Polylysine Crosslinked AIE Dye Based Fluorescent Organic Nanoparticles for Biological Imaging Applications a

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1 Full Paper Polylysine Crosslinked AIE Dye Based Fluorescent Organic Nanoparticles for Biological Imaging Applications a Meiying Liu, Xiqi Zhang, Bin Yang, Liangji Liu, Fengjie Deng, Xiaoyong Zhang,* Yen Wei* Fluorescent organic nanoparticles based on aggregation induced emission dyes are fabricated through a ring-opening reaction using polylysine as the linker. The fluorescent organic nanoparticles obtained are characterized by a series of techniques including UV vis absorption spectroscopy, fluorescence spectroscopy, Fourier Transform infrared spectroscopy, and transmission electron microscopy. A biocompatibility evaluation and the cell uptake behavior of the fluorescent organic nanoparticles are further investigated to evaluate their potential biomedical applications. It is demonstrated that these fluorescent organic nanoparticles can be obtained at room temperature in an air atmosphere without the need for catalyst or initiator. Furthermore, these crosslinked aggregation induced emission dye based fluorescent organic nanoparticles show uniform morphology, strong red fluorescence, high water dispersability, and excellent biocompatibility, making them promising candidates for various biomedical applications. 1. Introduction The biomedical applications of fluorescent nanomaterials have become one of the hottest research fields since the first report on using semiconductor nanocrystals Dr. M. Liu, Prof. F. Deng, Prof. X. Zhang Department of Chemistry/Institute of Polymers, Nanchang University, 999 Xuefu Avenue, Nanchang , China xiaoyongzhang1980@gmail.com Dr. X. Zhang, Dr. B. Yang, Prof. Y. Wei Department of Chemistry and Key Laboratory of Bioorganic Phosphorus Chemistry and Chemical Biology (Ministry of Education), Tsinghua University, Beijing , P. R. China weiyen@tsinghua.edu.cn Prof. L. Liu Affiliated Hospital of Jiangxi University of Traditional Chinese Medicine, 445 Bayi Avenue, Nanchang , P. R. China a Supporting Information is available from Wiley Online Library or from the author. as fluorescent biological labels. [1] When compared with small organic dyes, fluorescent nanomaterials exhibit unique nanostructural characteristics and superior optical properties, making them promising for biomedical applications ranging from environmental monitoring to disease diagnosis and treatment. [2 6] Based on their compositions, fluorescent nanomaterials can be divided into fluorescent inorganic nanoparticles (FINs) and fluorescent organic nanoparticles (FONs). Over the past few decades, the biomedical applications of FINs have attracted great research interest because of their controllable synthesis, tunable photoluminescence, superior photostability, and low cost. A variety of FINs, including semiconductor quantum dots, metal nanoclusters, carbon nanodots, photoluminescent silica nanoparticles, and Ln ion-doped nanomaterials, have been developed and some of them are commercially available on the market. [7 12] Despite the significant advances in FINs, their practical biomedical applications are still largely limited due to their non-biodegradability. [13 15] It is well known that 1260 wileyonlinelibrary.com DOI: /mabi

2 Polylysine Crosslinked AIE Dye Based Fluorescent... FINs tend to accumulate in the reticuloendothelial system after in vivo adminstration and remain in these organs for the long term. Other studies have also implied that FINs such as semiconductor quantum dots could cause significant toxic effects to cells and animals due to their heavy metal compositions. [16] The identification of biodegradable fluorescent nanoprobes with excellent biocompatibity is therefore highly desirable for their practical biomedical application. FONs have recently emerged as promising fluorescent nanoprobes for biomedical applications. [17 19] Their obvious advantages include the potential to biodegrade, the designability of small organic molecules, the ease of surface functionalization, and excellent biocompatibility. Different