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1 Supporting Information Basu et al /pnas SI Materials and Methods Synthesis of PLGA-9859 jugate 2. PLGA (5 mg,.12 mmol) was dissolved in 1-ml dimethylformamide (DMF) under nitrogen atmosphere in a round-bottom flask. Into the flask, HBTU (7 mg,.178 mmol) was added, followed by DIPEA (5 l,.238 mmol). The reaction mixture was stirred at room temperature for 15 min. The pale brown color indicates the activation of the carboxylic acid of PLGA. Activated PLGA was then added into 9859 (1 mg,.36 mmol) solution in 1-ml dry DMF and the reaction mixture was stirred at room temperature for 24 h. The PLGA-9859 conjugate was precipitated from the reaction mixture by diethyl ether (3 ml) and centrifuged at 3,22 g for 3 min. The precipitated polymer was collected and washed repeatedly with diethyl ether to remove the excess reagents. Finally, the polymer was dried under vacuum for 24 h to obtain the conjugated product. UV-VIS Spectrum. UV-VIS spectrum of the product shows 2 peaks at wavelength 35 nm and 297 nm, which are the characteristics peaks for a 9859 molecule. 1 H NMR (3 MHz): (ppm) (m, aromatic protons), (m, aromatic protons), (m, polymer protons), (m, polymer protons), 2.98 (s, -OCH 3, proton), (m, polymer proton). 13 C NMR (75 MHz): (ppm) 181.1, 179.5, 169.5, 169.4, 166.6, 154.8, 152.3, 148.3, 144.4, 143.4, 132.3, 127.9, 116.7, 113.1, 111.8, 11.2, 69.3, 69.1, 6.9, Synthesis of Activated PLGA 4. PLGA (5 mg,.12 mmol) was dissolved in 1 ml of dichloromethane (DCM) and cooled to C. Into the reaction mixture p-nitrophenylchloroformate (7 mg,.33 mmol) and pyridine (5 l,.56 mmol) were added and the reaction was stirred at room temperature for 4 h. The reaction was diluted with DCM and quenched with.1 N HCl solution. The organic layer was extracted by DCM (2 2 ml), washed with brine, and dried over anhydrous Na 2 SO 4. The solvent was evaporated to obtain the activated polymer 4. UV-VIS Spectrum: UV-VIS spectrum of the product shows a peak at 267 nm, which is the characteristics peak of p-nitrophenyl moiety. 1 H NMR (3 MHz): (ppm) (m, aromatic proton), (m, aromatic proton), (m, aromatic proton), (m, aromatic proton), (m, polymer protons), (m, polymer protons), (m, polymer proton). 13 C NMR (75 MHz): (ppm) 169.8, 166.8, 126.6, 125.8, 122.7, 116., 11.4, 69.7, 61.4, 54.4, 3.1, Synthesis of Polymer 6. Polymer 4 (1 mg,.24 mmol) and 5-aminoisophthalic acid were dissolved in 1-ml DMF. DIPEA (17 l,.95 mmol) was added to it and the reaction mixture was stirred at room temperature for 24 h. As soon as DIPEA was added, the reaction mixture turned to yellow, which indicates the liberation of p-nitrophenoxide anion in the solution. The polymer was precipitated out from the reaction mixture by adding diethyl ether (4 ml), centrifuged at 3,22 g for 4 min, and washed thoroughly with diethyl ether (5 5 ml) to remove excess reagents. The product polymer was dried under vacuum to obtain product 6. UV-VIS Spectrum: UV-VIS spectrum of the product shows a peak at 25 nm which is the characteristics peak of 5-aminoisophthalic acid moiety. 1 H NMR (3 MHz): (ppm) (m, aromatic proton), (m, aromatic proton), (m, aromatic proton), (m, polymer protons), (m, polymer protons), (m, polymer proton). 13 C NMR (75 MHz): (ppm) 17.4, 169.2, 154.2, 126., 125.2, 122.9, 116.5, 11.4, 69.5, 61., 54.5, 16.. Synthesis of Polymer 8. Polymer 6 (3 mg,.71 mmol) was dissolved in 2-ml DMF and the carboxylic acids were activated by N,N -dicyclohexyl carbodiimide (66 mg,.32 mmol) and N- hydroxy succinimide (37 mg,.32 mmol) at room temperature for 18 h. The formation of insoluble dicyclohexyl urea indicates the formation of the activated carboxylic acids. Next, 5-aminoisophthalic acid (58 mg,.32 mmol) and DIPEA (74 l,.43 mmol) were added and the reaction mixture was stirred at room temperature for another 24 h. Dicyclohexyl urea was filtered and washed thoroughly by DCM (5 5 ml). The solvent was evaporated and the polymer was precipitated out by diethyl ether (45 ml). The polymer was spun down at 3,22 g for 4 min and dried under high vacuum to obtain polymer 8. UV-VIS Spectrum: UV-VIS spectrum of the product shows a peak at 25 nm which is the characteristics peak of 5-aminoisophthalic acid moiety. 