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Polysaccharide-Coated PCL Nanofibers for Wound Dressing Applications Florence Croisier, Ganka Atanasova, Yves Poumay, and Christine Jérôme* already shown a positive effect on cellular growth.[2] Polysaccharides have recently drawn attention within the field of medical applications.[9] Among them, chitosan is a biosourced polymer derived from the chitin, intrinsically possessing haemostatic, mucoadhesive, antimicrobial and immunostimulant properties.[10–12] This polysaccharide has shown a great potential for biomedical and pharmaceutical applications, on account of its remarkable biocompatibility and biodegradability.[11,13–16] It has notably proved to stimulate cell proliferation and favor histoarchitectural tissue organization.[16] Nevertheless, the electrospinning of chitosan is challenging, notably as it requires high voltages[15] and needs the addition of poly(ethylene oxide), as chitosan can hardly be electrospun alone.[17–19] Moreover, chitosan possesses low mechanical resistance (low elongation at break), particularly in hydrated state, such as wound exudates or cell culture media,[20,21] and usually requires further cross-linking steps to keep a handable biomaterial. To overcome these limitations, we investigate here a novel two-step strategy for the preparation of core-shell fibers (i) having an aliphatic polyester core to sustain mechanical stresses, (ii) exhibiting charges at the core surface[17] to anchor a polyelectrolyte layer and (iii) possessing a polysaccharide coating to preserve the remarkable surface properties of chitosan for wound healing (Scheme 1). Indeed, as already reported,[22,23] poly(ε-caprolactone) (PCL) is a biodegradable[24–26] and biocompatible[27–30] thermoplastic that can be easily electrospun using low voltages. This material, used as the core of the nanofibers, would thus insure the mechanical resistance required to handle the nanofibers in aqueous environments. The presence of a copolymer bearing carboxylic acid groups within the fibers would then allow exposing some charges at the nanofiber surface, as previously reported for polylactide fibers,[17] and polyelectrolytes – such as chitosan and hyaluronic acid – could further be deposited on the fiber surface via a layer-by-layer process (Scheme 1). Layer-by-layer (LBL) assembly was developed[31] as a method for surface coating, based on the alternated adsorption of materials bearing complementary charged or functional groups.[32] LBL enables the controlled deposition of a variety of polyions whereof synthetic and natural materials (among which proteins, organic and inorganic species or nanoparticles) on a wide

Polysaccharide-based nanofibers with a multilayered structure are prepared by combining electrospinning (ESP) and layer-by-layer (LBL) deposition techniques. Charged nanofibers are firstly prepared by electrospinning poly(ε-caprolactone) (PCL) with a block-copolymer bearing carboxylic acid functions. After deprotonation of the acid groups, the layer-by-layer deposition of polyelectrolyte polysaccharides, notably chitosan and hyaluronic acid, is used to coat the electrospun fibers. A multilayered structure is achieved by alternating the deposition of the positively charged chitosan with the deposition of a negatively charged polyelectrolyte. The construction of this multilayered structure is followed by Zeta potential measurements, and confirmed by observation of hollow nanofibers resulting from the dissolution of the PCL core in a selective solvent. These novel polysaccharide-coated PCL fiber mats remarkably combine the mechanical resistance typical of the core material (PCL)—particularly in the hydrated state—with the surface properties of chitosan. The control of the nanofiber structure offered by the electrospinning technology, makes the developed process very promising to precisely design biomaterials for tissue engineering. Preliminary cell culture tests corroborate the potential use of such system in wound healing applications.

