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Self-Replication-Assisted Rapid Preparation of DNA Nanowires at Room Temperature and Its Biosensing Application Hongfei He, Jianyuan Dai, Guixiu Dong, Hongli Shi, Fang Wang, Yunran Qiu, Ruoxing Liao, Cuisong Zhou, Yong Guo, and Dan Xiao Anal. Chem., Just Accepted Manuscript • DOI: 10.1021/acs.analchem.8b05431 • Publication Date (Web): 22 Jan 2019 Downloaded from http://pubs.acs.org on January 24, 2019

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Analytical Chemistry

Self-Replication-Assisted Rapid Preparation of DNA Nanowires at Room Temperature and Its Biosensing Application Hongfei He,†,‡,# Jianyuan Dai,*,†,# Guixiu Dong,† Hongli Shi,† Fang Wang,§ Yunran Qiu,† Ruoxing Liao,† Cuisong Zhou,† Yong Guo,† and Dan Xiao*,†,§ † College

of Chemistry, Sichuan University, Chengdu 610064, China

‡ College

of Life Sciences, Sichuan University, Chengdu 610065, China

§ College

of Chemical Engineering, Sichuan University, Chengdu 610065, China

ABSTRACT: A rapid room-temperature DNA nanowires preparation strategy on the basis of self-replicating catalyzed hairpin assembly (SRCHA) was reported. In this system, three hairpin probes (P1, P2 and P3) were well-designed and partially hybridize to each other, and two split trigger DNA sequences were integrated into P1 and P3, respectively. When the SRCHA was initiated by the trigger DNA, a series of DNA assembly steps based on the toehold-mediated DNA strand displacement were activated and the Y shape DNA (P1-P2-P3) was formed. In that case, the two split trigger DNA sequences will come into close-enough proximity to form the trigger DNA replicas, which can initiate the additional SRCHA reaction cycles for DNA nanowire preparation, eventually a rapid room-temperature DNA nanowires preparation strategy without need of fuel strands was successfully developed. Furthermore, the prepared DNA nanowires have been used to develop a rapid and signal amplified sensing platform for sensitive adenosine triphosphate (ATP) detection.

replicas can be obtained in a short time.16 There are numerous examples of self-replicating machines in biology, but introducing self-replication into artificial biological systems remains a considerable challenge. Recently, several selfreplicating artificial biomaterials fabrication systems, such as self-replication of information-bearing nanoscale patterns17 and self-replication of DNA rings18 have been reported. However, these systems are also limited by the multiple chemical and thermal processing cycles,17 or the requirement of fuel strands for self-replication.18 Catalytic hairpin assembly (CHA) is an enzyme-free signal amplified DNA circuit and has been received great attention in the past decade.19−21 Recently, we reported a rapid signal amplification system based on the self-replicating catalyzed hairpin assembly (SRCHA), in which numerous target DNA replicas can be produced in the form of sticky end in the CHA products, and the signal amplification rate was significantly facilitated.22 Taking benefit from SRCHA system, herein, SRCHA system combined with sticky ends self-assembly were introduced into the DNA nanowire construction process, the prepared DNA nanowires consisting of numerous of trigger DNA replicas, which can initiate the additional SRCHA reaction cycles for DNA nanowire formation, then a rapid room-temperature DNA nanowires preparation strategy without need of fuel strands was successfully developed. In addition, we speculated that the non-DNA molecules also can trigger the DNA nanostructure formation. As proof-of-concept, adenosine triphosphate (ATP) was used as the model small molecule to demonstrate the feasibility of our proposed strategy and a rapid and sensitive ATP assay was developed.

