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Dynamically arranging gold nanoparticles on DNA origami for molecular logic gates Jing Yang, Zhichao Song, Shi Liu, Qiang Zhang, and Cheng Zhang ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.6b04992 • Publication Date (Web): 09 Aug 2016 Downloaded from http://pubs.acs.org on August 10, 2016

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ACS Applied Materials & Interfaces

Dynamically arranging gold nanoparticles on DNA origami for molecular logic gates Jing Yang,a Zhichao Song,a,b Shi Liu, a Qiang Zhang,c, * Cheng Zhangb, * a

School of Control and Computer Engineering, North China Electric Power University, Beijing

102206, China b

Institute of Software, School of Electronics Engineering and Computer Science, Key Laboratory

of High Confidence Software Technologies of Ministry of Education, Peking University, Beijing 100871, China c

Key Laboratory of Advanced Design and Intelligent Computing, Dalian University, Ministry of

Education, Dalian 116622, China *

To

whom

correspondence

should

be

addressed.

Email:

[email protected];

[email protected] KEYWORDS: DNA origami, DNA/Au conjugate, strand displacement, transmission electron microscopy, logic gate

ABSTRACT: In molecular engineering, DNA molecules have been extensively studied owing to their capacity for accurate structural control and complex programmability. Recent studies have shown that the versatility and predictability of DNA origami make it an excellent platform for constructing nanodevices. In this study, we developed a strand-displacing strategy to selectively

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and dynamically release specific gold nanoparticles (AuNPs) on a rectangular DNA origami. A set of DNA logic gates (“OR”, “AND” and “three-input majority gate”) were established based on this strategy, in which computing results were identified by disassembly between the AuNPs and DNA origami. The computing results were detected using experimental approaches such as gel electrophoresis and transmission electron microscopy (TEM). This method can be used to assemble more complex nanosystems and may have potential applications for molecular engineering.

Introduction Recently, DNA self-assembly has become a powerful tool for building nanoscale structures and has been widely applied for constructing various two- and three-dimensional objects, including planar arrays, cylindrical tubes, and other geometric shapes.1-10 Interestingly, DNA origami first developed by Rothemund, involves the hybridization of a single-stranded M13 scaffold with hundreds of short DNA helper strands to form predesigned nanostructures, providing a new effective way to design a wide range of artificial nanostructures with well-defined shapes and sizes.11 Actually, DNA origami has been applied in various areas such as single molecule detection12,

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and logic operation.14,

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Using extended helper strands as sequence-dependent

DNA tags, DNA origami has been utilized as a basic template to assemble functional metallic nanoparticles (NPs), carbon nanotubes, and proteins into sophisticated structures, with effective control of specifically designed distances.16-22 Notably, DNA origami-based nano-systems were well established with the advantages of specific spatial addressability and accurate vicinity control, which are especially suitable for creating dynamic nano-devices and assembling as artificial structures for engineering a wide variety nanosystems.


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Due to the unique structural and optical properties, organizing AuNPs with DNA assembly structures in a well-controlled manner has attracted a lot of attention in the fields of biosensing and nanodevices.23-31 For example, Elbaz and co-workers constructed a dynamic and fuel-driven AuNPs devce via a three-ring catenated DNA nanostructure.32 Nevertheless, the simple DNA rings can only provide limited and floating AuNPs attaching sites, and thus the challenge of achieving complicated and spatially addressable AuNPs arrangements still remains. Moreover, Yan and co-workers used a DNA origami template to control the assembly of AuNPs. Using this method, AuNPs of different sizes are specifically arranged, and the orientation and distance between nanoparticles can also be controlled.33 Although this study have demonstrated that NPs can be assembled with DNA origami in a static manner, it is still interesting to design an NP/DNA origami device with dynamic operation characteristics. In addition, in most previous NP/DNA origami based nano-systems, it is difficult to achieve logic operations induced by multiple inputs at the same time, which greatly hinders the utilization of DNA origami-based sensing systems. In this study, we constructed a logic system based on arrangement of AuNPs on rectangular DNA origami, in which AuNPs could be selectively and dynamically released from DNA origami in response to specific DNA signals. During the computing process, logic operations were implemented by specifically controlling the attachment of AuNPs onto DNA origami. Using this strategy, “OR” and “AND” logic gates were established by the arranging positions of two types of AuNPs (5 and 15 nm) on DNA origami. Moreover, by exploiting intra-connections between AuNP dimers, a complex three-input majority gate was also constructed, demonstrating the good expansibility and complexity of the logic gate.


