Electronic Supplementary Information. N and B Co-Doped Graphene: A Strong Candidate to. Replace Natural Peroxidase in Sensitive and Selective
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1 Electronic Supplementary Information N and B Co-Doped Graphene: A Strong Candidate to Replace Natural Peroxidase in Sensitive and Selective Bioassays Min Su Kim,, # Seongyeon Cho,, # Se Hun Joo,, # Junsang Lee, Sang Kyu Kwak,,* Moon Il Kim,, * Jinwoo Lee, * Department of Chemical Engineering, Pohang University of Science and Technology (POSTECH), Pohang, Gyeongbuk 37673, Republic of Korea Department of BioNano Technology, Gachon University, Seongnam, Gyeonggi 13120, Republic of Korea Department of Energy Engineering, School of Energy and Chemical Engineering, Ulsan National Institute of Science and Technology (UNIST), Ulsan 44919, Republic of Korea Department of Chemical and Biomolecular Engineering, Korea Advanced Institute of Science and Technology (KAIST), Daejeon 34141, Republic of Korea # These authors contributed equally to this work. *Corresponding author. S1
2 Tel: ; Fax: ; Tel: ; Fax: ; Tel: ; Fax: ; S2
3 EXPERIMENTAL SECTION Materials Graphite (SP-II graphite) was purchased from Bay Carbon. Concentrated sulfuric acid (H2SO4), concentrated phosphoric acid (H3PO4), potassium permanganate (KMnO4), concentrated hydrochloric acid (HCl), ethanol, ether, melamine, boric acid, dibenzyl disulfide, triphenylphosphine, sodium acetate, choline oxidase from Arthrobacter globiformis (ChOx), choline chloride, acetylcholine esterase from Electrophorus electricus (AChE), acetylcholine (ACh + ), horseradish peroxidase (HRP), 3,3,5,5 -Tetramethylbenzidine (TMB), human serum, 1-ethyl-3-[3-dimethylaminopropyl]carbodiimide (EDC), N-hydroxysulfo-succinimide (sulfo- NHS), and bovine serum albumin (BSA) were all purchased from Sigma-Aldrich (Milwaukee, WI), and 35% hydrogen peroxide (H2O2) solution was obtained from Junsei Chemical Co. (Japan). C-reactive protein (CRP) and its antibody were purchased from Santa Cruz Biotechnology (CA, USA). Amplex UltraRed Reagent (AUR) was acquired from Life Technologies. All other chemicals were of analytical grade and used without further purification. Aqueous solutions were prepared with double-distilled (DI) water purified by a Milli-Q Purification System (Millipore). Characterization Structures of synthetic materials were examined using TEM with a JEOL JEM-2010 microscope, HR-TEM with a JEOL JEM-2200FS (with Image Cs-corrector), and AFM with a INNOVA-LABRAM HR800 (Bruker). FTIR was measured using Nicolet (Thermo Fisher Scientific Instrument). X-ray photoelectron spectroscopy was performed on a VG SCIENTIFIC ESCALAB 250 (KRATOS NOVA). A Zetasizer (Malvern) was used for the zeta potential measurements. Spectrophotometry was conducted using a DU-800 UV-visible S3
4 spectrophotometer (Beckman). Raman spectra were measured using LabRam Aramis with a 514-nm Ar laser. Kinetic analysis Steady-state kinetic assays were performed at RT in a 1.5-mL tube using free rgo, N-rGO, B-rGO, BN-rGO, NB-rGO, and h-bn-rgo in 1 ml sodium acetate buffer (0.1 M, ph 4.0). For TMB, 100 mm H2O2 was added in 1 ml reaction buffer at diverse TMB concentrations. For H2O2, 500 μm TMB was added in 1 ml reaction buffer at diverse H2O2 concentrations. All reactions progresses were monitored by measuring the absorbance changes in a kinetic mode at 652 nm for 1 min. The kinetic parameters were determined using the equation ν = Vmax [S]/(Km + [S]), where ν is the initial velocity, Vmax is the maximal velocity, [S] is the concentration of the substrate, and Km is the Michaelis constant. The catalytic constant kcat was derived from kcat = Vmax/[E], where [E] is the molar concentration of the rgo-based nanozymes, which was calculated by from TEM images, assuming that each nanozyme is a disc with a radius of 100 nm and a width of 1 nm. Stability measurement Stabilities of NB-rGO and HRP were determined in aqueous buffer (0.1 M sodium acetate, ph 4.0) under non-shaking incubation conditions at RT T 90 and 2 ph 9. After NBrGO and HRP were exposed to combinations of T and ph for 2 h, their residual activities were measured using the typical colorimetric assays described above. Relative activities were calculated from the ratio of residual activity to the original activity before incubation. Preparation of CRP antibody-conjugated NB-rGO NB-rGO (10 mg) was first washed twice with MES buffer (0.1 M, ph 6.0) and resuspended in the same buffer (10 ml), then EDC (90 mm) and sulfo-nhs (5 mm) were added. The mixture was further incubated at 25 o C for 30 min under shaking with sonication at every 10 S4
