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Cite This: ACS Appl. Bio Mater. 2019, 2, 2988−2993
Catalytic Formation of Luminescent Complex Clusters Based on Autonomous Strand Exchange Reaction of DNA Yusuke Kitamura,* Akihiro Nozaki, Rie Ozaki, Yousuke Katsuda, and Toshihiro Ihara* Division of Materials Science and Chemistry, Faculty of Advanced Science and Technology, Kumamoto University, 2-39-1 Kurokami, Chuo-ku, Kumamoto 860-8555, Japan
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ABSTRACT: DNAs can act as flexible interfaces for arranging particular reactant partners such as biomolecules and other functional molecules modified on DNAs in close proximity to increase their effective concentrations. Here, we focused on dynamic programmability of the DNA structure based on sequence-specific autonomous strand exchange reactions triggered by an initiator DNA, i.e., DNA circuits, to achieve a catalytic reaction providing physical and chemical signals. For analytical applications, DNA-templated formation of luminescent lanthanide (Ln) complexes was combined with the described amplification system. An appropriate microenvironment for the accommodation of a lanthanide ion [Ln(III)] was constitutively generated by ethylenediaminetetraacetic acid (a chelator) and 1,10phenanthroline (a sensitizer) tethered to the ends of assembled DNAs to form a luminescent complex. For DNA circuits, we used hybridization chain reaction and catalytic hairpin assembly to construct linear and cruciform DNA structures, respectively, as scaffolds of Ln cluster formation. Both systems were designed for complex formation at every site where the ends of constituent DNAs faced each other on the DNA scaffolds by addition of an initiator. After optimization of the reaction conditions, amplified luminescence of a Tb(III) complex was obtained, which implies formation of a large number of complexes after addition of the initiator DNA. The formation of lanthanide complex clusters can be simply governed by the thermodynamics of duplex hybridization, which can be rationally controlled by wellestablished parameters such as the DNA length and sequence, concentration, temperature, and ionic strength. The emission color of the Ln cluster can be easily changed by choosing Ln ions with the desired color. The principle behind this technique is simple; therefore, it can be applied to various catalytic DNA-templated reactions by replacing lanthanide complex ligands by other functional molecules and materials. KEYWORDS: DNA circuit, luminescent lanthanide complex, DNA-templated reaction, metal complex clusters, functional nanomaterials
1. INTRODUCTION Among various molecules that form self-assemblies, nucleic acids are widely recognized as being one of the most versatile and robust materials because of their sequence fidelity and ease of chemical synthesis and modification and because they can be duplicated by using the polymerase chain reaction. DNA has attracted considerable attention as a useful scaffold for arranging and distributing molecules at desired positions. The precise introduction of functional molecules into these scaffolds can provide unique DNA-based materials and interfaces such as luminescent molecular sensors,1−5 conductive wires,6−11 chiral selective catalysts,12−15 and microenvironments for DNA-templated reactions.16−19 For several years, we have been studying DNA-templated reactions such as metal complex formation,20−22 photochemical reactions,23−25 supramolecular inclusion complex formation,26,27 and allosteric assembly of DNA conjugates.28 In a series of studies, we found that luminescent lanthanide (Ln) complexes could be successfully formed by sequence-specific © 2019 American Chemical Society
hybridization between a template and two DNA conjugates carrying ethylenediaminetetraacetic acid (EDTA) and 1,10phenanthroline (phen) as metal-capturing and sensitizer moieties, respectively. The two ligands were modified at each end of the DNAs, which were designed to be complementary to the tandem sequences of the template. Therefore, these ligands faced each other on the template to form an appropriate microenvironment for accommodation of Ln ions, e.g., Tb(III) and Eu(III).20,21 Stoichiometric formation of Ln complexes was confirmed at both the junction sites in tandem duplexes21 and the terminus of stem in the molecular beacon-like DNA nanodevice.22 One luminous lanthanide complex (product) is obtained per template in those simple DNA-templated reactions. Received: April 17, 2019 Accepted: May 27, 2019 Published: May 27, 2019 2988
DOI: 10.1021/acsabm.9b00326 ACS Appl. Bio Mater. 2019, 2, 2988−2993
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amplification techniques for the detection of biomolecules.29 In this system, kinetically stable DNA hairpins assemble to yield long nicked double helixes via a cascade of hybridizations triggered by the addition of an initiator strand. Here, we tried to form a lanthanide complex at each of the junction sites between the constituent DNAs in the HCR product to provide a lanthanide complex wire (linear Ln cluster) (Figure 1). Four
Recent progress in DNA circuit techniques, which rely on autonomous repeating strand exchange, has highlighted the dynamic programmability of the DNA structure. Such circuits, e.g., hybridization chain reaction (HCR),29−31 catalytic hairpin assembly (CHA),32−35 and entropy-driven catalytic strand exchange,36,37 have attracted much interest for use in robust molecular programs that can execute dynamic actions such as catalytic signal transduction38−43 and in molecular machines.44−46 Their simple working principles and versatility motivated us to use our functional DNA conjugates in DNA circuit techniques to achieve catalytic signal amplification. In this study, we achieved the catalytic formation of luminescent Ln complex clusters on linear or cruciform DNA scaffolds, which were formed by autonomous strand exchange reactions triggered by an initiator. Four hairpin DNAs carrying metal chelators (EDTA) and sensitizers (phen) on both ends were used as scaffold constituents. Luminescent complexes, i.e., EDTA−Ln(III)−phen, were formed at all the junction sites between the constituent DNAs of the assemblies, and Ln complex clusters were generated.