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Experimental Section Materials. All DNA strands were purchased from Sangon Biotech Co. Ltd. Unmodified strands were purified by polyacrylamide gel electrophoresis (PAGE), and modified DNA strands with disulfide and fluorophore were purified by high-performance liquid chromatography. The sequences of all strands are listed in Table S1. DNA strands were dissolved in water as stock solution and quantified using a TU-1901 spectrophotometer (Beijing Purkinje General Instrument Co., Ltd., Beijing, China), and absorption intensities were recorded at λ = 260 nm. M13mp18 DNA was purchased from New England Biolabs, Inc. AuNPs (5- and 15-nm) were purchased from Ted Pella Inc. Bis (psulfonatophenyl) phenylphosphine dihydrate dipotassium salt (BSPP) was purchased from J&K Chemical Ltd. Gels were prepared using TAE/Mg2+ buffer (40 mM Tris, 20 mM acetic acid, 2 mM EDTA and 12.5 mM magnesium acetate, pH 8.0), and 500mL mother liquor of acrylamide at a concentration of 45% (217 g acrylamide and 8 g N, N'methylenebisacrylamide). Other chemicals were of reagent grade and were used without further purification. Preparation of the DNA origami template. To synthesize the rectangular DNA origami, 1.6 nM of the M13mp18 strand was mixed with the staple strands at a ratio of 1: 10 in 1 × TAE/Mg2+ buffer, and annealed from 90 °C to room temperature. Moreover, several staple strands at selected positions on the origami template were replaced by the capture strands to generate the binding sites. The product was purified using a 50K filter device (MWCO, Amicon, Millipore) to eliminate the excess staple DNA strands. Preparation of DNA/AuNP conjugates. A few copies of the thiolated DNA strand a1' attached onto the 15-nm AuNPs to form the NP-A conjugate, and strands b1' and c1'


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attached onto the 5-nm AuNPs to produce the NP-B and NP-C conjugates, respectively. The NP-DE conjugate was produced by using two strands (d1' and e1') to attach onto one single 5-nm AuNP simultaneously at a 1:1:1 molar ratio. Subsequently, the conjugates were fully modified with a layer of five nucleotides of thiolated ssDNA (5'-SH-TTTTT3') to maintain stability of the AuNPs in the presence of high salt concentrations for the DNA scaffold. To remove the unbound DNA strands, conjugates were then obtained by the same method as that applied to the DNA origami. Finally, the rectangular DNA origami was mixed with these freshly obtained DNA/AuNP conjugates and annealed from 40 °C to room temperature at a 1: 30 ratio. The assembled DNA conjugates were analyzed by gel electrophoresis. Additionally, the target band was run into a glass fiber filter membrane assisted by a dialysis membrane (MWCO 14000). These conjugates were then collected for imaging by TEM. TEM Analysis. Purified DNA/AuNP conjugates were freshly isolated. A 3−6 µL droplet of the sample was deposited on TEM grids (400 mesh, Ted Pella), and the excess solution was removed by using a piece of filter paper. After this, the grid was washed with Milli-Q water 1−3 times. TEM images were obtained by a Hitachi H-7650 transmission electron microscope. Results and Discussion As illustrated in Figure 1a, a rectangular DNA origami-1 was employed with the dimensions of 90 nm × 60 nm × 2 nm, composed of a ~7000 bp circular single-stranded M13 DNA and 202 short staple strands using the method of Rothemund (Figure S1 and S2). Three AuNP-capturing positions (64, 44, and 149) were designed on the origami surface from the extended helper strands, designated as a1, b1, and c1. Additionally, three types of DNA/AuNP conjugates, i.e., NP-A, NP-B and NP-C (with diameters of 15, 5 and 5 nm, respectively), were prepared by


