Functionalization of Magnetic Nanowires by Charged Biopolymers

Each contact angle value results from the averaging of 5 measurements. ... with the water contact angle oscillating from ∼55 to ∼30°, depending o...
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Biomacromolecules 2008, 9, 2517–2522

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Functionalization of Magnetic Nanowires by Charged Biopolymers D. Magnin,† V. Callegari,† S. Ma´te´fi-Tempfli,‡ M. Ma´te´fi-Tempfli,‡ K. Glinel,§ A. M. Jonas,† and S. Demoustier-Champagne*,† Unite´ de Physique et de Chimie des Hauts Polyme`res (POLY), Universite´ Catholique de Louvain, Place Croix du Sud, 1, B-1348 Louvain-la-Neuve, Belgium, Unite´ de Physico-Chimie et de Physique des Mate´riaux (PCPM), Universite´ Catholique de Louvain, Place Croix du Sud, 1, B-1348 Louvain-la-Neuve, Belgium, and FRE 3101, Polyme`res, Biopolyme`res, Surfaces, CNRS-Universite´ de Rouen, Bd Maurice de Broglie, F-79821, Mont-Saint-Aignan, France Received May 16, 2008; Revised Manuscript Received June 25, 2008

We report on a facile method for the preparation of biocompatible and bioactive magnetic nanowires. The method consists of the direct deposition of polysaccharides by layer-by-layer (LbL) assembly onto a brush of metallic nanowires obtained by electrodeposition of the metal within the nanopores of an alumina template supported on a silicon wafer. Carboxymethylpullulan (CMP) and chitosan (CHI) multilayers were grown on brushes of Ni nanowires; subsequent grafting of an enzyme was performed by conjugating free amine side groups of chitosan with carboxylic groups of the enzyme. The nanowires are finally released by a gentle ultrasonic treatment. Transmission electron microscopy, electron energy-dispersive loss spectroscopy, and x-ray photoelectron spectroscopy indicate the formation of an homogeneous coating onto the nickel nanowires when one, two, or three CMP/CHI bilayers are deposited. This easy and efficient route to the biochemical functionalization of magnetic nanowires could find widespread use for the preparation of a broad range of nanowires with tailored surface properties.

Introduction Magnetic nanostructures are playing increasingly important roles in biotechnology and biomedical fields.1 One area that is particularly promising is the use of functional magnetic nanoparticles to selectively manipulate and probe biological systems. There is already a broad range of applications for such magnetic nanoparticles including cell separation, studies of cellular function, biosensing, in vivo imaging, and magneto-thermal therapy.1,2 To date, the magnetic particles used are generally spherical, consisting of a single magnetic species and a suitable coating to allow functionalization with bioactive ligands. Nanowires present, however, a growing interest in the biomagnetics field.2,3 Indeed, due to their elongated shape leading to anisotropic physical properties, nanowires can interact with cells and biomolecules in fundamentally new ways. Moreover, nanowires can be grown from nanometer to micrometer sizes, spanning many relevant biological length scales. Among the different strategies to synthesize anisotropic nanostructures, the hard-template method is a versatile technique4,5 allowing the elaboration in high yield of various monodisperse metallic, magnetic,6 and conjugated polymer nanowires,7 with independently tunable diameters and lengths. Though scalable preparative routes to high-quality magnetic nanowires are wellestablished, surface modification chemistries are far less developed, which limits their utility in biological applications. In this context, the objective of this work is to develop a controlled and ubiquitous surface modification method for the * Authors to whom correspondence should be addressed. E-mail: [email protected]. Telephone: +32-10-472702. Fax: +3210-451593, † Unite´ de Physique et de Chimie des Hauts Polyme`res (POLY). ‡ Unite´ de Physico-Chimie et de Physique des Mate´riaux (PCPM). § FRE 3101, Polyme`res, Biopolyme`res, Surfaces.

