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1 SUPPLEMENTARY INFORMATION DOI: /NNANO Protein-Inorganic Hybrid Nanoflowers Jun Ge, Jiandu Lei, and Richard N. Zare Supporting Online Material Materials Proteins including albumin from bovine serum (BSA) (lyophilized powder), α-lactalbumin from bovine milk, laccase from Trametes versicolor, carbonic anhydrase from bovine erythrocytes, and lipase from Candida antarctica were purchased from Sigma-Aldrich. Chemicals including copper(ii) sulfate pentahydrate, syringaldazine, p-nitrophenyl butyrate, ethylenediaminetetraacetic acid, glutaraldehyde (25% in H 2 O), ( )-epinephrine, ( )-norepinephrine, dopamine hydrochloride, phenol, m-cresol, and 2,4-dichlorophenol at the highest purity were purchased from Sigma-Aldrich. Phosphate buffered saline (PBS, 1X, ph 7.4) is from Invitrogen. Synthesis and characterization of the protein-incorporated inorganic hybrid nanoflowers In a typical experiment, 20 μl of aqueous CuSO 4 solution (120 mm) in molecular biology grade water were added to 3 ml of PBS (ph 7.4) containing proteins with different concentrations, followed by incubation at 25 o C for 3 days. For SEM, the suspension of the prepared nanoflower was filtered and dried on a membrane (pore size: 0.1 μm) and sputter coated with gold. For TEM, a drop of the suspension of the prepared nanoflower was added to a carbon grid and dried at room temperature. For XRD analysis, 20 mg of BSA was dissolved in 200 ml of PBS (ph 7.4), followed by addition of 1.33 ml of aqueous CuSO 4 solution followed by incubation at 25 o C for 3 days. The nanoflower precipitate was collected, washed with deionized water, and dried at 80 o C before XRD measurement. The protein concentration in the supernatant was measured by the Branford protein assay (Bio-Rad, Catalog. No ) using BSA as a standard. This measurement allowed us to find the encapsulation yield of protein. For determination of the weight percentage of protein in nanoflowers, the nanoflower precipitate was centrifuged, collected, and dried under vacuum. The weight percentage of protein in nanoflowers was calculated based on the encapsulation yield and the weight of the powder. For the nanoflowers made from using 0.5 mg/ml (NF-1), 0.1 mg/ml (NF-2), 0.02 mg/ml (NF-3) BSA in solution, the encapsulation yield of BSA is ~12%, ~78%, and ~82%, respectively. The weight percentage of BSA in the nanoflowers is calculated to be ~14%, ~9%, and ~7%. The precipitate formed from adding CuSO 4 to PBS under the same conditions in the absence of BSA was prepared as a control. XRD patterns of the particles with BSA (Fig. S1A) and without BSA (Fig. S1B) fit well with the crystal pattern from Cu 3 (PO 4 ) 2 3H 2 O (JPSCD ). In both cases, some NaCl crystals NATURE NANOTECHNOLOGY 1
2 (JPSCD ) were also found in the products originating from PBS. Figure S2 presents the SEM image of the crystals obtained by adding aqueous CuSO 4 solution to PBS in absence of protein. 2
3 3
4 Fig. S1. XRD patterns of particles: (A) nanoflowers obtained with BSA and (B) particles of crystals obtained without BSA. (C) Comparison between peaks from the nanoflowers (top), the Cu 3 (PO 4 ) 2 3H 2 O (JPSCD ) (middle), and NaCl crystals (JPSCD ) (bottom). Fig. S2. SEM image of the crystals obtained by adding aqueous CuSO 4 to PBS in the absence of protein. The protein-incorporated Cu 3 (PO 4 ) 2 3H 2 O nanoflowers that are treated with glutaraldehyde (0.8 wt%) in solution for 48 hours, followed by incubation with EDTA (1 wt%). For calcination, the suspension of protein-incorporated nanoflowers was dried on silica and heated at 350 o C for 2 hours. For trypsin digestion, the suspension of protein-incorporated nanoflowers was incubated with 25 μg/ml of trypsin. Figure S3 shows the SEM images of the BSA-incorporated nanoflowers before and after treatment. 4
5 Fig. S3. SEM images of BSA-incorporated nanoflower NF-2 (A, C, E) without treatment and with treatment by (B) glutaraldehyde-edta, (D) calcination, and (F) trypsin, respectively. The images of the untreated nanoflowers (A, C, E) were obtained from the sample of BSA nanoflower NF-2. The images of the treated nanoflowers (B, D, F) were obtained at low magnification from the same samples shown in Figure 2e-g. 5
