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Multiplexed activity of perAuxidase: DNAcapped AuNPs act as adjustable peroxidase Mustafa Salih Hizir, Meryem Top, Mustafa Balcioglu, Muhit Rana, Neil M. Robertson, Fusheng Shen, Jia Sheng, and Mehmet Veysel Yigit Anal. Chem., Just Accepted Manuscript • DOI: 10.1021/acs.analchem.5b03926 • Publication Date (Web): 11 Dec 2015 Downloaded from http://pubs.acs.org on December 14, 2015
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Analytical Chemistry
Multiplexed activity of perAuxidase: DNA-capped AuNPs act as adjustable peroxidase Mustafa Salih Hizir†, Meryem Top†, Mustafa Balcioglu†, Muhit Rana†, Neil M. Robertson†, Fusheng Shen†, Jia Sheng†, ‡ and Mehmet V. Yigit †, ‡ † Department of Chemistry, University at Albany, State University of New York, 1400 Washington Avenue, Albany, New York 12222, United States. ‡ The RNA Institute, University at Albany, State University of New York, 1400 Washington Avenue, Albany, New York 12222, United States. Correspondence: M. Yigit*, Email:
[email protected]; Tel: (1) 518-442-3002
Supporting Information Placeholder ABSTRACT: In this study, we have investigated the intrinsic peroxidase-like activity of citrate-capped AuNPs (perAuxidase) and demonstrated that the nanozyme function can be multiplexed and tuned by integrating oligonucleotides on nanoparticle surface. Systematic studies revealed that by controlling the reaction parameters, the mutiplexing effect can be delayed or advanced and further used for aptasensor applications.
INTRODUCTION: In the past few decades, the investigation on artificial enzymes has been increasing due to multiple advantages over their biological counterparts. Low-cost, bulk-preparation and greater stability of artificial enzymes make them attractive for various applications, particularly for biochemical analysis. A wide variety of inorganic nanomaterials such as metal and 1-6 metal-oxide nanoparticles, transition metal decalcogenide 7-9 10-14 (TMD) nanosheets, nanocarbon oxides, and their vari15-18 have been reported to display speous hybrid formations cific enzymatic behaviors. Some of these nanomaterials, referred as nanozymes, are reported to act as mimics of nuclease, esterase, glucose oxidase, superoxide dismutase, silicatein, catalase, phosphatise, nitrate reductase and peroxi19 dase. In general, nanozymes work in broader pH and temperature ranges, therefore, for this matter, are advantageous over biological catalysts. For instance, colloidal gold nanoparticle (AuNP) is considered as one of the robust nanozymes and a variety of its artificial enzymatic activities 19 have been reported. Particularly, its peroxidase-like activity has attracted a significant attention for biochemical 20 studies. Peroxidases are known to catalyze the oxidation of their substrates in the presence of peroxide species. AuNPs catalyze the same oxidation reactions using the same substrates. Among different functional AuNPs, negatively charged citrate-capped AuNP has been investigated predominantly due to its favorable electrostatic interaction with the positively charged 3,3',5,5'-Tetramethylbenzidine (TMB) substrate. The intrinsic peroxidase-like activity of gold nanoparticle is highly attractive alone, however adsorption of single
stranded functional oligonucleotides can tune this enzymatic 21 behavior and offer a wide spectrum of applications. Oligonucleotides are extraordinary biopolymers offering diverse functionality to the nanoparticles due to their highly programmable features, target-specific binding or cleavage, structure-switching capability and unique interactions at the bio-nano interfaces. Having these remarkable features, DNA nanotechnology has been integrated into a wide range of applications including nanoelectronics, biosensing, environ22-24 mental analysis, gene delivery and manipulation, and etc. For instance, DNA origami has been employed to engineer programmable architectural designs for biological 25,26 nanodevices while aptamer or DNAzyme (functional oligonucleotides) technology was integrated into biosensor 27,28 designs for biological or environmental applications. Our group has previously employed DNA technology to study 29 controllable assembly of gold nanoparticles, simultaneous 30,31 detection of circulating miRNAs, and single-nucleotide 32 polymorphism (SNP) identification. As aforementioned, oligonucleotides hold a great potential for various applications due to the versatile manipulation features. For the nanoparticles displaying enzyme-mimicking behaviors, DNA binding may significantly enhance nanozyme quality, offer multiplexed enzymatic capacity, and lead to 33-36 easily controllable catalytic activity. Studies have demonstrated that the presence of DNA at the interface between nanozymes and their substrates inhibits the enzymatic activity due to the physical hindrance or electrostatic repul37,38,16,39,40 On the other hand, Liu et al and Hu et al resion. ported that oligonucleotides at the nano-interface enhance the intrinsic enzymatic activity of the nanozymes remarkably 41,42 by contributing to the enzyme-substrate affinity. In this study, we have investigated the intrinsic peroxidase-like activity of citrate-capped AuNPs (perAuxidase) and demonstrated that the nanozyme function can be multiplexed and further tuned by integrating oligonucleotides on nanoparticle surface. Systematic studies revealed that by controlling the reaction parameters, the mutiplexing effect can be delayed or advanced and further used for aptasensor applications.