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modifying AuNPs with thiolated complementary DNA strands a1', b1', and c1', respectively. In the initial state, the origami-1 was hybridized with one 15-nm NP-A and two 5-nm NP-B and NP-C, as shown in Figure 1a. Then, the assembled AuNP/origami productⅠwas analyzed by gel electrophoresis (Figure 1b, lane 2). Interestingly, the band of product Ⅰ had less mobility than that of the bare rectangular origami-1 (Figure 1b, lane 1) owing to the AuNP attachments. In this computing system, logic operations were achieved by selectively releasing AuNPs on the origami surface using DNA strand displacement. In the “OR” gate, NP-B and NP-C were designed as potential releasing targets and NP-A was introduced as a structural reference. Here, DNA input strands b1-L and c1-L were designed to recognize the toehold regions of helper strands b1 and c1, and could preferentially displace strands b1' and c1', respectively, thus resulting in release of the NP-B or NP-C from the origami surface. The true output was represented by disassembly of any AuNP from origami-1. First, strand c1-L was introduced to trigger release of the NP-C from the product Ⅰ (Figure 1a, ①). After strand displacing, the new product Ⅱ was generated with only NP-A and NP-B attached onto the origami-1. Interestingly, the gel results demonstrated that product Ⅱ had slightly higher mobility than product Ⅰ (Figure 1b, lane 4). Second, in the presence of strand b1-L, NP-B could be totally displaced, leading to the generation of product Ⅲ, with NP-A and NP-C remaining on the origami surface.


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Figure 1. (a) Illustration of the “OR” gate system. (b) Gel electrophoresis analysis. Lane 1, the DNA origami-1 template; lane 2, the origami-1 with NP-A, NP-B, and NP-C; lane 3, the origami-1 with NP-A and NP-C; lane 4, the origami-1 with NP-A and NP-B; lane 5, the origami1 with NP-A. (c) TEM images and statistical analysis. From the gel results, the running mobility of product Ⅲ was similar to that of product Ⅲ because the same numbers of AuNPs were attached to the origami for both products (Figure 1b, lane 3). Finally, when b1-L and c1-L were added simultaneously, product Ⅳ was generated, with only NP-A remaining on the origami after release of both NP-B and NP-C (Figure 1a, ③). Notably, the gel results showed that product Ⅳ had a higher mobility than products Ⅱ and Ⅲ (Figure 1b, lane 5). Additionally, all AuNPs/origami products were further purified for analysis


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by TEM. By statistical counting, the yield of products Ⅰ, Ⅱ, Ⅲ, and Ⅳ were ~58.3%, ~69.6%, ~61.4%, and ~87.6% (Figure 1c, Figure S5). The TEM results well demonstrated the selective release of AuNPs from the DNA origami. Moreover, an “AND” logical system was also established, in which a single AuNP was released only after simultaneous addition of d1-L and e1-L inputs. The true output was represented by disassembly of any AuNP from origami-2. To fabricate the assembly structure, the rectangular origami-2 was purified as described above. In this design, two thiolated DNA strands, d1' and e1', were mono-functionalized onto one single 5-nm AuNP simultaneously in a 1:1:1 molar ratio to produce the NP-DE conjugate. Thus, the conjugate NP-DE-1 could connect with origami-2 via the hybridization between both strands d1'/e1' and helper strands d1/e1. Additionally, the 15-nm conjugate NP-A was also prepared for attachment onto the origami, acting as a positional marker. In the experiment, the conjugates NP-DE-1 and NP-A were mixed with the origami-2 and annealed from 40 °C to room temperature at a 1: 30 ratio. The product Ⅴ was then generated with attachment of both 15-nm and 5-nm conjugates (Figure 2a). First, input d1-L (with longer complementary hybridizing region between d1-L and d1) was added to react with product Ⅴ. In this condition, no separation of the NP-DE-1 conjugate from the origami-2 was observed, because d1-L could only displace strand d1', and the hybridization of e1' and e1 was still present (Figure 2a). The gel results in lane 3 of Figure 2b confirmed our experimental design that, the band representing the displaced product exhibited approximately the same mobility as that of product Ⅴ in lane 2, demonstrating that no department occurred between nanoparticles and origami-2. Similarly, the addition of input strand e1-L could only displace strand e1' on the 5-nm AuNPs, and did not lead to the separation of the NP-DE-1 conjugate and the origami-2, because the hybridization of d1' and d1 still existed. The gel results


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shown in lane 4 of Figure 2b also confirmed that there was no separation between nanoparticles and origami-2. In this case, no matter whether input d1-L or e1-L is added alone, the 5 nm AuNP will not be released from the origami template. However, when both inputs d1-L and e1-L were added, strand displacement occurred between strands d1'/e1' and helper strands d1/e1, thus leading to release of the NP-DE-1 conjugate from the origami-2.