1. Introduction The electrospinning (ESP) technique[1] enables the preparation of polymer fibers whose diameter depends on the polymer characteristics and processing conditions,[2] typically ranging from a few nanometers to several microns. The electrospun fiber mats possess high porosity and large specific area, and represent great candidates for biomedical applications, notably for the preparation of wound dressings, artificial skin or tissue engineering scaffolds.[2–8] Indeed, the fiber mats structure mimics skin extracellular matrix and the nanometric scale of electrospun fibers has Dr. F. Croisier, Prof. C. Jérôme Center for Education and Research on Macromolecules (CERM) Department of Chemistry University of Liège Allée de la Chimie 3, B6A Liège 4000, Belgium E-mail: [email protected] Dr. G. Atanasova, Prof. Y. Poumay Cell and Tissue Laboratory URPHYM University of Namur rue de Bruxelles 61 Namur 5000, Belgium

DOI: 10.1002/adhm.201400380

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Scheme 1. Schematic description of the investigated two-step process for the fabrication of the polyelectrolyte-multilayer coated fibers. Step 1: electrospinning of PCL in presence of a copolymer bearing carboxylic acid groups, followed by the immersion of the fibers in pH = 8 medium to obtain the negatively charged fiber core. Step 2: the layer-by-layer deposition of polyelectrolytes on the charged PCL core, to produce the final multilayer-coated fiber.

range of substrates, with defined layer structure and thickness at nanometric scale.[33] The method exploits mainly electrostatic interactions and in this particular case, fabrication of multilayered coatings is accessed by consecutive adsorption of polyanions and polycations on a charged surface.[32] By alternating the deposition of chitosan with the deposition of a negatively charged polyelectrolyte, the construction of such multilayered system becomes accessible. Among negatively charged polyelectrolyte, hyaluronic acid (HA) is a polysaccharide naturally present in the body and deeply involved in the healing process. Indeed, it has already proved a positive effect on cellular proliferation reducing scar formation.[34,35] A wound dressing containing both chitosan and hyaluronic acid could offer great prospects to improve and even accelerate the healing process.[35] Only few examples of layer-by-layer deposition on as-electrospun charged fibers are reported in the literature; main contributions deal with negatively charged cellulose acetate (CA) fibers covered with polyelectrolytes.[36–46] Poly(vinylalcohol) (PVA) fibers showing negative charges were also studied[47,48] as well as poly(acrylic acid) containing fibers.[49] Aiming at evaluating electrospun core/shell fibers with respect to wound dressing applications, we investigated the effect of the polysaccharide coating on cell adhesion and proliferation. For this purpose, we compared fibers coated with a

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chitosan monolayer to fibers coated with a multilayer assembly of chitosan and hyaluronic acid, prepared by layer-by-layer deposition.

2. Results and Discussion 2.1. Preparation of Polysaccharide-Coated Nanofibers To establish the possible beneficial role of chitosan as coating of PCL nanofibers for cells attachment and growth, we first investigated the feasibility to prepare PCL core/polysaccharide multilayer shell nanofibers. For that purpose, we advantageously combined two well-documented technologies, i.e., the electrospinning of poly(ε-caprolactone) in presence of a charged copolymer and the layer-by-layer deposition of polyelectrolytes (Scheme 1). As we formerly reported for polylactide (PLA),[17] charged fibers can be obtained by electrospinning a mixture of PLA and a polyelectrolyte precursor dissolved in a common solvent. In the present work, PCL, another aliphatic polyester which degrades more slowly than PLA, was electrospun in presence of a poly(methyl methacrylate48-b-methacrylic acid25) diblock copolymer from an organic solvent mixture until a manipulable