2. EXPERIMENTAL SECTION 2.1. Materials. DNAs were purchased from the Japan Bio Services Co., Ltd. (Saitama, Japan) or synthesized with an NTS-M2-MX synthesizer (Nihon Techno Service Co., Ltd., Ibaragi, Japan) from dimethoxytrityl phosphoramidite purchased from Glen Research (VA, USA). All other reagents were purchased and used without purification. DNAs were purified by reversed-phase high-performance liquid chromatography (RP-HPLC) with an LC-2000plus inert system (JASCO) equipped with an ODS column [InertSustain C18, 4.6 mm (φ) × 150 mm (w), GL Science, Tokyo, Japan]. The DNAs and DNA conjugates were analyzed by matrix-assisted laser desorption ionization mass spectrometry (MALDI-TOF MS) with an AutoFlex II mass spectrometer (Bruker, MD, USA) in negative-ion mode with 3-hydroxypicolinic acid as a matrix. 2.2. Preparation of DNA Conjugates. DNA conjugates carrying EDTA and phen at both ends were synthesized by a previously reported method.20 Briefly, the amino groups at both ends of a DNA were coupled with EDTA anhydride or an active ester of phen to obtain EDTA- (H1, H2, H5, and H7) and phen-modified DNA conjugates (H3, H4, H6, and H8), respectively. The synthesized conjugates were purified by RP-HPLC and identified by MALDITOF MS. 2.3. Nondenaturing Gel Electrophoresis. The HCR products were evaluated as follows. The DNA conjugates (1 μM H1, H2, H3, and H4) were incubated in 10 mM phosphate buffer (pH 7.0) containing 1 M NaCl in the absence and presence of an initiator (0.1 to 0.5 μM) at 25 °C for 24 h. In the case of cruciform products, 200 nM H5, H6, H7, and H8 were incubated in 10 mM HEPES buffer (pH 7.0) containing 0.1 M NaCl in the absence and presence of an initiator (20 nM to 1 μM) at 0 °C for 20 h. Gel electrophoresis was performed on 10% or 15% polyacrylamide nondenaturing gel and run in 1 × TBE buffer (pH 7.4) at 4 °C under a constant current of 20 mA for 1 h. After gel electrophoresis, the gel was stained with Gel Star and visualized with ATTO printgraph AE-6933FXES. 2.4. Luminescence Measurements. Luminescence measurements were performed with a JASCO FP-8500 spectrofluorometer equipped with a Peltier thermal controller, under N2 purging to prevent moisture condensation on the cell. A high-speed chopper was used to obtain time-resolved emission spectra, with a xenon lamp as the excitation light source (280 nm).
Figure 1. Schematic diagram of catalytic formation of linear luminescent lanthanide complex clusters.