Figure 2. (a) Illustration of the “AND” logic operation system. (b) Gel electrophoresis analysis using NP-DE-1. Lane 1, the DNA origami-2; lane 2, the product of origami-2 with NPA and NP-DE; lane 3, the product after adding strand d1-L; lane 4, the product after adding strand e1-L; lane 5, the product after adding strands d1-L and e1-L. (c) TEM images and statistical analysis. (d) Gel electrophoresis analysis using NP-DE-2. Lane 1, the product of


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origami-2 with NP-DE-2; lane 2, the product after adding strand d1-L; lane 3, the product after adding strand e1-L; lane 4, the product after adding strands d1-L and e1-L. In addition, TEM images also demonstrated the operations of the “AND” logic gate. In the initial state, product Ⅴ was purified from the gel band, and TEM results showed that 15- and 5nm NPs assembled with origami-2 (Figure 2c). In the presence of either input d1-L or e1-L, the arrangement of nanoparticles was the same as that of product Ⅴ (Figure S6). Notably, only when both d1-L and e1-L were added, the 5-nm AuNPs successfully separated from the origami-2, as shown in TEM images in Figure 2c. The yield of this target structure was ~70%. Although the displaced product Ⅳ in lane 5 showed slightly higher mobility than product Ⅴ in lane 2, the difference was not obvious (Figure 2b). To further verify the effects of the two-input “AND” logic, another AuNP/origami assembly, product Ⅵ, was generated, in which the DNA origami dressed with single 15-nm AuNPs via hybridizations of strands d1'/e1' and helper strands d1/e1 (NP-DE-2) (Figure 2d, lane 1). Obviously, the addition of either d1-L or e1-L did not induce the removal of the 15-nm AuNPs (Figure 2d, lanes 2-3). Interestingly, when both inputs d1-L and e1-L were present, the 15-nm AuNPs were released from the origami-2 due to the strand displacement reaction. The disappearance of the band of product Ⅵ in lane 4 of Figure 2d well demonstrated that the 15-nm AuNPs were indeed removed from the DNA origami. To explore the capacity of this system for large-scale operations, a three-input majority “AND ” logic gate was constructed based on three input strands f1-L, g1-L, and T-L. As illustrated in Figure 3a, NP-M (15-nm) was monomodified with two thiolated strands, f1' and T1, at a 1:1:1 ratio. Additionally, NP-N (15 nm) was coated with two other strands, g1' and T2, at a 1:1:1 ratio. Then, these two AuNP conjugates were passivated by a layer of thiolated poly 5T ssDNA. In the


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presence of bridging strand T (complementary with strands T1 and T2), the functionalized NP-M and NP-N can be hybridized to produce a dimer structure NP-T (Figure 3b). Gel electrophoresis showed that the band representing NP-T in lane 1 had a slower gel running speed than that of any other NP in lanes 2 and 3. The obtained NP-T product was purified and mixed with the origami-3 via hybridization of strands f1/f1' and g1/g1' (at room temperature for 8 h in a 1: 30 ratio). Control experiment was implemented to choose the proper concentrations of strands T1 and T2 (Figure S3). In this way, the hybridized product Ⅶ was generated as the initial logic gate to implement three-input majority computation.

Figure 3. (a) Illustration of NP-T formation. (b) Gel electrophoresis analysis of the AuNP dimer. Lane 1 corresponds to the dimer of NP-T. Lane 2 corresponds to NP-M modified with strands f1' and T1. Lane 3 corresponds to NP-N hybridized with strands g1' and T2. Next, three unique input strands (T-L, f1-L, and g1-L) were used to release the AuNPs on product Ⅶ by strand displacement and the true output was represented by disassembly of any AuNP from origami-3. For this three-input majority gate, the output would be true if any two or all inputs strands were introduced. First, in the presence of one input signal (e.g., f1-L), strand


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f1-L could recognize strand f1 via the toehold region, initiating the displacement reaction (Figure 4a, ①), and no AuNPs were released from the origami-3. In this case, a pair of AuNPs on the origami was still clearly observed from the TEM images (Figure 4b). In addition, the band in lane 4 showed the same mobility as that of product Ⅶ in lane 3, demonstrating that AuNP disassembly did not occur. Similarly, the results of adding only one input, T-L or g1-L, are shown in the Supporting Information (Figure S4). Therefore, the addition of only one input did not induce AuNP disassembly, and the computing results were false.

