DNA Origami and G-Quadruplex Hybrid Complexes Induce Size

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DNA Origami and G-Quadruplex Hybrid Complexes Induce SizeControl of Single-Walled Carbon Nanotubes via Biological Activation Hiroshi Atsumi, and Angela M. Belcher ACS Nano, Just Accepted Manuscript • DOI: 10.1021/acsnano.8b02720 • Publication Date (Web): 16 Jul 2018 Downloaded from http://pubs.acs.org on July 16, 2018

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DNA Origami and G-Quadruplex Hybrid Complexes Induce Size-Control of Single-Walled Carbon Nanotubes via Biological Activation Hiroshi Atsumi1,2 and Angela M. Belcher1,2,3* 1

The David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of

Technology, Cambridge, Massachusetts 02139, USA. 2

Department of Biological Engineering Massachusetts Institute of Technology, Cambridge,

Massachusetts 02139, USA. 3

Department of Materials Science and Engineering, Massachusetts Institute of Technology,

Cambridge, Massachusetts 02139, USA. * Corresponding author: [email protected]

ABSTRACT

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DNA self-assembly has enabled the programmable fabrication of nanoarchitectures, and these nanoarchitectures combined with nanomaterials have provided several applications. Here, we develop an approach for cutting single-walled carbon nanotubes (SWNTs) of pre-determined lengths, using DNA origami and G-quadruplex hybrid complexes. This approach is based on features of DNA: 1) wrapping SWNTs with DNA to improve the dispersibility of SWNTs in water; 2) using G-quadruplex DNA to confine hemin in close proximity to SWNTs and enhance the biological activation of hydrogen peroxide by hemin; and 3) forming DNA origami platforms to allow for the precise placement of G-quadruplexes, enabling size control. These integrated features of DNA allow for temporally efficient cutting of SWNTs into desired lengths, thus expanding the availability of SWNTs for applications in the fields of nanoelectronics, nanomedicine, nanomaterials, and quantum physics, as well as in fundamental studies.

KEYWORDS: DNA origami; single-walled carbon nanotubes (SWNTs); DNA-wrapped SWNTs; G-quadruplex; SWNT lengths; hemin; luminol


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DNA self-assembly has enabled fabrication of rationally assembled nanoarchitectures.1-4 In particular, the DNA origami technique, in which a long single-stranded DNA is folded using staple DNA strands, has led to the construction of well-defined, programmable, and complicated nanoarchitectures.5,6 This technique has led to great interest in the field of nanotechnology and has provided several applications, such as organic and/or inorganic materials-integrated templates,7-9 a template to observe chemical reactions or DNA structural changes,10-12 and DNA actuators for a membrane channel and a drug transporter.13,14 Recently, more practical applications were described in which DNA origami allowed for the transfer of spatial information to graphene and inorganic materials.15,16 However, the development of practical applications involving these materials still remains challenging.

Single-walled carbon nanotubes (SWNTs) are a promising nanomaterial, due to their unique optical, electrical, and mechanical properties, which depend on the chirality and length of SWNTs. Recently, short SWNTs (200 nm) and short SWNTs (700 nm length and (6,5) chirality were purchased from Sigma-Aldrich (#704148). DNA-wrapped SWNTs. DNA-wrapped SWNTs were prepared according to a previous report.25 100 µl of DNA (1 mg/ml G-DNA, nG-DNA, or B-DNA) dissolved in water was diluted by 200 µl of 150 mM NaCl. 0.1 mg of SWNTs was dissolved in the DNA solution. The mixed solution was sonicated in an ice bath for 30 minutes at a power of 20% using an Ultrasonic Processor (Cole-Parmer, 750 W) with a tip sonicator (COUPLER, 630-0421). The resulting solution was


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centrifuged at 15,000 rpm for 1 h, and then the black precipitate was removed. 800 µl of 30 mM MgCl2 was added to the supernatant, and the solution was centrifuged at 15,000 rpm for 30 minutes. The supernatant was carefully removed and the precipitated DNA-wrapped SWNTs were dispersed in 200 µl of 0.5x TBE buffer (Polysciences, Inc.). Excess solid EDTA was added to the resulting solution, and then the solution was centrifuged at 15,000 rpm for 2 minutes. Precipitated EDTA was carefully removed. All DNA-wrapped SWNTs were adjusted to the same concentration using absorbance peaks at about 990 nm, and their concentrations were calculated based on OD990 nm = 13 µg/ml.47 Luminol experiments. The luminol experiments were performed according to a previous report.48 4 µl of 25 µM luminol was added to 10 µl of 67 µg/ml DNA-wrapped SWNTs in 50 mM Tris-HCl buffer (pH 8.0) containing 50 mM KCl and 5 µM hemin. To initiate the oxidation, 20 µl of 60 mM hydrogen peroxide was added to the hemin solution, and then the chemiluminescence of luminol was measured in a dark room. The measurement was performed with a fluorophotometer under the following conditions: integration time, 0.1 s; wavelength, 462 nm; slit size, 1 nm. Random cutting of SWNTs. 10 µl of 67 µg/ml DNA-wrapped SWNTs were dissolved in 90 µl of 20 mM Tris-HCl buffer (pH 8.0) containing 50 mM KCl. The solution was incubated at 70 °C for 10 minutes and then cooled down to 15 °C over 55 minutes at a rate of -1 °C/min. 1 µl of 250 µM hemin dissolved in DMSO was added to 49 µl of the annealed solution and incubated at room temperature for 1 h. 50 µl of 600 µM hydrogen peroxide was added to the sample, which was further incubated at room temperature for 1 h to induce random cutting. The random cutting was characterized by PL measurement and Raman spectroscopy. AFM was performed with the