hairpin DNA conjugates carrying EDTAs (H1 and H2) or phens (H3 and H4) at both ends of the DNAs were synthesized as constituents of a lanthanide complex wire. Each hairpin consists of a 6-nt (nucleotides) loop, 12-bp (base pairs) stem, and 6-nt sticky end to provide a toehold for strand exchange with hairpin opening (Table S1). All four conjugates are kinetically trapped in identical hairpin structures and retain their monomer secondary structures, even when they are mixed together in the same solution until the initiator strand is added. The sequences of these hairpin DNAs are designed so that EDTAs and phens are in proximity at each boundary site on the resulting duplexes. The HCR efficiency was assessed by gel electrophoresis in the presence of fewer amounts of initiator compared with each hairpin (Figure S1). The products were observed as smear bands in the high-molecular-weight region as previously reported.29 Increasing the initiator (Ih) concentration resulted in higher consumption of monomer hairpins. Slight leakage from the reaction in the absence of Ih was observed for incubation at 25 °C, but this was almost completely suppressed at 15 °C. Metal-centered luminescence from Ln(III) complexes is widely exploited in bioassays. The long luminescence lifetime
3. RESULTS AND DISCUSSION 3.1. Formation of Ln Complex Wire (Linear Cluster). The HCR, which was first reported by Pierce in 2004, is regarded as one of the most useful signal transducing and 2989
DOI: 10.1021/acsabm.9b00326 ACS Appl. Bio Mater. 2019, 2, 2988−2993
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those at 25 °C because of temperature-dependent quenching processes such as phonon-assisted back transfer or ligand− metal charge transfer quenching.47,48 On the basis of these results, subsequent experiments were performed at 15 °C. The emission intensities in the presence of 100 mM or 1 M NaCl were compared to determine the optimum salt concentration. A solution containing 100 mM NaCl gave a better contrast between the emission intensities for the samples with and without Ih (Figure 2c). This means that nonspecific leakage during the HCR was lower, and promotion of the HCR efficiency by Ih was higher, at 100 mM NaCl. In addition, the emission intensities increased significantly when the buffer solution was changed from sodium phosphate (pH 7.0) to HEPES (pH 7.0). In sodium phosphate buffer solution, the abundant phosphate ions compete with EDTA for Tb(III), and some of the Tb(III) is removed from the microenvironment of binary ligands consisting of EDTA and phen (Figure 2d). The effects of the initiator concentration were assessed, and the results are shown in Figure 3a. Decreasing the
(up to the millisecond range) enables the use of time-gating techniques to separate the short-lived (nanosecond range) fluorescence background present in biological samples. In addition, large Stokes shifts minimize crosstalk between excitation light and emission signals, and narrow emission bands in the NIR to UV range enable performance of multicolor assays. Because of shielding by the outer 5s and 5p orbitals, the 4f orbitals of lanthanides are not involved in bonding with ligands. Their emission wavelengths are therefore scarcely affected by the ligand field and surrounding environments; this leads to unique emission colors that depend on the metal center.47,48 We evaluated the formation of lanthanide complex clusters by measuring their luminescence. Time-gated luminescence spectroscopy gave the typical emission spectrum of the Tb(III) ion [maximum at 546 nm (5D4 → 7F5)] with almost no background signal in the presence of H1, H2, H3, H4, and Ih (Figure 2a). The time courses of the emission intensities were monitored after addition of Ih at 15 and 25 °C (Figure 2b). The emission intensity reached a plateau faster at 25 °C than at 15 °C, which implies a higher HCR rate at 25 °C, but the emission intensities at 15 °C were higher than
Figure 3. (a) Time courses of emission intensity changes in the absence (gray) and presence of 0.1 μM (blue), 0.25 μM (green), and 0.5 μM (red) Ih. (b) Comparison of emission intensities of lanthanide complexes formed on tandem duplex and HCR products in the presence of 0.5 μM template DNA and Ih, respectively. Excitation wavelength was 280 nm. Concentrations of each hairpin and Tb(III) were 1 μM and 5 μM, respectively. Measurements were performed in 10 mM sodium phosphate buffer (pH 7.0) containing 100 mM NaCl at 15 °C.
