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Different Stability of DNA Origami Nanostructure between on Interface and in Bulk Solution Yi Chen, Ping Wang, Yan Xu, Xiaodi Li, Yuanjie Zhu, Ying Zhang, Jun Zhu, Gang Huang, and Dannong He ACS Appl. Bio Mater., Just Accepted Manuscript • DOI: 10.1021/acsabm.8b00379 • Publication Date (Web): 09 Oct 2018 Downloaded from http://pubs.acs.org on October 9, 2018
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Different Stability of DNA Origami Nanostructure Between on Interface and in Bulk Solution Yi Chen,§a Ping Wang, §*b Yan Xu,b Xiaodi Li,c Yuanjie Zhu, c Ying Zhang, b Jun Zhu, b Gang Huang,*c Dannong He*ab School of Materials Science and Engineering, Shanghai Jiao Tong University, Shanghai, 200240, China. National Engineering Research Center for Nanotechnology, Shanghai, 200241, China. Tel: 86-21-34291286-8035; Email:
[email protected] c Shanghai University of Medicine &Health Sciences, Shanghai, 201318, China KEYWORDS: DNA origami stability interface bulk solution a b
ABSTRACT: DNA origami possesses a promising prospect in the fields including cancer therapy, enhancing catalytic activity, controllable nanorobot, etc. However, all the brilliant performances are based on its structural integrity, which is a big challenge for this technology. In this paper, we investigated the effects of interface on the stability of DNA origami and found that with the treatments like heating, pH fluctuation, reducing ionic strength, the origami on interface always showed better stability than that in bulk solution because of the restriction imposed by the bond between solid surface and origami. Our results have a great potential to inspire the researchers to develop a complex which can provide origami an interface to strengthen its stability.
Introduction DNA origami, which can be easily synthesized by annealing the premixed solution containing a long single strand (M13mp18) and many short strands called staples, has always been considered the most promising template for precise nano assembly. Advantages of DNA origami include easy editing of its shape by changing the sequence of staples, flexible modification of diverse nanoparticles almost at arbitrary position, naturally excellent biocompatibility etc. which have attracted a great number of researchers in various fields. For example, DNA origami is considered as one of the best carriers of doxorubicin for targeted cancer therapy which can even combine with cellular imaging.1-7 Currently, a report shows that it is also capable of drug resistance circumvention when mixed with gold nanorod.8 Besides, many nano-systems templated by DNA origami show dramatic single-molecule surface Raman scattering9, which can be utilized in the design of highsensitivity sensors.10-12 What more impressive is that the electrical circuit may be self-assembled in a nanometer scale with the guidance of DNA origami, which is much smaller than the current SiO2 circuit and could be a giant leap for the information industry.13 For the sake of this, the electrical properties of DNA have been investigated and nanowires based on DNA origami were also reported.14-16 However, all the brilliant performances of DNA origami are based on its structural integrity, thus a lot of work have been done to investigate its stability property under diverse conditions such as treated by heat,17-18 immersed in organic solvents like hexane, ethanol and toluene,19 incubated in cell lysate and so on 20-21. After these, the origami all retain their structures well. On the other hand, the presence of crystallization buffer,22 chaotropic agents,23 insufficient ionic strength2425 and too high or too low pH19, 26 will lead to its degradation.
Accordingly, approaches to increase the stability of DNA origami through graphene encapsulation or crosslinking have been demonstrated.27-29 Though the rigidity of DNA origami has enabled it high performance in many fields, there is still a higher demand of their stability. For example, the origami loaded with doxorubicin is expected to keep intact within the tumor for a longer time to get a slow release effect. Looking into the results of stability study, it kept intact after severe treatment in Kim’s paper19 but did not behave that robust as Ramakrishnan23 reported. One point easy to ignore is that the origami in the former experiment was deposited on the silicon substrate while the latter was immersed in the solution. We suspect that if the existence of interface between origami and silicon wafer resulted in this difference, yet there are not any research papers on this aspect so far. Hereafter, we shall report our study on the stability of DNA triangle origami structure influenced by the solid-liquid interface. Temperature, pH and ionic strength fluctuating in a wide range and the morphology of origami deposited on the mica or dispersed in solution was recorded. These processing conditions were chosen because of their relevance to the actual challenge when the origami was employed as the templates such as modification for catalysis performance and controlled release of drug in photothermal cancer therapy. The results comply with our hypothesis that the origami has better stability on interface than in bulk solution (Figure 1), which may provide theoretical support to the strength of DNA origami.
