SUPPORTING INFORMATION. Sonochemically Produced Polydopamine Nanocapsules with Selective Antimicrobial Activity
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1 SUPPORTING INFORMATION Sonochemically Produced Polydopamine Nanocapsules with Selective Antimicrobial Activity Gil Yeroslavsky, Michal Richman, Li-or Dawidowicz and Shai Rahimipour Department of Chemistry, Bar-Ilan University, Ramat-Gan 52900, Israel. Fax: ; rahimis@biu.ac.il S1
2 EXPERIMENTAL SECTION All chemicals and reagents were of analytical grade. Unless otherwise stated, all chemicals were obtained from Sigma-Aldrich (Rehovot, Israel) and used as received. Synthesis of fluorescent probes. Fluorescent probes were synthesized by solid-phase peptide synthesis, employing the common Fmoc strategy and using the Rink Amide 4- methylbenzhydrylamine (MBHA) resin. Coupling was carried out in N-methyl-2- pyrrolidone (NMP) using 2-(1H-benzotriazol-1-yl)-1,1,3,3-tetramethyluronium hexafluorophosphate (HBTU) as the coupling agent. Following attachment of either Fmoc-Cys(Trt)-OH or Fmoc-Ala-OH to the resin and their coupling to O-[2-(Fmocamino)-ethyl]-O -[2-(diglycolyl-amino)ethyl]ethylene glycol, the terminal Fmoc groups were removed by 30% piperidine in dimethylformamide (DMF) and the resins were washed with DMF. The N-terminals of the anchored compounds were then reacted with 4-nitrobenzo-1,2,5-oxadiazole (NBD) as a fluorescent probe in a mixture of DMF and N,N-diisopropylethylamine (DIPEA). Fluorescent probes 1 (bearing a Cys residue) and 2 (bearing an Ala residue) were cleaved from the resin using a 95:2.5:2.5 mixture of trifluoroacetic acid (TFA), triisopropylsilane, and H 2 O, and purified to homogeneity by RP-HPLC. The pure probes were analysed using MALDI-TOF/TOF, or ESI mass spectrometry. Preparation of PDA capsules. PDA capsules were prepared sonochemically as described previously. 1, 2 In brief, a solution of DA hydrochloride ( mg) in Tris buffer (30 ml, 100 mm, ph 8.5) was overlayered with either canola oil or n-dodecane. The tip of a high intensity ultrasonic probe was then placed at the aqueous organic interface and the mixture was irradiated at an acoustic power of 150 W cm -2 (20 khz) for 12 min while being cooled in an ice-water bath. Under these conditions, a very thin layer of PDA capsules was generated as a black suspension between the organic phase and the aqueous solution. PDA capsules were also prepared from solutions of DA hydrochloride (10 mg) containing 0.5 or 3.3 mg ml -1 CuSO 4. This approach reduced the irradiation time required for capsule formation to 6 min. After overnight refrigeration, the mixture was centrifuged (1000 rpm) for 10 min and the gray-black phase was separated and washed twice with H 2 O. PDA-capsules generated either in the absence or presence of Cu(II) were also loaded with Nile red (as a fluorescent model for non-aqueous soluble compounds) by dissolving the dye (5 mg) directly in n-dodecane or canola oil (20 ml). PDA-nanocapsules were produced by precipitating the PDA capsules prepared in the presence or absence of Cu(II) with increasing concentrations of acetone (50 100%). Surface modification of PDA-nanocapsules (50 µl) was achieved by agitating them overnight in a solution of fluorescent probe 1 (0.5 ml, 2 mg ml -1 ) in Tris buffer (100 mm, ph 8). Nanocapsules incubated with probe 2 and Tris buffer (100 mm, ph 8) were S2
3 used as controls. The particles were washed four times with H 2 O and resuspended in PBS prior to FACS analysis. Characterization of PDA capsules. The shape and morphology of the PDA capsules were characterized by optical-fluorescence microscopy (Apo-Tome AxioImager.z1 microscope, Zeiss, Germany), scanning electron microscopy (SEM, FEI Quanta 200 FEG, Hillsboro, Oregon), high-resolution transmission electron microscopy (HR TEM; JEM 2100, JEOL, Japan), Raman spectroscopy (Micro Raman Spectroscopy System. Renishaw Invia Spectrometer system, UK) and confocal microscopy (Leica-SPE microscope, Mannheim, Germany). For