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blue color (oxidized TMB) was specific to only the synchronous presence of all reagents.
RESULTS AND DISCUSSION: Here, the peroxidase-like activity of AuNPs (perAuxidase, 15 nm in diameter, Figure S9) with and without DNA capping was validated using 3,3',5,5'-Tetramethylbenzidine (TMB) and hydrogen peroxide (H2O2). Before evaluating the nanozyme potential of AuNP, its stability was evaluated in various concentrations of reaction buffer (NaOAc) at pH 4.0. The nanoparticles remained stable up to 50 mM NaOAc at pH 4.0 for at least 24h, Figure S1. Later, in order to characterize the peroxidase-like activity of AuNPs and determine the optimum reaction condition, the concentration of each component (AuNPs, H2O2, TMB and NaOAc) in the reaction was varied systematically, Scheme S1.
Figure 1. Effect of perAuxidase (AuNP) and H2O2 concentration on the catalytic activity of the nanozyme. Increasing concentration of (a) perAuxidase and (b) H2O2 leads to accelerated OD increase at 650 nm and TMB oxidation.
To monitor the effect of the AuNPs concentration on the enzymatic activity; TMB oxidation reaction was performed with various concentrations of AuNPs (referred to as perAuxidase) using H2O2 and TMB in 10 mM NaOAc at pH 4.0 (working buffer). As the concentration of AuNPs increased in the reaction mixture, the observed color change due to TMB oxidation amplified, suggesting that the reaction rate can be increased with AuNP concentration, Figure 1a. Experiments with no perAuxidase did not display any color change. Next, the effect of H2O2 concentration was tested by varying its concentration from 0.1 to 30 mM with fixed AuNP concentration (200 μM perAuxidase). As the H2O2 concentration increased, a higher TMB oxidation was observed, Figure 1b. Experiments with no H2O2 did not display any color change. Before each measurement the AuNPs were removed with centrifugation to avoid signal interference from AuNPs.
Figure 2. (a) Visual analysis demonstrates that the enzymatic reaction takes place only in the presence of all reagents. (b) Absorbance spectra (inset) and end point readings at 650 nm, at the end of 30 mins incubation, shows the necessity of each component for TMB oxidation.
Next, we studied the tuning of the peroxidase-like activity of AuNP through its interaction at the biointerface. Because the enzymatic reaction occurs at the surface of the nanozyme, we hypothesized that perAuxidase activity can be manipulated by changing the surface properties. DNA has been chosen as an interfacing biopolymer due to its favorable 21 interaction with gold surface through nucleobases. We have observed that the DNA adsorption enhanced the peroxidase activity of the gold nanoparticles significantly after 30 minutes of reaction. In order to study this multiplexing effect, 200 μM perAuxidase was incubated with various concentrations of (5, 10, 20, 30, 40, 50 or 1000 nM) scrambled DNA. Following incubation and TMB oxidation reaction for 30 mins, the absorbance readings were recorded for each sample. Results demonstrate that with increasing DNA concentrations, the catalytic reaction is amplified which was observed as an OD increase at 650 nm, Figure 3a. Absence test confirmed that the DNA coupled with gold nanoparticles display significantly greater catalytic activity than gold nanoparticles alone, Figure 3b. On the other hand, the results with same amount of DNA alone were not statistically different than the blank samples which suggest that the DNA itself does not catalyze the reaction. The experiments were performed with different pH, temperatures and incubation times with DNA, Figure S5, S6 and S8. Durability tests were performed for perAuxidase and DNA-capped perAuxidase (perAuxidase-DNA), Figure S7.