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to the morphology of the uncoated ones (Figure 1a). Nevertheless, the fibers surface appears more granular in the case of PSS, while smooth with slightly thickened fibers are obtained in the case of hyaluronic acid. These observations could result from the polyelectrolyte deposition. To confirm the actuality of the multilayer assembly, indirect Zeta potential experiments were performed on the fiber mats at each step of the multilayer construction. This technique was previously used to estimate the charge of surfaces made of electrospun fiber mats[17] and was found helpful for estimating the charges present at the nanofiber surface. Figure 2 shows the alternation of the Zeta potential sign along with the succesive deposition of polyelectrolyte layers. As already mentioned, the starting PCL blended fibers (firstly immersed in phosphate buffer) exhibits a negative Zeta potential due to the presence of deprotonated carboxylic acid functions. Then, when fibers are dipped Figure 1. SEM images of PCL fibers electrospun in presence of the poly(MMA48-b-MA25) in the chitosan solution, the Zeta potential (a), covered with chitosan and a bilayer of PSS/chitosan (b) and covered with chitosan and becomes clearly positive, and becomes nega4 bilayers of HA/chitosan (c). tive again when the fibers are dipped in hyaluronic acid solution. Finally, when the fibers are immersed for a second time in chitosan solution, the potenhomogeneous fiber mat was obtained (i.e., 30 min). In the used tial becomes positive again. These results thus clearly display conditions (15wt%, 12kV), no beaded defect was observed in the mat that shows regular fibers of ca. 350 nm in diameter (Figure 1a). The anchoring of a first chitosan layer on the electrospun PCL-based nanofibers was made possible by the presence of the methacrylic acid-based copolymer in the fiber. Indeed, by immersing the fiber mat in a pH = 8 buffer solution during 1 min, the deprotonation of the carboxylic acid functions present at the surface occurs, generating a negatively charged surface as depicted by an indirect Zeta potential around –60 mV measured on the fibers (Figure 2). The fiber mats were then used as substrate for the layer-bylayer deposition of polyelectrolytes. Chitosan, a polysaccharide bearing glucosamine moieties that are positively charged in acidic medium, was used as polycation. In order to validate the multilayer construction, we first used as polyanion the wellknown polystyrene sulfonate (PSS), commonly used in layerby-layer process.[50] In a second time, hyaluronic acid (HA), another polysaccharide, containing carboxylic acid functions and thus bearing negative charges in neutral or basic media, was used as polyanion. Concentration and pH of the solutions for the layer-by-layer deposition process were chosen according to literature.[51–53] LBL technique allows the deposition of layers with a typical thickness of a few to a ten of nanometers.[31,51] Figure 1 shows a representative SEM image of the fibers before (a) and after deposition of chitosan and 1 bilayer of PSS/ Figure 2. Graphic representation of the evolution of the indirect Zeta chitosan (b) or 4 bilayers of HA/chitosan (c). In both cases, the potential of electrospun PCL/poly(MMA-b-MA) fibers at each step of the SEM images clearly evidence the preservation of the nanofilayer-by-layer deposition of chitosan and hyaluronic acid multilayer. The brillar morphology of the samples after the LBL process. At error bars in the figure represent the standard deviation derived from a first glance, the coated fibers morphology remains similar multiple measurements (n = 4).