5 min, to have labile intermediated on the surface of NB-rGO. The unreacted components were removed three-time washing with PBS. The activated NB-rGO (1 mg) was incubated in 1 ml PBS solution contaning CRP antibody (100 µg/ml). Antibodies were allowed to conjugate for 2 h at RT, then further incubated overnight at 4 to make sure that reaction had occurred between antibodies and NB-rGO. To cap the unreacted sulfo-nhs functionality, the NB-rGO was incubated in Tris-HCl buffer (0.1 M, ph 7.4) for 1 h at RT under shaking (250 rpm). Finally, the CRP antibody-conjugated NB-rGO was harshly washed with PBS buffer three times, the incubated in a buffer containing 1% BSA for 1 h at RT to prevent nonspecific binding. The final product (1 mg/ml) was resuspended in PBS containing 1% BSA and stored at 4 until use. Colorimetric immunoassay to detect CRP Capture antibody (100 μl at 0 μg/ml in PBS buffer) was first allowed to bind to a transparent 96-well plate (Nunc, Thermo Fisher Scientific, MA, USA) overnight at 4. The plates were washed with excessive PBS solution, the 3% BSA solution was applied to the wells and incubated for 2 h at 37 to block antibody-free sites. The plates were washed twice with PBS containing 0.05% tween20 (PBST), then 100 μl of samples containing different concentrations of CRP were added to the antibody-coated wells and incubated for 2 h at 37. The plates were washed several times with PBST and incubated with 100 μl of antibody-conjugated NBrGO (final 0.5 mg/ml) for 2 h at 37 to induce the specific antigen-antibody interaction. The unbound NB-rGO was removed by washing with excess PBS solution, then 100 μl of reaction mixture containing 0.5 mm TMB with 200 mm H2O2 was added to each well to allow development of a color signal. After 3 min, the reaction was stopped by transferring the supernatant solution to the designated well of another 96-well plate. Spectrophotometric measurements were performed using the microplate reader described above. S5
6 In experiments that used HRP-based ELISA to detect CRP, a monoclonal antibody against CRP from mouse (0.05 mg ml -1 ) and HRP-conjugated secondary antibody against mouse IgG (0.5 mg ml -1 ) were used sequentially, instead of CRP antibody-conjugated NB-rGO, and reaction mixture containing 2 mm H2O2 was used instead of 200 mm H2O2. The other procedures were the same as those used for the immunoassay using the NB-rGO. S6
7 Figure S1. Schematic diagram of synthesis of N-rGO, B-rGO, NB-rGO, BN-rGO, and h-bnrgo. Figure S2. TEM images of (a) GO, (b) rgo, (c) B-rGO, (d) N-rGO, (e) BN-rGO, and (f) NBrGO. S7
8 Figure S3. AFM images of (a) rgo, (b) N-rGO and (c) NB-rGO. Figure S4. FTIR spectra of rgo, N-rGO and NB-rGO S8
9 Table S1. Calculated atomic concentrations of atoms in various B or N doped graphene. At% N B O C rgo N-rGO B-rGO NB-rGO h-bn-rgo Figure S5. Survey and high-resolution XPS spectra of (a) N-rGO, (b) B-rGO, and (c) BN-rGO. S9
10 Figure S6. XPS survey spectra of various B or N doped graphene. Figure S7. Raman spectra of h-bn-rgo and NB-rGO. S10
11 Figure S8. Zeta potential values of rgo, N-rGO, NB-rGO and B-rGO S11
12 Table S2. Relative atomic percentages of various functional groups in NB-rGO. Fitting of C1s (relative atomic percentage/%) C-C C-O C=O O-C=O NB-rGO Figure S9. Schematic diagram of synthesis of doped graphene sets. S12
13 Figure S10. (a, b) Photographs (top) of color-generating reaction of TMB (left) and ABTS (right) in the presence of H2O2, and (bottom) their corresponding absorption spectra. Figure S11. Effect of (a) ph with several buffers, (b) H2O2 concentration, and (c) temperature on the catalytic activity for TMB oxidation by NB-rGO. Bars: ± 1 s.d., n = 3. S13
14 Figure S12. Catalytic stabilities of NB-rGO and HRP against (a) temperature and (b) ph. NBrGO and HRP were incubated at given temperature or ph for 2 h and their residual activity relative to the initial activity were measured under standard conditions. Bars: ± 1 s.d., n = 3. S14