Later, the various concentrations of substrate (TMB) was used to determine optimum reaction condition to monitor the colorimetric change. We have observed that TMB concentrations higher than 0.5 mM was sufficient to display the enzymatic reaction totally, Figure S2a. The dependence on the NaOAc concentration was determined in similar fashion and all concentrations between 1 to 10 mM displayed same oxidation validated visually and spectroscopically, Figure S2b. Then, in order to validate the necessity of each component for perAuxidase activity of gold nanoparticles, an absence test was performed. As seen in Figure 2, in the absence of any of the components, the reaction does not display any color change. On the other hand, the oxidation reaction is catalyzed with TMB and H2O2 in NaOAc at pH 4.0 when AuNPs were present in the reaction medium, Figure 2. Aforementioned findings reveal that the absorbance signal of
Figure 3. (a) DNA concentration-dependent accelerated TMB oxidation is observed as absorbance increase at 650 nm. (b) Absorbance end point data demonstrate significant enhancement of perAuxidase activity in the presence of both DNA and the perAuxidase.
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Here, ssDNA interacts with citrate-capped AuNPs through its nucleobases and, in such conformation, negatively 21 charged DNA backbone is exposed to the environment. We hypothesize that the presence of this multiple negative charges and the hydrogen bonding moieties provided by DNA bases could attract the positively charged aromatic substrate (TMB) molecule by interacting through intermolecular forces and, therefore, multiplex the enzymatic reaction rate by increasing localized substrate concentration around perAuxidase.
Figure 4. Absorbance spectra at 650 nm demonstrating (a) slower transition for catalysis in first 10 min followed by the accelerated enzymatic trend by perAuxidase-DNA (b) the fast formation of oxidized TMB product in first 10 min by perAuxidase only. Inset figures display first 10 min of the reaction. PerAuxidase-DNA oxides 2.5 times more TMB than perAuxidase alone does as indicated by the gap and double head arrow.
In order to understand the multiplexing effect in the presence of DNA, perAuxidase was tested with and without 100 nM scrambled DNA. We have observed that while the peroxidase activity was slowed down initially, the enzymatic reaction is multiplexed in later time points, Figure 4a and inset. The initial boost in the OD at 650 nm with AuNPs was inhibited by the stabilization provided by DNA adsorption in the DNA-capped AuNPs (perAuxidase-DNA). The multiplexing effect observation was in parallel with the recent report 41 about DNA-capped iron oxide nanoparticles. After 10 min, the peak that appeared at 650 nm intensified as the reaction proceeded (Figure 4b and Figure S3) and resulted in almost 2.5 fold enhancement compared to the naked perAuxidase at the end of 2 hrs of reaction.
multiplexing phase to a later time point. As seen in Figure 5, DNA adsorption on perAuxidase enabled us to control the enhancement effect back and forward, and change the reaction profile by changing H2O2 concentration. This is an important finding because combining the anti-sense or functional oligonucleotide technologies with the artificial enzyme features of gold nanoparticles could be highly useful for oligonucleotide-based colorimetric or spectroscopic detection methodologies. Later, we studied the effect of DNA sequence on this multiplexed catalytic activity. We tested different polynucleotide sequences while keeping the total nucleotide concentration constant. Polynucleotides with A10, T10, C10, or G10 sequences were adsorbed on perAuxidase and tested for catalysis of TMB oxidation reaction. Results demonstrate that poly purine-modified perAuxidases (A10, G10) displayed a remarkable enhancement while poly pyrimidine-modified perAuxidases (T10, C10) were slightly higher than unmodified perAuxidase, Figure 6a. Results demonstrate that the multiplexed effect observed with surface-adsorbed purine bases is different than pyrimidine bases, which could be due to the difference in the interaction between TMB and the surface-adsorbed nucleobases. Next, we evaluated the multiplexed catalytic activity in the presence of different polyA strands with different (A5, A10, A15) lengths while keeping the total nucleotide concentration constant. Results suggest that TMB oxidation in all three cases were not statistically different than each other; however, significantly higher than the perAuxidase activity without polyA capping, Figure 6b. Later, we tested whether RNA has similar tendency in this multiplexing effect, and performed the studies using scrambled RNA and A15 RNA, the RNA counterparts of scrambled DNA and A15 (DNA), respectively. The results show that both the RNA and DNA behave similarly and are not statistically different than each other, Figure 6c. Nearby catalytic amplification achieved by RNA also implies the potential of RNA in manipulating the properties of functional nanomaterials and its possible applications when coupled with nanozymes.