FONs based on polymerizable conventional organic dyes, conjugated polymers, polydopamine, and aggregation induced emission (AIE) dyes have previously been developed. [20 37] The basic principle for fabrication of FONs is the integration of hydrophobic organic dyes with hydrophilic molecules, thus forming a dye containing amphiphilic copolymers. These copolymers can be further self-assembled into FONs in pure aqueous solution. In this work, hydrophobic dyes were encapsulated in the core of FONs and the hydrophilic moieties covered the hydrophobic core, forming a shell. However, FONs obtained in this way often suffer from a significant fluorescence intensity decrease due to the notorious aggregation caused quenching (ACQ) effect. [24] AIE is an abnormal fluorescent phenomenon, which suggests that some organic dyes emit much stronger fluorescence intensity in the aggregated state than in the dispersed state. [38] Since Tang et al. first reported the AIE phenomenon in 2001, a variety of dyes with the AIE property, including tetraphenylethene, [39,40] siloles, [41,42] triphenylethene, [20,43,44] distyrylanthracene, [45,46] and cyano-substituted diarylethene, [47,48] have been discovered. These AIE dyes with different chemical structures and fluorescent properties have been widely utilized for the fabrication of AIE based FONs and explored for various biomedical applications. [49 56] However, most of these FONs are formed through the self-assembly of AIE dye containing amphiphilic copolymers, which are often unstable in dilute solution below the critical micelle concentration. Therefore, the preparation of crosslinked FONs to enhance their stability is highly desirable for use in biomedical applications. However, to the best of our knowledge, the preparation of crosslinked AIE dye based FONs has seldom been reported. [50] Polylysine (Ply) is a positively charged synthetic polymer with good biocompatibility and a number of amino groups. [57] It has been extensively investigated for various biomedical applications ranging from enhancement of cell attachment to antimicrobial and gene delivery. [57] In the present work, Ply served as the linker for fabrication of crosslinked AIE dye based FONs through a one-pot ringopening (RO) reaction at room temperature under an air atmosphere without the need for catalyst or initiator. As shown in Scheme 1, AIE dye (denoted PNH 2 ) was first reacted with 4,4 0 -oxydiphthalic anhydride (OA) through RO polymerization. Ply was then added to further react with RO-OA via a RO condensation reaction. Due to the many amino groups existing on Ply, crosslinked AIE based FONs (denoted RO-OA-Ply FONs) could be prepared in a facile manner through the RO reaction. To further explore their potential biomedical applications, the biocompatibility and cell uptake behavior of RO-OA-Ply FONs were further evaluated. 2. Experimental Section 2.1. Materials and Measurements Phenothiazine, 1-bromooctadecane, N,N-dimethylformamide (DMF), 1,2-dichloroethane, phosphoryl chloride, 4-aminobenzyl cyanide, tetrabutylammonium hydroxide (0.8 M in methanol), N,Ndimethylacetamide (DMAc), and 4,4 0 -oxydiphthalic anhydride (purchased from Alfa Aesar) were used as received. All other agents and solvents were purchased from commercial sources and used directly without further purification. Tetrahydrofuran (THF) was distilled from sodium/benzophenone. Ultra-pure water was used in the experiments. UV-visible absorption spectra were recorded on a UV/Vis/NIR Perkin-Elmer lambda750 spectrometer (Waltham, MA, USA) using quartz cuvettes of 1 cm path length. Fluorescence spectra were Scheme 1. Schematic showing the preparation of crosslinked RO-OA-Ply FONs through ring-opening polymerization (ROP) and cell imaging applications of RO-OA-Ply FONs. 1261