concentration of Ih lowered the reaction rate because fewer seeds were available for HCR initiation. In the presence of 0.5 μM Ih, the emission intensity with HCR amplification was ca. six times larger than that without HCR amplification (Figure 3b). Although only one Ln complex was formed at a junction site through tandem duplex formation without the HCR, many complexes were formed at every junction site on the polymer of HCR product, i.e., a Ln complex wire. 3.2. Formation of Ln Complex Clusters on Cruciform DNA. The CHA technique has enabled great progress in the engineering of dynamic actions such as catalytic formation of the specific DNA structures, cross-catalytic duplex formation with exponential kinetics, and DNA walkers.32 Here, we combined this technique with DNA-templated metal complexation to achieve catalytic formation of Ln complex clusters composed of four complexes formed at each terminus of a cruciform DNA scaffold. As shown in Figure 4, we synthesized four hairpin DNA conjugates with EDTAs (H5 and H7) or phens (H6 and H8) at both ends. Each hairpin consists of a 7nt loop, 14-bp stem, and 7-nt sticky end as a toehold for the strand exchange reaction. The sequences are listed in Table S2. On addition of Ic to a mixed solution of the conjugates, in which they all exist as kinetically stable hairpins, H5 is opened
Figure 2. (a) Time-resolved emission spectrum of solution containing H1, H2, H3, H4 (1 μM in each case), and Tb(III) (5 μM) in the presence of 0.5 μM Ih. Excitation wavelength was 280 nm. Measurements were performed in 10 mM HEPES buffer (pH 7.0) containing 100 mM NaCl. Delay time: 50 μs. Gate time: 2 ms. (b) Time courses of emission intensity changes in the presence (solid curve with filled circles) and absence (dotted curve with open circles) of Ih at 25 °C (black) and 15 °C (red). Concentrations of each hairpin, Ih, and Tb(III) were 1 μM, 0.5 μM, and 5 μM, respectively. Measurements were performed in 10 mM sodium phosphate buffer (pH 7.0) containing 1 M NaCl. (c) Time courses of emission intensity changes in the presence (solid curve with filled squares) and absence (dotted curve with open squares) of Ih at 15 °C. Concentrations of each hairpin, Ih, and Tb(III) were 1 μM, 0.5 μM, and 5 μM, respectively. Measurements were performed in 10 mM sodium phosphate buffer (pH 7.0) containing 100 mM (red) or 1 M NaCl (black). (d) Time courses of emission intensity changes in the presence (solid curve with filled squares) and absence (dotted curve with open squares) of Ih at 15 °C. Concentrations of each hairpin, Ih, and Tb(III) were 1 μM, 0.5 μM, and 5 μM, respectively. Measurements were performed in 10 mM sodium phosphate buffer (pH 7.0) containing 100 mM (red) or 1 M NaCl (black). 2990
DOI: 10.1021/acsabm.9b00326 ACS Appl. Bio Mater. 2019, 2, 2988−2993
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Figure 4. Schematic diagram of catalytic formation of lanthanide complex clusters generated on cruciform DNA scaffolds.
by hybridization with the initiator strand (Ic) via toeholdmediated strand exchange to form the first intermediate, Ic− H5. The newly exposed accessible region on H5 then opens a second hairpin, H6, to form a second intermediate complex, Ic−H5−H6. In the same way, Ic−H5−H6 opens H7 to form a third intermediate, Ic−H5−H6−H7, and it opens H8 to form the cruciform complex, H5−H6−H7−H8, with release of Ic. Ic is recycled for initiation of the next hybridization cycle. In the cruciform structure, EDTAs and phens are placed proximately at each of the ends of the four stems in the cruciform DNA complex. On addition of Ic, the emission intensities of Tb(III) complexes rapidly increased in the presence of H5, H6, H7, and H8. Temperature-dependent quenching of Tb(III) ions was also observed in this system. The emission intensities gradually decreased with increasing temperature from 0 to 25 °C (Figure S2). The NaCl concentration was optimized on the basis of the emission intensities in the presence and absence of Ic (Figure 5a−c). Although a higher emission intensity was obtained in the presence of Ic, a moderate emission was also observed in the absence of Ic in 1 M NaCl. In 0.02 M NaCl, a significant decrease in the emission intensity was observed, even in the presence of Ic, which resulted in a lower signal contrast. Ic might not bind efficiently to open the hairpin structure of H5 and therefore would not act as an effective initiator of the CHA reaction. Both a high emission intensity with Ic and low nonspecific leakage without Ic were achieved in the presence of 0.1 M NaCl. As shown in Figure 5d, the addition of Ic led to a clear green emission, typical of a Tb(III) complex, which could be recognized even by the naked eye. On the basis of these results, the salt concentration was fixed at 0.1 M in subsequent experiments. Catalytic formation of cruciform DNAs was confirmed by gel electrophoresis. A clear band from the cruciform DNA complex, H5−H6−H7−H8, was observed in the presence of Ic (Figure 6). A faint band from cruciform DNA, which was formed as a result of nonspecific leakage, was observed in the absence of Ic. This shows that almost all the conjugates can retain their metastable hairpin structures even after incubation for 20 h. Other minor bands were also observed in the presence of Ic. These arise from formation of kinetically entrapped intermediates and metastable assembly.
Figure 5. Time courses of emission intensity changes in the absence (black dotted curves with open circles) and presence (red solid curves with filled circles) of Ic. Excitation wavelength was 280 nm. Concentrations of each hairpin, Ic, and Tb(III) were 0.2 μM, 0.2 μM, and 0.8 μM, respectively. Measurements were performed in 10 mM HEPES phosphate buffer (pH 7.0) containing (a) 0.02 M, (b) 0.1 M, and (c) 1 M NaCl at 0 °C. (d) Fluorescence images of solutions of H5−H6−H7−H8 with (left) and without (right) Ic after incubation at 0 °C for 1 h. Excitation source was a low-pressure mercury lamp (6 W).
