Abstract
The introduction of a hydrophobic moiety on chitosan enhances the self-assembling properties, mucoadhesion, the permeability of the macromolecule and aids in target specific delivery. Our group synthesized a hydrophobic trans N-(6,6-Dimethyl-2-hepten-4-ynyl)chitosan derivative (CSD) and studied the surface modification of ZnS nanoparticles in a single pot reaction. X-ray diffraction studies and FESEM imaging confirms the nano size and morphology of the surface modified Zinc sulfide nanoparticles (ZnS-CSD NPs). The proposed ZnS-CSD NPs showed excellent emission at 457 nm. Photostability studies indicate that the surface modified ZnS-CSD NPs possess better photostability than Rhodamine B and FITC. Cell viability tests confirmed the biocompatibility of the modified nanoparticles. All these features of ZnS- CSD NPs makes these candidates an excellent choice in a wide range of in vitro or in vivo studies as fluorescent biological labels.
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Introduction
Human cervical cancer is the fourth most cause of tumor-related deaths [1]. Although imaging techniques such as Positron emission tomography (PET), and Single photon emission computed tomography (SPECT) are available to detect changes at the cellular level, they suffer from spatial resolution. On the other hand, Magnetic resonance imaging (MRI) offers good spatial resolution but lacks imaging at molecular level due to low sensitivity for the detection of contrast agents. To achieve spatial resolution and the sensitivity to detect biochemical events several hybrid systems with morphological and molecular imaging capabilities are exploited [2]. Nanoparticle-based imaging agents known as exogenous optical contrast agents emerged as promising nano-sized fluoroprobes. They possess high surface to volume ratio, excellent photostability, and optical properties to image at cellular levels [3]. Among many nanoparticles in use, ZnS has its unique features such as biocompatibility and wide band gap energy of 3.6–3.9 eV. Moreover, ZnS exhibits luminescence at room temperature [4, 5]. Though ZnS nanoparticles possess some unique properties, the photostability remains a challenge. For fluorescence imaging, the material should exhibit stable and intense luminescence. To improve the photostability, the surface of ZnS modified with suitable capping agents like 3-Mercaptobutyric Acid, Chitosan, and PVA [6–8]. Particularly several works attracted chitosan as capping agent [9, 10].
Chitosan is a linear, semi-crystalline polysaccharide, composed of (1➔ 4) -2-amino-2-deoxy-β-D-glucosamine unit, is the most abundant bio-based polymer next to cellulose. This biopolymer have been extensively studied in several biomedical applications, because of its biocompatible and biodegradable nature [11]. The degradation products of chitosan are non-toxic and non-carcinogenic [12, 13]. In the field of nanotechnology, chitosan and its derivatives have been studied in drug delivery, tissue engineering, mucoadhesion and many other applications [14]. Biocompatibility and biodegradability are one of the key parameters decide the utility of the nanoparticles systems in biological applications. These properties of chitosan are well studied and documented by both in vitro and in vivo studies [15–18].
Chitosan has attracted several works in nanoparticle synthesis for surface modifications of an inorganic core. In further improvement, chitosan is modified structurally to target specific applications. Self-assembly over a core is the main objective of structural modifications because, in this spontaneous process organized structures are formed with specific functions and properties without further processing. In the multi-component self-assembling process, the molecular structure plays an important role driven by electrostatic interactions or hydrogen bonds between chitosan and the other molecule [19]. One of the main advantages of the self-assembly is its cost-effectiveness to prepare hybrid nanoparticles with an inorganic core and organic surface modifications. The Self -assembly process is a bottom-up approach in which parameters such as temperature, reaction time, stoichiometric mole ratios can be controlled to define the size and morphology. Also, the self-assembly process of chitosan and its derivatives resembles many biological molecules (DNAs, RNAs).
The introduction of moieties such as alkyl [20], phthaloyl [21], polyester [22], fatty acid [23], cholesterol [24] functionality on chitosan enhances the hydrophobic nature to achieve the intended purpose. Based on our current research work, we communicate a surface modifying agent based on chitosan with structurally significant hydrophobic side chain which is new and not reported elsewhere. In the current research work, we modified chitosan using trans N-(6,6-Dimethyl-2-hepten-4-ynyl) side chain (Fig. 1). The chemical modification attempted on chitosan provides a hydrophobic moiety to the structure of native chitosan which enhances the self-assembling capabilities by increasing intermolecular hydrophobic interaction between the segments.
