Salt-induced Assembly Transformation of DNA-AuNPs Conjugates

Jun 26, 2018 - We developed a simple method to adjust the structural transformation of DNA-gold nanoparticles conjugates from linear arrays to nanorin...
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Salt-induced Assembly Transformation of DNA-AuNPs Conjugates Based on RCA Origami: From Linear Arrays to Nanorings Zhiqing Zhang, Shuzhen Liu, Ting Zhou, Hongzhi Zhang, Fang Wang, Guodong Zhang, Xiufeng Wang, and Tingting Liu Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.8b01505 • Publication Date (Web): 26 Jun 2018 Downloaded from http://pubs.acs.org on June 27, 2018

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Salt-induced Assembly Transformation of DNA-AuNPs Conjugates Based on RCA Origami: From Linear Arrays to Nanorings Zhiqing Zhang*†, Shuzhen Liu†, Ting Zhou*, Hongzhi Zhang, Fang Wang, Guodong Zhang, Xiufeng Wang, Tingting Liu College of Science, China University of Petroleum, Qingdao 266580, China Supporting Information ABSTRACT: We developed a simple method to adjust the structural transformation of DNA-gold nanoparticles assemblies from linear arrays to nanorings by increasing salt concentrations. A DNA nanoladder constructing from RCA origami acted as templates to assemble periodic AuNPs arrays by a terminal thiol located on staple oligonucleotides. The linear AuNPs arrays could be transformed into nanorings only by changing the concentration of NaCl aqueous solution during the assembly process. It was proved that the electrostatic repulsion, being asymmetrically diminished by the high concentration of NaCl, caused the formation of nanorings architectures. KEYWORDS: Rolling circle amplification, DNA-AuNPs conjugates, DNA nanoladder, salt-induced, structure transition

INTRODUCTION Gold nanoparticles (AuNPs) assemblies with geometric control are becoming the focus of attention of scientists recently, which exhibit novel optical, electronic and magnetic properties in the field of materials application.1-3 In various assembly methods, DNA-directed assembly has shown great progress in constructing one-dimensional (1D), 2D, and 3D periodic or discrete gold nanoparticle architectures.4-10 One of the most common strategies to obtain DNA-directed assembly structures is to link DNA molecules with AuNPs through a monothiol modification and followed by conjugating the DNA-AuNPs onto DNA scaffolds through the programmable base-pairing interaction.11-15 Previous work on structural DNA nanotechnology has shown that linear DNA,16,17 DNA tiles,18,19 and DNA origami 20-23 can provide appropriate templates for binding AuNPs to form precisely periodic arrays, such as AuNP clusters, AuNP triangles, AuNP squares, AuNP cages, AuNP satellites, AuNP tubes and so on. 24-31 In all of the above studies, few studies have been given on the controllable adjustment of the AuNPs structures because of the definite DNA assembly frameworks. Meanwhile, the complicated scaffold design and the low loading yield in DNA assembly frameworks are the challenges as AuNPs conjugated templates. Herein, we provide a straightforward method to mediate the assembly of discrete structures of gold nanoparticles by mediating the concentration of the salt during the assembly process.

RESULTS AND DISCUSSION Rolling circle amplification (RCA) is an isothermal nucleic acids amplification strategy that produces long single-stranded DNA (ssDNA) from a primer by replicating a circular DNA template many times in the presence of special phi29 polymerase and deoxynucleotide triphosphates (dNTPs) (Figure 1a). 32-35 Long ssDNAs were folded into a DNA nanoladder by using two RCAamplified scaffold ssDNAs containing 63-base periodic units and

four staple strands (Figure 1b). In RCA process, DNA polymerase extends DNA from a primer by replicating a circular DNA template to yield a long ssDNA scaffold that is typically tens of hundreds of repeat units. The sequences of circular template, primer, ligation template and complementary sequence were provided in Table S1. The two long ssDNA scaffolds with 63-base periodic unit were used as the scaffolds of nanoladders, and four staple strands were designed to fix the scaffolds. The chain segments of the two longer staple strands consisted of three parts: the middle parts containing 21 bases were base-pair complementary each other to serve as the rungs of ladders, while 21 bases on both sides could hybridize with the two long sscDNA scaffolds to form duplex. Additionally, a 6-T (thymine) linker on the 5’ end of the first staple strands was modified with thiol group in order to target AuNPs. To make the nanoladder more stable, two other short staple strands with 21 bases allowed specific hybridization with the rest 21 bases of the two RCA scaffolds (Figure 1b). The RCA products and the nanoladders assemblies were analyzed by agarose gel shown in Figure S1a. The successful formation of nanoladders was confirmed by atomic force microscopy (AFM) and transmission electron microscope (TEM) imaging (Figure 1c and 1d, Figure S1b and S1c). RCA reaction products are flexible long DNA single strands. 36,37 AFM images revealed that nanoladders with relatively rigid structure were formed after DNA selfassembling. The final products are more or less similar to nanoribbons due to the image resolution. The width of the nanoladders includes the length of the rungs and the diameters of two DNA scaffolds duplexes. The rung of 21 bases that corresponded to 2 helical turns, is about 3.6×2=7.2 nm long (The length of each helical turn is about 3.6 nm). For the scaffolds duplexes, on both sides of ladder, its width is about 2.0×2=4.0 nm. So the total width of the nanoladders should theoretically be 7.2+4=11.2 nm. TEM images indicated that the nanoladders showed a width of 12.0 nm, which is consistent with the theoretical value. Because