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into round samples (as shown in Figure 4). It is worth noticing that the culture tests are carried out in hydrated state, which may have an impact on the mechanical properties of the tested samples. Indeed, as mentionned in the introduction, chitosan possesses low elongation at break and stress at break in hydrated state (around 23% and 0.1 MPa for chitosan fiber samples, respectively), as compared to pure PCL fiber samples in the same conditions (around 220% and 3.7 MPa, respectively).[54] Tensile testing experiments performed on PCL fibers coated with chitosan and HA layers revealed that the mechanical properties of the samples are mainly dictated by the fiber core (i.e., PCLbased), rather than by the polysaccharide coating (regarding a LBL deposition at least up to 6 bilayers of chitosan and HA on PCLbased fiber core).[54] The fiber mats produced in this work thus present the great advantage Figure 3. TEM images of PCL fibers blended with poly(MMA-b-MA) copolymer, immersed in to be easily manipulated in hydrated state phosphate buffer and covered with chitosan and 3 bilayers of PSS and chitosan (a), and the (notably in cell culture media) – without same fibers after immersion in chloroform (b and c). tearing up, as chitosan fiber samples would do. The following cell culture experiments could consequently be performed with ease. the shift of the surface charge in accordance with the sign of the charge of the last deposited polyelectrolyte layer. This is in Either a monolayer of chitosan or 4 bilayers of polysacchaline with the construction of the multilayered coating. rides (5 layers of chitosan and 4 layers of HA) were deposited on the fiber mats. These samples were brought into contact with keratinocytes and SEM analyses were performed after 1 day and 7 days of culture, to evaluate the growth and pro2.2. Preparation of Hollow Fibers liferation of the cells. The results are presented in Figure 5 (1 day of culture) and Figure 6 (7 days of culture). Another experiment was additionally performed to confirm the formation of a multilayered coating on the surface of the fibers. After one day of cell culture, the most spread cells are the ones The PCL core of the core/shell fibers was dissolved in a seleccultured over the fiber mats covered with a chitosan monolayer. tive solvent to observe the remaining polyelectrolyte sheath. This Keratinocytes seem more isolated when cultured on the uncovwas perfomed by immersing the core/shell fibers (electrospun ered fibers or on the fibers covered with chitosan and HA. and coated directly on TEM grids) in chloroform, a selective solAfter 7 days of cell culture, the keratinocytes have prolifervent of the PCL fiber core. The experiment was carried out with ated over the 3 types of substrates. The best results are obtained PCL blended fibers coated by chitosan and 3 bilayers of PSS/chifor fiber mats covered with a chitosan monolayer (Figures 5B tosan. The high viscosity of the HA solution prevents the use of and 6B). this polysaccharide, as it sticks on the copper grids and obstructs As already reported by Dong et al.,[55] although cells can them, preventing the TEM observation. Figure 3 shows the attach to hyaluronic acid thanks to receptors such as CD44, Transmission Electron Microscopy (TEM) analyses performed they are difficult to spread on hyaluronic acid-based materials. on the fibers before (a), and after (b-c) immersion in chloroform. This could be a reason of the lower amount of cell attachment Figure 3 (b and c) clearly illustrates hollow fibers resulting from the dissolution of the PCL core. This experiment thus confirms the presence of a multilayered coating on the fiber surface, strong enough to resist dissolution and keep a tubular shape. As the preparation of hollow fibers only aimed at confirming the successful formation of the chitosan coating, they were not used in the following in order to beneficiate of the mechanical resistance of the PCL core.

2.3. Cell Culture on Fiber Mats For cell culture experiments, fiber mats were electrospun during 30 min, then removed from the aluminum foil and cut

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Figure 4. Fiber mat being peeled-off from aluminum foil (left) and fiber mat samples cut for their utilization as substrate of cell culture (right).

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FULL PAPER Figure 5. SEM images of keratinocyte grown one day on (A) PCL fibers electrospun in presence of poly(MMA-b-MA), (B) PCL blended fibers covered with a chitosan monolayer and (C) PCL blended fibers covered with chitosan and 4 bilayers of HA/chitosan. Left and right pictures illustrate different magnifications (scale bars: left 100 µm and right 50 µm).

and proliferation observed in the case of hyaluronic acid containing fibers. The monolayer of chitosan deposited on the fiber mat allows better proliferation than the uncovered fiber mat sample. The cell-culture results obtained for the chitosan-coated fibers are consistent with those reported in the literature for pure chitosan fibers.[56] Considering the better mechanical properties of the samples obtained by the present strategy, it is thus very promising and open prospects for application of such fiber mats particularly in cutaneous wound healing applications.

3. Conclusion A novel strategy has been developed for the preparation of fibers containing an aliphatic polyester core and a polysaccharide coating. The nature of the coating can be modulated to bring new surface properties to the fibers. In this work, chitosan and hyaluronic acid were notably considered, as they possess remarkable regenerative properties. A preliminary testing of

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cell culture on such novel systems evidenced that they appear to be suitable as support for culture of normal cells, the best results being obtained for a monolayer of chitosan deposited on the PCL-based fibers. This chitosan-coated sample maintains the outstanding surface properties of chitosan, while circumventing the limitations of directly electrospinning chitosan. This is a value-added system, as it requires a limited amount of chitosan. A complete biological study is however required to identify the best system. Such study is under current investigations and will be the topic of a dedicated paper. In this preliminary study, hyaluronic acid did not seem to positively affect the cellular growth. The fibers produced with the present technique could take part in the next future in the frame of wound healing applications. In this respect, it is worth noticing that if PCL-based fibers prove to degrade too slowly, the nature of the aliphatic polyester could be adapted to meet the requirement of a precise application – for example, by using polylactide[17] (or even a copolymer of polylactide and polyglycolide), instead of PCL.