DNA-based nanostructures have emerged as a useful tool in the fields of biosensing, biocomputing platforms, biomedicine and biotechnology.1,2 Up to now, numerous DNA nanostructures with diverse geometry, including DNA nanowire,3 DNA dendrimer,4 DNA nanosphere5 and DNA nanotube,6 etc. have been developed through DNA selfassembly. Among these DNA nanostructures, DNA nanowire has been received considerable attention due to its simple structure, easy preparation and the ability to incorporate various functionalities into its nanostructure. Willner and coworkers reported a signal amplified DNA assay through the autonomous assembly of the Mg2+-dependent DNAzyme nanowires.7 Silva and co-workers designed a quadruplex DNA nanowire with controlled structural periodicity by using the quadruplex folding principles.8 Huang and co-workers developed a localized catalytic hairpin assembly (LCHA) strategy for intracellular miR-21 imaging by using DNA nanowires.9 Recently, Tanaka and co-workers reported a long, uninterrupted straight-chain silver-DNA hybrid nanowire using metallobase pairs formed by natural nucleobases.10 Although above DNA self-assembly-based DNA nanostructures preparation methods are simple and effective, they are still limited by long preparation time.7−14 Solution annealing is an alternative method for rapid DNA nanostructures construction but it performed at high temperature (95 °C) by using temperature controller.15 The development of a rapid room-temperature preparation method for DNA nanostructures construction is still challengeable. Self-replication is a behavior of a system that reproduces itself by its own power or inherent nature, and large amounts of

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EXPERIMENTAL SECTION Materials and reagents. Trishydroxymethylaminomethane hydrochloride (Tris-HCl), magnesium chloride, sodium chloride, adenosine triphosphate (ATP), guanosine triphosphate (GTP), cytidine triphosphate (CTP) and uridine triphosphate (UTP) were purchased from Sigma-Aldrich (St. Louis, MO). DNA oligonucleotide sequences were synthesized by Sangon Biotechnology Co., Ltd. (Shanghai, China) and purified by high-performance liquid chromatography (HPLC). The sequences of oligonucleotides were in Table S1. All other reagents were of analytical grade and were used without further purification. Ultrapure water obtained from a Millipore water purification system (≥ 18.2 M Ohm cm) was used in all experiments. Instrumentation. Atomic force microscopy (AFM) images were recorded on a MFP-3D-BIO (Oxford Instruments Asylum Research, Inc.) using the tapping mode in ambient air. All fluorescence measurements were carried out on a RF-6000 fluorescence spectrophotometer (Shimadzu, Japan). Images of gel electrophoresis were scanned by the ChemiDoc XRS Imaging System (Bio-Rad Laboratories Co., California, USA) and the yield of the DNA nanowires was then analyzed. Preparation of DNA nanowires and AFM imaging. All samples were prepared in 20 mM Tris-HCl (pH 7.6) buffer containing 5 mM MgCl2. Hairpin probe P1, P2 and P3 were heated to 95 °C for 5 min in buffer solution and then cooled to room temperature for 3 h before use. Then 5 nM trigger DNA were incubated with P1 (300 nM), P2 (300 nM) and P3 (300 nM) in 100 μL buffer solution for 20 min at room temperature. The DNA nanowires solution was deposited on a freshly cleaved mica surface (Ted Pella, Inc., USA), dried in air, and gently washed with double-distilled water. The excess water was removed with filter paper, the sample was dried again in air, and then the AFM images were recorded. Agarose gel electrophoresis. 10 μL of different reaction products with loading buffer were loaded into the lanes of the freshly prepared agarose gel (1%). The agarose gel was prepared using a 1 × TBE buffer (45 mM Tris, 1.0 mM Na2EDTA, pH 8.0). The ethidium bromide (EB) was mixed with agarose gel to image the position of DNA. The gel was run at 100 V for 45 min in a 1 × TBE buffer with ice-cold water bath and finally photographed with the gel image analysis system. Fluorometric detection of ATP. Pretreated P1, P2 and P3 hairpin probes were prepared as above. For the ATP detection, different concentrations of ATP were mixed with the triggeraptamer (T-A, 200 nM) and blocking probe (BP, 600 nM) in 20 μL Tris-HCl buffer solution (20 mM, 300 mM NaCl, 5 mM MgCl2, pH 7.6) and then incubated for 10 min at room temperature. Subsequently, 60 μL of P1 (330 nM), P2 (330 nM) and P3 (330 nM) were respectively added into the above mixed solution and incubated for another 20 min. According to the fluorescent properties of FAM, the excitation wavelength was set at 490 nm, slit width for both excitation and emission was set at 5.0 nm. Finally, the resulted solutions were characterized by a RF-6000 fluorescence spectrophotometer with a 2 mm × 10 mm quartz cell containing 200 μL of solution.

