DNAzyme-Controlled Cleavage of Dimer and Trimer Origami Tiles

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DNAzyme-Controlled Cleavage of Dimer and Trimer Origami Tiles Na Wu, and Itamar Willner Nano Lett., Just Accepted Manuscript • DOI: 10.1021/acs.nanolett.6b00789 • Publication Date (Web): 02 Mar 2016 Downloaded from http://pubs.acs.org on March 3, 2016

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DNAzyme-Controlled Cleavage of Dimer and Trimer Origami Tiles Na Wu and Itamar Willner* Institute of Chemistry, The Center for Nanoscience and Nanotechnology, The Hebrew University of Jerusalem, Jerusalem 91904, Israel

ACS Paragon Plus Environment

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ABSTRACT: Dimers of origami tiles are bridged by the Pb2+-dependent DNAzyme sequence and its substrate, or by the histidine-dependent DNAzyme sequence and its substrate to yield the dimer T1-T2 and T3-T4, respectively. The dimers are cleaved to monomer tiles in the presence of Pb2+-ions or histidine as triggers. Similarly, trimers of origami tiles are constructed by bridging the tiles with the Pb2+-ion-dependent DNAzyme sequence and the histidine-dependent DNAzyme sequence and their substrates yielding the trimer T1-T5-T4. In the presence of Pb2+ions and/or histidine as triggers, the programmed cleavage of trimer proceeds. Using Pb2+ or histidine as trigger cleaves the trimer to yield T5-T4 and T1 or the dimer T1-T5 and T4, respectively. In the presence of Pb2+-ions and histidine as triggers, the cleavage products are the monomer tiles T1, T5 and T4. The different cleavage products are identified by labeling the tiles with 0, 1 or 2 streptavidin labels and AFM imaging.

KEYWORDS: DNA; Nanotechnology; Logic gate; Histidine; Pb2+-ion; AFM

The programmed self-assembly of 2D or 3D origami nanostructures provides a revolutionary method for the high-yield synthesis of pre-designed structures and shapes.1,2 The method is based on the computer-aided folding of long, single-stranded, DNAs, e.g., M13 phage, with hundreds of short oligonucleotide staple strands to form the desired origami shapes. Also, within the process of the assembly of the origami structures, the pre-designed positioning of functional protruding capturing strands is feasible, thus allowing the precise anchoring of additional components, such as proteins,3 nanoparticles4 or carbon nanotubes5 onto the origami scaffolds. Not surprising, origami nanostructures play a key role in the rapidly developing area of DNA


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nanotechnology.1c, 4a, 6 Different applications of origami structures were suggested, including, for example, the precise positioning of plasmonic nanoparticles and the assembly of plasmonic antennas,7 the assembly of chiral plasmonic nanostructures,8 the use of origami as a functional surface for the activation of enzyme cascades,9 the implementation of origami surfaces for programmed operation of DNA machines, such as “walkers”,10 and the use of origami frameworks as organizing units for probing, at real-time, chemical reactions on DNA, using fast scanning AFM experiments.11,12 The base-sequence encoded in DNA structures has been widely-applied to develop stimuli-responsive DNA structures that allowed the construction of DNA switches13 and DNA machines,14 such as “tweezers”,15 “walkers”16 or switchable DNA catenanes17 rotaxanes.18 Different external triggers such as fuel/anti-fuel strands,16b, 19 pH,15b, 20 formation of aptamerligand complexes21 or light22 have been applied to operate these DNA devices. Also stimuliresponsive origami units were implemented to assemble reconfigurable and switchable systems.23 For example, origami subunits were used for the self-assembly of photoresponsive microcapsules that were unlocked to release nanomaterial loads upon irradiation.24 Similarly, origami units were used to construct tweezers assemblies that were triggered between open and closed by fuel/anti-fuel strands,25 nanochambers that were reconfigured by fuel/anti-fuel strands,26 and origami-clamps loaded with antibodies and locked by aptamer strands, were unlocked and released the load through the formation of aptamer-ligand complexes.27 Also, origami hexagons modified at their edges with photoresponsive oligonucleotide tethers were used as functional units for the reversible light-induced formation and dissociation of programmed oligo-origami structures.28


