase. The images of the interface (insets in Figure 5A and 5B) before the application of the magnetic field show very narrow interfaces for a comparison. Very weak signal assigned to the encapsulated perylene (inset in Figure 5A) indicates very small concentration of the nanocapsules at the interface that significantly increased only during the magnetic pulling experiment.

Scheme 2. Scheme of magnetic navigation of the capsules between the aqueous and oil phases.


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Figure 5. Fluorescent microscopy images of the oil/water interface after 30 min of magneticallydriven pulling of the capsules from water to oil: A – observation in the FL1 channel selective for the perylene fluorescence, B – observation in the Fl2 channel selective for the rubrene fluorescence. The insets present the respective images captured before application of the magnetic field. The penetration of the capsules into the oil phase could be noticed also by optical microscopy (Figure S7). It is certainly not a spontaneous process as no changes were observed at the oil/water interface in the absence of magnetic field or far from the location where it was applied. The capsules were also magnetically pulled from water into the oil phase with dissolved perylene and then transported back to the aqueous phase. The presence of the encapsulated perylene after magnetically-driven loading of the capsules was confirmed by confocal microscopy (Figure 6) and fluorescence spectroscopy (Figure S8 in SI) measurements. Apparently, perylene molecules managed to penetrate through the capsules’ shell into the hydrophobic core while the capsules were pulled into the oil phase. Importantly, the capsules stayed intact after returning to the aqueous


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phase as no significant aggregation of the oil nanodroplets was observed as a result of that experiment and the stable nanoemulsion did not change their appearance (Figure S9 A and D in SI). What is more, the photographs of the same systems but shined with an ultraviolet light (Figure S9 B and C in SI) indicate the presence of perylene in the aqueous phase after loading the capsules and their back transfer to water. It is important to mention that perylene does not exhibit a measurable fluorescence in an aqueous medium and it is only sparingly soluble in water (nM level)67 so the observed fluorescence must be assigned to the perylene residing in the oil cores of the capsules.

Figure 6. The confocal fluorescence image of chitosan-based nanocapsules templated on oleic acid magnetic cores after magnetic navigation with encapsulated perylene that was withdrawn from the oleic phase (DAPI fluorescence filter cube – excitation bandpass filter (340-380 nm); emission bandpass filter (435-485 nm)). Photooxidation of the encapsulated perylene after magnetic navigation process Photooxidation of the encapsulated perylene was used as a model reactions to show the applicability of the system as dispersion of reusable photoreactors that can be cyclically loaded


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with reactants using remote navigation of the capsules. Photooxidation of perylene leads to nonflourescent perylenequinones (Scheme 3) so the progress of the reaction could be easily followed by measuring perylene fluorescence. In the first step, the magnetic capsules were loaded with perylene by bringing them magnetically to the oil phase containing dissolved perylene and subsequent magnetically-driven transfer to the aqueous phase (Figure 7, black curve). This aqueous phase was then subjected to photooxidation that resulted in complete disappearance of the fluorescence signal (Figure 7, red curve) indicating completion of the reaction. The same aqueous dispersion of the capsules was again brought into contact with the oil phase and the magneticallydriven procedure was repeated. Very strong fluorescence signal of perylene (Figure 7, blue curve) indicated very efficient reloading of the nanocapsules with perylene. Importantly, no visible changes of the nanoemulsion was noticed after the photooxidation experiments.

Scheme 3. Composition of the capsules through the magnetic navigation and photo oxidation process


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Figure 7. Steady-state emission spectra of aqueous dispersions of the capsules: loaded for the first with perylene via magnetically-driven transfer to the oil phase containing dissolved perylene (black curve), subjected to photooxidation (red curve), and subsequently reloaded with perylene (blue curve) (excitation wavelength, λex = 410 nm).

CONCLUSIONS Chitosan-based core-shell nanocapsules with magnetic liquid cores were fabricated and applied as robust magnetically reloadable nano(photo)reactors. Superparamagnetic iron oxide nanoparticles (SPIONs) coated with oleic acid were first synthesized and thoroughly characterized. Thanks to their oleic acid coating they could be easily dispersed in both oleic acid and n-octadecane as model hydrophobic solvents. The maghemite structure of the SPIONs was confirmed using XRD and Mösbauer spectroscopy that together with their small size (20-30 nm) ensured their superparamagnetic properties at temperatures above 170 K. The capsules with chitosan-based shells were then formed in a facile one-step process by sonication-assisted mixing of an aqueous solution of the modified chitosan and the oil dispersion of SPIONs. The capsules with an average diameter of 500-600 nm were shown to be very stable (at least 2 months) and able to be magnetically guided to cross the oil/water interface as it was shown using fluorescence


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microscopy. Importantly, the capsules could be loaded with hydrophobic substances dissolved in the oil phase and transfer back to the aqueous phase without disintegration. The performance of the system as robust reloadable nanoreactors was shown for an example of photooxidation of perylene. The capsules were loaded first with perylene via magnetically-driven transfer to the oil phase and then pulled back to the aqueous phase to conduct the photooxidation. After completing the reaction the capsules were reloaded using the same procedure as evidenced via fluorescence spectroscopy. The demonstrated encapsulation of hydrophobic molecules in the studied water-dispersible capsules by bringing them remotely to the oil phase and back is a very promising feature for their applications as reusable and easily reloadable nanoreactors. The crossing of the oil/water interface by the capsules is also important for their potential biomedical applications related to e.g., forced delivery of encapsulated actives through the cell membranes. Thanks to utilization of chitosan, a biocompatible natural polymer, in fabrication of the capsules, those applications will be further developed. ASSOCIATED CONTENT Supporting Information. The following files are available free of charge. Scheme of the magnetic navigation experiment, characterization of the SPIONs: FT-IR spectrum, XRD pattern, magnetic susceptibility, Mӧssbauer spectra and their detailed analysis; characterization of the capsules: DLS measurements, STEM images of capsules, optical microscopy images for the magnetic navigation experiment, photographs of the nanoeulsions before and after the magnetic navigation, fluorescence spectrum of the capsules loaded with perylene. (PDF)


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AUTHOR INFORMATION Corresponding Author To whom correspondence should be addressed, email: [email protected] (Prof. dr. habil. Szczepan Zapotoczny) Author Contributions The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. Notes The authors declare no competing financial interest.

ACKNOWLEDGMENTS J. O. acknowledges the financial support by the Polish National Science Centre (Grant No. 2016/23/N/ST5/01563). E. G.-C. has been partly supported by the EU Project POWR.03.02.0000-I004/16. A. R. acknowledges support by the Ministry of Science and Higher Education of Poland under contract No. 11.11.110.295. C. K., S. F. and T. S. acknowledge a support by the Faculty of Physics and Applied Computer Science AGH UST statutory tasks No. 11.11.220.01/6 within subsidy of Ministry of Science and Higher Education.

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