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Artificial Smooth Muscle Model Composed of Hierarchically Ordered Microtubule Asters Mediated by DNA Origami Nanostructures Kento Matsuda, Arif Md. Rashedul Kabir, Naohide Akamatsu, Ai Saito, Shumpei Ishikawa, Tsuyoshi Matsuyama, Oliver Ditzer, Md. Sirajul Islam, Yuichi Ohya, Kazuki Sada, Akihiko Konagaya, Akinori Kuzuya, and Akira Kakugo Nano Lett., Just Accepted Manuscript • DOI: 10.1021/acs.nanolett.9b01201 • Publication Date (Web): 30 Apr 2019 Downloaded from http://pubs.acs.org on April 30, 2019

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Artificial Smooth Muscle Model Composed of Hierarchically Ordered Microtubule Asters Mediated by DNA Origami Nanostructures Kento Matsuda,†,# Arif Md. Rashedul Kabir,‡,# Naohide Akamatsu,¶ Ai Saito,† Shumpei Ishikawa,¶ Tsuyoshi Matsuyama,¶ Oliver Ditzer,∥ Md. Sirajul Islam,§ Yuichi Ohya,¶,§ Kazuki Sada,†,‡ Akihiko Konagaya,⊥ Akinori Kuzuya,*,¶,§ and Akira Kakugo*,†,‡

†

Graduate School of Chemical Sciences and Engineering, Hokkaido University, Sapporo 060-

0810, Japan. ‡

Faculty of Science, Hokkaido University, Sapporo 060-0810, Japan.

¶

Department of Chemistry and Materials Engineering, Kansai University, Osaka 564-8680,

Japan. ∥

Faculty of Chemistry and Food Chemistry, Technische Universität Dresden, Prüfungsamt,

01062 Dresden, Germany. §

Organization for Research and Development of Innovative Science and Technology, Kansai

University, Osaka 564-8680, Japan. ⊥

Department of Computational Intelligence and Systems Science, Tokyo Institute of

Technology, Kanagawa 226-8502, Japan.

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ABSTRACT

DNA has been well known for its applications in programmable self-assembly of materials. Nonetheless, utility of DNA origami, which offers more opportunity to realize complicated operations, has been very limited. Here we report self-assembly of a biomolecular motor system, microtubule-kinesin mediated by DNA origami nanostructures. We demonstrate that a rod-like DNA origami motif facilitates self-assembly of microtubules into asters. A smooth-muscle like molecular contraction system has also been realized using the DNA origami, in which selfassembled microtubules exhibited fast and dynamic contraction in the presence of kinesins through an energy dissipative process. This work provides potential nanotechnological applications of DNA and biomolecular motor proteins.

KEYWORDS Artificial muscle, Molecular engine, Self-organization, DNA origami, Kinesin, Microtubule


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The advancement of "molecular machines" has enabled construction of "molecular robots", which is fabricated through implementation of three major molecular components of robots; sensors, processors, and actuators.1 DNA has emerged as a versatile interface for molecular robots owing to its unique features including programmability and high selectivity.2–7 Except for a few completely "organic" molecular robots,8 most of the robots employ DNA either as a processor, sensor, or a chassis. Very recently, we have combined DNA and microtubule–kinesin, a biomolecular motor system, to construct "molecular swarm robots",9,10 mimicking the macroscopic and mechanical swarm robots.11,12 Kinesins act as the actuator that propel microtubules, and DNA functions as both sensors and the processor. Fusion of DNA and biomolecular motors rationally and reversibly controlled flocking of self-propelling microtubule "swarm robots" and dissociation of the swarms. Two kinds of microtubules modified with distinct single-stranded DNA (ssDNA) were prepared and subjected to an in vitro motility assay. These DNA-modified microtubules independently and efficiently glided on a kinesin coated surface without any mutual interference. Addition of another ssDNA, which bears sequences complementary to both the ssDNAs introduced to the microtubules, consequently bridges the microtubules in the system, and facilitates spontaneous formation of microtubules assembly. By tuning the mechanical property of microtubules, obtaining selective control over the translational and rotational movements of the microtubule swarms was possible. Moreover, introduction of a photo-responsive residue, azobenzene, to the ssDNAs realized photocontrol of the swarm robots. Although the above DNA-based systems successfully implemented a primitive idea of DNA nanotechnology, simple employment of interactions between ssDNAs requires large numbers of strands and sequences to realize more complicated operations and information processing.13 One possible way to address is to utilize DNA origami,14 which can provide solid nanostructures and properties, and thus is often used to construct mechanical DNA machines