preparation of magnetic nanowires with enhanced biocompatibility, hydrophilicity, and improved stability in physiological medium. Layer-by-layer (LbL) assembly of polycations and polyanions has emerged as a facile technique to fabricate functional multilayered films.8–12 LbL, which primarily exploits the electrostatic attraction between oppositely charged species alternately adsorbing on a surface from aqueous solution, has been used to modify the surface of substrates of varying nature, shape, and size, using a large variety of compounds. In particular, LbL was demonstrated to be well-suited to the encapsulation of nanoparticles13–16 and nanowires or nanotubes17–19 by functional polymers. For biomedical applications, polysaccharide-based polyelectrolyte multilayers have attracted considerable interest because of their frequent antifouling and biocompatibility properties.20–30 Though coating magnetic nanowires by polysaccharides is in principle feasible by LbL, the LbL functionalization of nanoparticles and nanowires is a time-consuming process that requires using centrifugation after each deposition cycle, as typically done when fabricating multilayered capsules.31 It is therefore important to devise alternate methodologies that could considerably simplify the process, which is the primary purpose of the present paper. Here, positively-charged chitosan (CHI) and negativelycharged carboxymethylpullulan (CMP; Figure 1) are LbLassembled onto the surface of brushes of nickel nanowires before releasing the wires to obtain biocompatible and biofunctional magnetic nanowires (Figure 2.) Nickel nanowire brushes were prepared by electrodeposition of the metal within the nanopores of an alumina template supported onto a silicon wafer, followed by the chemical dissolution of the template. This nanostructured substrate is then

10.1021/bm8005402 CCC: $40.75  2008 American Chemical Society Published on Web 08/21/2008

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Figure 1. Chemical structures of (a) chitosan repeating unit (with n ) DA or degree of acetylation) and (b) carboxymethylpullulan (with R ) H or CH2COO-).

Figure 2. Preparation of biocoated nickel nanowires. Step 1, electrochemical deposition of nickel within the nanopores of a supported alumina template; Step 2, dissolution of the alumina template; Step 3, LbL assembly of polysaccharides onto the Ni nanowires; and Step 4, biocoated Ni nanowires taking off from the substrate by a gentle ultrasonic treatment.

sequentially dipped in CMP and CHI solutions to encapsulate them in a thin polysaccharidic layer. Using TEM and XPS, we demonstrate the efficiency of the process for growing a thin homogeneous CMP/CHI coating onto the nanowires. In a subsequent step, the amino-functional groups present on the CHI outer layer are successfully used to graft bioactive ligands (enzymes) onto the surface of the magnetic nanowires. Finally, the nanowires are released by a gentle ultrasonic treatment. Because the biofunctionalization of the nanowires is performed before their release from the surface, our method eliminates the relatively heavy centrifugation steps used when processing suspension of nanoparticles used by previous researchers. A further advantage of the method is that it can easily be adapted to nanowires of most metallic materials, irrespective of their detailed chemical nature.

Experimental Section Materials. The structures of the polysaccharides used in this study are presented in Figure 1. Chitosan (CHI, Figure 1a) with Mw )