the SEM analysis, a sample (5 μl) of the PDA capsules was spotted onto a stainless steel grid, followed by drying and carbon sputtering. The samples were then analyzed by SEM operated at 3 kv. For HR-TEM analyses, samples were loaded on gold grids and dried for 20 minutes. Samples were the analysed at 200 kv. The size of the nanocapsules were determined by a Malvern Zetasizer Nano ZS dynamic light scattering (DLS) system (Malvern, UK). X-ray photoelectron spectroscopy (XPS) and inductively coupled plasma (ICP) analyses were carried out with a Kratos AXIS-HS spectrometer (Manchester, UK) and ULTIMA2 (Horiba Scientific, Edison, NJ), respectively, while thermogravimetric analysis (TGA) was performed with a Q500 (TA instruments, US) analyzer. Cell cultures and conditions. PC12 cells were routinely maintained in low-glucose Dulbecco's modified Eagle's medium (DMEM) supplemented with horse serum (10%) and fetal bovine serum (FBS; 5%), L-glutamine (2 mm), penicillin (100 U ml -1 ), and streptomycin (100 mg ml -1 ) in a 5% CO 2 atmosphere at 37ºC. NIH/3T3 cells were maintain in similar conditions, however the medium contained regular DMEM supplemented with 10% FBS. To determine the toxicity of the capsules, cells (10,000 and 20,000 cells well -1 for PC12 and NIH/3T3, respectively) were plated in 96-well tissueculture plates in the medium (100 µl) and incubated overnight to allow attachment. The medium was then replaced with 100 µl of fresh medium containing various amounts (5 40 µl, 12.5 mg ml -1 ) of acetone-precipitated PDA nanoparticles generated in the absence or presence of CuSO 4 (0.5 and 3.3 mg ml -1 ) and the incubation was continued at 37ºC for an additional 24 h. Cell survival was then determined by the 3-(4,5- dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide (MTT) assay as described. 1 Antimicrobial activity. A suspension of gram-positive Staphylococcus aureus (10 µl, strain 1313, hospital-grade) and Streptococcus mutans (10 µl, strain, ), and gramnegative E. coli (10 µl, strain C600), and Pseudomonas aeruginosa (10 µl, strain PAO1) in lysogeny broth (LB) containing 30% glycerol were added to 5 ml of LB in a sterile 15 ml tube. The suspensions were then incubated at 37 C with shaking at 200 rpm for 16 h. After centrifugation (2700 rpm, 10 min), the cells were washed with PBS (ph 7.4) and resuspended at a concentration of cells ml -1 in PBS. The cell suspension (0.8 ml) was then incubated for various time periods with PDA capsules (50 µl; 12.5 mg S3
4 ml -1 ) prepared in the absence or presence of Cu(II) (0.5 or 3.3 mg ml -1 ) and the volume was completed to 1 ml with sterile PBS. Serial dilutions of Lysostaphin (1.62 µg ml -1 ; 10 µl), Penicillin (10,000 units ml -1 ) and Streptomycin (10 mg ml -1 ) were used as the positive controls. Similar bacterial solutions without the capsules served as a negative control. After incubation and shaking at 37ºC, 10 µl of each sample was serially diluted in 10 fold steps in PBS and then 50 µl aliquots of the diluted solutions were spread evenly on growth agar plates (1.5% agar in LB broth) for colony counting. Plates were incubated at 37ºC overnight, photographed, and the numbers of colonies were determined manually or digitally using ImageJ software. Experiments were conducted in triplicates and repeated twice. The antibacterial activity of PDA capsules was also determined microscopically using the live/dead fluorescent assay (BacLight, Molecular Probes) following the manufacture s protocol. S4
5 Scheme S1. A possible mechanism for dopamine oxidation to reactive polydopamine and its interaction with Cu(II). 3 S5
6 Fig. S1. Physico-chemical properties of the PDA nanocapsules prepared from 6 min irradiation of DA (0.3 mg ml -1 ) and CuSO 4 (0.84 mg ml -1 ). (a) HR-TEM image of acetone-precipitated PDA nanocapsule showing the thickness of about 5 nm and the crystallinity of the particles. (b) Corresponding EDS analysis of PDA nanocapsules demonstrating the presence of C, N, O and Cu elements in PDA nanocapsules. (c) XRD analysis of the PDA nanocapsules showing crystallinity. The XRD peak at 2θ = 23.4º may correspond to the d-spacing of about 3.87 Å that is consistent with π π interactions between oligomeric PDA subunits and other -stacked structures. 4 S6