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Figure 6. SEM images of keratinocytes grown seven days on (A) PCL fibers electrospun in presence of poly(MMA-b-MA), (B) PCL blended fibers covered with a chitosan monolayer or (C) PCL blended fibers covered with chitosan and 4 bilayers of HA/chitosan. Left and right pictures illustrate different magnifications (scale bars: left 100 µm and right 50 µm).

4. Experimental Section Electrospinning of the Poly(ε-caprolactone) Blend: Poly(ε-caprolactone) (Mn = 80 000 g mol−1, PDI < 2) was purchased from Sigma Aldrich. Poly(methyl methacrylate-b-methacrylic acid), i.e., poly(MMA48-b-MA25), block copolymer was synthesized by atom transfer radical polymerization (ATRP) of methyl methacrylate and trimethylsilyl methacrylate initiated by 2-bromo-ethylisobutyrate and catalyzed by dibromo-bis(triphenylphosphine) nickel.[57] The pendant silylated groups were then hydrolyzed as reported elsewhere.[58,59] PCL and poly(MMA-b-MA) were dissolved in a 1:1 tetrahydrofurane (THF)/N,N-dimethylformamide (DMF) mixture at a concentration of 15% by weight and with a PCL to poly(MMA-b-MA) ratio of 9:1. The electrospinning process was then conducted as follows: the polymer solution was transferred into a glass syringe with an orthogonally cut-ended needle (0.8 mm in external diameter). This needle-end was placed at 15 cm of a grounded aluminum collector plate. A syringe driver was used to regulate the flow rate of solution to 1 mL/h. To produce poly(ε-caprolactone) blended with poly(MMA-b-MA) nanofibers, a voltage of 12 kV was applied between the collector and the syringe needle. Fibers were

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collected on an aluminum foil of 20 cm x 20 cm placed on the grounded collector. For the sake of comparison, fibers made of pure PCL (reference fibers) – without any copolymer – were prepared in the same electrospinning conditions by using a 15 wt% PCL solution in a 1:1 THF/DMF mixture. Layer-by-layer Deposition on the Nanofiber Surface: Aqueous solutions of polyelectrolytes were prepared as follows; Chitosan (42 000 g mol−1, Acetylation Degree = 11%, KitoZyme) was dissolved at a concentration of 5 g L−1 in 0.1 M NaCl[60] aqueous solution containing 1 vol% of glacial acetic acid. Poly(sodium 4-styrene sulfonate) (PSS) (Aldrich, Mw = 70 000 g mol−1) was dissolved at a concentration of 5 g L−1 in 0.1 M NaCl aqueous solution. Hyaluronic acid sodium salt from Streptococcus equi (Sigma Aldrich, 53747, high molecular weight) was dissolved at a concentration of 5 g L−1 in 0.1 M NaCl aqueous solution. This solution presents high viscosity. The layer-by-layer deposition of chitosan and PSS (or hyaluronic acid) on the surface of the charged fibers was conducted as follows: PCL fiber mats containing poly(MMAb-MA) were immersed during 1 min in a phosphate buffer solution (pH = 8) in order to deprotonate the carboxylic acid functions. Afterwards, fiber mats were dipped in the chitosan solution for 30 min,

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Acknowledgements F.C. is grateful to the Belgian ‘‘Fonds pour la Formation à la Recherche dans l’Industrie et dans l’Agriculture’’ (FRIA) for financial support. The present work has been supported by the Science Policy Office of the Belgian Federal Government (IAP 7/05). CERM thanks the Walloon Region for supporting researches on chitosan in the frame of CHITOPOL, TARGETUM and GOCELL projects. GA was a research fellow also supported by the GOCELL project in the University of