Magnin et al. 1100000 g · mol-1 and a degree of acetylation, DA ) 21%, was provided by Vanson, Inc. (Redmond, WA). Carboxymethylpullulan (CMP, Figure 1b) with Mw ) 426000 g · mol-1 and a substitution degree in carboxymethyl groups of 0.9 ( 0.05 per anhydroglucose unit was prepared from pullulan (Hayashibara Biochemical Laboratory, Japan) according to a procedure already described.32 Glucose oxidase (GOx) was purchased from Sigma-Aldrich. 1-Ethyl-3-[3-dimethylaminopropyl]carbodiimide hydrochloride (EDC, 98+%) and (N-hydroxysulfosuccinimide (NHS, 98+%), potassium phosphate monobasic (KH2PO4, 99+%), and potassium phosphate dibasic (K2HPO4, 98%) were purchased from Sigma-Aldrich. Buffer phosphate was homemade (PBS; 20 mM K2HPO4 and KH2PO4, 0.15 M NaCl, pH 7.5). The water used in all experiments was purified by a Millipore system (Milli-Q water of 18 MΩ · cm resistivity). Nickel(II) sulfate hexahydrate (NiSO4.6H2O) was purchased from PROLABO (VWR International) and boric acid (H3BO3) from Merck, both of them for analytical grade. Oxalic acid (COOHCOOH · 2H2O) and ortho-phosphoric acid (H3PO4, 85%), with the highest available purity, were purchased from Merck. CHROMANORM water for HPLC was used for nanoporous alumina and nanowires preparation and was purchased from PROLABO (VWR International). Substrates Used for LbL Assembly. LbL assembly was first performed for reference on flat nickel surfaces, prepared by cathodic pulverization of Ni on a silicon wafer. Nickel deposition was made by DC magneton sputtering with a Plassys MP 500 system. The sputtering was performed in an argon atmosphere at 10 mTorr. For LbL assembly onto nanowires, nickel nanowire brushes were prepared by the electrodeposition of nickel into the nanopores of a supported alumina template. The nanoporous alumina was prepared33 by electrochemical oxidation of Al (1000 nm) layer supported on Au-coated (30 nm) Si wafer. Metallic layers were sputtered in conditions similar to the previously described Ni layer deposition. Anodization of the aluminum was conducted in 0.3 M oxalic acid solution at 2 °C at constant voltage of 60 V to obtain an average interpore distance of ∼150 nm. Pore enlargement to diameters of about 95 nm was performed in a 5 wt % ortho-phosphoric acid solution at 30 °C. Nanowire Synthesis. Nickel electrodeposition was performed in a conventional one compartment cell with a three electrodes configuration using an EG&G Princeton Research 263A potentiostat/galvanostat. A porous alumina template supported on gold-coated silicon wafer served as working electrode. The counter electrode was a platinum wire and the reference electrode was a Ag/AgCl electrode. Nickel was deposited from a 0.5 M NiSO4 and 30 g/L of H3BO3 aqueous solution at -1.05 V.6 Template Removal. After electrodeposition of the nanowires, the alumina template was removed by dissolution in an aqueous 5 M NaOH at 70 °C. The brush of magnetic nanowires attached to the silicon surface was cleaned with ethanol 95% in order to avoid reprecipitation of alumina onto the nanowires. LbL Assembly Procedure. Polyelectrolyte multilayers were built by the layer-by-layer technique.8 An aqueous solution of CMP 10-2 M in monomer unit at pH 5.5. CHI was first dissolved at a concentration of 10-2 M in monomer unit into a 5% acetic acid solution. Then the pH of the solution was raised to 5.5. LbL assembly was performed by first immersing the substrates (either a flat nickel surface or the Ni nanowire brushes attached to a silicon wafer) into the CMP solution for 20 min followed by a rinsing step with milli-Q water. The adsorption/rinsing step was repeated for CHI. Then, the whole process was cycled until the desired number of bilayers was obtained. Biomolecule Grafting onto Nanowires. Polysaccharides-coated magnetic nanowire brushes, with CHI as outermost layer, were used for the covalent immobilization of biological molecules. Glucose oxidase was chosen as model system. Ni polysaccharide-coated nanowire brushes were immersed for 1 h in an aqueous solution containing glucose oxidase (0.1 mg/mL in PBS), 0.2 mol · L-1 EDC and 0.05 mol · L-1 NHS. At the end of the chemical coupling reaction, the substrate was abundantly rinsed with PBS and milli-Q water.