1 H NMR (3 MHz): (ppm) (m, aromatic protons), (m, aromatic protons), (m, aromatic protons), (m, polymer protons), (m, polymer protons), (m, polymer proton). Synthesis of FITC-Labeled PLGA. PLGA (5 mg) was dissolved in 75 l dichloromethane. N- hydroxy succinimide (1 mg) and N-(3- Dimethylaminopropyl)-N -ethylcarbodiimide (15 mg) were added into the reaction mixture and stirred at room temperature for 2 h. Next, 6-mg FITC was dissolved in 25- l dichloromethane and 25- l pyridine. The FITC solution in pyridine was added into the activated PLGA solution and the reaction mixture was stirred at 4 C for 24 h in the dark. The reaction was diluted with 5-ml DCM and quenched with.1 N HCl solution. The organic layer was extracted with DCM (2 ml 2), washed with water (1 ml 2), and brine (2 ml), and dried over anhydrous sodium sulfate. The organic layer was filtered and evaporated to obtain the crude product. The PLGA-FITC conjugate was precipitated out from the crude product by addition of diethyl ether (4 ml). The polymer was centrifuged at 3,22 g for 3 min. The supernatant was discarded and the polymer was washed thoroughly by diethyl ether (5 ml 3) and dried under vacuum overnight. Synthesis of PLGA-PEG jugate 1. PLGA (5 mg,.12 mmol) was dissolved in DMF (1 ml). The carboxylic acid of PLGA was activated by HBTU (7. mg,.18 mmol) and DIPEA (9 l,.5 mmol) for 1 min at room temperature. The pale brown color indicates the activation of the carboxylic acid of PLGA. The activated PLGA was then added into amino polyethylene glycol (PEG-NH 2 ) (36 mg,.18 mmol) solution in 1-ml dry DMF and the reaction mixture was stirred at room temperature for 24 h. The PLGA-PEG conjugate was precipitated out from the reaction mixture by adding diethyl ether (4 ml) and centrifuged at 3,22 g for 3 min. The supernatant was discarded and the polymer was washed with diethyl ether (3 5 ml) to remove excess reagents. Finally, the polymer was dried under vacuum for 24 h to obtain the conjugated product. The polymer was characterized by 1 H NMR spectroscopy. 1 H NMR (3 MHz): (ppm) (m, PLGA CH-), (m, PLGA CH 2 -), (m, PEG CH 2 -), 1.28 (s, PLGA CH 3 -). Synthesis of PLGA-PEG-Biotin jugate 11. PLGA (25 mg,.6 mmol) was dissolved in DMF (1 ml). The carboxylic acid of PLGA was activated by HBTU (4. mg,.9 mmol) and DIPEA (5 l,.3 mmol) for 1 min at room temperature. The pale brown color indicates the activation of the carboxylic acid of PLGA. The activated PLGA was then added into amino biotin polyethylene glycol amine (Biotin-PEG-NH 2 ) (3 mg,.9 mmol) solution in Basu et al. 1of6
2 1-ml dry DMF and the reaction mixture was stirred at room temperature for 24 h. The PLGA-PEG-Biotin conjugate was precipitated out from the reaction mixture by adding diethyl ether (4 ml) and centrifuged at 3,22 g for 3 min. The supernatant was discarded and the polymer was washed with diethyl ether (3 5ml) to remove excess reagents. Finally, the polymer was dried under vacuum for 24 h to obtain the conjugated product. The polymer was characterized by 1 H NMR spectroscopy. 1 H NMR (3 MHz): (ppm) (m, PLGA CH-), (m, PLGA CH 2 -), (m, biotin protons), (m, PEG CH 2 -), (m, biotin protons), (m, biotin protons), (m, PLGA CH 3 -), (m, biotin protons), (m, biotin protons), (m, biotin proton). Synthesis of the Nanoparticles. Nanoparticles were formulated using an emulsion-solvent evaporation technique as described: 5 mg PLGA-9859 (or FITC-PLGA) conjugate was dissolved completely in 2.5-ml acetone and.5-ml methanol. The entire solution was emulsified into 25-ml 2% aqueous solution of PVA (8% hydrolyzed, Mw 9, 1,) by slow injection with constant homogenization using a tissue homogenizer. This mini-emulsion was added to a 1-ml.2% aqueous solution of PVA (8% hydrolyzed, Mw 9, 1,) with rapid mixing for4hatroom temperature to evaporate any residual acetone or methanol. Nanoparticle-size fraction was recovered by ultracentrifugation at 2, and 8, g. Sizing was performed by DLS and TEM. The nanoparticles were washed thoroughly with double distilled water to remove excess PVA before preparing the sample for TEM. Electron Microscopy. The nanoparticles were washed thoroughly with double distilled water to remove excess PVA before preparing the sample for TEM. For TEM, the nanoparticles were fixed in 2.5% gluteraldehyde, 3% paraformaldehyde with 5% sucrose in.1m sodium cacodylate buffer (ph 7.4), embedded in lowtemperature agarose and postfixed in 1% OsO 4 in veronal-acetate buffer. The sample was stained in block over night with.5% uranyl acetate in veronal-acetate buffer (ph 6.), then dehydrated and embedded in epon-812 resin. Sections were cut on a Leica ultra cut UCT at a thickness of 7 nm using a diamond knife, stained with 2.