Experimental Section Materials, synthesis of DNA origami, deposition of DNA origami onto mica are the same with our previous work.30
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Figure 1. DNA origami showed different stability between
on interface and in bulk solution
Thermal stability of DNA origami on the interface. Sample was fixed on the stage of environment controllable atomic force microscope (Nanonavi E-Sweep, Seiko Inc, Japan), changed environment temperature and lasted 10 minutes after stabilization, then monitored the morphology of origami. Probes were purchased from Olympus. Thermal stability of DNA origami in solution. 20 μl DNA origami solution was immersed into heated water of 40 ℃, 60 ℃, 80 ℃ or placed in a refrigerator set to -20℃, -40 ℃, 60 ℃ and -80 ℃, and kept 10 minutes after stabilization. At last deposited 2.5 μl solution on mica with the same procedure showed before. Influence of pH, ionic strength to DNA origami on the interface. 10 μl solution of different pH or ionic strength was dropped onto the mica surface with deposited DNA origami for 3 minutes, then washed by 70 μl 9/1 (v/v) ethanol/water solution for 3 seconds, dried by N2. All the solution used for
pH experiment was freshly prepared. For example, pH 4 solution dropped on the interface was prepared in this ratio: 200 μl 10× Mg2+ TAE buffer, 1790.8 μl Q water, and 9.2 μl HCl (36.0%~38.0%). We do advise researchers to correct the solution before use. Influence of pH, ionic strength to DNA origami in solution. 18 μl solution was added to 2 μl DNA origami solution to get a final mixture of desired pH or ionic strength. Then deposited 2.5 μl of it onto mica.
Results and Discussion Triangular DNA origami was used for this assay due to its relatively higher stability, clearer topography and better performance than the other shape origami. The length of each side is about 120 nm and the height is around 2 nm. The base sequence of each staple is developed by Rothemund31 and has been adopted by many researchers. All the DNA strands can be purchased directly, and very regular triangular origami can be easily obtained by annealing (Figure 2A).
High temperature treatment is often used in origami templated fabrication such as heating the deposited DNA origami to a certain temperature during chemical vapor deposition and controlling drug release within the cell
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when choosing photothermal therapy, so we first investigated the thermal stability of DNA origami under the effect of interface. Environment controllable atomic force microscope was used for the analysis of origami on interface. The origami was deposited on the freshly cleaved mica surface and then the environment temperature was changed to a certain value rapidly. After 10 minutes incubation, its morphology was recorded. From the images in Figure 2 (top), we can see that shrinkage and bend appeared from the structure side at 60 ℃ and some origami had lost the characteristic of hollow structure, when heated to 80 ℃, this phenomenon became more obvious. However, most origami still kept a clear triangular shape and its height got a small increase within 1 nm. In solution, the origami was not so stable as on interface. When incubating the DNA triangle at 40 ℃ for 10 minutes, it did not destroy the geometric but lead a uniform expansion of the three sides and a smaller cavity of the triangle. At 60 ℃, the origami all got strange distortions and hardly any of it looked like a triangle, we can see that small pieces separated from the single origami appeared on the substrate. At 80 ℃, only some finally separated pieces remained, the density of residuals decreased as well. Though the morphology of origami changed a lot as temperature increased, its height was stable at about 2 nm, close to that on interface. We also tested the origami at low temperature with a gradient of 20 ℃ until -80 ℃, it all maintained a very regular appearance both on interface and in solution (Figure S1). DNA nanostructures were usually used as a nanorobot with a switch controlled by pH value32-33, therefore we evaluated the stability of DNA origami when pH changed. AFM images are shown in Figure 3. It’s clear that more acidic or alkaline bring more serious change of the origami shape. On interface, most origami kept intact at pH 10, yet at pH 4, only portion of it remained a fuzzy triangle shape. Changing pH to 11 or 3, it totally melted. In solution, the origami shape became more serious than that on interface in the same pH group. At pH 10, significant shrinkage occurred and their internal cavity disappeared, and at pH 4, the structure totally degraded and we can only recognize some residuals that may come from one single origami. When pH came to 11, there was very little aggregates left, and at pH 3, more irregular residuals were observed with the height were little lower than others. It seems like the single chains detached from the origami but did not diffuse far from their original positions, which leads a threedimensional stacking and degenerated into flat aggregate with the height reduced by about 1 nm. Both groups at pH 12 and pH 2 were tested. In such extreme conditions, only little residual remained on interface while nothing left in solution (Figure S2).