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or molecular robots,2,5–7,15,16 although only a few study utilized DNA origami in combination with biomolecular motors.17,18 Here we report the first successful application of DNA origami motifs in programmed assembly of microtubules, and realization of a smooth-muscle like molecular contraction system. Figure 1 shows the design of the DNA origami used in this study. A tubular structure called 6 helix bundle (6HB) DNA origami, which is composed of six DNA helices bundled to make a hexagonal cross section, originally reported by Shi et al.,19,20 was adapted with a folding pattern of the scaffold and staples redesigned from scratch (Figure 1a). The expected dimensions of the motifs are 390 nm (1209 nt) long and 6 nm thick. To each one of two helices, 13 acceptor strands (39 in total) with the sequence of 5'-TTTTCAACAACAACAACAA-3' (T4(CAA)5)) were attached 27 nm (84 nt) apart, by extending the 3'-ends of corresponding staples (Figure 1b, see Supplementary Figure S1 for details). AFM imaging of the resulting 6HB motifs prepared by the standard protocol for DNA origami annealing on mica revealed quite uniform fiber-like structures with reasonable dimensions (Figure 1c). After preparation of the 6HB DNA origami we next explored the utility of the origami in programmed self-assembly of microtubules. As mentioned above, 6HB DNA origami has 39 acceptor strands of T4(CAA)5 on its surface. These acceptor strands are expected to hybridize with

a

complementary

single-stranded

DNA

(ssDNA)

with

sequence

5'-

TTGTTGTTGTTGTTG-3' ((TTG)5), which we previously conjugated to microtubules to create molecular swarm robots.9,10 We first prepared microtubules from rhodamine-dye labeled tubulin dimers, and conjugated the (TTG)5 ssDNA to the microtubules through azide-alkyne cycloaddition reaction (Scheme 1). The (TTG)5 conjugated microtubules and 6HB DNA origami were then mixed at a prescribed molar ratio and kept at room temperature for 12 hours, after which the microtubules were observed using a fluorescence microscope. The (TTG)5 conjugated microtubules were found to form aster-like structures, size of which was larger than


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the length of individual microtubules (Figure 2a). No such microtubule asters were formed when microtubules without (TTG)5 conjugation were mixed with the DNA origami (Figure 2b). Domains of closely packed multiple asters were also observed at relatively higher concentration of microtubules (Figures 2a and Supplementary Figure S2). The above results confirm successful utilization of the 6HB DNA origami in the self-assembly of microtubules into asters. Next we explored the utility of the 6HB DNA origami in dynamic contraction of microtubule network. The experimental design was based on the use of tetrameric kinesin crosslinkers, together with the microtubules and DNA origami, in order to facilitate contraction of the microtubule network in the presence of adenosine triphosphate (ATP). The tetrameric kinesin crosslinkers were prepared by mixing streptavidin with kinesins containing avidin tag. During the purification of the kinesin, biotin was attached to the avidin tag of the kinesins so that it may facilitate binding of the tagged kinesin with streptavidin and allow formation of tetrameric kinesin crosslinkers. The kinesin-streptavidin tetrameric conjugates may simultaneously interact with multiple microtubules that should allow the kinesins to work as crosslinkers facilitating formation of a global microtubule network. In order to demonstrate the dynamic contraction, di-block microtubules were prepared in which one part of a microtubule filament was conjugated with ssDNA, while the other part was preserved without any DNA conjugation (Scheme 2). First, very short microtubules (seed microtubules) were prepared from a mixture of azide- and TAMRA-labeled tubulin. The seed microtubules were then elongated by polymerizing Alexa488-labelled tubulins from the ends of the seed microtubules (Figure 2c). Conjugation of (TTG)5 ssDNA to the seed microtubules was accomplished through azidealkyne cycloaddition reaction between the azide-tubulins and DBCO in the (TTG)5 ssDNA. The reaction was almost quantitative as presented in our previous study.9 Here, the di-block microtubules were employed so that the Alexa488-labeled part of the di-block microtubules can interact with tetrameric kinesin crosslinkers, whereas the (TTG)5-conjugated seed-