Figure 6. Native polyacrylamide gel electrophoresis (15%) analysis of cruciform DNA scaffolds. Lane 1: H5 + Ic (0.2 μM); lane 2: H5 + H6 + Ic (0.2 μM); lane 3: H5 + H6 + H7 + Ic (0.2 μM); lane 4: H5 + H6 + H7 + H8 (0.2 μM); lane 5: H5 + H6 + H7 + H8 + Ic (0.02 μM); lane 6: H5 + H6 + H7 + H8 + Ic (0.1 μM); lane 7: H5 + H6 + H7 + H8 + Ic (0.2 μM); lane 8: H5 + H6 + H7 + H8 + Ic (0.4 μM); lane 9: H5 + H6 + H7 + H8 + Ic (1 μM). Each hairpin was annealed individually and mixed with (final concentration of each: 0.2 μM) and incubated in 10 mM HEPES containing 0.1 M NaCl (pH 7.0) for 20 h at 0 °C in the presence or absence of Ic.
Figure S3 shows that the rate of catalytic formation of the Ln complex clusters on cruciform DNAs was affected by the initiator concentration, similarly to the case for linear Ln clusters, and decreased in proportion to the concentration decrease. The reaction rate in this system was faster than that for linear cluster formation. While the amplification factor (defined as the ratio of emission intensities with/without 100 nM initiator) for a cruciform system was ca. 8.5 after incubation for 30 min, formation of a linear scaffold progressed slowly, resulting in a lower emission ratio (ca. 1.8). The final 2991
DOI: 10.1021/acsabm.9b00326 ACS Appl. Bio Mater. 2019, 2, 2988−2993
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ACS Applied Bio Materials product in the cruciform Ln cluster system is a tetramer at most. In contrast, the strand exchange reactions for linear Ln clusters take place successively on one of the ends of the growing high-molecular-weight DNA polymer to propagate the Ln wire. The formation of cruciform Ln clusters is more favorable than linear cluster formation, mainly because of its lower steric hindrance and better diffusion, which increase the efficiency of effective collisions for the strand exchange reaction. We can design and control the formation of luminescent lanthanide clusters on the basis of knowledge of DNA hybridization thermodynamics and kinetics.
Toshihiro Ihara: 0000-0001-6236-7818 Author Contributions
Y. Kitamura and T. Ihara wrote the paper with contributions from A. Nozaki, and R. Ozaki conducted the experiments and analyzed the data. Y. Katsuda discussed experimental work and reviewed the work. All authors have given approval to the final version of the manuscript. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This research was partly supported by a grant-in-aid for Scientific Research (C) (No. 16K05819 to Y. Kitamura) and grant-in-aid for Scientific Research (B) (No. 15H03829 to T. Ihara) from the Ministry of Education, Culture, Sports, Science, and Technology, Japan. We thank Helen McPherson, PhD, from Edanz Group (www.edanzediting.com/ac) for editing a draft of this manuscript.
4. CONCLUSIONS We achieved catalytic formation of luminescent lanthanide complex clusters on linear and cruciform DNA scaffolds generated by DNA circuits, via autonomous assembling of hairpin DNAs. A set of four hairpin DNAs was used for making both types of DNA scaffold. Two of the hairpins carried EDTAs on both ends, and the other two carried phens. Only the directions (polarities) of the hairpin sequences were different for each of the hairpin sets of the two DNA scaffolds. For the linear scaffold, each of the hairpin DNAs divergently propagated to form a long duplex. In contrast, each of the hairpin DNAs gave convergent binding to form a closed cruciform tetramer. The Ln complex clusters showed the typical luminescence properties intrinsic to Ln complexes, i.e., long lifetimes, large Stokes shifts, and unique emission spectra. Each complex was formed at every junction site of the constituent DNAs on a linear Ln wire and at the four terminuses of a cruciform duplex to build up Ln complex clusters, which provided intense emission spots because of their collective effect. Cruciform Ln clusters enable rapid labeling because of their good formation kinetics. Ln wires are high-molecular-weight polymers; therefore, although they have moderate formation kinetics, their diffusion is suppressed. This gives high spatial resolution in imaging techniques for monitoring specific signals from target organelles or events in cells. The emission color of the Ln cluster can be easily changed by using Ln ions of the desired color. Because it is based on a simple principle, this technique can be used in various catalytic DNA-templated reactions by replacing the lanthanide complex ligands with other functional molecules and materials.