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following steps: a 2 µl sample of SWNTs was dropped on a freshly cleaved mica substrate (Electron Microscopy, #71856-01) for 10 minutes and then dried using nitrogen gas; the sample was washed with 50 µl of water followed by drying using nitrogen gas; and the dried sample was scanned using AFM in tapping mode with an RFESP-75 cantilever (Bruker Corporation). PL measurement. PL measurements were performed with a near-infrared photometer using 532 nm laser excitation under the following conditions: integration time, 0.5 s; slit size, 10 nm. Raman spectroscopy. 2 µl samples were dropped and naturally dried on Si wafers (10 mm x 10 mm) that are pre-sonicated with DI water, acetone, and isopropanol for 1 minute each. Raman spectra of DNA-wrapped SWNTs were collected on a Horiba LabRAM spectrometer using 532 nm laser excitation under the following conditions: hole size, 500 nm; slit size, 100 nm; microscope objective, 10x; RTD exposure time, 5 s; exposure time, 5 s; accumulation number, 5 times. Measurement of SWNT-lengths. All statistical histograms were based on AFM or TEM images, and the lengths of SWNTs were analyzed by hand in ImageJ. Typically, 250 to 400 SWNTs were measured for each histogram. TEM. In sample preparation for negative stained-electron microscopy, 7 µl of the samples were dropped on a 200 mesh copper grid coated with a continuous carbon film. After 40 seconds, the excess solution was removed. Subsequently, 10 µl of 1% phosphotungstic acid solution was dropped on the TEM grid, and immediately removed. 10 µl of 1% phosphotungstic acid solution was dropped on the TEM grid again. After 40 seconds, the excess solution was removed, and the grid was dried at room temperature. Finally, the grid was mounted on a JEOL single tilt holder


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equipped in the TEM column. The specimens were cooled down by liquid-nitrogen and imaged by JEOL 2100 FEG microscope. All images were recorded on a Gatan 2k x 2k UltraScan CCD camera. Preparation of the DNA origami template. A molar ratio of 1:5 for M13mp18 viral ssDNA and staple strands was used. G-quadruplex staple strands and biotin-modified staple strands were added at a concentration 5x greater than that of normal staple strands. DNA origami was assembled in 1x TAE buffer (40 mM Tris; 20 mM acetic acid; 2 mM EDTA (pH 8.0)) containing 12.5 mM magnesium acetate (TAE-Mg2+ (1x)) with 20 mM KCl incubated at 90 °C for 10 minutes and annealed from 90 °C to 65 °C over 25 minutes, and then cooled down to 15 °C over 150 minutes. The excess staple strands were mostly removed by filtration using an Amicon Ultra centrifuge filter (MWCO: 100 K) (Millipore Corporation, UFC510096). The concentrated sample was recovered to 50 µl using 1x TAE-Mg2+ containing 20 mM KCl. The recovered sample was mixed with 1.88 µM streptavidin and incubated at room temperature for 12 hours. The mixture was combined with 250 µM hemin and then incubated at room temperature for 1 h. To remove excess streptavidin and hemin, gel electrophoresis was performed using a 1% agarose gel containing 12.5 mM MgCl2 and 20 mM KCl (Fig. S6). After excising the desired band on the gel, the product was extracted by using a Quantum Prep Freeze ‘N Squeeze DNA gel extraction spin column (Bio-Rad, #7326165). The obtained DNA origami structure was observed by AFM. A 1-D origami polymer template was prepared by the addition of 100 nM linker-DNA strands in 1x TAE-Mg2+ with 20 mM KCl and incubated overnight at room temperature. 0.5 µl of 17 µg/ml B-DNA-SWNT was mixed with 4 µl of the 1-D origami polymer template and incubated overnight. Finally, the complex of the 1-D origami polymer template with SWNTs was imaged by AFM using the following steps: 10 µl of 1 mM NiCl2 was dropped on a freshly cleaved mica