% uranyl acetate followed by.1% lead citrate, and examined using a Philips EM41. Synthesis of Gold-Nanoparticle Decorated PEGylated Nanoparticle. Lyophilized biotinylated nanoparticle was suspended in PBS and incubated with streptavidine-coated gold nanoparticles (.1% gold) at 3 C for 48 h. The gold nanoparticle-coated PLGA-PEG- Biotin nanoparticles were isolated by ultra centrifugation at 8, g. The excess streptavidin-gold nanoparticles were removed by through washing using double distilled water. The gold nanoparticle-coated pegylated nanoparticles were processed for TEM as described earlier, and imaged using a Philips EM41 Physicochemical Release Kinetics Characterization nanoparticles were suspended in 1 ml of tumor cell lysate, and dialyzed (MWCO 1, Da) against 1-ml PBS buffer at room temperature with gentle shaking. Next, 1 l of aliquot was extracted from the incubation medium at predetermined time intervals, dissolved in 9- l DMF, and released 9859 was quantified by UV-VIS spectroscopy at characteristic wavelength of 9859, 297 nm. After withdrawing each aliquot, the incubation medium was replenished by 1 l of fresh PBS. Apoptosis Study. Induction of apoptosis following treatment was quantified using AnnexinV-Alexa Fluor 488 binding. Cells were stained in binding buffer (1 mm Hepes, 14 mm NaCl, 2.5 mm CaCl 2, ph 7.4) for 15 min in the dark, according to the manufacturer s protocol. Cells were then washed with binding buffer, counterstained with propidium iodide, and analyzed using a Becton Dickinson FACSCalibur flow cytometer (excitation 488 and 585 nm, respectively). AnnexinV-Alexa Fluor 488, propidium iodide or both were omitted for the negative controls. Drug Uptake and Metabolism. and B16/F1 cells were seeded on glass coverslips in 24-well plates until subconfluency, and then treated with FITC-conjugated nanoparticles (FITC-NP) for a time-course ranging from 3 min to 24 h. At the indicated times, cells were washed twice in PBS and incubated in LysoTracker Red (Ex: 577 nm; Em: 59 nm) for 3 min at 37 C. Cells were then washed again, fixed in 4% paraformaldehyde, and mounted using Prolong Gold antifade reagent (Invitrogen). Images taken in 3 random fields were captured at 2 and 4 using an inverted microscope (Nikon) equipped with blue and green filters to visualize FITC-NP and LysoTracker Red fluorescence, respectively. Cells incubated either only FITC-NP or LysoTracker Red served as negative controls. Immunoblotting of Cell Extracts. Cells were washed twice with PBS and directly lysed in 3 loading buffer containing 12% SDS, 15% 2-mercaptoethanol, 1-mM sodium orthovandate, and protease inhibitor mixture tablets (Roche Applied Science). Proteins were electrophoretically resolved on SDS/PAGE gel, transferred onto polyvinylidene difluoride membranes, blocked for 1 h with 7% nonfat dry milk, and subsequently incubated overnight at 4 C with primary antibodies directed against the phosphorylated or total forms of ERK1//2 and AKT. Proteins were detected with horseradish peroxidase-conjugated anti-rabbit secondary antibodies and Lumi-LightPLUS Western Blotting Substrate (Roche Applied Science). The blots were developed using GeneSnap, and optical density of the protein bands was quantified using GeneTools (both from SynGene). Predetermined molecular weight standards were used as markers. Proteins were normalized against actin. In Vivo Murine B16/F1 Melanoma Tumor Model. Male C57/BL6 mice (2 g) were injected with BL6/F1 melanoma cells into the flanks. The drug therapy was started after the tumors attained volume of 25 mm 3. The animals were injected through the tail vein with free 9859 or 9859-nanoparticles (equivalent dose of free 9859, 5 mg/kg). Animals receiving cisplatin were injected with the cytotoxic (1.25 mg/kg, i.p.) after one day of the 9859 administration. The total volume of injection was 1 l. The tumor volumes and body weights were monitored on a daily basis. The animals were killed on day 14. Tumor volume was measured as a function of the