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Figure 1. DNA origami is used to fold long scaffolds from RCA into DNA nanoladders. (a) Preparation of long, singlestranded scaffold DNA by RCA reaction. (b) Schematic illustration of the folding pathway of the single-stranded RCA product to form DNA nanoladders. (c) and (d) are AFM and TEM images of nanoladders, respectively. The length of the nanoladder is fairly long and reaches a micrometer scale, such a large ratio of length to diameter results in certain flexibility in the single nanoladder, the winding between the assemblies can therefore be clearly seen on the TEM and AFM image. Although twisted and enwound together, it still can be seen that the width of the single nanoladder in the TEM images (12 nm, Figure S1d and e) is approximately equal to the theoretical calculation value (11.2 nm). Taking the complexity of self-assembling into consideration, we firstly prepared the DNA-AuNP conjugates consisted of citrate stabilized 6 nm AuNPs that were functionalized with the first staple oligonucleotides through a terminal alkylthiol (e.g., 5’thiol-TTTTTT-staple strands). Previous studies 38-40 have shown that low-density monolayer packing of oligonucleotides lies on the AuNP’s surface after incubating them directly (Figure 2a). DNA and AuNP are highly negatively charged and cannot pack densely without electrostatic screening. However, a high concentration of NaCl is added to screen the charge, AuNPs aggregation occurs before a high density of DNA is attached. To solve this problem, NaCl solution was stepwisely added to the DNA/AuNP mixture which process is known as “salt aging”. 40 Owing to compressing the repulsive interactions between neighboring strands, higher salt concentrations generally result in higher oligonucleotide densities until steric constraints prohibit further adsorption. The oligonucleotides are prone to standing on the surface of AuNPs. Absorption spectra of thiol DNA-AuNP conjugates with different concentration of NaCl were compared with that of free

Figure 2. The conformation transition of thiol DNA-AuNPs conjugates at different concentration of NaCl. (a) Schematic of attaching thiolated DNA to negatively charged AuNPs using the salt aging method. (b) and (c) are the UV-vis absorption spectra and DLS curves of thiol DNA-AuNP conjugates at different concentrations of NaCl, respectively. AuNPs as references in Figure 2b. The wavelength values according to absorbance maximum (λmax= 512 nm) exhibited no significant differences between them, indicating that there is no obvious AuNPs aggregation after the stepwise addition of NaCl. DLS measurement was used to investigate the size change during the salt aging process. As shown in Figure 2c, the size of naked AuNPs is 5.9 nm, which is consistent with the result of absorption spectra. The diameters of the thiol DNA-AuNP conjugates are significantly higher than that of naked AuNPs, which is mainly due to the anchoring of thiol staple DNA. More interestingly, the size of DNA-AuNP conjugates is increasing gradually with the increasing of the salt concentration. These changes of size can be well explained and are in a good agreement with the mechanism mentioned above. To organize the AuNPs on the scaffold of DNA nanoladder origami, the thiol DNA-AuNP conjugates prepared above were annealed with the two long RCA molecules and the rest of three staple strands. As shown in the Figure S2, the mixture was incubated at room temperature for 16 h without extra addition of sodium chloride. The AuNP arrays based on the DNA nanoladder are 1.0-2.0 µm long in an approxi-mate parallel fashion on TEM grids (Figure 3a and Figure S3). Generally, RCA reaction in our procedure typically yields products containing dozens to hundreds of repeating sequences. The amount of the AuNPs loading on each nanoladder is about forty to one hundred, which means that there are 40-100 repeating units in one nanoladder (the average number is 70). Hence the average length of the arrays is in theoretically about 63×70×0.34=1500 nm, which is corresponding to the length of the nanoladders. Due to the electronegativity, the intense electrostatic repulsion between AuNP/AuNP and AuNPs/DNA leads to the formation of linear assemblies. The mechanism of the AuNPs connected with the DNA nanoladders was shown in Figure S2. Surprisingly, assembly structures of AuNPs arrays are

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Figure 3. (a) Linear AuNP arrays loaded on DNA nanoladders without sodium chloride. (b1) and (b2) are TEM and AFM images of AuNP nanorings embedded in DNA nanoladders at high concentration of NaCl, respectively. (c), (d) and (e) are UV-vis absorption spectra, DLS curves and Zeta potential of AuNPs/DNA nanoladders assemblies at different concentration of NaCl.