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Figure 2. AFM images of DNA origami under different heating temperature. Image a, b, c and d represent different heating temperature of 20 ℃,40 ℃, 60 ℃ and 80 ℃ respectively. Image A, B, C, D represent the same heating temperature with the image of corresponding lowercase letter but in solution.
Figure 3. AFM images of DNA origami under different pH incubation. Image a, b, c and d represent different pH of 3, 4, 10 and 11 on interface respectively. Image A, B, C, D represent the same pH with the image of corresponding lowercase letter but in solution.
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case letter but in solution.
Figure 4. AFM images of DNA origami under different Mg2+
concentration incubation. Image a and b represent different Mg2+ concentration of 0.1× and 0.5× respectively. Image A and B represent the same Mg2+ concentration with the image of corresponding lowercase letter but in solution.
As a polyanion, DNA origami can easily disintegrate due to internal electrostatic repulsion if there were no cation to balance it. So the cation concentration is an important factor that shall be taken into account in all aspects of processing. We changed the Mg2+ concentration of the solution to 0.1× or 0.5× to determine whether there was difference between origami on interface and in solution. As Figure 4 shows, under 0.5×Mg2+ incubation, the morphology of origami on interface was well maintained with little expansion of three sides but cavity disappeared in solution. When the Mg2+ concentration decreased to 0.1×, much origami on interface showed similar appearance to the origami in 0.5×Mg2+ solution, the others melted and merged into bigger aggregates. In solution, the origami dispersed into a round residual and small “particles” appeared on the substrate. The height of origami in all four groups did not change greatly. We also tested the stability of origami under UV irradiation. UV is a common method used for remove organic compound from samples. From the images (Figure 5) we can see that even after 30 minutes irradiation, DNA origami still maintained a regular triangular shape and shrinkage seemed not happen both in solution and on interface. However, a very obvious height reduction appeared in the interface group and the reduced value is proportional to the irradiation time. When irradiated for 5 min on interface, its height decreased to about 1 nm, and for 30 min it was almost less than 0.5 nm, quarter of its original height. Yet height of origami in the solution changed little. Discussion As a three-dimensional nanostructure maintained by the hydrogen bond between single chains, DNA origami is easy to denature under excessive temperature, over-acidic or alkaline conditions. But in our experiment, the DNA origami in solution and on interface showed different resistance to the environment fluctuation. We assume that the interface between DNA origami and mica sheet surface should be to blame for this. We all know that the mica tablet is a very suitable base for the morphology observation of DNA origami because the interaction between these two hydrophilic materials is strong enough to keep origami integral after rinsing and drying. When DNA origami is deposited on the mica surface, each part of it is subject to the gravitational force from its adjacent mica, unlike the gravitational force from the dynamic solution, it is constant and stronger.
