Sonosensitizer for ROS-Mediated Eradication
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1 (Supporting Information for Nano Letters) Long-Circulating Au-TiO 2 Nanocomposite as a Sonosensitizer for ROS-Mediated Eradication of Cancer V. G. Deepagan,,# Dong Gil You,,,# Wooram Um,, Hyewon Ko, Seunglee Kwon, Ki Young Choi, Gi-Ra Yi, Jun Young Lee, Doo Sung Lee, Kwangmeyung Kim, Ick Chan Kwon, and Jae Hyung Park,,* School of Chemical Engineering, College of Engineering, Sungkyunkwan University, Suwon 16419, Republic of Korea. Center for Theragnosis, Biomedical Research Institute, Korea Institute of Science and Technology, Seoul 02792, Republic of Korea. Department of Health Sciences and Technology, SAIHST, Sungkyunkwan University, Seoul 06351, Republic of Korea. # These authors contributed equally to this work. Corresponding Author * jhpark1@skku.edu 1
2 Materials and reagents. Anatase TiO 2 NPs (25 nm in diameter), chloroauric acid, carboxymethyl dextran (CMD) sodium salt (Mw=10,000 20,000 Da), 1-ethyl-3-(3-dimethylaminopropyl)- carbodiimide hydrochloride (EDC HCl), N-hydroxysulfosuccinimide (NHS), dopamine HCl, 1,3-diphenylisobenzofuran (DPBF), and sodium citrate dihydrate were purchased from Sigma Chemical Co. (St. Louis, MO, USA). Cy5.5 was purchased from Amersham Biosciences (NJ, USA). Singlet oxygen ( 1 O 2 ) sensor green reagent was purchased from Life Technologies Korea LLC (Seoul, Korea). All other reagents were analytical grade. The deionized water (DIW) was prepared using an Aqua Max-Ultra water purification system (Younglin Co., Anyang, Korea). The SCC7 cell line was purchased from the American Type Culture Collection (ATCC, Rockville, MD, USA). For cell culture, RPMI-1640, trypsin-edta, and fetal bovine serum (FBS) were purchased from Welgene Inc. (Daegu, Korea). All experiments involving live animals were carried out in accordance with the relevant laws and institutional guidelines of Sungkyunkwan University. The Sungkyunkwan University institutional committees approved all experimental protocols. Methods Synthesis of Au-TiO 2 nanocomposites (NCs). NCs-1, NCs-2 and NCs-3 were produced by photoreduction of Au 3+ on the surface of the TiO 2 NPs. In a typical experiment 10 mg of TiO 2 NPs was suspended in 10 ml of DIW containing 3.5 mg (0.012 mmol) of sodium citrate. To this, 10 µl of 2 N NaOH solution was added and the mixture was sonicated for 5 min using a probe type sonicator. Next, chloroauric acid (10 mm, 100 µl) was added and stirred under UV irradiation (wavelength = 256 nm, power output = 4 Watts). The size and distribution of the NPs were controlled by adjusting the irradiation time with UV light. 2
3 When the reaction was carried out for 3 min small Au NPs formed on the surface of the TiO 2 NPs (NCs-1), whereas a 10 min irradiation time resulted in the formation of large Au NPs and disappearance of some of the smaller Au NPs (NCs-2). A further increase in reaction time (up to 12 h) resulted in the complete transformation of small Au NPs into larger Au NPs (NCs-3). The morphology of the NCs was observed using TEM (JEM-2100F, JEOL, Japan) at an accelerating voltage of 200 kev. The NCs were characterized using XRD (D8 ADVANCE, Bruker Corporation, USA), ICP-MS (Agilent 7500, SpectraLab Scientific Inc, Canada), and UV vis spectrophotometer (Optizen 3220UV, Mecasys Inc., Korea). Synthesis of HTiO 2 NPs and HAu-TiO 2 NCs. Chemical conjugation of CMD on the surface of the nanoparticles was performed by a similar procedure to that described earlier. 1 All reactions involving TiO 2 NPs and NCs were carried out in the dark to avoid any unwanted photoreaction. First, dopamine-decorated TiO 2 NPs and NCs-2 nanocomposites were prepared with a dopamine: TiO 2 NPs ratio of 25:1 for both TiO 2 NPs and NCs-2. For this, 2 nmol dopamine was added to 5 ml of formamide solution containing 10 mg of TiO 2 NPs (anatase) under vigorous stirring. The suspension was allowed to react for 6 h at room temperature and then purified by centrifugation at 13,000 rpm. The dopamine-decorated TiO 2 NPs and NCs-2 were purified by three rounds of centrifugation at 13,000 rpm and washing with formamide. Finally, the samples were suspended in 10 ml formamide. Second, the CMD coating was generated by chemically conjugating CMD to the dopamine via EDC and NHS chemistry. In brief, 200 mg of CMD was added to 20 ml of formamide with EDC (76.7 mg, 0.4 mmol) and NHS (57.5 mg, 0.49 mmol) and stirred overnight. To this activated CMD, 2 ml of dopamine-decorated TiO 2 NPs and Au-TiO 2 NCs was added and stirred overnight to yield HTiO 2 NPs and HAu-TiO 2 NCs. Finally, 100 µl of 0.1 N NaOH was added and stirred for 1 h to complete the reaction. The byproducts and the 3