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Catalytic nucleic acids (DNAzymes or ribozymes) attract substantial interest as materials mimicking protein-based enzymes.29 One specific class of DNAzymes are sequence-specific metal-ion (e.g., Mg2+, Zn2+, Cu2+) or cofactor (e.g., amino acids) dependent DNAzymes.30,31 These DNAzymes were widely applied as catalytic labels for amplified sensing,32 catalytic units for logic gate operations and the design of computing circuitries,33 catalytic labels for gating and unlocking drug-loaded nanoparticles34 and catalysts for programmed synthesis.35 Recently, the supramolecular structure of the Zn2+--dependent DNAzyme and its substrate was embedded in origami frames, and the catalytic functions of the DNAzyme were monitored at the singlemolecule level.36 In the present study, we functionalize specific edges of origami tiles with nucleic acid tethers that dictate the assembly of dimer or trimer origami-tiles bridged by specific DNAzyme sequences (the Pb2+-dependent DNAzyme or the histidine-dependent DNAzyme). We demonstrate the programmed specific cleavage of the oligomeric origami tiles. The systems represent the first step toward “origami chemistry”, where origami tiles act as analogs for atoms that assemble into molecules that reveal dictated chemical reactivities. Figure 1(A) depicts the assembly of the Pb2+-responsive origami dimer consisting of tile T1 and T2. The tile T2 is labeled with streptavidin that binds to a protruding biotinylated strand. The streptavidin is introduced into the origami surface to facilitate the imaging of the different tiles used in the study. The edges of T1 and T2 are modified with the free single strands L1 and L2. Bridging of the tiles is achieved by the substrate strand S1 that includes complementary domains x, x’ to strand L1 and L2 and the ribonucleobase-functionalized sequence k that provides the specific substrate domain for binding of the Pb2+-dependent DNAzyme sequence C1. In the presence of Pb2+-ions, the DNAzyme is activated, resulting in the cleavage of the origami dimers T1-T2. Figure 1(B), panel I, depicts a representative AFM image of the resulting origami-dimers


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(blue arrows) and impurities of the non-bridged monomers (yellow arrows). The enlarged image of the dimer is shown as an inset at the bottom left of the image. Figure 2(B), panel II, depicts the representative image of the origami dimers sample after treatment with Pb2+-ions, 5mM, for a time-interval of 12 hours. Again, the origami dimers are marked with blue arrows, whereas the single tiles are marked with a yellow arrow. The insert in panel II, upper part-left, shows the enlarged pattern of the separated tiles. Evidently, the results demonstrate the rich population of dimeric tiles prior to the addition of Pb2+-ions and an enriched population of the single tiles, after treatment with Pb2+-ions. Figure 1(C) depicts the quantitative analysis of the origami-dimers before and after treatment of the system with Pb2+-ions. Evidently, prior to the addition of Pb2+ions ca. 80% of the tiles exist as dimers, while after treatment of the system with Pb2+-ions, only ca. 30% of the tiles exist as dimers, implying that the Pb2+-ion-stimulated cleavage of the dimeric tiles occurred (For the detailed analysis of large-area domains see Figure S1, supporting information). The cleavage of the dimers T1-T2 is specific and proceeds only in the presence of Pb2+-ions, Figure S2, demonstrating the selectivity of the DNAzyme to Pb2+-ions. Figure 2(A) depicts the schematic construction of the dimer origami, stimuli-responsive histidine-dependent DNAzyme. The dimer is composed of the tiles T3 and T4. The tile T3 is labeled, through a biotinylated, protruding tether, with one streptavidin unit, and the tile T4 is labeled by two streptavidin units linked to two protruding strands associated with T4. The edges of T3 and T4 are functionalized with the capturing strands L3 and L4. The substrate strand S2 includes domains y and y’, complementary to the anchoring strands L3 and L4, respectively. The domain l associated with S2 provides the specific ribonucleo-base substrate sequence for cleavage by the histidine-dependent DNAzyme sequence C2. The tiles T3 and T4 are then bridged by S2 capture that binds C2 to yield the T3-T4 origami tiles dimer. In the presence of the histidine