3 M. Liu et al. measured on a PE LS-55 spectrometer with a slit width of 3 nm for both excitation and emission. The FT-IR spectra were obtained in transmission mode on a Perkin-Elmer Spectrum 100 spectrometer (Waltham, MA, USA). Typically, 8 scans at a resolution of 1 cm 1 were accumulated to obtain one spectrum. Transmission electron microscopy (TEM) images were obtained on a JEM-1200EX microscope operating at 100 kv; the TEM specimens were made by placing a drop of the nanoparticle suspension on a carboncoated copper grid. The size distribution of RO-OA-Ply FONs in water and phosphate buffer solution (PBS) was determined using a zeta Plus apparatus (ZetaPlus, Brookhaven Instruments, Holtsville, NY) Preparation of RO-OA-Ply FONs PNH 2 (37 mg, mol) and 4,4 -oxydiphthalic anhydride (19 mg, mol) were dissolved in 10 ml of DMAc. This mixture was stirred under an air atmosphere at room temperature for 2 h. Next, Ply (10 mg, mol) was added to the mixture and stirred for 30 min. The polymerization was then stopped and the mixture dialyzed against tap water for 24 h and against ethanol for 6 h using 7000 Da M w cutoff dialysis membranes. Finally, the solution in the dialysis bag was freezedried to obtain the product Cytotoxicity of RO-OA-Ply FONs Observations of the cell morphology were used to examine the effects of RO-OA-Ply FONs on A549 cells. Briefly, cells were seeded in 6-well microplates at a density of cells ml 1 in 2 ml of respective media containing10% fetal bovine serum (FBS). After cell attachment, plates were washed with PBS and cells were treated with complete cell culture medium, or different concentrations of RO-OA-Ply FONs prepared in 10% FBS containing media for 24 h. Then all samples were washed with PBS three times to remove any uninternalized nanoparticles. The morphology of the cells was observed using an optical microscope (Leica, Germany). The overall magnification was 100. The cell viability of RO-OA-Ply FONs on A549 cells was evaluated using a cell counting kit-8 (CCK-8) assay, based on a method in our previous reports. [58] Briefly, cells were seeded in 96-well microplates at a density of cells ml 1 in 160 mlof the respective media containing 10% FBS. After 24 h of cell attachment, the cells were incubated with 10, 20, 40, 80, or 120 mgml 1 RO-OA-Ply FONs for 8 and 24 h. Then the nanoparticles were removed and the cells were washed three times with PBS. 10 ml of CCK-8 dye and 100 ml of Dulbecco s modified eagle medium (DMEM) cell culture medium were added to each well and incubated for 2 h at 37 8C. Plates were then analyzed with a microplate reader (VictorIII, Perkin-Elmer). Measurements of formazan dye absorbance were carried out at 450 nm, with the reference wavelength at 620 nm. The values were proportional to the number of live cells. The percent reduction of CCK-8 dye was compared to controls (cells not exposed to RO-OA-Ply FONs), which represented 100% CCK-8 reduction. Three replicate wells were used per microplate, and the experiment was repeated three times. Cell survival was expressed as absorbance relative to that of untreated controls. Results were presented as mean standard deviation (SD) Confocal Microscopic Imaging of Cells Using RO-OA-Ply FONs A549 cells were cultured in DMEM supplemented with 10% heatinactivated FBS, M glutamine, 100 U ml 1 penicillin, and 100 mgml 1 of streptomycin. The cell culture was maintained at 37 8C in a humidified condition of 95% air and 5% CO 2 in culture medium. The culture medium was changed every 3 d to maintain exponential growth of the cells. On the day prior to treatment, cells were seeded in a glass bottom dish with a density of cells per dish. On the day of treatment, the cells were incubated with RO-OA- Ply FONs at a final concentration of 10 mgml 1 for 3 h at 37 8C. Afterwards, the cells were washed three times with PBS to remove the RO-OA-Ply FONs and then fixed with 4% paraformaldehyde for 10 min at room temperature. Cell images were taken with a confocal laser scanning microscope (CLSM) Zeiss channel (Zeiss, Germany) with an excitation wavelength of 543 nm. 3. Results and Discussion PNH 2 was prepared following a synthetic route described in our previous report and was characterized and confirmed by standard spectroscopic methods. [59] As shown in Scheme 2 and Scheme S1 in the Supporting Information, PNH 2 with two amino end groups was first reacted with OA through RO polymerization at room temperature for 2 h. The designed degree of polymerization of RO-OA was 5, with anhydride end functional groups according to the feed molar ratio. The number average molecular weight of PNH 2 -OA determined by gel permeation chromatography (GPC) was 9616 Da according to our previous report. [59,60] Then Ply with a number of amino groups was added to react Scheme 2. Chemical structure of PNH 2, OA, and Ply. 1262