Figure 5. AFM images of DNA origami under UV irradiation. Image a and b represent irradiation time of 5 min and 30 min respectively. Image A and B represent the same UV irradiation time with the image of corresponding lower-
When temperature increases, pH changes or Mg2+ concentration decreases, the hydrogen bond between double strands cleavages, and the produced single chains tend to diffuse to form a homogeneous system. The origami in solution all appears irregular and even nothing remains without the limitation of mica base, while on interface it all shows better morphology except for the UV group, espe-
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cially the origami on 80 ℃ heating mica still keeps a clear triangular shape which should be due to the lack of origami-solution interface compared with the other two groups (pH and Mg2+ concentration). Changing the pH, origami suffers not only the cleavage of hydrogen bond but also the hydrolysis of phosphodiester bonds and glycosidic bonds, so we can see that only very little residuals remained at pH 2 or pH 12. And because of the better alkali resistance of DNA, the origami survives better in alkali than acidic conditions when the concentration of H+ and OH- is the same. When Mg2+ concentration decreases, the most difference between the origami in solution and on interface is that the diffusion path and resistance. In solution, the denatured origami takes a spherical diffusion while on interface it can only diffuse towards the solution side. With the additional imitation imposed by the mica base, the origami on interface behaved worse than temperature group, but better than pH group due to the lack of hydrolysis effect. The UV group is the only one that received the reversible result that the origami in solution showed higher stability. In our experiment the UV light intensity was set the same, but the actual intensity that the origami in solution received should be lower than that on interface because of the barrier of container wall and solution. Besides, origami in solution does Brownian movement, therefore the angle between UV light and origami plane had been changing all the time, the DNA cannot get a sustained and stable UV exposure like the structure on interface which caused a covalent attachment of adjacent pyrimidine nucleosides and a clear height reduction as a result. We speculate that the interaction between origami and mica surface do affect the movement in molecule level that caused this difference between interface group and solution group. Considering the change of origami a whole “reaction”, it involves two steps that influenced by the interface: one is collision of activated molecules, another is diffusion of reaction products. For the physical reaction like heating and Mg2+ ion concentration fluctuation, the diffusion of single short chains separated from the origami was greatly slow down because of the limitation of interface. Then the whole reaction process seems to be blocked. And for the chemical reaction like pH change, the collision between activated bond in origami and H+ or OH- was almost half of the origami in bulk solution. In the interface side, the ion concentration is very low comparing with the other liquid side, so the effective collision almost can be overlooked. This may inspire us that if we can give bind the origami with one compatible surface such as phospholipid film, the origami may retain a longer time at a severe condition. Conclusion
In summary, we tested the interface effect on DNA origami stability under different physical and chemical treatment. The results confirmed our hypothesis that the origami is more stable on interface than in bulk solution, especially in not-so extreme conditions. It may be due to the restriction imposed by the mica surface, so it is reasonable to speculate that if giving DNA origami an affinity interface, its stability in diverse circumstance may receive a considerable promotion. ASSOCIATED CONTENT Supporting Information Additional AFM images of triangular DNA origami. This material is available free of charge via the Internet at http://pubs.acs.org.
AUTHOR INFORMATION Corresponding Author *E-mail:
[email protected] ACKNOWLEDGMENT This work was supported by National Key R&D Program of China (2016YFA0201200), Shanghai outstanding technical leaders plan (16XD1424700), China National Science Funds for Young Scholars (21403156) The AFM tests was done in the Analytical Test center of Shanghai Jiao Tong University and National Engineering Research Center of Nanotechnology, we greatly appreciate the guidance for the test provided by Huiqin Li and Ying Zhang.
REFERENCES (1) Yan, J.; Hu, C. Y.; Wang, P.; Zhao, B.; Ouyang, X. Y.; Zhou, J.; Liu, R.; He, D. N.; Fan, C. H.; Song, S. P. Growth and Origami Folding of DNA on Nanoparticles for High-Efficiency Molecular Transport in Cellular Imaging and Drug Delivery. Angew. Chem. Int. Ed. 2015, 54 (8), 24312435. (2) Kong, F.; Zhang, H. B.; Qu, X. M.; Zhang, X.; Chen, D.; Ding, R. H.; Makila, E.; Salonen, J.; Santos, H. A.; Hai, M. T. Gold Nanorods, DNA Origami, and Porous Silicon Nanoparticle-functionalized Biocompatible Double Emulsion for Versatile Targeted Therapeutics and Antibody Combination Therapy. Adv. Mater. 2016, 28 (46), 10195-10203. (3) Ora, A.; Jarvihaavisto, E.; Zhang, H. B.; Auvinen, H.; Santos, H. A.; Kostiainen, M. A.; Linko, V. Cellular Delivery of Enzyme-Loaded DNA Origami. Chem. Commun. 2016, 52 (98), 14161-14164. (4) Zhang, Q.; Jiang, Q.; Li, N.; Dai, L. R.; Liu, Q.; Song, L. L.; Wang, J. Y.; Li, Y. Q.; Tian, J.; Ding, B. Q.; Du, Y. DNA Origami as an In Vivo Drug Delivery Vehicle for Cancer Therapy. Acs Nano 2014, 8 (7), 66336643. (5) Zhuang, X. X.; Ma, X. W.; Xue, X. D.; Jiang, Q.; Song, L. L.; Dai, L. R.; Zhang, C. Q.; Jin, S. B.; Yang, K. N.; Ding, B. Q.; Wang, P. C.; Liang, X. J. A Photosensitizer-Loaded DNA Origami Nanosystem for Photodynamic Therapy. Acs Nano 2016, 10 (3), 3486-3495. (6) Xia, Z.; Wang, P.; Liu, X.; Liu, T.; Yan, Y.; Yan, J.; Zhong, J.; Sun, G.; He, D. Tumor-Penetrating Peptide-Modified DNA Tetrahedron for Targeting Drug Delivery. Biochemistry 2016, 55 (9), 1326-1331.