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cofactor, the substrate S2 is cleaved, leading to the separation of the dimer. Figure 2(B), panel I, depicts the AFM image of the T3-T4 identified by the streptavidin labels associated with the respective tiles. The dimer units are marked with red arrows, whereas the single origami tiles are marked with yellow arrows. Figure 2(B), panel I, inset (right upper corner) depicts the enlarged origami-dimer labeled with the respective streptavidin units. The yield of origami-dimer structures is ca. 70%, Figure 2(C). Treatment of the origami-dimer mixture with histidine results in the high yield ca. 80% cleavage of the dimer structures. Figure 2(B), panel II depicts the AFM image of the system generated by subjecting the origami-dimers to histidine, 5mM, 12 hours reaction time-interval. Evidently, most of the structures are single origami tiles labeled by the respective streptavidin units (see inset). The population of dimers in the system decreased to ca. 10% (For a detailed analysis of large-area domains see Figure S3, supporting information). The cleavage of the T3-T4 origami dimers by the histidine-dependent DNAzyme is selective, and the treatment of the C2/S2-bridged dimers with other amino acids, e.g., alanine, cysteine, tyrosine or D-histidine, did not lead to the cleavage of the dimer structures. Finally, Figure 3(A) depicts the assembly of the trimer composed of the origami tile T1T5-T4 that is bridged by the Pb2+-dependent DNAzyme sequence C1, and the substrates S1 that bridges the tiles T1 and T5 and the histidine-dependent DNAzyme sequence C2 that bridges the tiles T5 and T4 in the presence of the substrate S2. Figure 3(B) shows the AFM image of the trimer T1-T5-T4 and the yield of the trimer structure (45%). Figure 3(B) top-right presents an enlarged image of the trimer nanostructure with the respective streptavidin labels. Treatment of the trimer with Pb2+-ions is anticipated to separate the T1-T5 tile of the trimer leading to the formation of single T1 tiles and dimeric T5-T4 tiles. In turn, subjecting the origami-trimer to the histidine cofactor cleaves off the tile T4 from the dimer T1-T5. Finally, treatment of the trimer-


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origami structure with Pb2+ ions and histidine separates all tiles and yield individual tiles composed of T1, T4 and T5. Since the tiles T4 and T5 are labeled with two streptavidin and one streptavidin units, respectively, the nature of the resulting dimers T1-T5 or T5-T4 can be identified by the streptavidin units associated with the trimer-origami-tile structures. The mixture consists of intact trimers ca. 45%, dimers T1-T5 bridged by the Pb2+-dependent DNAzyme, 15%, dimers T5-T4 bridged by the histidine-dependent DNAzyme, 7%, and single non-bridged tiles of T1, T5 and T4, 7%, 8% and 13%, respectively (For a detailed analysis of large-area domains see Figure S4, supporting information). Treatment of the mixture with Pb2+-ions, Figure 3(C), panel I, results in a significant decrease in the population of the trimers (a decrease from 45% to 14%). The dimers composed of the histidine-bridged DNAzyme tiles, T5-T4, increase from the population of ca. 7% to ca. 25% upon treatment of the system with Pb2+-ions and the population of single T1 increased significantly from the value of 7% for in the original trimer solution to the value corresponding to 30%, Panel I. The percentage of the other single tiles is unchanged. These results are consistent with the selective Pb2+-ion-triggered cleavage of the bridging units linking the T1 and T5 tiles in the trimer, a process that reduces significantly the population of the trimer, and enriches the content of the dimers T5-T4 and increases the content of single tile T1. Figure 3(C), panel II, shows the AFM image of the origami structures generated by treatment of the original trimer-origami solution with the histidine cofactor. The content of the trimer origami structures decreased from ca. 45% to ca. 7% after treatment with histidine. At the same time the content of the dimeric origami structures bridged by the Pb2+-dependent DNAzyme sequence increased from a content of ca. 15% to a value that corresponds to 40%, and concomitantly the content of the individual T4 tiles increased from 13% to 22%. These results are consistent with the selective, histidine-induced cleavage of the trimer origami structure to form the T1-T5 dimers