4 Polylysine Crosslinked AIE Dye Based Fluorescent... with the anhydride end groups of RO-OA; thus crosslinked AIE dye based FONs (RO-OA-Ply) were obtained. The 1 H NMR of RO-OA-Ply in DMSO is shown in Figure S1 in the Supporting Information. Chemical information for PNH 2 and Ply were both found in the 1 H NMR spectra, demonstrating the successful preparation of RO-OA-Ply. Due to the large number of carboxyl groups generated on FONs in the RO reaction procedure, RO-OA-Ply FONs showed good dispersibility in aqueous solution (inset of Figure 1A). On the other hand, due to the amphiphilic properties of RO-OA-Ply, these copolymers readily selfassembled into organic nanoparticles in aqueous solution. In the FONs, hydrophobic segments (such as PNH 2 ) served as the core and hydrophilic segments (such as carboxyl groups) covered the surface of the FONs as a shell, which gave them excellent dispersibility in water. More importantly, due to the partial aggregation of PNH 2, RO-OA-Ply FONs were expected to emit strong fluorescence in aqueous solution. The successful formation of RO-OA-Ply FONs was confirmed using a series of characterization techniques, such as UV-vis spectroscopy, fluorescence spectroscopy, transmission electron microscopy (TEM), and infrared (IR) spectroscopy. As shown in Figure 1A, the UV-vis spectrum of RO-OA-Ply FONs showed that the maximum absorption wavelength of RO-OA-Ply FONs was located at 470 nm. From the UV-vis spectrum, it was also found that the entire spectrum started to increase in absorption from 800 nm, indicating that RO-OA-Ply copolymers were self-assembled into nanoparticles in pure aqueous solution (Figure 1A). As both Ply and the AIE dye do not show adsorption at wavelengths larger than 600 nm, adsorption in the range nm could be ascribed to the scattering of nanoparticles derived from the self-assembly of the AIE dye containing polymers. Due to the large number of carboxyl groups that existed on the surface of RO-OA-Ply FONs, the FONs could be well dispersed in pure aqueous solution Figure 1. Characterization of PNH 2, and RO-OA-Ply FONs. A) UV-vis spectrum of RO-OA- Ply FONs; inset is the optical image of RO-OA-Ply water dispersion. B) PL spectra of RO- OA-Ply (in water); the emission wavelength of RO-OA-Ply FONs is 600 nm. The excitation (Ex) spectrum showed that the excitation wavelength is very broad. Inset are optical images of RO-OA-Ply FONs in water under a UV lamp (l ¼ 365 nm). (inset of Figure 1A). No appreciable precipitation was found, even after they were deposited for more than one week (Figure S2 in the Supporting Information). On the other hand, RO-OA-Ply FONs showed strong red fluorescence in water when they were irradiated by a UV lamp (l ¼ 365 nm) (inset of Figure 1B). The photoluminescent (PL) properties of RO-OA-Ply FONs in water were also investigated using a PL spectrometer. As shown in Figure 1B, the emission peak of RO-OA-Ply was located at 600 nm and was evidenced in PL spectra under excitation at a wavelength of 490 nm. More importantly, RO-OA-Ply FONs can be excited in the broad wavelength region from 325 to 590 nm, as evidenced in the excitation (Ex) spectrum of RO-OA-Ply FONs. Finally, the obtained RO-OA-Ply FONs exhibited excellent photostability in water (Figure S3 in the Supporting Information). These remarkable PL properties make RO-OA-Ply FONs very promising for biological imaging applications. The morphology and size distribution of RO-OA-Ply were further characterized with TEM and dynamic laser scattering (DLS) analysis. As shown in Figure 2A and Figure S4 in the Supporting Information, uniform spherical nanoparticles with diameters ranged from nm could be clearly identified. The TEM images demonstrated the successful