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substrate; after 10 min, 2 µl of the DNA sample was dropped on the pretreated substrate for 10 minutes; and the sample was scanned with 50 µl of 1x TAE-Mg2+ containing 20 mM KCl using AFM (Veeco Multimode with NanoScopeV) in tapping mode with an SNL-10 cantilever (Bruker Corporation). Cutting SWNTs to a designated length. 200 µl of DNA origami monomer purified by agarose gel electrophoresis was concentrated to 50 µl by using an Amicon Ultra centrifuge filter (MWCO: 100 K). The concentrated sample was incubated with 100 nM linker-DNA strands containing 1x TAE-Mg2+ and 120 mM KCl (DNA origami:linker-DNA = 5:1 v/v) at room temperature for 1 h. 12 µl of the 1-D origami polymer or origami monomer was incubated with 1 µl of 67 µg/ml B-DNA-SWNT overnight. 6 µl of the complex was further incubated with 1 µl of 2.4 mM hydrogen peroxide for 1 h, after which the defects of SWNTs on the DNA origami were measured by Raman spectroscopy. For the PL measurement, 2 µl of 67 µg/ml B-DNA-SWNT was added to 97 µl of the DNA origami, and the complex was incubated overnight. 1 µl of 30 mM hydrogen peroxide was added to the complex and further incubated for 1 h, and then the PL of SWNTs was measured. Before AFM, the DNA origami was digested by DNase, and the sample was incubated at 37 °C for 1 h. The sample was put on a mica substrate, followed by washing with water twice. SWNTs were scanned using AFM in tapping mode with an RFESP-75 cantilever (Bruker Corporation). ASSOCIATED CONTENT Supporting Information The Supporting Information is available Free of charge on the ACS Publications website.


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Photographs and UV-Vis spectrum of G-DNA-SWNTs; Luminol oxidation assay; Raman spectra of G-DNA-SWNTs after random cutting; D/G ratio, PL spectra, and AFM of nG-DNA-SWNTs, Raman spectra of nG-DNA-SWNTs; The agarose gel separation of the DNA origami monomer; The predictions of DNA origami perturbations; Assembly of SWNTs on DNA origami monomer templates; Raman spectra of B-DNA-SWNTs after origami polymer-cutting and origami monomer-cutting; AFM image of B-DNA-SWNTs before SWNT-cutting; SWNT-cutting of BDNA-SWNTs with cross-shaped DNA origami; SWNT-cutting of B-DNA-SWNTs with 1-D origami polymer; SWNT-cutting of B-DNA-SWNTs with short rectangular-shaped DNA origami; SWNT-cutting of B-DNA-SWNTs with long rectangular-shaped DNA origami; Peaks, averages with standard errors, and standard deviations with uncertainties of SWNT-length after SWNT-cutting (PDF). AUTHOR INFORMATION Corresponding Author *Email: [email protected] The authors declare no competing financial interests. Author Contributions H.A. and A.M.B. conceived of the project. A.M.B. supervised the overall work. H.A. designed the experiments, prepared all samples, performed the experiments, and H.A. and A. M. B. analyzed the data. H.A. wrote this manuscript and A.M.B. made edits on this manuscript. A.M.B. provided financial support. ACKNOWLEDGMENTS


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We thank Koch Institute Nanotechnology Material Core for technical support. This work was supported by the Institute for Collaborative Biotechnologies through Grant W911NF-09-0001 from the U.S. Army Research Office. The content of the information does not necessarily reflect the position or the policy of the Government, and no official endorsement should be inferred. H.A acknowledges Research Fellowship (23–4277) from the Japan Society for the Promotion of Science for Young Scientists. Dr. Ngozi Eze helped to edit this manuscript. Dr. Ching-Wei Lin discussed the data and gave helpful comments on the manuscript. Dr. Dong Soo Yun helped with TEM imaging. REFERENCES (1)

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ACS Nano

Figure 1. SWNT-cutting platforms. (a) DNA-wrapped SWNTs, in which the DNA

includes G-quadruplex DNA, allowing for random cutting. (b-e) DNA origami platforms; (b) SWNT–cross-shaped DNA origami monomer, (c) 1-D origami polymer, (d) short rectangular-shaped DNA origami, and (e) long rectangular-shaped DNA origami complexes, in which SWNTs are wrapped by biotin-modified DNA, allowing for sizecontrolled cutting.


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ACS Nano

Figure 2. Random SWNT-cutting. (a) A scheme for SWNT-cutting with the G-DNASWNT platform. (b) The D/G ratio from Raman spectra for G-DNA-SWNTs (black) in the presence of hemin (green), hydrogen peroxide (light blue), and both (red). The data represent the mean values ± s.d of three measurements. Significant differences were determined by student's t-test (**P

DNA Origami and G-Quadruplex Hybrid Complexes Induce Size

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