4 excess polymer were removed by dialysis against sodium borate buffer (ph 8.6) at 4 C using a 50-kDa cut-off membrane for 48 h with buffer changes every 6 h. The dialysate was sonicated briefly for 10 seconds (Sonic Vibracell VCX 750, CT, USA) and filtered to remove the large aggregates. Finally, the nanosuspension was filtered through a 0.8-µm filter and lyophilized for future use. For in vivo imaging, Cy5.5-conjugated NPs were prepared by reacting NHS-activated HTiO 2 NPs and HAu-TiO 2 NCs with amine-functionalized Cy5.5. The Cy5.5-labeled NPs were purified by dialysis to remove the byproducts, followed by lyophilization. The chemical structure of NPs were then confirmed using FT-IR (IFS-66/S, Bruker Corporation, USA). The hydrodynamic size of NPs were measured by dynamic light scattering using a Zetasizer (Nano ZS90, Malvern Instruments, UK) with a He-Ne laser (633 nm) at 90 collecting optics. The stability of HTiO 2 NPs and HAu-TiO 2 NCs was assessed by monitoring the sizes of NPs for 6 days using the Zetasizer (Nano ZS90, Malvern Instruments, UK), in physiological saline and in the presence of 10% FBS. In vitro ROS generation of NCs, HTiO 2 NPs, and HAu-TiO 2 NCs. The in vitro ROS generation potential of all NCs and NPs was determined using DPBF. In brief, 0.5 ml of the sample (Ti 1M) suspension was added to 0.5 ml of DPBF ( M) solution. The mixture was then placed in a 3% (W/V) agarose gel mold and exposed to a pre-clinical high intensity focused ultrasound system (VIFU 2000, Alpinion Medical Systems, Seoul, Korea) equipped with a single element spherical-focused transducer (1.5MHz, 2cm x 1.5cm in size) under 10% duty cycle (power: 30 W, pulse repetition frequency: 1 Hz, X,Y interval: 2 mm) for 330 seconds. The concentration of DPBF was determined by measuring the absorbance at 413 nm as a function of time using a UV-vis spectrometer (G1103A, Agilent, USA). The rate constant for 1 O 2 generation by HTiO 2 NPs and HAu-TiO 2 NCs was calculated using the following equation [ln([dpbf] t /[DPBF] 0 )= -kt]. 4
5 Cell culture. SCC7 cells (mouse squamous carcinoma cell line) were cultured in RPMI 1640 supplemented with 10% FBS, 100 U/mL penicillin, and 100 µg/ml streptomycin at 37 C in a humidified incubator with 5% CO 2 atmosphere. In vitro cytotoxicity assay. The biocompatibility of HTiO 2 NPs and HAu-TiO 2 NCs was tested using SCC7 cells. In a typical experiment cells/well were seeded in 96-well flat-bottomed plates and incubated for 24 h. The cells were then washed twice with PBS and replenished with media containing various concentrations of the test samples. After treatment the cells were washed once with PBS and replenished with 100 µl of basal media containing 10% MTT solution (5 mg/ml). After incubation for 3 h the spent medium was removed and the MTT crystals were dissolved in DMSO. The absorbance of each well was measured at 570 nm using a microplate reader (VERSA max, Molecular Devices Corp., USA). For the apoptosis assay, SCC7 cells were seeded in 6-well plates at a density of cells/well and incubated until they formed a monolayer. The cells were washed twice with PBS and replenished with media containing 100 µg/ml of the test sample. After incubation, the cells were harvested and incubated with FITC-labeled annexin V antibody and propidium iodide for 30 min. The level of apoptosis was measured using flow cytometry (Guava easycyte, Merck Millipore, USA). In vivo biodistribution. To observe the in vivo biodistribution of nanoparticles, a SCC7 flank tumor model was prepared by subcutaneous injection of 80 µl of cell suspension containing cells in PBS into athymic mice. After 10 days, Cy5.5-labeled NPs were injected into the tail vein of the mice at a dose of 3 mg/kg. To observe the biodistribution of the NPs at predetermined time points, the animals were imaged using the Explore Optix system (Optix MX3, Advanced Research Technologies Inc., Canada) with the 670 nm 5