formation of nanoparticles when RO-OA-Ply copolymers were dispersed in aqueous solution. Moveover, DLS analysis was also utilized to determine the size and size distribution of RO-OA-Ply FONs in water and phosphate buffer solution (PBS). The results suggested that the average size of RO-OA-Ply was nm (the polydispersity index was 0.167) in water and nm in PBS. The different size distribution of RO-OA-Ply in water and PBS is likely to be because the ions in PBS can decrease electrostatic repulsion between the FONs and therefore influence their hydrodynamic stability. When compared with the size determined by DLS, the lateral size obtained from TEM was somewhat smaller, which is likely due to shrinkage of the micelles during the drying process or aggregation of RO-OA-Ply FONs in water suspension. The IR spectra of PNH 2, Ply, OA, and RO-OA-Ply are displayed in Figure 2B. It can be seen that a series of absorbance bands located between cm 1 existed in the PNH 2 sample. These IR absorbance bands were assigned to the stretching vibration of polycyclic aromatic rings in PNH 2. A small absorption peak located at 3400 cm 1 was also observed. This was ascribed to the stretching vibration of the N H band of the amino groups in PNH 2. Furthermore, much stronger absorbance peaks located at 2840 and 2920 cm 1, attributed to the stretching vibration of the C H band, were also identified, 1263

5 M. Liu et al. Figure 2. A) TEM images of RO-OA-Ply FONs; the images show that the diameters of RO-OA-Ply FONs are about nm. B) Normalized IR spectra of PNH 2, Ply, OA, and RO-OA-Ply FONs. Strong stretching vibration bands of C5O, which are located at 1732 cm 1, and C O stretching vibration bands, which are located at 1108 cm 1, were observed in the sample of RO-OA-Ply FONs, suggesting RO-OA-Ply FONs were successfully fabricated. indicating the present of alkyl chain in PNH 2. [61,62] When compared with the spectrum of PNH 2, the absorption intensity of the OH stretching vibration band (located at 3400 cm 1 ) was significantly enhanced, suggesting the RO reaction did occur. Additionally, a new absorption peak located at 1108 cm 1 appeared, indicating the carboxyl group existed in RO-OA-Ply. These IR spectra further evidenced the successful formation of RO-OA-Ply via a RO reaction. Although great effort has been devoted to the preparation of AIE dye based FONs and exploiting their biomedical applications, only a few methods have been developed for the fabrication of crosslinked AIE dye based FONs. [50] In this work, a rather facile method has been developed for the fabrication of crosslinked AIE based FONs via a one-pot RO reaction using Ply as the linker. When compared to previous reports, the crosslinked AIE based FONs have many advantages for biomedical applications. [51,54] First, RO-OA-Ply FONs are expected to be more stable in dilute solution because RO-OA was crosslinked by Ply. The RO reaction occurs at room temperature under an air atmosphere without the need for catalyst or initiator. It is rather simple, effective and scalable. More importantly, apart from Ply, many other polyamine compounds, such as polyethylenimine, polyamines and others, could also be utilized for the fabrication of crosslinked AIE based systems through the RO condensation reaction. Finally, a number of carboxyl groups were generated on the surface of RO-OA-Ply FONs during the RO procedure, thus many other functional components, such as targeting agents, drugs, and imaging agents, could be further integrated into the luminescent system. Multifunctional crosslinked AIE based theranostics can therefore be facilely fabricated. To evaluate their potential biomedical applications, the biocompatibility of RO-OA-Ply FONs with human lung adenocarcinoma epithelial (A549) cells was determined. [63 68] As shown in Figure 3A 3C and Figure S5 in the Supporting Information, cells still adhered to the cell plate even when the concentration of RO-OA-Ply FONs was as high as 120 mgml 1 (Figure S3 in the Supporting Information). No significant cell morphology changes were observed when cells were incubated with 80 mgml 1 of RO-OA-Ply