length and breadth using the equation l b 2.All animal procedures were approved by Harvard University Institutional Use and Care of Animals Committee. Tumor Immunohistology. Permeabilized paraformaldehyde-fixed tumor sections from different treatment groups were probed overnight for phospho-erk using a rabbit polyclonal primary antibody against phosphoerk (dilution 1:25). The sections were washed in TBS (with Triton and Tween), and reprobed with a FITCconjugated secondary anti-rabbit antibody (1:5 dilution) for 2 hours at room temperature. The sections were washed and counterstained with propidium iodide. A separate tumor section was stained with H&E for general pathological analysis. A third section was probed for apoptosis using a TUNEL staining, performed using Texas Red-labeled nucleotide as per the manufacturer s instructions (Roche). The sections were imaged using a Nikon Eclipse epifluorescence microscope. Basu et al. 2of6
3 Fig. S1. Demonstration of surface coating of nanoparticles with PEG. Bioitinylated nanoparticles were engineered from PLGA-b-PEG-biotin conjugate and probed with 5-nm streptavidine-gold nanoparticles (NP). The nanoparticles were cross-sectioned and imaged using TEM. The gold-np-streptavidin complxes with the surface biotinylated-peg. The TEM image of the cross section of a gold-np-coated pegylated nanoparticle shows PLGA-PEG core with dark gold-np at the surface. The DLS shows the size distribution of the biotinylated-pegylated nanoparticles. Basu et al. 3of6
4 48 hours 2 1 [1μM] -NP [1μM] [1μM] -NP [1 μm] -NP [5 μm] [1μM] -NP [1μM] [1μM] -NP [1μM] B16/F1 24 hours 72 hours # [1μM] -NP [1μM Fig. S2. Effect of 9859-loaded nanopaticles on B16/F1,, and LLC cell proliferation. The cells were incubated with free 9859 (), nanoparticle (-NP), or vehicle (control), for 24, 48, or 72 h. MTS assays was used to determine the temporal cytotoxicity of increasing concentrations of free 9859 and 9859-nanoparticles (NP). Data are expressed as % of vehicle-treated control (considered as 1%), and represent mean SEM (n 3)., P.5 vs. vehicle control (ANOVA followed by Dunnet s post hoc test). The 24- and 72-h data for B16/F1 and cells are shown in the main text. LLC Basu et al. 4of6
5 B16-F1 MDA-231 Vehicle NP ±SEM 985±SEM NP-±SEM UL.22±.3.22±.14.25±.3 UR.21±.3.9±.1.14±.3 LL 98.21± ± ±.9 LR 1.36±.22.98± ±.12 B16-F1 ±SEM 985±SEM NP-±SEM UL.2±.1 1.2±.26.2±.1 UR.16± ± ±2.26 LL 72.45± ± ±1.78 LR 27.36± ± ±2.56 Fig. S3. Representative plots following FACS analysis of apoptosis in and B16/F1 cell lines. Cancer cells were incubated with the nanoparticle or free drug for 48 h of incubation. The cells were harvested and stained with AnnexinV-Alexa Fluor 488 and counterstained with propidium iodide. The cells were analyzed using a Becton Dickinson FACSCalibur flow cytometer (excitation 488 and 585 nm, respectively). AnnexinV-Alexa Fluor 488, propidium iodide, or both were omitted for the negative controls. The table shows the mean SE from n 3 independent experiments, where each quadrant represents the percentage of cells in early apoptosis (Lower right, LR), late apoptosis (Upper right, UR), necrosis (Upper left, UL), and healthy cells (Lower left, LL). Basu et al. 5of6
6 (A) B16/F1 phosphoerk Total ERK PiERK2/ERK B16-F1 -NP PiERK1/Total ERK (B) -NP B16-F1 -NP B16/F1 3 min 15 min -NP phosphoerk Total ERK PiERK1/Total ERK NP PiERK2/ERK NP 24 hours 12 hours 2 hours Fig. S4. Mechanisms underlying the effect of the 9859-nanoparticle in vitro. (A) Expression and phosphorylation status of ERK1/2 in B16/F1 and MDA-MB231 cells. Representative Western blots show the levels of phospho-erk normalized to total ERK levels in cells treated with 9859 (), 9859-nanoparticles (-NP) or vehicle control (con). The graphs represent densitometric data expressed as mean SEM from 3 independent experiments. (B) Epifluorescence imaging of tumor cells for monitoring internalization of nanoparticles. B16/F1 melanoma and breast-cancer cells were incubated with FITC-labeled nanoparticles at different time points (15 min, 3 min, 2 h, 12 h, and 24 h). Lysosomal compartments of live cells were stained with red LysoTracker probes. Merged images (yellow) indicate that the FITC-nanoparticles have been internalized into the lysosomes. Basu et al. 6of6
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