In the present work, the side chain formed by direct N-alkylation eliminates toxic by-products observed in the Schiff base route to synthesize similar products [25]. In the Schiff base route, Chitosan reacted with aldehydes or ketones to yield corresponding aldimine or ketimine. Sodium borohydride(NaBH4), Sodium cyanoborohydride(NaBH3CN) are used to reduce the imine to get the N-alkyl derivative. NaBH3CN is widely used in reductive alkylation because of selectivity it offers in reactions. However, it generates toxic by-products such as HCN or NaCN [26]. In the direct N-alkylation of Chitosan, no such toxic by-products are envisaged. In addition to the synthetic advantage, the presence of trans-hydrogen, alkene and alkyne functionalities in the structure of the ZnS –CSD NPs will aid in adapting to the complex, undefined biological domains.
The N-alkylation attempted would enable the derivative soluble in water even at higher degree of substitution (DS) due to amphiphilic nature of the molecule and possible protonation of the resultant secondary amine group, though the side chain is hydrophobic [27].Whereas in hydrophobic modifications through N-acylations of chitosan solubility in aqueous conditions is limited beyond certain DS [28]. With this background and objective of modifying the surface of ZnS nanoparticles based on enhanced self-assembly, trans N-(6,6-Dimethyl-2-hepten-4-ynyl) chitosan used in the current work would provide nanostructures in which the hydrophobic entities can assemble away from the core ZnS. Further conjugation of ZnS- CSD NPs with suitable cancer targeting ligand like folic acid through EDC coupling chemistry is possible. This modification would make these nanoparticles utilisable in detecting other forms of cancer [29, 30]. Application of proposed ZnS –CSD NPs in drug delivery needs to be explored. Because of its fluorescence properties the synthesized nanoparticle may function as theranostic agent [31].
Materials and Methods
Materials
Chitosan powder (MW 50 kDa, 100% deacetylation) of crab shell origin was supplied by Panvo Organics Pvt. Ltd., (Chennai, India). 1-chloro–6, 6–dimethyl–2–hepten–4-yne was purchased from Hangzhou Volant Technology Co Ltd. (Hangzhou, China). Zinc acetate, Sodium sulfide, Sodium Carbonate, Sodium hydroxide, Glacial Acetic acid, Acetone, Methanol and other reagents were purchased from Avantor Performance Materials India Ltd. (Thane, India).
Synthesis of trans N-(6,6-Dimethyl-2-Hepten-4ynyl)chitosan (CSD)
Chitosan (3.0 g, 0.0186 mol) was dissolved in 3% w/v aqueous acetic acid (300 ml) under mechanical stirring for two hours at room temperature. pH of the mass was adjusted to 6.0 using 5%w/v sodium hydroxide solution. Sodium carbonate (3.0 g, 0.026 mol) was added and under vigorous stirring 1-chloro–6,6–dimethyl–2–hepten–4yne (3.0 g 0.019 mol) was introduced over 10 min. The heterogeneous reaction mixture temperature was raised to 90 °C and stirred for 4 h. The product was precipitated by adding to acetone (1.5 l) under good mixing, filtered and washed thoroughly with methanol. The collected precipitate dried under vacuum at 50 °C. The yield was 3.35 g (64.42% ). Figure 2a provides reaction methodology.
Synthesis ZnS, ZnS-CSD and ZnS-CS Nanoparticles
0.1 M of Zn(OAc)2, 0.01% w/v CSD in aqueous acetic acid were taken in a beaker. With constant stirring (1000 rpm), 0.1 M Na2S aqueous solution (2.5 ml) was added, and the pH of the solution was raised to 10 by adding 1 M NaOH. This mixture was stirred at 60 °C for 3 h and cooled to room temperature. The precipitate was collected by centrifugation (2500 rpm) and washed thoroughly with milliQ water and dried under vacuum to get ZnS-CSD nanoparticles. The same procedure was followed using various concentrations of CSD (0.02, 0.03, 0.04 and 0.05% w/v) to modify ZnS NPs. In another experiment, surface modification of ZnS using 0.01% aqueous solution of native chitosan was carried to get ZnS-CS nanoparticles. The unmodified ZnS was prepared by following the same procedure without the addition of surface modifiers [32].
Characterization
X-ray diffraction (XRD) of the prepared samples were done using Bruker D8 diffractometer with Cu Kα radiation (λ = 1.5418 Å) within the the2θ range of 10–80°. FTNMR studies were carried out using (BruckerAvance, 500 MHz).FTIR of the samples recorded with Perkin-ElmerSpectrum II. Elemental analysis was performed using a Perkin Elmer elemental analyzer, (Model 2400), Field Emission Scanning Electron Microscopy (FESEM) and Energy Dispersive Analysis X-Ray (EDAX) of ZnS-CSD NPs were investigated using CARLZEISS (FESEM-SUPRA 55). Fluorescence spectra were recorded on Varian Cary-Eclipse fluorescence spectrophotometer.