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rinsed in water for 1 min in order to form the chitosan monolayer. From this step, bilayers were deposited by alternatively dipping the fiber mats in the PSS (or HA) solution for 30 min, rinsing them for 1 min, dipping them in chitosan solution for 30 min, and rinsing them again, to finally obtain the multilayered system. The samples were then dried under reduced pressure at ambient temperature for 2 days. Indirect Zeta Potential Measurements: Indirect Zeta potential measurements on fiber surfaces were performed using the flat surface cell of a Beckman Coulter Delsa Nano C analyzer. The data were processed via the Delsa Nano UI 2.21 software. All the measurements were carried out at 25 °C at a measuring angle of 15°, with standard particles for solid samples (Otsuka Electronics co., LTD, A54496). This technique allowed estimating the charges of the fiber surfaces, at each step of the layer-by-layer deposition process. In view of the analysis, fiber mats electrospun during 30 min were peeled off the aluminum foil and cut with scissors to fit into the analyzing flat surface cell. Measurement of the Zeta potential was repeated on four different samples taken from the same batch to assure the reproducibility of the results. Preparation of Hollow Fibers: To obtain hollow fibers, the electrospun PCL fibers blended with the poly(MMA-b-MA) copolymer and coated by 3 bilayers of chitosan and PSS were immersed in chloroform (Aldrich) for 1 min. The samples were let to dry under air and at ambient temperature before TEM analysis. SEM and TEM Observations: Platinum coating was deposited onto the fiber samples before Scanning Electron Microscopy analysis (SEM, JEOL JSM-840A). For Transmission Electron Microscopy (TEM) analysis (Phillips CM100, Olympus Camera and Megaview system), the nanofibers were directly electrospun on a copper grid. Cell Culture on Fiber Mats: Cell culture experiments were finally performed on the fiber mats. In this case, fiber mats were removed from aluminum foil after electrospinning and before layer-by-layer deposition of polyelectrolytes. The fiber mats were cut into round samples, 3 cm in diameter. The LBL deposition was then performed as described before. The samples were then dried under reduced pressure at ambient temperature for 2 days. They were sterilized in pure ethanol (Aldrich), dried at ambient temperature, and put into cell culture with human epidermal keratinocytes during 7 days, to evaluate the cell attachment. Keratinocyte cultures were established from human skin biopsies. Keratinocytes were grown in specific medium (KGM-2, Clonetics) supplemented with antibiotics (50 U mL−1 penicillin and 100 µg mL−1 streptomycin, Sigma) and with KGM-2 SingleQuots (Clonetics) corresponding to final concentrations of 50 µg mL−1 bovine pituitary extract, 10 ng mL−1 EGF, 5 µg mL−1 insulin, 5 µg mL−1 transferrin, and 5 10−7 M hydrocortisone. Cultures were maintained at 37°C in a humidified atmosphere containing 5% CO2. Time course evaluations of cell morphology, adhesion, and spreading were investigated by microscopic examination after 1 day and 7 days of cell culture. In brief, the fiber mats and cells were fixed for 10 min at 4 °C in 2.5% glutaraldehyde in sodium cacodylate buffer (0.1 M sodium cacodylate, pH = 7.4, 0.1% CaCl2). After being rinsed three times for 5 min in sodium cacodylate buffer, samples were dehydrated in graded ethanol at 25, 50, 75, 95, and 100%.[56] Due to the presence of poly(εcaprolactone) in the fibers, the samples could not be subjected to critical point drying (fibers were melting). The samples were dried at ambient temperature.

Namur. A. Colige from the ULg is also acknowledged for the cell culture experiments. Received: July 4, 2014 Revised: September 2, 2014 Published online:

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Adv. Healthcare Mater. 2014, DOI: 10.1002/adhm.201400380

Polysaccharide-coated PCL nanofibers for wound dressing applications.

Polysaccharide-based nanofibers with a multilayered structure are prepared by combining electrospinning (ESP) and layer-by-layer (LBL) deposition tech...
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