Scheme 1 Principle for the rapid room-temperature DNA nanowires preparation and ATP detection based on the DNA selfreplication and sticky ends self-assembly.

RESULTS AND DISCUSSION The principle of the proposed rapid room-temperature DNA nanowires preparation strategy is illustrated in Scheme 1. Three hairpin DNA probes (P1, P2 and P3) were welldesigned and partially hybridize to each other (DNA sequences were listed in Table S1), and two split trigger DNA sequences were integrated into P1 and P3, respectively (sequences with pink color in P1 and P3). P3 was also chosen as signal unit by labeling with fluorophore (FAM) and quencher (BHQ1). Once the SRCHA was initiated by the trigger DNA, a series of DNA assembly steps based on the toehold-mediated DNA strand displacement were activated and short life intermediate Trigger-P1-P2-P3 was formed (Scheme 1, step 1-3), then the fluorescence of P3 was restored.23,24 This intermediate is inherently unstable and trigger DNA can be displaced by P3 through the spontaneous disassembly. Then the released trigger DNA will be reused to form the additional P1-P2-P3 complexes (step 4). In the formation process of P1-P2-P3, the two split trigger DNA sequences will come into close-enough proximity and the trigger DNA replicas in the form of sticky ends of P1-P2-P3 was obtained, then the additional SRCHA reaction cycles for the formation of P1-P2-P3 complexes were triggered by the trigger replicas (step 5-8), leading to the rapid and significant enhancement of fluorescence signal. Meanwhile, since the rest of sticky ends of P1-P2-P3 (sequences with blue color in P1P2-P3) were complementary to each other, the autonomous sticky ends self-assembly between P1-P2-P3 complexes would occur, then the helix DNA nanowires consisting of numerous of trigger DNA replicas were finally obtained (step 9-10). To demonstrate the feasibility of this strategy, we used atomic force microscopy (AFM) image and cross-section analysis to confirm the hypothetical morphology of DNA nanowires. AFM image of the DNA nanowires was shown in Figure 1A. The nanowires are varied in length and the height of them is around 1.9 nm (Figure S1), which is similar to previously reported literatures.9,25 The length of the DNA nanowires were analyzed statistically and the results showed that the most of the DNA nanowires are shorter than around 0.75 μm (Figure S2). Although some DNA nanowires with the


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Analytical Chemistry previously reported DNA nanowires9 or DNA polymer chains.27 In order to investigate the role of DNA selfreplication, a conventional non-self-replicating CHA system (non-SRCHA) was designed as control, in which the two split trigger DNA sequences in P1 and P3 were replaced by thymine-rich sequences, and the rest sequences were similar to P1 and P3 (P1-C and P3-C sequences were listed in Table S1). The AFM image of this non-SRCHA system was also recorded and only a few short DNA nanowires were observed (Figure S4), indicating that the self-replication of trigger DNA play a key role in the process of the rapid DNA nanowire formation. Agarose gel electrophoresis was also used to further illuminate the proposed rapid DNA nanowires preparation mechanism. As shown in Figure 1B, the SRCHA system exhibits an increased appearance of the high molecular weight smeared band (lane 5) compared to the non-SRCHA system (lane 3), indicating that the self-replication catalyzed DNA nanowires rapid formation was truly occurred. Meanwhile, we can see that the molecular weight for the most of generated DNA nanowires is less than around 2000 bp. According to the nm-to-bp value of 0.334,27 the length of the generated DNA nanowires can be calculated to be shorter than around 0.67 μm, which is roughly consistent with the frequency distributions of the length of DNA nanowires (Figure S2). The relative yield of DNA nanowires was also calculated by using the agarose gel electrophoresis image.19,28 As shown in Figure S5, the brightness of the band of the reaction system decreased obviously after 20 min (Figure S5 (A)), and the relative yield of DNA nanowire increased quickly and reach a plateau at 20 min with around 71% relative yield (Figure S5 (B)), indicating that the reaction equilibrium was reached. The preparation time of the DNA nanowires (20 min) is much faster than the reported non-selfreplicating systems (Table S2).7,11−14 For a better understanding of the reaction process, timedependent fluorescence spectroscopy measurements were performed to quantitatively evaluate the growth kinetics of the two different systems. As shown in Figure 2, when the trigger