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ABBREVIATIONS Ln, lanthanide; EDTA, ethylenediaminetetraacetic acid; phen, 1,10-phenanthroline; HCR, hybridization chain reaction; CHA, catalytic hairpin assembly; RP-HPLC, reversed-phase high-performance liquid chromatography; MALDI-TOF MS, matrix-assisted laser desorption ionization mass spectrometry; TBE, tris-borate-EDTA; HEPES, 2-[4-(2-hydroxyethyl)piperazin-1-yl]ethanesulfonic acid
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(1) Tyagi, S.; Kramer, F. R. Molecular beacons: Probes that fluoresce upon hybridization. Nat. Biotechnol. 1996, 14, 303−308. (2) Ikeda, S.; Kubota, T.; Yuki, M.; Okamoto, A. Exciton-controlled hybridization-sensitive fluorescent probes: Multicolor detection of nucleic acids. Angew. Chem., Int. Ed. 2009, 48, 6480−6484. (3) Kashida, H.; Takatsu, T.; Fujii, T.; Sekiguchi, K.; Liang, X.; Niwa, K.; Takase, T.; Yoshida, Y.; Asanuma, H. In-stem molecular beacon containing a pseudo base pair of threoninol nucleotides for the removal of background emission. Angew. Chem., Int. Ed. 2009, 48, 7044−7047. (4) Gaspar, I.; Hövelmann, F.; Chamiolo, J.; Ephrussi, A.; Seitz, O. Quantitative mRNA imaging with dual channel qFIT probes to monitor distribution and degree of hybridization. ACS Chem. Biol. 2018, 13, 742−749. (5) Pianowski, Z.; Gorska, K.; Oswald, L.; Merten, C. A.; Winssinger, N. Imaging of mRNA in live cells using nucleic acidtemplated reduction of azidorhodamine probes. J. Am. Chem. Soc. 2009, 131, 6492−6497. (6) Tanaka, K.; Tengeiji, A.; Kato, T.; Toyama, N.; Shionoya, M. A discrete self-assembled metal array in artificial DNA. Science 2003, 299, 1212−1213. (7) Tanaka, K.; Clever, G. H.; Takezawa, Y.; Yamada, Y.; Kaul, C.; Shionoya, M.; Carell, T. Programmable self-assembly of metal ions inside artificial DNA duplex. Nat. Nanotechnol. 2006, 1, 190−194. (8) Clever, G. H.; Carell, T. Controlled stacking of 10 transitionmetal ions inside a DNA duplex. Angew. Chem. Int. Ed 2007, 46, 250− 253. (9) Liu, S.; Clever, G. H.; Takezawa, Y.; Kaneko, M.; Tanaka, K.; Guo, X.; Shionoya, M. Direct conductance measurement of individual metallo-DNA duplexes within single-molecule break junctions. Angew. Chem., Int. Ed. 2011, 50, 8886−8890. (10) Schreiber, R.; Luong, N.; Fan, Z.; Kuzyk, A.; Nickels, P. C.; Zhang, T.; Smith, D. M.; Yurke, B.; Kuang, W.; Govorov, A. O.; Liedl, T. Chiral plasmonic DNA nanostructures with switchable circular dichroism. Nat. Commun. 2013, 4, 1−6.
ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsabm.9b00326. Sequences of DNAs, native polyacrylamide gel electrophoresis (10%) of HCR product, time courses of emission intensity changes for the CHA system in the presence and absence of initiator at different temperature, and time courses of emission intensity changes in the absence and presence of several concentrations of initiator (PDF)
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REFERENCES
AUTHOR INFORMATION
Corresponding Authors
*E-mail:
[email protected] (Y. Kitamura). *E-mail:
[email protected] (T. Ihara). ORCID
Yusuke Kitamura: 0000-0001-6157-6546 2992
DOI: 10.1021/acsabm.9b00326 ACS Appl. Bio Mater. 2019, 2, 2988−2993
Article
ACS Applied Bio Materials (11) Teschome, B.; Facsko, S.; Schönherr, T.; Kerbusch, J.; Keller, A.; Erbe, A. Temperature-dependent charge transport through individually contacted DNA origami-based Au nanowires. Langmuir 2016, 32, 10159−10165. (12) Boersma, A. J.; Klijn, J. E.; Feringa, B. L.; Roelfes, G. DNAbased asymmetric catalysis: Sequence-dependent rate acceleration and enantioselectivity. J. Am. Chem. Soc. 2008, 130, 11783−11790. (13) Boersma, A. J.; Coquiere, D.; Geerdink, D.; Rosati, F.; Feringa, B. L.; Roelfes, G. Catalytic enantioselective syn hydration of enones in water using a DNA-based catalyst. Nat. Chem. 2010, 2, 991−995. (14) Wang, C.; Li, Y.; Jia, G.; Liu, Y.; Lu, S.; Li, C. Enantioselective Friedel-Crafts reactions in water catalyzed by a human telomeric Gquadruplex DNA metalloenzyme. Chem. Commun. 2012, 48, 6232− 6234. (15) Park, S.; Ikehata, K.; Watabe, R.; Hidaka, Y.; Rajendran, A.; Sugiyama, H. Chem. Commun. 2012, 48, 10398−10400. (16) Gartner, Z. J.; Tse, B. N.; Grubina, R.; Doyon, J. B.; Snyder, T. M.; Liu, D. R. DNA-templated organic synthesis and selection of a library of macrocycles. Science 2004, 305, 1601−1605. (17) He, Y.; Liu, R. A sequential-displacement strategy enables efficient six-step DNA-templated Synthesis. J. Am. Chem. Soc. 2011, 133, 9972−9975. (18) McKee, M. L.; Milnes, P. J.; Bath, J.; Stulz, E.; Turberfield, A. J.; O’Reilly, R. K. Multistep DNA-templated reactions for the synthesis of functional sequence controlled oligomers. Angew. Chem., Int. Ed. 2010, 49, 7948−7951. (19) Velema, W. A.; Kool, E. T. Fluorogenic templated reaction cascades for RNA detection. J. Am. Chem. Soc. 2017, 139, 5405−5411. (20) Kitamura, Y.; Ihara, T.; Tsujimura, Y.; Osawa, Y.; Sasahara, D.; Yamamoto, M.; Okada, K.; Tazaki, M.; Jyo, A. Template-directed formation of luminescent lanthanide complexes: versatile tools for colorimetric identification of single nucleotide polymorphism. J. Inorg. Biochem. 2008, 102, 1921−1931. (21) Kitamura, Y.; Ihara, T.; Tsujimura, Y.; Tazaki, M.; Jyo, A. DNAtemplated cooperative formation of the luminous lanthanide complex and its analytical application to gene detection. Chem. Lett. 2005, 34, 1606−1607. (22) Kitamura, Y.; Yamamoto, S.; Osawa, Y.; Matsuura, H.; Ihara, T. Chem. Commun. 2013, 49, 285−287. (23) Ihara, T.; Fujii, T.; Mukae, M.; Kitamura, Y.; Jyo, A. Photochemical ligation of DNA conjugates through anthracene cyclodimer formation and its fidelity to the template sequences. J. Am. Chem. Soc. 2004, 126, 8880−8881. (24) Mukae, M.; Ihara, T.; Tabara, M.; Jyo, A. Anthracene-DNA conjugates as building blocks of designed DNA structures constructed by photochemical reactions. Org. Biomol. Chem. 2009, 7, 1349−1354. (25) Arslan, P.; Jyo, A.; Ihara, T. Reversible circularization of an anthracene-modified DNA conjugate through bimolecular triplex formation and its analytical application. Org. Biomol. Chem. 2010, 8, 4843−4848. (26) Ihara, T.; Wasano, T.; Nakatake, R.; Arslan, P.; Futamura, A.; Jyo, A. Electrochemical signal modulation in homogenous solutions using the formation of an inclusion complex between ferrocene and βcyclodextrin on a DNA scaffold. Chem. Commun. 2011, 47, 12388− 12390. (27) Futamura, A.; Uemura, A.; Imoto, T.; Kitamura, Y.; Matsuura, H.; Wang, C.-X.; Ichihashi, T.; Sato, Y.; Teramae, N.; Nishizawa, S.; Ihara, T. Rational design for cooperative recognition of specific nucleobases using β-cyclodextrin-modified DNAs and fluorescent ligands on DNA and RNA scaffolds. Chem.-Eur. J. 2013, 19, 10526− 10535. (28) Kitamura, Y.; Ihara, T.; Okada, K.; Tsujimura, Y.; Shirasaka, Y.; Tazaki, M.; Jyo, A. Asymmetric cooperativity in tandem hybridization on enantiomeric metal complex-tethered short fluorescent DNA probes. Chem. Commun. 2005, 4523−4525. (29) Dirks, P. M.; Pierce, N. A. Triggered amplification by hybridization chain reaction. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 15275−15278.