Cell Culture and in Vitro Cytotoxicity Studies
HeLa cells were procured from National Centre for Cell Sciences (NCCS, Pune, India) and cultured in DMEM supplemented with 10% fetal bovine serum (FBS) in the presence of penicillin and streptomycin in a humidified incubator with 5% CO2 at 37 °C. Cell viability was assessed using MTT assay as reported earlier with slight modifications [33, 34].
Results and Discussions
The degree of substitution (DS) of a chitosan derivative is calculated by comparing C and N molar ratio obtained from the elemental analysis data. Elemental analysis of CSD was calculated for (C6H11NO4)0.78(C15H23NO4)0.22 0.47 H2O. Calculated: C,48.89: H,7.51:N,7.15. Obtained results: C,48.79: H,7.87:N,6.87. Based on the elemental analysis, DS was calculated and provided in Table 1. From the data, it can be found that there is an increase in carbon percentage on CSD which confirmed the substitution. From the C/N molar ratios, the increase in mass was obtained as 2.285 g/mol and DS was found to be 0.25. The heterogeneous nature of the synthesis step followed could have limited the substitution.
The proton NMR spectra were recorded to confirm the structure of CSD in D2O/DCl. Figure 2b shows the proton NMR spectra of CSD. The chemical shifts assigned for the respective protons are summarized in Table 2.
No proton peak of the CH2 group (H7) attached to the Nitrogen observed. This observation could be because of the merger of the peak in the region 3.0–4.0 where the pyranose protons (H3toH6) of chitosan appear. FTNMR studies confirmed the structure of CSD.
Figure 2c shows the FT-IR spectra of CSD and ZnS-CSD NPs. The characteristic IR frequencies of CSD were assigned as follows: 3441 cm−1 was attributed to the stretching vibrations of –OH group. The peak at 2871 cm−1 was assigned to –CH stretching of pyranose moiety. The –NH deformation peak appeared at 1636 cm−1. The band at 1094 cm−1 was due to the –CO stretching. The C ≡ C (alkyn) vibrational band was observed at 2212 cm−1. All the observed IR bands confirmed the N-alkylation on Chitosan. For ZnS-CSD NPs, the stretching vibrations of ZnS appeared at 1120 cm−1 along with all the characteristic peaks of CSD which confirmed the nanoparticles formation [35].
Figure 3 shows the fluorescence spectra of ZnS, ZnS-CSD and ZnS-CS nanoparticles. The fluorescence spectra in Fig. 3I (a) shows fluorescence of CSD. Figure 3I (b) shows fluorescence spectrum of unmodified ZnS nanoparticle. Figure 3I (c-g) shows the impact on the fluorescence intensity of ZnS-CSD NPs with the increase in CSD concentration used to modify ZnS NPs surface. When CSD concentration increased up to 0.04%w/v, fluorescence intensity increased. Further, with an increase in the CSD concentration to 0.05% w/v, the fluorescence intensity decreased. From the fluorescence studies, the optimized concentration of CSD to prepare ZnS-CSD NPs was identified as 0.04% w/v. It was also observed that CSD played an important role in controlling the size of the ZnS-CSD NPs and this could be possible because of combined effect of intramolecular hydrogen bonding, electrostatic interactions and Van der waals forces exerted by the polymer on ZnS NPs [19]. Later, the optimized concentration (0.04%w/v) which showed maximum intensity in fluorescence studies was used in cell imaging. In Fig. 3I (a) blue shift can be observed at 457 nm. Normally, ZnS nanoparticles exhibit enhanced intensity as well as blue shift in the 400-550 nm region which are associated with the surface defects arisen due to the presence of increased vacant surface oxygen sites over the nanomaterial [36, 37]. In the fluorescence studies, the intensity of ZnS-CSD NPs got quenched when CSD concentration increased beyond 0.05% during synthesis. The reason for the decreased fluorescence response with the increase in the concentration of CSD NPs might be due to the self-quenching effect, which is the result of a collision between the molecules of the fluorophore.
To understand and evaluate the impact of the N-substitution of chitosan on surface modification of ZnS, fluorescence and morphology studies were carried out for the native chitosan modified ZnS nanoparticles(CS-ZnS NPs). Figure 3 (II) presents the emission spectrum of ZnS-CS NPs which indicated that even at the lowest concentration of 0.01% chitosan the intensity of fluorescence is not significant. Quenching even at this lowest concentration could be due to polycationic nature of the polymer. Presence of hydroxyl and amine groups in chitosan would exert strong the inter and intramolecular hydrogen bonding and other non covalent interactions. In a net effect, a non uniform self assembly of chitosan over ZnS NPs might happen which could have impacted the fluorescence [19].