Figure 4. (a) Illustration of a three-input majority “AND” logic operation system. (b) TEM images of products Ⅶ and Ⅷ. (c) Gel electrophoresis by UV. Lane 1: M13 strand; lane 2: DNA origami-3; lane 3: product Ⅶ; lane 4: the product after adding strand f1-L; lane 5: the product after adding two strands, g1-L and T-L; lane 6: the product after


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adding three strands, f1-L, g1-L, and T-L. (d) Photograph of gel electrophoresis results. Lane 1: product Ⅶ; lane 2: the product after adding strand f1-L; lane 3: the product after adding two strands, g1-L and T-L; lane 4: the product after adding three strands, f1-L, g1L, and T-L. The blue arrows indicate the polymer products. The green arrows indicate the released AuNPs. Moreover, when any two input signals (e.g., T-L and g1-L) were introduced at the same time, strands T-L and g1-L could recognize strands T and g1', respectively, via their own toehold regions, thereby triggering separation of the nanoparticle NP-N from the origami3 (Figure 4a, ①②). From the gel results, the band of the displaced product Ⅷ ran slightly faster than that of product Ⅶ (Figure 4c, lane 5; Figure 4d, lane 3). This could be explained by the presence of only one AuNP on product Ⅷ, whereas two AuNPs were still present on product Ⅶ. As demonstrated by the TEM images in Figure 4b, the structure of product Ⅶ was a single DNA origami connected with a single 15-nm AuNP, with a yield of ~87%. Additional TEM results are shown in Figure S6. Similarly, two other combinations of input strands (T-L/f1-L and f1-L/g1-L) were also used to implement this gate (Figure S4). Finally, in the presence of all three inputs (Figure 4a, ①②③), strands T-L, f1-L, and g1-L could recognize strands T, f1', and g1', respectively, thus leading to disassembly between NPs and origami. Notably, gel results showed that the band of the previous structure disappeared, indicating that the two AuNPs were completely released from the origami (Figure 4d, lane 4). Conclusion In summary, we successfully developed a programmable strategy to selectively and dynamically control specific AuNPs on a rectangular DNA origami. This strategy was extended to establish a


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series of DNA logic gates (OR, AND, three-input majority gate), in which the operations could be conducted by adding DNA inputs. The designs were confirmed by gel electrophoresis and TEM images. The operations of these logic gates provide a promising method for constructing complicated molecular circuits and nanodevices. It is noteworthy that the system described here can provide a potential approach for nano-engineering and control with several following features. Firstly, positions of AuNPs are regulated not only by static hybridizations, but also based on the dynamic and cooperative controls of multi-inputs. Moreover, the operating results can be obtained by directly observing specific positions of AuNPs and DNA origami. Finally, intra-signal-relationship was established between AuNPs dimer by specific mono-functionalizing DNA on to one nanoparticle, thus demonstrating the elaborated controls to fulfill dynamic structural arrangements of AuNPs/origami systems. By integrating with a wide variety nano-engineering strategies, this method could also be used to assembling large programmable structures and pave the way for the sensitive detection of various molecular conformations. Thus, we anticipate that this strategy has the potential applications in biosensing and molecular engineering.

ASSOCIATED CONTENT Supporting Information. Materials, experimental methods, and additional experimental data. This material is available free of charge via the internet at http://pubs.acs.org. AUTHOR INFORMATION Corresponding Author *To

whom

correspondence

should

be

addressed.

Email:

[email protected],

[email protected]


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Author Contributions The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. Notes The authors declare no competing financial interest. ACKNOWLEDGMENT This work was supported by National Natural Science Foundation of China (Grants 61370099, 61272161, 61425002, 61472333, 61572046 and 61320106005). ABBREVIATIONS AuNPs, gold nanoparticles; TEM, transmission electron microscopy; PAGE, native polyacrylamide gel electrophoresis. REFERENCES 1.

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