Figure 4. Mechanism of the assembly transition with the increasing of NaCl concentrations. AuNPs/DNA nanoladder linear assemblies are constructed because of intense electrostatic repulsion at low concentration of NaCl. The assemblies will be bended toward to the direction away from AuNPs because of the asymmetric force, when high concentration of NaCl solution is added. changed with addition of salt during the assembling process. The size and structure transition of DNA-AuNPs assemblies at different concentration of NaCl was shown in the Table S2. It was found that the salt urged the transformation of the linear structure into a curved structure at 100 mM NaCl (Figure S7). The homogeneous nanorings could be observed in TEM images when the NaCl concentration is raised to 300 mM (Figure 3b1 and 3b2, Figure S4 and S5). Further investigation in higher magnification, indicates that the nanorings with the diameters from 300 to 500 nm are constructed from AuNPs embedded in DNA nanoladders (Figure S4). In Figure 3c, the typical absorption spectra of nucleic acid at 260 nm are almost the same at different concentration of

NaCl. However, the absorption spectra of AuNP arrays show red shift compared to that of the pure 6nm AuNPs. Surface plasmon resonance (SPR) phenomenon would happen once the AuNPs assembled in DNA nanoladders. 41-43 Light scattering experiment shows that there are two groups of peaks in DLS graphs (Figure 3d). The value of small-sized group of peaks, corresponding to the diameters of the excess thiol DNA-AuNP conjugates, is increaseing with stepwise addition of sodium chloride. On the contrary, the hydrodynamic radius of AuNPs arrays embedded in DNA nanoladders are decreasing with NaCl concentrations increasing (see the large-sized group of peaks). The results indicate the diffuse electric double layer of AuNPs arrays are compressed as the

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addition of NaCl. 44,45 The decrease of electrostatic repulsion causes the assembly bending from linear structure to a nanoring gradually. It's worth noting that our experiments also proved that the structure transition of DNA/AuNPs assembly is reversible by decreasing of NaCl concentrations (Figure S8). Zeta potential measurements were used to estimate the stability of the assemblies at different concentration of NaCl. From Figure 3e, the zeta potential values of the assemblies at both 0 and 300 mM NaCl are comparatively high, indicating that the linear structure and the nanoring are two stable states in the process of assembling. The low potential values of the assemblies at the concentration of 10100 mM NaCl signify the structure transformation from line to nanoring can easily happen. The possible mechanism of the assembly transition is described in Figure 4. There is only one thiol staple strand in each periodic unit of DNA nanoladder. Especially, the location of sulfhydryl is not centered in the nanoladder, which results in AuNPs located on one side of the origami. At low salt concentration, intense electrostatic repulsion by the negative charges in both DNA and AuNPs maintains the linear structure of the assembly. According to the DLVO theory, electrostatic repulsion will be diminished when high concentration of salts solution is added. Thus, the assemblies will be bended toward to the direction away from AuNPs because of the asymmetric force. 46 Finally, amazing nanorings constructed from AuNPs embedded in DNA nanoladders are formed.

CONCLUSION In conclusion, we have successfully prepared ordered arrays of AuNPs by combining rolling circle amplification and DNA origami. On this base, we have demonstrated that this method provided a simple procedure to adjust the structure transformation of AuNPs-DNA assemblies from linear arrays to nanorings by only changing the concentration of the salt (NaCl) during the assembly process. Meanwhile, our experiments also proved 13 nm AuNPs can perform the similar conformational transformation instead of 6 nm AuNPs (Figure S9). The results presented in this work may be further extended towards to other nanoparticles, which could efficiently control the structure regulation and achieve versatile functionalities. Moreover, this strategy in combination with the periodic templates and nanoparticles could be very helpful for the construction of hybrid systems, which represents a rosy prospect in nanodevice applications, for example, creating salt-based nanomotors, fabricating DNA-based nanocircuits and constructing targeted cancer diagnosis, et al.