Functionalization of Magnetic Nanowires Characterization Methods. Contact Angle Measurements. Changes of the hydrophobic/hydrophilic properties of Ni surfaces at each step of the LbL process were followed by the sessile drop method. The water droplet volume was 0.3 mL (Milli-Q water). Each contact angle value results from the averaging of 5 measurements. The standard deviation associated with a set of measurements was about 0.8°. X-ray Photoelectron Spectroscopy (XPS). The surface chemical composition of the various substrates was characterized by XPS, using a SSX 100/206 photoelectron spectrometer from Surface Science Instruments (USA) equipped with a monochromatized micro focused Al X-ray source (powered at 20 mA and 10 kV). The pressure in the analysis chamber was ∼10-6 Pa. The energy resolution was set to 1.4 eV and the photoelectron takeoff angle was 55°. The binding energies were referenced to C1s core level at 286.3 eV (C-O binding due to the importance of this type of binding in CMP and CHI). Data treatment was performed with the CasaXPS program (Casa Software Ltd., U.K.). Some spectra were decomposed with the least-squares fitting routine provided by the software with a Gaussian/Lorentzian (85/15) product function and after subtraction of a nonlinear baseline. Atomic ratios were calculated using peak areas normalized on the basis of acquisition parameters and sensitivity factors provided by the manufacturer. Electron Microscopy. Nickel nanowires were detached from the substrate by an ultrasonic treatment and collected either on an aluminum sample holder with a carbon-based adhesive tape, or on carbon-coated grids, for SEM analysis or TEM analysis, respectively. The dimensions (length and diameter) of as-prepared Ni nanowires were first determined by SEM using a high resolution FEG Digital Scanning Microscope 982 Gemini from Leo. The morphology of bare and polysaccharidecoated Ni nanowires was analyzed by TEM, using a LEO 922 Microscope operating at 200 kV and equipped with an Electron Energy Loss Spectroscopy (EELS) detector. TEM/EELS analyses were performed in spot mode with a spot size of 1.3 nm.

Results and Discussion Growth of LbL Multilayers on Flat Nickel Substrates. We first investigated the ability of growing LbL multilayers of polysaccharides onto a nickel substrate by using flat nickel surfaces as model systems. The results (Supporting Information) were essentially identical to what was reported before for similar systems,27 with the water contact angle oscillating from ∼55 to ∼30°, depending on the nature of the outermost layer, CHI or CMP (SI, Figure S1), respectively and the Ni substrate signal disappearing in XPS after only three cycles of deposition (SI, Table S1). Growth of LbL Multilayers on Nickel Nanowire Arrays. Nickel nanowires of different aspect ratios were grown by electrochemical deposition of Ni into the nanopores of supported alumina templates (Figure 2, step 1). Here, we essentially concentrate on nickel nanowires presenting a diameter of 98 ( 8 nm and a length of 1000 ( 110 nm. The template was then removed by dissolution of alumina in an aqueous 5 M NaOH solution at 70 °C, leading to an ensemble of nanostructures that protrude from the surface like the bristles of a brush (Figure 2, Step 2). SEM pictures of the surface of an alumina membrane, of a brush of Ni nanowires and of free Ni nanowires are shown in Figure 3a-c, respectively. To further grow polysaccharide multilayers, nickel nanowires were cleaned to remove any remaining alumina. Two types of cleaning procedures were tested: Ni nanowires were either abundantly rinsed with milli-Q water or with ethanol (95%). TEM pictures in Figure 3 clearly show that rinsing with milli-Q water induces reprecipitation of alumina onto the nanowire surfaces (Figure 3d), while it is not the case by rinsing with ethanol (Figure 3e). TEM-EELS (electron energy loss spectroscopy) investigations in spot mode were performed at the highlighted points indicated

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Figure 3. SEM pictures of (a) the surface of an alumina membrane, (b) a brush of Ni nanowires, and (c) free nickel nanowires. TEM pictures of (d) nickel nanowires rinsed with water after template dissolution and (e) nickel nanowires cleaned in ethanol 95% after template dissolution. EELS-Al-K spectrum (f) recorded in spot mode at the points highlighted by a cross in pictures (d) and (e).

by a red cross in Figure 3d,e and show the presence of alumina (Al peak at 1585 eV) on Ni nanowires rinsed with milli-Q water, while no alumina was present on Ni nanowires rinsed with ethanol (Figure 3f). Water is a proton donor and when used as solvent to clean nickel nanowires, the excess of water displaces the chemical equilibrium of equation 1 to the formation of alumina, that reprecipitates onto the Ni nanowire surfaces.