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(7) Zhao, Z.; Fu, J.; Dhakal, S.; Johnson-Buck, A.; Liu, M.; Zhang, T.; Woodbury, N. W.; Liu, Y.; Walter, N. G.; Yan, H. Nanocaged Enzymes with Enhanced Catalytic Activity and Increased Stability Against Protease Digestion. Nat Commun 2016, 7, 10619. (8) Song, L. L.; Jiang, Q.; Liu, J. B.; Li, N.; Liu, Q.; Dai, L. R.; Gao, Y.; Liu, W. L.; Liu, D. S.; Ding, B. Q. DNA Origami/Gold Nanorod Hybrid Nanostructures for the Circumvention of Drug Resistance. Nanoscale 2017, 9 (23), 7750-7754. (9) Zhao, M. Z.; Wang, X.; Ren, S. K.; Xing, Y. K.; Wang, J.; Teng, N.; Zhao, D. X.; Liu, W.; Zhu, D.; Su, S.; Sho, J. Y.; Song, S.; Wang, L. H.; Chao, J.; Wang, L. H. Cavity-Type DNA Origami-Based Plasmonic Nanostructures for Raman Enhancement. Acs Appl. Mater. Interfaces 2017, 9 (26), 21942-21948. (10) Prinz, J.; Heck, C.; Ellerik, L.; Merk, V.; Bald, I. DNA Origami Based Au-Ag-Core-Shell Nanoparticle Dimers with Single-molecule SERS Sensitivity. Nanoscale 2016, 8 (10), 5612-5620. (11) Puchkova, A.; Vietz, C.; Pibiri, E.; Wunsch, B.; Paz, M. S.; Acuna, G. P.; Tinnefeld, P. DNA Origami Nanoantennas with over 5000-Fold Fluorescence Enhancement and Single-Molecule Detection at 25 mu M. Nano Lett. 2015, 15 (12), 8354-8359. (12) Zhan, P.; Wen, T.; Wang, Z.-g.; He, Y.; Shi, J.; Wang, T.; Liu, X.; Lu, G.; Ding, B. DNA Origami Directed Assembly of Gold Bowtie Nanoantennas for Single-Molecule Surface-Enhanced Raman Scattering. Angew. Chem. Int. Ed. 2018, 57 (11), 2846-2850. (13) Livshits, G. I.; Stern, A.; Rotem, D.; Borovok, N.; Eidelshtein, G.; Migliore, A.; Penzo, E.; Wind, S. J.; Di Felice, R.; Skourtis, S. S.; Cuevas, J. C.; Gurevich, L.; Kotlyar, A. B.; Porath, D. Long-Range Charge Transport in Single G-Quadruplex DNA Molecules. Nature Nanotech. 2014, 9 (12), 1040-1046. (14) Magro, M.; Baratella, D.; Jakubec, P.; Zoppellaro, G.; Tucek, J.; Aparicio, C.; Venerando, R.; Sartori, G.; Francescato, F.; Mion, F.; Gabellini, N.; Zboril, R.; Vianello, F. Triggering Mechanism for DNA Electrical Conductivity: Reversible Electron Transfer between DNA and Iron Oxide Nanoparticles. Adv. Funct. Mater. 2015, 25 (12), 18221831. (15) Watson, S. M. D.; Pike, A. R.; Pate, J.; Houlton, A.; Horrocks, B. R. DNA-Templated Nanowires: Morphology and Electrical Conductivity. Nanoscale 2014, 6 (8), 4027-4037. (16) Teschome, B.; Facsko, S.; Schonherr, T.; Kerbusch, J.; Keller, A.; Erbe, A. Temperature-Dependent Charge Transport through Individually Contacted DNA Origami-Based Au Nanowires. Langmuir 2016, 32 (40), 10159-10165. (17) Rajendran, A.; Endo, M.; Katsuda, Y.; Hidaka, K.; Sugiyama, H. Photo-Cross-Linking-Assisted Thermal Stability of DNA Origami Structures and Its Application for Higher-Temperature Self-Assembly. J. Am. Chem. Soc. 2011, 133 (37), 14488-14491. (18) Wei, X.; Nangreave, J.; Jiang, S.; Yan, H.; Liu, Y. Mapping the Thermal Behavior of DNA Origami Nanostructures. J. Am. Chem. Soc. 2013, 135 (16), 6165-6176.