EXPERIMENTAL SECTION Materials. DNA (sequences are provided in Table S1) were obtained from Takara Bio Inc. GeneRuler 1kb Plus DNA Ladder, Phi29 DNA polymerase, Phi29 buffer, DNA T4 Ligase and dNTP were obtained from Thermo Scientific. Agarose, chloroauric acid ((HAuCl4·4H2O), ≥99.9%) was purchased from China Medicine Shanghai Chemistry Corporation. Sodium chloride, sodium citrate, ethanol and other chemical reagents were A.R grade. 6 nm AuNP were synthesized following the literature methods, 31,35 and

circular DNA templates for RCA reaction were synthesized using our previously-established protocol. 35 Instruments. UV-vis spectra were collected using a Beijing Purkinje TU-19 spectrometer at room temperature. TEM samples were prepared by depositing a drop of the sample solution onto a carbon-coated copper grid. The excess solution on the copper grid was absorbed by filter paper immediately after the deposition. Then, the copper grid was allowed to dry under ambient conditions. To stain the DNA assemblies, a drop of 1% aqueous solution of uranyl acetate was placed on the copper grid for 10 min. Then, the uranyl acetate solution was removed using a piece of filter paper, and the copper grid was dried under ambient conditions before observation. TEM characterizations were conducted on a JEM-2100 electron microscope at an accelerating voltage of 200 kV. AFM samples were prepared using the spin-coating technique. First, a drop of the solution was deposited onto a mica substrate. After the deposition, the substrate was set still for several minutes. Then, the excess solution was removed by spinning. Tapping-mode AFM measurements of the samples were conducted on a Nanoscope III microscope (Digital Instruments). The sizes of the nano-objects were analyzed using ImageJ 1.34s software. Zeta potential measurements were performed at 25 °C on a Zeta Sizer Nano ZS90 (Malvern Instrument). Dynamic light scattering (DLS) measurements were performed using a BI-200SM laser light scattering spectrometer. Before the measurements, all the solutions were filtered through 0.45 µm Millipore filters (hydrophilic Millex-LCR, PTFE) to remove dust and then kept at 25 °C for 5 min. The cumulant mode of DLS analysis was applied to obtain the ⟨Rh⟩ and PDI values. Rolling circle amplification. RCA products were synthesized in solution following our previously established protocol.30 A typical RCA reaction (200 µL) contained 50 pmol primer, 40 pmol circular template, 20 µL 10× RCA reaction buffer, dNTPs (10 µL, 1 mM) and 5 µL phi29 DNA polymerase. RCA was carried out at 30 oC for 10min and was terminated by heating at 65 o C for 10min. We characterized the size of the products by 0.5% agarose gel electrophoresis pre-stained with SYBR safe and imaged using a ChemiDoc transluminator (Bio-Rad). RCA products were purified by passing through a Nanosep 30K centrifugal device (PALL). Preparation of DNA-coated gold nanoparticles. 80 µL of 6 nm gold nanoparticle solution were measured into a tube, 10 µM thiolated DNA was added at a molar ratio of 200:1 DNA strands to particles. The mixed solution was incubated for 8 hours at 25 o C, then added different concentrations of NaCl into the solution, the PBS concentration is fixed at 12 mM. Let the solution sit overnight at room temperature. The size of the nanoparticle were determined by UV-vis absorption and measured the absorbance at 520 nm. Preparation of AuNP assemblies. The above solution was centrifuged at 14000 rcf for 15 min in presence of ethanol, and then the supernatant was discarded. The pelleted nanoparticles were re-suspended in 500 µL water. Repeat the centrifuge step two times, and the nanoparticles were re-suspended in 100 µL

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water finally. 100 µL of 0.5 µM DNA-coated gold nanoparticles were mixed with 5 µL of 0.1 µM DNA origami solution(ratio of scaffold/staple is 1/160) (Figure S2), then different volumes of NaCl solutions were added to adjust the NaCl concentrations. Solutions were annealed at 25°C for 16 hours. Time has a very significant effect on the structure of the assembly (Figure S6). Solutions of origami–nanoparticle conjugates must be made fresh before use. The size and the morphology of AuNP assemblies are measured by DLS and TEM.

ASSOCIATED CONTENT Supporting Information Experimental procedures, DNA sequences, PAGE bands and more TEM and AFM images. This material is available free of charge via the Internet at http://pubs.acs.org.

AUTHOR INFORMATION Corresponding Author *E-mail: [email protected], *E-mail: [email protected]

ORCID Zhiqing Zhang: 0000-0002-6854-8430 Author Contributions † These authors contributed equally.

Notes The authors declare no conflict of interest.

ACKNOWLEDGMENT This work is supported by the National Natural Science Foundation of China (21703286, 21603276, 21303267), the Natural Science Foundation of Shandong Province, China (ZR2017MB045, ZR2016BL14), the Fundamental Research Funds for the Central Universities and the scholarship of China Scholarship Council.

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Salt-induced Assembly Transformation of DNA-AuNPs Conjugates Based on RCA Origami: From Linear Arrays to Nanorings Zhiqing Zhang, Shuzhen Liu, Ting Zhou, Hongzhi Zhang, Fang Wang, Guodong Zhang, Xiufeng Wang, Tingting Liu

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