Figure 1. (A) AFM image of the resulting DNA nanowires. P1, P2 and P3 concentration: 300 nM; Trigger DNA concentration: 5 nM. (B) 1% Agarose gel electrophoresis analysis. Lane 1: P1 only; Lane 2: P1-C + P2 + P3-C; Lane 3: P1-C + P2 + P3-C + trigger; Lane 4: P1 + P2 + P3; Lane 5: P1 + P2 + P3 + trigger; Lane 6: DNA ladder. P1, P1-C, P2, P3 and P3-C concentration: 300 nM; Trigger DNA concentration: 5 nM; Reaction time: 20 min.

lengths of over several micrometers can also be observed. It should be noted that the diameter of our prepared DNA nanowire in AFM is larger than those of the previously reported DNA nanowires,11,26 this result can be ascribed to different structures of the precursor monomer and growth direction of the nanowires. In our work, the precursor monomer for DNA nanostructure construction is Y shape DNA, DNA nanowire would grow along the helix direction due to the rigid structure of the Y shape DNA, and finally a DNA nanowire with the helix structure was formed (Figure S3 (A)). The diameter of the DNA nanowire in Figue 1 (A) actually is the diameter of the helix DNA nanostructure (d2), not the DNA nanowire (d1). For the literature reported DNA nanowires, the precursor monomer for DNA nanostructure construction is linear DNA, DNA nanowire would grow along the linear direction and linear DNA nanowire was finally formed (Figure S3 (B)). Obviously, the diameter of helix DNA nanostructure (d2) is much larger than that of the linear DNA nanowire (d3), which is consistent with the AFM result. In addition, some nodular-like structures in DNA nanowires were also observed in the AFM image. We speculated that these nodular-like structures might be ascribed to the overlap of the DNA nanowires themselves during the deposition process on the mica surface for AFM imaging. Similar nodular-like structures also can be observed in the AFM images of the

Figure 2. Time-dependent fluorescence changes of selfreplicating system (a) and non-self-replicating system (b) in the presence of trigger DNA, self-replicating system (c) and non-selfreplicating system (d) in the absence of trigger DNA. Excitation wavelength was set at 490 nm and emission wavelength at 520 nm; Concentration of P1, P2, P3, P1-C and P3-C: 100 nM; Trigger DNA concentration: 5 nM.



DNA was free, then it triggers the SRCHA reaction and the autonomous sticky ends assembly, generating DNA nanowires with many terminal arms containing trigger DNA replicas. These replicas can repeat the above reactions and significantly accelerate the formation of DNA nanowires, thus causing the rapid and significant enhancement of fluorescence signal (Figure S6). Therefore, a rapid signal amplified ATP assay based on the SRCHA reaction and autonomous sticky ends assembly can be successfully constructed. In order to achieve the best assay performance, the experimental conditions including the concentration of hairpin probes (P1, P2 and P3) and the length of blocking probe (BP) were optimized (Figure S7). Under the optimized experimental conditions, the sensitivity of our proposed approach for ATP detection was examined. As shown in Figure 3A, the fluorescence intensity gradually increased with the increase of ATP concentration, indicating that the SRCHA reaction was triggered by ATP and more DNA nanowires were formed at higher concentration of ATP. The calibration plot obtained for the determination of ATP with different concentrations was shown in Figure 3B, and a linear dependence of the fluorescence intensity on the ATP concentration from 20 to 1000 nM (R2=0.99) was obtained. The detection limit was calculated to be 7 nM according to the signal-to-noise ratio of three. This detection system exhibits a superior or comparative sensitivity to the reported assays but has a significantly shorter detection time (Table S3).31−39 Furthermore, to validate the selectivity of the proposed ATP strategy, several other ATP analogous molecules, such as GTP, CTP and UTP were examined as controls. As shown in Figure S8, only ATP could trigger the self-replicating system and form the DNA nanowires, which implied that the strategy we proposed here exhibited a good selectivity.