Figure 4 exhibits FESEM image, energy dispersive X-Ray analysis (EDAX), and XRD of ZnS-CSD nanoparticles. The morphology of ZnS-CSD NPs was spherical as observed from Fig. 4a and the particle sizes ranged from 40 to 130 nm as shown in Fig. 4b. FESEM studies confirmed that CSD played an important role in controlling the shape and size of ZnS-CSD NPs. Figure 4c shows the morphology of CS-ZnS NPs. From the FESEM images of CS-ZnS NPs, we can observe the undefined particle shape and uncontrolled non-uniform particle size. This indicate that the surface modification of ZnS NPs with modified chitosan lead to NPs with uniform morphology. Figure 4d shows EDAX spectrum of ZnS-CSD which confirmed the stoichiometric purity of nanoparticles.
Figure 4e shows XRD pattern of ZnS and ZnS-CSD. The diffraction peaks at 28.5, 47.5 and 56.1 correspond to the lattice planes of (111), (220) and (311) which can be observed in both ZnS and ZnS-CSD.The crystalline XRD pattern matches very well with published literature of ZnS nanoparticles [38–40]. All the corresponding diffraction peaks matched very well with the cubic zinc blende structure (JCPDS No. 05–0566). The absence of any other peaks indicated that the prepared materials were free from impurities. ZnS –CSD peak intensities increased when compared to unmodified ZnS, suggesting that the crystallite size of ZnS decreased as a result of the modification with CSD. Peak broadening of ZnS and ZnS-CSD indicated the nanocrystalline nature of the synthesized materials. Using Debye-Scherrer formula (Eq. 1), crystallite size was calculated.
Where D is the mean grain size, k is constant, λ is the X-ray wavelength (1.54 A° for Cu-Kα), β is the full width at half maximum of the diffraction peak, and θ is the Bragg angle. The average crystallite sizes of ZnS and ZnS-CSD were found as 80 nm and 40 nm respectively which was due to passivation of CSD over ZnS surface.
Photostability of a fluorescence probe is one of the essential parameters decides the effective usage of the probe in imaging applications [41]. In particular, extended time imaging of cancer cells or tissues is a key parameter significant in biological studies for a proper understanding of the malignancy Fig. 5 shows the photostability of ZnS-CSD NPs along with fluorescein isothiocyanate (FITC), and Rhodamine B. To evaluate the photostability of the ZnS-CSD NPs, 0.02% w/v ZnS-CSD solution was irradiated constantly using UVlamp. The emission spectra of tested samples were measured from 0 to 130 min at every 10 min time interval. As shown in Fig. 5, ZnS- CSD NPs exhibits significant photostability when compared with the other two dyes studied even after 130 min of UV exposure. Hence, it was concluded that ZnS-CSD NPs has significant photostability in comparison with Rhodamine B and FITC.
Figure 6 shows the cell viability study results using Methyl thiazolyl tetrazolium (MTT) assay, and Fig. 7 shows the photographs of ZnS-CSD co-cultured with HeLa cells at different concentrations. Cell toxicity assay exhibited that even at a concentration of 250 μg/ml, more than 90% of cells were viable. Hence ZnS-CSD NPs can be used as a fluoroprobe in cancer cell imaging and as a carrier molecule in drug delivery in the future.
Investigations of ZnS-CSD NPs reported in the current work support the fact that surface modification of ZnS NPs using the chitosan derivative (CSD) lead to better self-assembly which yielded the nanoparticles with uniform size and morphology. The findings correlate very well with the polymer assisted surface modification results published in the literature [42].
Conclusions
In summary, the surface of the ZnS nanoparticle was successfully modified using transN-[6,6,-Dimethyl-2-hepten-4-ynyl]chitosan. Fluorescence properties of the surface modified nanoparticles was studied at room temperature. ZnS-CSD NPs exhibited emission at 457 nm and the photostability of ZnS-CSD was found better when compared with Rhodamine B and FITC. The optimized concentration to modify ZnS surface was identified as 0.04% to achieve significant fluorescence. The sizes of ZnS-CSD nanoparticles were in the range of 40-130 nm as observed from FESEM and showed spherical morphology. XRD studies confirmed the cubic zinc blende structure of ZnS-CSD and size of nanoparticles. MTT assay studies confirmed the biocompatibility of ZnS-CSD NPs. Easy of synthesis and better photostability of ZnS-CSD NPs could make these candidates a promising fluorescence probe to image cancer cells both in Vitro and in Vivo.
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Jothimani, B., Sureshkumar, S. & Venkatachalapathy, B. Synthesis and Characterization of Surface Modified, Fluorescent and Biocompatible ZnS Nanoparticles with a Hydrophobic Chitosan Derivative. J Fluoresc 27, 1277–1284 (2017). https://doi.org/10.1007/s10895-017-2059-5
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DOI: https://doi.org/10.1007/s10895-017-2059-5