Al2O3 + 2OH- h 2AlO2 + H2O

(1)

In the sequel, brushes of Ni nanowires were thus rinsed with ethanol prior to further functionalization. Layer-by-layer deposition onto the brushes of nickel nanowire arrays was easily performed before nanowire release by alternatively dipping the substrate in CMP and CHI solutions (Figure 2, step 3). It should be stressed that the nanowire functionalization strategy presented here is by far more simple to carry out than the usually reported methods where freestanding nanowires suspended in solution are used.17,34 Indeed, by using a metal nanowire array attached to a solid substrate, centrifugation, and filtration to recover the nanowires at each step of the LbL process are no longer required. Moreover, depending on the aimed application, one can use the as-prepared functionalized nanowire array or coated nanowires can be freed from the substrate by ultrasonic treatment as will be shown below. Samples with different numbers of bilayers were prepared and observed by TEM after release by ultrasonic treatment. For samples coated with no more than three bilayers, well-isolated wires could be obtained after release (Figure 4.) By contrast, for larger numbers of deposition cycles, the coating of the Ni nanowires was either heterogeneous, or the nanowires were entrapped in a composite gel (Supporting Information, Figure S2). Because of the magnetic interaction, bare Ni nanowires

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Figure 5. XPS spectra of Ni nanowires coated with one CMP/CHI bilayer: (a) Ni 2p 3/2 photoemission spectrum and (b) N 1s decomposed photoemission spectrum. Table 1. XPS Atomic Ratios for Bare and CMP/CHI-Coated Nickel Nanowires

Figure 4. TEM pictures of bare nickel nanowires (a, b, and c) and of nickel nanowires coated with two CMP/CHI bilayers (d, e, and f).

tended to cluster in solution and on TEM grids, as shown in Figure 4a. In contrast, released nanowires coated with three or less bilayers were found to disperse much more easily in solution, allowing isolated nanowires to be observed by TEM (Figure 4d). This strong reduction of the aggregation of the Ni nanowires is attributed to the efficient counterbalancing of the interwire magnetic interactions by electrostatic repulsive forces, induced by the charged polysaccharide coating. TEM pictures of the lateral surface of both types of nanowires are shown in Figure 4b,e, showing that a 6-8 nm thick homogeneous organic coating is present on the entire lateral surface of the Ni nanowires that have undergone two cycles of LbL process, while no organic coating appears on the bare nanowires. Likewise, the tips of the nanowires were examined, and did not appear to be different from the lateral side of the nanowires (Figure 4c,f). Although this was expected for the top extremity of the nanowires, the presence of a coating at the broken extremities of the nanowires is more surprising. Different mechanisms will be considered to be responsible for this observation, such as the plasticity of the water-swollen layers, the folding of stretched films onto the bare tip of the nanowires after release, or even partial chain mobility in the films. EELS investigations focused on Ni-L2 ray, and N-K ray atoms were performed on bare and coated nanowires to confirm the composition of the coating. As expected, only nickel was present on bare nanowires (spectrum not shown), and no nitrogen was detected. However, on coated nanowires, a peak centered at ∼400 eV appears in the N-K spectrum (spectrum not shown), characteristic for amine and amide groups that are present in the chitosan component. The formation of the polysaccharide multilayers onto the Ni nanowires was further confirmed by X-ray photo-

entry

sample

Ni/N

1 2 3

bare Ni nanowires Ni nanowires with 1 bilayer Ni nanowires with 2 bilayers

31.5 8.7 0.15

electron spectroscopy (XPS). The Ni 2p 3/2 spectrum of Ni nanowires coated with one CMP-CHI bilayer shows one small peak at 852 eV, corresponding to metallic Ni, and two main peaks located at 856 and 861 eV (Figure 5a). These contributions result from the formation of nickel oxide and/or Ni(OH)2 (resulting from the treatment with NaOH for dissolving the alumina template) on the surface of the Ni nanowires. The N 1s spectrum of coated Ni nanowires (Figure 5b) presents two main components: the first one, centered at 399.6 eV, originates from amine (-NH2) and amide (N-CdO) groups and the second one located at 401.5 eV comes from protonated amine groups (-NH3+). This N1s spectrum is the one expected for chitosan as it contains these 3 types of functional groups. In Table 1, the Ni/N ratios of bare nickel nanowires and LbLcoated Ni nanowires are indicated. As already observed on flat nickel surface (SI, Table 1), the Ni/N ratio strongly decreases with increasing number of polysaccharide layers deposited onto the nanowires. These data, in complete agreement with TEM and TEM-EELS results, prove the formation of a uniform coating of CMP and CHI on the nickel nanowire surfaces. Biomolecule Immobilization onto Polysaccharide-Coated Ni Nanowires. For several applications of nanowires in medical sciences, it is required to immobilize proteins (antibodies, enzymes, and so on) onto the nanowire surface. We therefore tried to immobilize glucose oxidase, chosen as model system, onto polysaccharide-coated nickel nanowires. For that purpose, we prepared magnetic nanowires coated with one functional CMP/CHI bilayer. Glucose oxidase (GOx) was immobilized onto the nanowires before release by reacting with the aminogroups of the outermost CHI layer in the presence of an EDC-