Figure 3. (A) Fluorescence spectra of the detection system in the presence of ATP with different concentrations (from bottom to top: 0, 0.02, 0.05, 0.1, 0.4, 0.7, 1, 1.5, 2, and 5 μM). (B) Relative fluorescence intensity of FAM at different concentrations of ATP. The inset shows the fluorescence responses to the ATP at low concentration from 0.02 to 1 μM. FT and F0 are the corresponding fluorescence intensity of the sensing platform in the presence and absence of ATP, respectively. Excitation wavelength was set at 490 nm and emission wavelength at 520 nm; Concentration of P1, P2 and P3: 100 nM.

CONCLUSION To sum up, we have successfully developed a novel and convenient strategy for rapid room-temperature DNA nanowires preparation based on the self-replicating CHA reaction and autonomous sticky ends self-assembly, and DNA nanowires can be rapidly formed in 20 min with the help of numerous trigger DNA replicas. Compared to the literatures reported self-replicating artificial biomaterials fabrication systems, our system does not require multiple chemical and thermal processing cycles, or the requirement of fuel strands for self-replication. Moreover, the obtained DNA nanowires have been successfully used to develop a rapid and signal amplified fluorescent sensing platform by using ATP as a model molecule. Since the aptamer and blocking probe sequences used in this strategy can be changed flexibly, thus the detection of different targets can be easily realized by simply modifying the aptamer sequences. Meanwhile, this self-replication based DNA nanostructures preparation method can be easily extended to the rapid formation of more complicated two-dimensional or three-dimensional DNA nanostructures and exhibits a great potential application in DNA nanotechnology.

DNA initiates the SRCHA reaction, the fluorescence intensity increased quickly and only took around 20 min to reach a plateau, which is much faster than that of the non-SRCHA system. Clearly, the dramatical enhancement of signal was resulted from the continuous generation of trigger DNA replicas. Besides DNA, we speculated that the non-DNA molecules also can trigger the rapid formation of DNA nanowires, and ATP was chose as the model molecule to proof this hypothesis. ATP plays an important role in energy exchanges and metabolic processes that occur in all living cells. Abnormal concentration of ATP is associated with many diseases, such as Alzheimer’s and Parkinson’s diseases.29,30 Owing to the importance of ATP in biochemical studies and clinical diagnosis, exploring rapid, sensitive and selective methods for ATP detection is thus still highly required. As shown in Scheme 1, the DNA probe, trigger-aptamer (T-A), which contains trigger DNA and ATP aptamer sequences was designed to partially hybridize to the blocking probe (BP). In the absence of ATP, there is no SRCHA reaction occurred since the trigger DNA was blocked by BP. Once ATP was added, the ATP aptamer was recognized by ATP and trigger

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Corresponding Author * E-mail: [email protected]; [email protected].

Author Contributions # H.H.

and J.D. contributed equally to this work.

Notes The authors declare no competing financial interest.

ACKNOWLEDGMENT This work was financially supported by the Fundamental Research Funds for the Central Universities (No. 20826041A4031) and National Natural Science Foundation of China (No. 21475091, 21777108 and 21775106).

Supporting Information Sequences of DNA used in the experiments, comparison of different approaches for DNA nanowires preparation, comparison of ATP detection in sensitivity and detection time, conditions optimization and selectivity of the system for ATP detection. This material is available free of charge via the Internet at http://pubs.acs.org.

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Analytical Chemistry

Scheme 1 Principle for the rapid room-temperature DNA nan-owires preparation and ATP detection based on the DNA self-replication and sticky ends self-assembly. 84x57mm (300 x 300 DPI)

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Figure 1. (A) AFM image of the resulting DNA nanowires. P1, P2 and P3 concentration: 300 nM; Trigger DNA concentration: 5 nM. (B) 1% Agarose gel electrophoresis analysis. Lane 1: P1 only; Lane 2: P1-C + P2 + P3C; Lane 3: P1-C + P2 + P3-C + trigger; Lane 4: P1 + P2 + P3; Lane 5: P1 + P2 + P3 + trigger; Lane 6: DNA ladder. P1, P1-C, P2, P3 and P3-C concentration: 300 nM; Trigger DNA concentration: 5 nM; Reaction time: 20 min. 42x74mm (300 x 300 DPI)

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