6 excitation pulsed laser set to an output power of 10 µw for 0.3 seconds/point. The tumortargeting characteristics of NPs were evaluated by measuring the NIR fluorescence intensity at the tumor site (28 mm 2 ). All data were calculated using the region of interest function of Analysis Workstation software (Optix MX3, Advanced Research Technologies Inc., Canada). The distribution of nanoparticles in tumor tissue was analyzed using a small-animal imaging system (OV-100, Olympus, Center Valley, PA) with the green fluorescent protein (GFP) channel (λ ex = nm, λ em = nm) and Cy5.5 channel (λ ex = nm, λ em = nm). The skin over the tumor of the mice was scraped off 12 h after intravenous injection of Cy5.5-labeled NPs (3 mg/kg) and the NIR fluorescence images of the tumor were recorded. To visualize the tumor blood vessels, FITC-labeled dextran (10 mg/kg) was administered intravenously to the mice immediately before measurement. In vivo ROS imaging. To determine in vivo ROS generation SCC7 tumor-bearing mice were prepared as described earlier. The mice were divided into six groups: (a) saline, (b) saline + US, (c) HTiO 2 NPs (Ti 3 mg/kg), (d) HTiO 2 NPs (Ti 3 mg/kg) + US, (e) HAu- TiO 2 NCs (Ti 3 mg/kg), and (f) HAu-TiO 2 NCs (Ti 3 mg/kg) + US. Each sample was administered intravenously. At 12 h post injection, 100 µl of 1 O 2 sensor green reagent (50 µm) was injected directly into the tumor mass, which was immediately treated with US (power: 30 W, frequency: 1.5 MHz, duty cycle: 10%, pulse repetition frequency: 1 Hz, interval: 2 mm, time: 30 s). The same ultrasound system and transducer as we used for in vitro ROS generation were employed. After US exposure, a portion of tumor tissue was collected and cryosectioned at 10-µm thickness. Fluorescence images of tumor sections were obtained by fluorescence microscopy (IX81-ZDC, Olympus, Tokyo, Japan) using a GFP filter. 6
7 Antitumor efficacy of SDT with HTiO 2 NPs and HAu-TiO 2 NCs. The antitumor efficacy of nanoparticles was determined by measuring the tumor volume once every 2 days for 32 days. Tumor-bearing mice were prepared by subcutaneous injection of 80 µl of SCC7 cell suspension containing approximately cells into the flank region of C3H/HeN mice. When the tumors reached a volume of 250 mm 3, the mice were divided into six groups: (a) saline, (b) saline + US, (c) HTiO 2 NPs (Ti 3 mg/kg), (d) HTiO 2 NPs (Ti 3 mg/kg) + US, (e) HAu-TiO 2 NCs (Ti 3 mg/kg), and (f) HAu-TiO 2 NCs (Ti 3 mg/kg) + US. Each sample was injected intravenously into mice. US (power: 30 W, frequency: 1.5 MHz, duty cycle: 10%, pulse repetition frequency: 1 Hz, interval: 2 mm, time: 30 s) was administered 12 h post injection. For SDT, the experimental set-up for ultrasound exposure was exactly same as the one we used for in vivo ROS imaging. This treatment was given once every 4 days with the pre-set conditions. The mice were ethically sacrificed when the tumor volume exceeded 5000 mm 3. Tumor volumes were calculated as a b , where a represents the largest and b the smallest diameter. Histology. For the histopathologic study the major organs including liver, heart, kidneys, and spleen were excised from mice 24 h post injection. Organs were fixed in 3.7% neutral buffered formalin, processed into paraffin, sectioned into approximately 4-µm slices, and stained with hematoxylin and eosin (H&E). Samples were chosen at random and examined by bright-field microscopy (BX51, Olympus, Japan). 7
8 Figure S1. Physicochemical characterization. (a) XRD patterns of bare TiO 2 NPs and NCs, (b) Representative EDS spectrum of NCs, (c) XRD spectra and (d) UV-vis spectra of bare TiO 2 NPs and NCs. 8
9 500 Size (nm) HTiO 2 NPs HAu-TiO 2 NCs Time (days) Figure S2. Stability of HTiO 2 NPs and HAu-TiO 2 NCs in the presence of serum. The error bar represents standard deviation (n=3). 9
10 Figure S3. UV-vis spectra of DPBF with increasing exposure time (a) HTiO 2 NPs and (b) HAu-TiO 2 NCs. 10
11 Figure S4. Toxicity of HTiO 2 NPs. (a) In vitro cytotoxicity of HTiO 2 NPs and HAu-TiO 2 NCs, measured by the MTT assay. Apoptosis assay for (b) HTiO 2 NPs and (c) HAu-TiO 2 NCs by flow cytometry. 11
12 Figure S5. H&E staining of major organs after SDT (Scale bar, 250 µm). 12
13 REFERENCES 1. You, D. G.; Deepagan, V. G.; Um, W.; Jeon, S.; Son, S.; Chang, H.; Yoon, H. I.; Cho, Y. W.; Swierczewska, M.; Lee, S.; Pomper, M. G.; Kwon, I. C.; Kim, K.; Park, J. H. Sci. Rep. 2016, 6,
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