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Table 2. XPS Data for CMP/CHI-Coated Nickel Nanowires before and after GOx Immobilization atom

without GOx (% or ratio)

with GOx (% or ratio)

C O N Ni S Ni/N

49.3 44.7 0.6 5.4 0 9.0

58.4 32.8 5.5 3 0.35 1.8

NHS activating solution, as we previously showed that this coupling chemistry does not alter the activity of GOx.35 Moreover, using EDC-NHS solution also leads to the crosslinking of the polysaccharide coating through the formation of amide bonds between CHI and CMP. This is a serious advantage as it increases the robustness of this coating. Indeed it has already been reported that cross-linked polyelectrolyte multilayers have an increased rigidity and impermeability and are mechanically more resistant than native films.36 XPS analysis of the biofunctionalized nanowires confirms the attachment of GOx onto the CMP/CHI-coated magnetic nanowires (Table 2.) The immobilization of GOx leads to a strong increase in the nitrogen content (from 0.6% for CMP/CHI-coated Ni nanowires without GOx to 5.4% for CMP/CHI-coated Ni nanowires with GOx), combined with the appearance of a weak sulfur peak (from 0% for CMP/CHI-coated Ni nanowires without GOx to 0.35% for CMP/CHI coated Ni nanowires with GOx), and a strong decrease in the Ni/N ratio (from 9.0% for CMP/CHIcoated Ni nanowires without GOx to 1.8% for CMP/CHI-coated Ni nanowires with GOx). This indicates the successful anchoring of the GOx enzyme on the nanowires, which could be released from the silicon substrate by a gentle ultrasonic treatment, as described previously.

Conclusion It was shown that the layer-by-layer assembly of polysaccharides, and the grafting of proteins to the LbL coating, can be efficiently performed on brushes of metallic nanowires, using the classical method of LbL deposition. The nanowires can then be released after assembly, providing fully covered nanostructures that can be used for biological applications. The process is very advantageous compared to the direct encapsulation of released nanowires because all time-consuming steps related to nanowire centrifugation, rinsing, and redispersion are eliminated. Although the process was demonstrated for Ni nanowires, it could be easily transferred to other metals or inorganic nanowires as well; in addition, the use of other types of polysaccharides is a direct extension of the present work, providing direct access to a large range of functional bionanostructures. Furthermore, the brush of nanowires could be used itself to increase the surface area of a biodevice. This simple and robust methodology is thus expected to find widespread application for the production of biofunctional hybrid anisotropic nanostructures. Acknowledgment. The authors wish to thank CIFA laboratory (UCL) for providing access to the XPS equipment, Michel Genet for useful discussions about XPS results and Dr. Severian Dumitriu for providing us with the chitosan (pharmaceutical grade). Financial support by the Wallonia Region (NANOTIC program), by the European Community (FAME Network of Excellence), and by the Belgian Federal Public Planning Service Science Policy (IUAP-FS2). S.D.-C. also thanks the Belgian

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National Fund for Scientific Research F.R.S-FNRS for her Research Associate position. Supporting Information Available. XPS results and water contact angle measurements on flat bare and CMP/CHI-coated nickel surfaces are given. Images showing the formation of composite gels for large numbers of CMP/CHI deposition cycles onto nickel nanowires are shown. This material is available free of charge via the Internet at http://pubs.acs.org.

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