6 Fig. S4. SEM image of solid precipitates formed from the solution containing 0.1 mg/ml BSA, 10 mm HPO 4 2-, 2 mm H 2 PO 4 -, and 0.8 mm Cu 2+. Fig. S5. Crystal structures of (A) α-lactalbumin (PDB: 1A4V), (B) laccase (PDB: 1GYC), (C) carbonic anhydrase (PDB: 1V9E), and (D) lipase (PDB: 2VEO) with the solvent accessible surface area of N-atoms in the protein structures marked in blue. Characterization of the catalytic performance of the laccase-incorporated inorganic hybrid nanoflowers Laccase-incorporated nanoflowers were prepared by the same approach at a protein concentration of 0.1 mg/ml. The encapsulation yield and weight percentage of laccase in the nanoflower was determined to be 64% and 9%. For the detection of catecholamines in urine and phenols in water, laccase needs to work at conditions near neutral ph (physiological liquid and environmental water). The activity of laccase was measured in 40 μm syringaldazine in PBS buffer (ph 7.4) at 25 C, in which one unit is the active amount allowing 1.0 μmol substrate to be oxidized per minute. The activity was measured by determining the absorbance of the product at 530 nm. The activity of laccase-incorporated Cu 3 (PO 4 ) 2 3H 2 O nanoflowers is measured to exhibit ~650% increase compared to free laccase. As a control experiment, the activity of free laccase in the presence of Cu 2+ without immobilization was measured by introducing 0.8 mm 6
7 Cu 2+ in the enzyme solution and immediately detecting its activity toward oxidation of syringaldazine. The activity was measured to be 2.3 times higher than that of free laccase in the absence of Cu 2+. Epinephrine, dopamine, or norepinephrine, each at 50 μg/ml, is dissolved in 1 mm HCl solution. Oxidation of epinephrine, dopamine, and norepinephrine by laccase or laccase nanoflower in phosphate buffer (0.1 M, ph 6.5) was monitored by absorption at 485 nm. Oxidative coupling reactions between phenols and 4-aminoantipyrine catalyzed by laccase or laccase-incorporated nanoflower in phosphate buffer (0.1 M, ph 6.5) were monitored by absorption at 495 nm. Fig. S6. Kinetics of the oxidation of epinephrine by free laccase and laccase-incorporated nanoflowers (Free: free laccase, Nano: laccase nanoflowers). Fig. S7. The fluorescence intensity of the oxidized product of epinephrine at different concentrations (Ex. 375 nm, Em. 506 nm, enzyme concentration 50 μg/ml, fluorescent intensity measured 10 min after adding enzyme to the solution of epinephrine). To test the recycling of the laccase nanoflowers, epinephrine (30 μg/ml) was added to 3 ml of suspension of laccase nanoflower (~60 μg/ml enzyme) in phosphate buffer (ph 6.5), followed by reaction at 25 o C for 20 min. Then, the suspension was immediately centrifuged at 7000 rpm for 2 min, followed by measuring the absorption of the supernatant at 485 nm. The precipitate was washed with phosphate buffer and centrifuged again. The precipitate was then subjected to the next catalytic cycle. The absorption of the supernatant at 485 nm for the first measurement was set as 100%. 7
8 Fig. S8. Repeated use of the same laccase nanoflowers for detecting epinephrine. The relative activity of laccase nanoflowers toward epinephrine was determined after each cycle. Fig. S9 Kinetics of the oxidation coupling of phenol by free laccase and laccase-incorporated nanoflowers (Free: free laccase, Nano: laccase nanoflowers). Fig. S10. Kinetics of the oxidation coupling of m-cresol by free laccase and laccase-incorporated nanoflowers (Free: free laccase, Nano: laccase nanoflowers). 8
9 Fig. S11. Kinetics of the oxidation coupling of 2,4-dichlorophenol by free laccase and laccase-incorporated nanoflowers (Free: free laccase, Nano: laccase nanoflowers). Fig. S12. Visible detection of 2,4-dichlorophenol by laccase nanoflowers in solution. Bottles from left to right containing 27.6, 13.8, 6.9, 1.4, and 0.28 μg/ml of 2,4-dichlorophenol. By varying the substrate (syringaldazine) concentration, laccase nanoflowers were measured to exhibit non-michaelis-menten kinetics for enzymatic activity. Fig. S13. Non-Michaelis-Menten kinetics for the measurement of the activity of laccase nanoflowers. Characterization of the catalytic performance of the carbonic anhydrase-incorporated and lipase-incorporated inorganic hybrid nanoflowers Carbonic anhydrase-incorporated and lipase-incorporated nanoflowers were prepared by the same approach at a protein concentration of 0.5 mg/ml and 0.02 mg/ml respectively. The 9
10 encapsulation yield of carbonic anhydrase in the nanoflower was determined to be 10% and 50% respectively. The activity of carbonic anhydrase was measured in terms of Wilbur-Anderson Units (1). The activity of free carbonic anhydrase was determined to be ~1100 units/mg, whereas after encapsulation in nanoflowers the activity of carbonic anhydrase was ~2880 units/mg. The activity of lipase was measured by hydrolysis of p-nitrophenyl butyrate (pnpb). In a typical experiment, acetonitrile solution of pnpb was added to PBS solution containing lipase to reach a final pnpb concentration of 5 mm (containing 5% v/v acetonitrile in the final solution), followed by measuring the absorption of the solution at 348 nm at 25 o C. The activity of free lipase and lipase nanoflowers was calculated to be ~45 U/mg, and ~43 U/mg, respectively. References (1) Wilbur, K.M. and Anderson, N.G. (1948) Journal of Biological Chemistry176,
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