(30) Zhu, G.; Zheng, J.; Song, E.; Donovan, M.; Zhang, K.; Liu, C.; Tan, W. Self-assembled, aptamer-tethered DNA nanotrains for targeted transport of molecular drugs in cancer theranostics. Proc. Natl. Acad. Soc. U. S. A 2013, 110, 7998−8003. (31) Xuan, F.; Hsing, I.-M. Triggering hairpin-free chain-branching growth of fluorescent DNA dendrimers for nonlinear hybridization chain reaction. J. Am. Chem. Soc. 2014, 136, 9810−9813. (32) Yin, P.; Choi, H. M. T.; Calvert, C. R.; Pierce, N. A. Programming biomolecular self-assembly pathways. Nature 2008, 451, 318−322. (33) Jiang, Y. S.; Li, B.; Milligan, J. N.; Bhadra, S.; Ellington, A. D. Real-time detection of isothermal amplification reactions with thermostable catalytic hairpin assembly. J. Am. Chem. Soc. 2013, 135, 7430−7433. (34) Lv, Y.; Peng, R.; Zhou, Y.; Zhang, X.; Tan, W. Catalytic selfassembly of a DNA dendritic complex for efficient gene silencing. Chem. Commun. 2016, 52, 1413−1415. (35) Bi, S.; Xiu, B.; Ye, J.; Dong, Y. Target-catalyzed DNA four-way junctions for CRET imaging of microRNA, concatenated logic operations, and self-assembly of DNA nanohydrogels for targeted drug delivery. ACS Appl. Mater. Interfaces 2015, 7, 23310−23319. (36) Zhang, D. Y.; Turberfield, A. J.; Yurke, B.; Winfree, E. Engineering entropy-driven reactions and networks catalyzed by DNA. Science 2007, 318, 1121−1125. (37) Bar-Ziv, R. DNA circuits get up to speed. Science 2007, 318, 1078−1079. (38) Choi, H. M. T.; Chang, J. Y.; Trinh, L. A.; Padilla, J. E.; Fraser, S. E.; Pierce, N. A. Programmable in situ amplification for multiplexed imaging of mRNA expression. Nat. Biotechnol. 2010, 28, 1208−1212. (39) Lin, R.; Feng, Q.; Li, P.; Zhou, P.; Wang, R.; Liu, Z.; Wang, Z.; Qi, X.; Tang, N.; Shao, F.; Luo, M. A hybridization-chain-reactionbased method for amplifying immunosignals. Nat. Methods 2018, 15, 275−278. (40) Li, B.; Ellington, A. D.; Chen, X. Rational, modular adaptation of enzyme-free DNA circuits to multiple detection methods. Nucleic Acids Res. 2011, 39, No. e110. (41) Wei, Q.; Huang, J.; Li, J.; Wang, J.; Yang, X.; Liu, J.; Wang, K. A DNA nanowire based localized catalytic hairpin assembly reaction for microRNA imaging in live cells. Chem. Sci. 2018, 9, 7802−7808. (42) Han, D.; Zhu, Z.; Wu, C.; Peng, L.; Zhou, L.; Gulbakan, B.; Zhu, G.; Williams, K. R.; Tan, W. A logical molecular circuit for programmable and autonomous regulation of protein activity using DNA aptamer-protein interactions. J. Am. Chem. Soc. 2012, 134, 20797−20804. (43) Lv, Y.; Cui, L.; Peng, R.; Zhao, Z.; Qiu, L.; Chen, H.; Jin, C.; Zhang, X.-B.; Tan, W. Entropy beacon: A hairpin-free DNA amplification strategy for efficient detection of nucleic acids. Anal. Chem. 2015, 87, 11714−11720. (44) Engelen, W.; Meijer, L. H. H.; Somers, B.; de Greef, T. F. A.; Merkx, M. Antibody-controlled actuation of DNA-based molecular circuits. Nat. Commun. 2017, 8, 14473. (45) Shin, J.-S.; Pierce, N. A. A synthetic DNA walker for molecular transport. J. Am. Chem. Soc. 2004, 126, 10834−10835. (46) Jung, C.; Allen, P. B.; Ellington, A. D. A stochastic DNA walker that traverses a microparticle surface. Nat. Nanotechnol. 2016, 11, 157−163. (47) Sabbatini, N.; Guardigli, M.; Lehn, J.-M. Luminescent lanthanide complexes as photochemical supramolecular devices. Coord. Chem. Rev. 1993, 123, 201−228. (48) Bünzli, J.-C. G.; Piguet, C. Taking advantage of luminescent lanthanide ions. Chem. Soc. Rev. 2005, 34, 1048−1077.
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DOI: 10.1021/acsabm.9b00326 ACS Appl. Bio Mater. 2019, 2, 2988−2993