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bridged by the Pb2+-dependent DNAzyme sequence and the separation of the T4 tiles from the trimer. Figure 3(C), panel III, depicts the AFM image of the origami structures observed upon treatment of the trimer origami structures with the Pb2+-ions and the histidine cofactor. The population of the trimers drops from the value of ca. 45% before the addition of the Pb2+-ions and histidine, Figure 3(B), to a minute content of 4%. Also, the content of dimers T1-T5 and T5T4 is minute 8% and 7%, respectively. In turn, high contents of the monomer tiles T1 (30%), T5 (27%) and T4 (24%) are observed. These results are consistent with the cleavage of three-tile origami systems to the separated individual tiles. One may consider the Pb2+-ions and histidine as inputs that operate on the three-tile origami scaffolds, to yield an “AND” logic gate. The structures generated in the presence of the two inputs provide the output of the logic operation. In conclusion, the present study has introduced the first step toward “origami chemistry” where origami tiles provide structural analogs to atoms that assemble into origami-based “molecules” that undergo programmed dictated reactions. The use of nanoparticles as functional components mimicking atoms attracts recent research efforts,37 and, thus, the use of origami tiles as building units of reactive “origami molecules” seems as a further interesting path to follow. The rich tool-box of switchable and catalytic nucleic acid structures suggests that complex oligomeric origami nanostructures undergoing controlled cleavage or ligation functions, and exhibiting different chemical reactivity patterns, such as substitution, isomerization or rearrangement of tiles, may be envisaged.

Experimental Section The DNA origami tiles were assembled in a TAE buffer solution consisting of Tris buffer 20 mM that included acetic acid 20 mM, EDTA 1 mM, magnesium acetate, 12.5 mM, pH = 8.0.


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Single-stranded M13mp18 phage DNA (New England Biolabs), 5 nM was dissolved in the buffer solution and the short staple strands (unmodified staple strands, functionalized specific edge staple strands and biotinylated staple strands) (Integrated DNA Technologies), 50 nM was added to the M13mp18 buffer solution. The mixture was heated to 95˚C in a thermal cycler and then allowed to cool down to 20˚C at a rate of 0.1˚C every 10 seconds. The respective origamitile samples were purified using 100 KD MWCO centrifuge filters to eliminate the excess of unreacted staple strands. The separately-prepared respective origami tiles were introduced into the buffer solution and the respective DNAzyme sequence and its substrate were added to the origami tiles mixture at a molar ratio of 1:40:20 for the origami tiles: DNAzyme sequence: substrate, respectively. The resulting mixture was annealed from 45˚C to 15˚C at a rate of 0.1˚C/minute for the assembly of the dimers and at a rate of 0.05˚C/minute for the assembly of the origami trimers. For the identification of the different tiles, biotinylated staples associated with the respective tiles were modified with one or two streptavidin units. The cleavage of the origami dimers linked by the Pb2+-dependent DNAzyme sequence was performed in a 25 mM Tris-acetate buffer solution that included NaCl 300 mM, CaCl2 10 mM, pH = 6.0. Pb(OAc)2, 5 mM was added to the solution and the cleavage of the dimers was allowed to proceed for 12 hours at 30˚C. The cleavage of the dimers linked by the histidinedependent DNAzyme sequence was performed in the TAE buffer solution, pH = 8.0, that included KCl, 200 mM, in the presence of histidine, 5 mM, at 30˚C for a time-interval of 12 hours. The cleavage of the trimer-origami tiles was performed in 25 mM Tris-acetrate buffer solution that included NaCl 300 mM, CaCl2 10 mM, KCl 200 mM, pH = 6.0, using Pb(OAc)2


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and/or histidine, each 5 mM. The mixture was allowed to react for 12 hours at 30˚C. The AFM imaging of the different origami samples was performed using a Multi-mode Nanoscope VIII AFM (Bruker) and DNP-S probes (Bruker). A drop, 2 µl, of the respective origami-tile was deposited on freshly cleaned mica and allowed to adsorb for 5 minutes. The imaging was performed by covering the surface with the TAE buffer solution.