15 Figure S13. Steady-state kinetic assays of (a) rgo, (b) B-rGO, (c) N-rGO, (d) h-bn-rgo, (e) BN-rGO, and (f) NB-rGO for TMB and H2O2, and their corresponding double reciprocal (Lineweaver-Burk) plots of activity. y-axis values are obtained from the absorbance at 652 nm. Bars: ± 1 s.d., n = 3. S15
16 Table S3. Comparison of the kinetic parameters of rgo sets and various catalysts. [E] represents the concentration of catalysts, Km is the Michaelis-Menten constant, Vmax is the maximal reaction velocity, and kcat is turnover number. Sample Single particle volume (nm 3 ) [E] (M) Substrate K m (mm) V max (μm s -1 ) k cat (s -1 ) Ref rgo sheets π TMB H 2O N-rGO sheets π TMB H 2O B-rGO sheets h-bnrgo sheets π π TMB H 2O TMB H 2O This work BNrGO sheets π TMB H 2O NBrGO sheets π TMB H 2O HRP TMB H 2O S1 Fe 3O 4 particles 4/3 π TMB H 2O S1 Co 3O 4 cubes TMB H 2O S2 Pt particles 4/3 π TMB H 2O S3 S16
17 Figure S14. (a) Undoped graphene model (rgo). (b) B doped graphene model (B-rGO). (c) quaternary N doped graphene model (N(q)-rGO). (d) pyridinic N doped graphene model (N(p)- rgo). (e) N, B co-doped graphene model (NB-rGO). Gray: carbon; white: hydrogen; red: oxygen; pink: boron; blue: nitrogen. S17
18 Figure S15. Gibbs free energy diagram of peroxidase reaction for several potential active sites (i.e., one edge site and four basal plane sites) in (a) rgo, (b) B-rGO, (c) N(q)-rGO, (d) N(p)- rgo, (e) NB-rGO. Asterisk: adsorbed state of the reaction intermediate; red star: active site for peroxidase reaction. S18
19 Figure S16. Optimized structures of reaction intermediates adsorbed on potential active sites of the rgo. Gray: carbon; white: hydrogen; red: oxygen; pink: boron; blue: nitrogen. S19
20 Figure S17. Optimized structures of reaction intermediates adsorbed on potential active sites of the B-rGO. Gray: carbon; white: hydrogen; red: oxygen; pink: boron; blue: nitrogen. S20
21 Figure S18. Optimized structures of reaction intermediates adsorbed on potential active sites of the N(q)-rGO. Gray: carbon; white: hydrogen; red: oxygen; pink: boron; blue: nitrogen. S21
22 Figure S19. Optimized structures of reaction intermediates adsorbed on potential active sites of the N(p)-rGO. Gray: carbon; white: hydrogen; red: oxygen; pink: boron; blue: nitrogen. S22
23 Figure S20. Optimized structures of reaction intermediates adsorbed on potential active sites of the NB-rGO. Gray: carbon; white: hydrogen; red: oxygen; pink: boron; blue: nitrogen. S23
24 Figure S21. Effect of ph on the catalytic activity for AUR oxidation by NB-rGO. S24
25 Figure S22. Dose-response curve for H2O2 detection by NB-rGO and its corresponding linear calibration plot. Bars: ± 1.s.d., n = 3. S25
26 Figure S23. Fluorescence intensities of NB-rGO-based assay to specifically detect ACh +. The employed concentration of ACh + is 100 μm, while those for negative control samples are all 1 mm. Bars: ± 1.s.d., n = 3. S26
27 Figure S24. Dose-response curve for choline detection by (a, b) HRP and (c, d) Pt NPs and their corresponding linear calibration plots. Bars: ± 1.s.d., n = 3. S27
28 Table S4. Detection precision of the NB-rGO-based assay system for the determination ACh + in real serum samples. S28
29 Figure S25. Comparison of the initial activities of NB-rGO and NB-rGO conjugated with CRP antibody (Ab-NB-rGO). Bars: ± 1.s.d., n = 3. Figure S26. Absorption intensities (left) of the blue color and their corresponding well plate images (right) to quantify [CRP] by using NB-rGO or HRP. Bars: ± 1.s.d., n = 3. S29
30 References S1. Gao, L.; Zhuang, J.; Nie, L.; Zhang, J.; Zhang, Y.; Gu, N.; Wang, T.; Feng, J.; Yang, D.; Perrett, S.; Yan, X. Intrinsic Peroxidase-Like Activity of Ferromagnetic Nanoparticles. Nat. Nanotechnol. 2007, 2, S2. Mu, J.; Wang, Y.; Zhao, M.; Zhang, L. Intrinsic Peroxidase-Like Activity and Catalase- Like Activity of Co3O4 Nanoparticles. Chem. Commun. 2012, 48, S3. Gao, Z.; Xu, M.; Hou, L.; Chen, G.; Tang, D., Irregular-Shaped Platinum Nanopa rticles as Peroxidase Mimics for Highly Efficient Colorimetric Immunoassay. Anal. Ch im. Acta 2013, 776, S30
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