FONs for 24 h (Figure 2C). These results imply the good biocompatibility of RO-OA-Ply FONs with A549 cells. Furthermore, a CCK-8 assay was carried out to quantitatively evaluate the effect of RO-OA-Ply FONs with A549 cells. [58,69 71] Cell viability measurements further confirmed the excellent biocompatibility of RO-OA-Ply FONs. As shown in Figure 3D, no cell viability decrease was observed when cells were incubated with mgml 1 of RO-OA-Ply FONs for 24 h. Even when the concentration of RO-OA-Ply FONs was as high as 120 mgml 1, the cell viability values of RO-OA-Ply FONs were still greater than 90%. To examine the potential biomedical applications of RO- OA-Ply FONs, their cell uptake behavior was evaluated using a confocal laser scanning microscope (CLSM). As shown in Figure 4, the cell uptake of RO-OA-Ply FONs was clearly observed after cells were incubated with 10 mgml 1 of RO-OA-Ply FONs for 3 h (samples were irradiated with a 543 nm laser). The successful dying of cells with FONs implies the potential for biological imaging applications of RO-OA-Ply FONs. Many dark areas with relatively weak fluorescence intensity could also be observed in CLSM images (Figure 4B). These dark areas were possibly the location of cell nuclei, which implies that RO-OA-Ply FONs can enter the cell nucleus. More importantly, due to the strong fluorescence intensity, cells could be successfully stained with only 10 mgml 1 of RO-OA-Ply FONs. The dosage needed for cell imaging applications is therefore much lower than their biocompatible dosage. Furthermore, 1264

6 Polylysine Crosslinked AIE Dye Based Fluorescent... Figure 3. Biocompatibility evaluation of RO-OA-Ply FONs. A C) Optical microscopy images of A549 cells incubated with different concentrations of RO-OA-Ply FONs for 24 h: A) control cells; B) 10 mgml 1 ;C)80mgmL 1 ; D) cell viability of RO-OA-Ply FONs with A549 cells (the concentration of RO-OA-Ply FONs ranged from mgml 1 ). Figure 4. CLSM images of A549 cells when they were incubated with 10 mgm 1 of RO-OA-Ply FONs for 3 h. A) Bright field; B) Excited with 543 nm laser; C) Merged image of A and B. Scale bar ¼ 20 mm. the dosage of RO-OA-Ply FONs could be further decreased if their surfaces were conjugated with targeting agents. By combining the advantages of AIE dyes, Ply, and the RO reaction, we therefore believe that RO-OA-Ply FONs have great potential for various biomedical applications. 4. Conclusion In summary, a novel method for the fabrication of crosslinked RO-OA-Ply FONs has been developed, through a one-pot RO reaction using Ply as the linker. This reaction occurs at room temperature under an air atmosphere without the need for catalyst or initiator. Because a number of carboxyl groups are generated during the RO reaction, the obtained RO-OA-Ply FONs readily assemble into FONs in pure aqueous solution. These FONs exhibit strong red fluorescence, high water dispersibility, uniform morphology, and excellent biocompatibility, making them potentially suitable for various biomedical applications. More importantly, a large number of carboxyl groups exist on the surface of RO-OA-Ply FONs, which can be further 1265

7 M. Liu et al. conjugated with other functional components such as targeting agents, drugs, and imaging agents; thus, multifunctional theranostic platforms based on RO-OA-Ply FONs could be fabricated. Acknowledgements: This research was supported by the National Science Foundation of China (Nos , , , ), the National 973 Project (No. 2011CB935700), and the China Postdoctoral Science Foundation (Nos. 2012M520388, 2012M520243, 2013T60100, 2013T60178). Received: March 20, 2014; Revised: April 15, 2014; Published online: May 22, 2014; DOI: /mabi Keywords: aggregation-induced emission; cell imaging; crosslinked; fluorescent organic nanoparticles; ring-opening reaction [1] M. Bruchez, M. Moronne, P. Gin, S. Weiss, A. P. Alivisatos, Science 1998, 281, [2] X. Feng, L. Liu, S. Wang, D. Zhu, Chem. Soc. Rev. 2010, 39, [3] E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott- Schwartz, H. F. Hess, Science 2006, 313, [4] B. 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