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Figure 1.

(A) Assembly of two origami tiles T1 and T2 by the Pb2+-dependent

DNAzyme sequence, and the schematic separation of the origami tiles, in the presence of Pb2+-ions, via the cleavage of the inter-tile bridges by the Pb2+-ion-dependent DNAzyme. The tile T2 is labeled with a streptavidin (bright spot) for identification. (B) AFM images corresponding to: Panel (I) – The origami dimers (blue) prior to the DNAzyme-induced cleavage. Panel II – The origami tiles generated in the presence of the Pb2+-dependent DNAzyme that consists mostly of monomer tile units (yellow). Scale bars correspond to 500nm. (C) Statistical analysis of the content of the dimer origami tiles before the addition of Pb2+-ions (red) and after the interaction of the system with Pb2+-ions (blue).


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Figure 2.

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(A) Assembly of the two origami tiles T3 and T4 by the histidine-dependent

DNAzyme sequence and the schematic separation of the origami tiles, in the presence of histidine, via the cleavage of the inter-tile bridges by the histidine-dependent DNAzyme. The tile T3 is labeled with a streptavidin unit and the tile T4 is labeled with two streptavidin units for identification (bright spots). (B) AFM images corresponding to:


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Panel I – The origami dimers (red) prior to the DNAzyme-induced cleavage. Panel II – The origami tiles generated in the presence of the histidine-dependent DNAzyme that consists mostly of monomer tile units (yellow). Scale bars correspond to 500nm. (C) Statistical analysis of the content of the dimer origami tiles before the addition of histidine (red) and after the interaction of the system with histidine (blue).


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Figure 3.

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(A) Assembly of the three-tiles origami structures T1 – T5 – T4, crosslinked

by the Pb2+- and histidine-dependent DNAzyme sequences, and the programmed


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cleavage of the trimer in the presence of Pb2+-ions and/or histidine. (B) Left-AFM image of the three-tiles origami structures, T1 – T5 – T4 , bridged by the Pb2+- and histidinedependent DNAzyme sequences, prior to cleavage. Right: Statistical analysis of the population of the three-tile origami structure and the accompanying origami structures (dimers, monomers). (C) Panel I – AFM image and statistical analysis of the different origami constituents formed by the cleavage of the three-tile origami structure with Pb2+ions. Panel II – AFM image and statistical analysis of the different origami constituents formed by the cleavage of the three-tile origami structure with histidine. Panel III – AFM image and statistical analysis of the different origami constituents formed by the cleavage of the three-tile origami structure with Pb2+-ions and histidine. Scale bars correspond to 500nm.

ASSOCIATED CONTENT Supporting Information. The detailed statistical analysis of large-area domains of the different origami structures, accompanied by AFM images provided and DNA sequences. This material is available free of charge via the Internet at http://pubs.acs.org.

AUTHOR INFORMATION Corresponding Author * E-mail: [email protected] Tel: +972-2-6585272. Fax: +972-2-6527715.


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Funding Sources This research is supported by the MULTI FET-OPEN EU project.

Notes The authors declare no competing financial interest. ACKNOWLEDGMENT This research is supported by the MULTI FET-OPEN EU project.


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For TOC Only

Programmed cleavage of a trimer tile origami nanostructure interlinked by the Pb2+- dependent DNAzyme and the histidine-dependent DNAzyme is demonstrated in the presence of Pb2+-ions and/or histidine as inputs.


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DNAzyme-Controlled Cleavage of Dimer and Trimer Origami Tiles

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