Figure 5. Controlling the multiplexing phase in the perAuxidase reaction profile. (a) higher hydrogen peroxide content (10 mM) results in earlier (10 min) multiplexing effect while (b) the lower content (5 mM) results in delayed (30 min) multiplexing effect.
Following the aforementioned studies showing that DNA coupled to the nanozyme display a higher TMB oxidation in later time points, we studied to control the perAuxidase activity further. Because the reaction kinetics depends on the precise experimental parameters, we were able to tune the
Figure 6. (a) Absorbance (OD at 650 nm) data demonstrate that (a) poly-purines enhance the catalysis more efficiently than poly-pyrimidines and (b) the length of the ssDNA does not influence the multiplexed catalysis. (c) The study with ssRNA molecules demonstrates that they act similar to ssDNA in multiplexing the catalysis. (d) The multiplexed peroxidase-like
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activity can be employed to detect thrombin using aptamer and perAuxidase complex.
Finally, in order to demonstrate a possible application of this multiplexing phenomenon, we have used aptamer technology coupled with AuNPs. 29 nucleobase-long DNA aptamer for thrombin was studied. First, the catalytic activity of perAuxidase was evaluated with and without thrombin. The results show that thrombin itself does not influence the peroxidase-mimicking activity of gold nanoparticles. Later, the nanoparticles were incubated with aptamer which increased the peroxidase activity (30 mins), therefore, the OD at 650 nm. On the other hand, when the aptamer was preincubated with thrombin, inhibiting the adsorption of the aptamer on the nanoparticle surface, this multiplexed effect was diminished, Figure 6d. Findings reveal that the difference in TMB oxidation with and without DNA adsorption can be employed for aptasensor development.
CONCLUSION: To conclude, our work demonstrates that the intrinsic peroxidase-like activity of artificial gold nanozyme could be multiplexed or diminished by integrating single stranded DNA or RNA molecules on nanoparticle surface. This multiplexing effect can be fine-tuned by altering the nucleotide components of the oligonucleotide sequences or changing the reaction parameters. Furthermore, the mechanism of enhancement can be conducted to detect small analytes or biological metabolites using target-specific aptamers. Such a versatile application tool holds a great potential for the realms of environmental science, toxicology and biology. In order to multiplex the inherent enzymatic activity of certain protein molecules, organic-inorganic hybrid structures have been employed. Zare and co-workers have coupled protein structures with copper (II) ions to achieve higher cata43 lytic activity. Hou and co-workers studied the immobilization of α-amylase using specific nanomaterials to demon44 strate the enhanced catalytic capability of the enzyme. In a recent study, Ocsoy and co-workers have also achieved enhanced catalytic activity of horseradish peroxidase using 45,46 copper (II) and iron (II) ions. Our study on the other hand reports the multiplexing and adjusting of the intrinsic peroxidase-like activity of gold nanoparticles using DNA and RNA molecules. Though others have shown a greater multiplexed effect by preparing gold hybrid structures using dif1,16,47,48 ferent sizes and morphologies, multiplexing the catalytic activity of gold nanoparticles using oligonucleotides with different nucleobase composition has not been reported previously. In the future, this property could enable us to characterize the base composition of DNA or RNA molecules.
ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website: Additional results (Figures S1-S9) and details of experimental methods are provided. TEM images, DLS data, and the durability of the nanoparticles are provided in the supporting information. The effects of incubation time with oligonucleotides, pH and temperature are reported in the supporting information.
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AUTHOR INFORMATION Corresponding Author Correspondence: M. Yigit*, Email:
[email protected]; Tel: (1) 518-442-3002
ACKNOWLEDGMENT We acknowledge the Ministry of National Education, Republic of Turkey, for providing financial support to Mustafa Salih Hizir with full scholarship during his doctoral studies. This work was supported by SUNY Albany Start-Up Funds.
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