7 Fig. S2. Size distribution analysis of (a) acetone precipitated PDA nanocapsules and (b) acetone precipitated PDA nanocapsules prepared in the presence of 3.3 mg ml -1 of CuSO 4 as recorded by DLS. S7
8 Fig. S3. Effect of sonication time, DA concentration and sonication energy on physical properties of the PDA capsules. (a) Increasing amounts of DA ( mg ml -1 ) were sonochemically irradiated in the presence of CuSO 4 (3 eq.) for different periods and the size of the capsules was determined by DLS. (b) PDA nanocapsules were also prepared from 6 min. irradiation of DA (0.3 mg ml -1 ) using different sonication energy and the size of the capsules were determined by DLS. (c) Representative HR-TEM image of PDA nanocapsules prepared from 6 min. irradiation of DA (3.3 mg ml -1 ) and CuSO 4 (8.4 mg ml -1 ) showing shell thickness of 12.2 nm. (d) DLS analysis of PDA capsules prepared from DA (0.3 mg ml -1 ) and CuSO 4 (0.84 mg ml -1 ), and irradiated for 6 (blue line), 12 (red line) and 30 min (green line). S8
9 Fig. S4. Linear correlation between different concentrations of CuSO 4 used for the sonochemical preparation of the PDA nanocapsules and the Cu content of the corresponding particles as analyzed by ICP. S9
10 Fig. S5. (a) UV-vis spectrum of PDA nanocapsules prepared in the absence (gray dotted line) or presence of 0.5 mg ml -1 CuSO 4 (black line). The UV-vis spectroscopy shows a wide peak at around 365 nm, consistent with the absorbance peak observed for PDA film produced in the presence of Cu(II). 5 (b) Raman spectra of PDA nanocapsules prepared in the absence (red line) or presence of 0.5 mg ml -1 CuSO 4 (black line). Raman peaks at 1390 and 1580 cm -1 corresponding to the stretching and deformation of the catechols in PDA (red line) are shifted to the lower wavenumbers upon complexation with Cu ions (black line). Peaks at wavenumber <630 cm -1 can most probably be assigned as Cu-O and Cu-N bonds. Furthermore, the decrease in intensity of the peak at by Cu(II) demonstrates that the NH group of PDA slightly shared in the coordination. (c) Cyclic voltammograms of PDA nanocapsules prepared in the presence or absence of CuSO 4. Measurements were carried out in phosphate buffered solution (100 mm, ph 7.4). The voltammogram of PDA shows a quasi-reversible electron transfer step at V (vs. Ag/AgCl), which most likely represents a two-electron, two-proton process oxidation to form the corresponding reactive ortho-quinone derivative. (d) Addition of CuSO 4 to the solution of PDA nanocapsules caused to gradual decrease of the CV peak at V, suggesting that the chelation of Cu ion by PDA is mediated through the catecholic hydroxyls. S10
11 Figure S6. Effect of PDA nanocapsules prepared in the absence (a) or presence (3.3 mg ml -1 ; b) of CuSO 4 on the cell viability of PC12 cells. The percent survival results are shown as the mean ± SD performed in quadruplicate. References: 1 M. Richman, S. Wilk, N. Skirtenko, A. Perelman and S. Rahimipour, Chem. Eur. J., 2011, 17, N. Skirtenko, M. Richman, Y. Nitzan, A. Gedanken and S. Rahimipour, Chem. Commun., 2011, 47, H. Lee, S. M. Dellatore, W. M. Miller and P. B. Messersmith, Science, 2007, 318, 426; B. Szpoganicz, S. Gidanian, P. Kong and P. Farmer, J. Inorg. Biochem., 2002, 89, D. R. Dreyer, D. J. Miller, B. D. Freeman, D. R. Paul and C. W. Bielawski, Langmuir, 2012, 28, 6428; X. Yang, J. Li, X. H. Zhao, H. W. Wang and Y. K. Shan, Acta. Crystallogr. C., 2007, 63, m171; Z. L. Chen, Y. Z. Zhang and F. P. Liang, Acta. Crystallogr. C., 2006, 62, m48. 5 F. Bernsmann, V. Ball, F. Addiego, A. Ponche, M. Michel, J. J. Gracio, V. Toniazzo and D. Ruch, Langmuir, S11
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