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(19) Kim, H.; Surwade, S. P.; Powell, A.; O’Donnell, C.; Liu, H. Stability of DNA Origami Nanostructure under Diverse Chemical Environments. Chem. Mater. 2014, 26 (18), 5265-5273. (20) Chen, H. R.; Li, R. X.; Li, S. M.; Andreasson, J.; Choi, J. H. Conformational Effects of UV Light on DNA Origami. J. Am. Chem. Soc. 2017, 139 (4), 1380-1383. (21) Mei, Q.; Wei, X.; Su, F.; Liu, Y.; Youngbull, C.; Johnson, R.; Lindsay, S.; Yan, H.; Meldrum, D. Stability of DNA Origami Nanoarrays in Cell Lysate. Nano Lett. 2011, 11 (4), 1477-1482. (22) Wang, D. M.; Da, Z. R.; Zhang, B. H.; Isbell, M. A.; Dong, Y. C.; Zhou, X.; Liu, H. J.; Heng, J. Y. Y.; Yang, Z. Q. Stability Study of Tubular DNA Origami in the Presence of Protein Crystallisation Buffer. Rsc Adv. 2015, 5 (72), 58734-58737. (23) Ramakrishnan, S.; Krainer, G.; Grundmeier, G.; Schlierf, M.; Keller, A. Structural Stability of DNA Origami Nanostructures in the Presence of Chaotropic Agents. Nanoscale 2016, 8 (19), 10398-10405. (24) Kielar, C.; Xin, Y.; Shen, B. X.; Kostiainen, M. A.; Grundmeier, G.; Linko, V.; Keller, A. On the Stability of DNA Origami Nanostructures in Low-Magnesium Buffers. Angew. Chem. Int. Ed. 2018, 57 (30), 94709474. (25) Varnai, P.; Timsit, Y. Differential Stability of DNA Crossovers in Solution Mediated by Divalent Cations. Nucleic Acids Res. 2010, 38 (12), 4163-4172. (26) Fang, W. N.; Fan, C. H.; Liu, H. J. Effect of pH on the Stability of DNA Origami. Acta Polym. Sin. 2017, (12), 1993-2000. (27) Lermusiaux, L.; Bidault, S. Increasing the Morphological Stability of DNA-Templated Nanostructures with Surface Hydrophobicity. Small 2015, 11 (42), 5696-5704. (28) Matković, A.; Vasić, B.; Pešić, J.; Prinz, J.; Bald, I.; Milosavljević, A. R.; Gajić, R. Enhanced Structural Stability of DNA Origami Nanostructures by Graphene Encapsulation. New J. Phys. 2016, 18 (2), 025016. (29) Zhang, D.; Paukstelis, P. J. Enhancing DNA Crystal Durability through Chemical Crosslinking. Chembiochem 2016, 17 (12), 11631170. (30) Chen, Y.; Wang, P.; Liu, Y.; Liu, T.; Xu, Y.; Zhu, S. S.; Zhu, J.; Ye, K.; Huang, G.; He, D. N. Stability and Recovery of DNA Origami Structure With Cation Concentration. Nanotechnology 2018, 29 (3). (31) Rothemund, P. W. Folding DNA to Create Nanoscale Shapes and Patterns. Nature 2006, 440 (7082), 297-302. (32) Wu, N.; Willner, I. pH-Stimulated Reconfiguration and Structural Isomerization of Origami Dimer and Trimer Systems. Nano Lett. 2016, 16 (10), 6650-6655. (33) Wang, P.; Xia, Z. W.; Yan, J.; Liu, X. W.; Yao, G. B.; Pei, H.; Zuo, X. L.; Sun, G.; He, D. N. A Study of pH-Dependence of Shrink and Stretch of Tetrahedral DNA Nanostructures. Nanoscale 2015, 7 (15), 6467-6470.
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