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microtubule part may interact with the 6HB DNA origami through hybridization with their (CAA)5 extensions. After preparation, the di-block microtubules were mixed with 6HB DNA origami. Formation of the microtubule asters was confirmed by the observation of the asters using a confocal laser scanning microscope (Figure 2d), which is in good agreement with the results discussed above. The DNA origami-microtubules were then mixed with tetrameric kinesin linkers (Scheme 3). Here, dense network of microtubules was formed (Figure 2e). Finally, ATP was added to the microtubule-DNA origami-kinesin mixture. Upon addition of the ATP, the microtubule network exhibited dynamic rearrangement, and within a few minutes, the global microtubule network contracted (Figure 2f and Supplementary Movie S1). According to the area of microtubule-DNA origami-kinesin mixture before and after contraction, the contraction yield of the microtubule network was ~97%. Relatively higher concentration of DNA-origami was favorable for larger contraction of microtubule network (Supplementary Figure S3). The dynamic contractile behavior of the microtubule network was not observed in the absence of the DNA origami (Supplementary Movie S2), which implies that the DNA origami plays a key role in the fast contraction of the microtubule network. To gain further insight, we analyzed the change in size (radius) of the global microtubule network with time (Figure 2g). From the result, we then estimated rate of contraction of the microtubule network. In the absence of DNA origami, the rate of contraction was ~583 nm/s, which was amplified to ~8725 nm/s in the presence of the DNA origami. The rate of contraction in the absence of DNA origami is found very close to the velocity of a single kinesin along microtubule (~500 nm/s) at room temperature.21,22 On the other hand, in the presence of DNA origami, the rate of contraction appears ~17 times higher than the velocity of a single kinesin. This difference suggests layered hierarchical organization of microtubules in the presence of 6HB DNA origami. Therefore, a rod-like DNA origami motif enhances the dynamics of smooth muscle like contraction of microtubules, probably by facilitating formation of hierarchically


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organized global microtubule network. Furthermore, in the absence of ATP, no appreciable dynamic contraction was observed (Supplementary Figure S4), which confirms that the interaction of tetrameric kinesin linkers with microtubules in the presence of ATP is a key criterion for realizing the contraction of the microtubule network. No dynamic contraction of microtubule network was observed using monoblock microtubules (Supplementary Figure S3, which further emphasizes the important role of kinesin linkers in the contraction of the microtubule network. Some previous works reported active contraction of MTs or actins realized by using MTs or actin associated biomolecular motors.23-26 None of the past studies, however, utilized DNA and its nanostructures in self-assembly of MTs and in their contraction; hence it might be difficult to add programmability to such systems. In the present study, a DNA origami nanostructure has been successfully utilized for demonstrating self-assembly and active contraction of the biomolecular motor system for the first time. Such utilization of DNA devices should offer a promising means to control self-assembly and contraction of biomolecular motors in a programmable fashion, which will be explored in detail in our future work. In place of DNA origami nanostructures, DNA-modified gold nanoparticles or nanorods might be usable, though precise control of numbers, ratio, and positions of the DNA acceptors may not be as easy as done with DNA origami nanostructures. By combining with a DNA origami motif, we successfully demonstrated programmed selfassembly of a biomolecular motor system. This combination appears promising by facilitating smooth-muscle like contraction of the biomolecular motors in a dynamic manner. Gels also have been known to contribute to robotics, i.e. gel-based robotics.27 However, a component that can account the dynamics of macroscale gel-based robots is still lacking. The present work may find potential applications as micro-valves in microfluidic devices, actuators for microcatheters and even for micro-robots. Introduction of reversibility, that is a limitation of


the present

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system, might facilitate and widen its future application. Utilization of DNA origami nanostructures in our previously reported molecular swarm robot is also an interesting and feasible challenge. It may help realize further control over multi-step and more complicated swarming of molecular robots both with programmed sequences in DNA acceptors and change in configuration of nanomechanical DNA origami itself. Thus, Present combination between DNA nanotechnology and biomolecular motor systems may open a new dimension in molecular robotics.1,28


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FIGURES

Figure 1. (a) Design of 6 helix bundle (6HB) DNA origami. (b) Folding pattern of the scaffold and staples in part (see Supplementary Figure S1 for the whole). Position of the attachment of acceptor strands are indicated with red stars. (c) A typical AFM image. The scale bar is 500 nm.


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Figure 2. Self-assembly of DNA-modified MTs in the presence of 6HB DNA origami (a). No aster formation was observed when MTs were not modified by ssDNA (b). Scale bars: 10 µm. (c) Fluorescence microscopy image of di-block MTs. The scale bar is 20 µm. (d) Confocal microscopy image of an aster formed by mixing di-block MTs and 6HB DNA origami. Scale bar: 10 µm. (e) A representative image of MT network formed upon mixing of ssDNA-modified di-block MTs, 6HB DNA origami and kinesin crosslinkers. Scale bar: 10 µm. (f) Fluorescence microscopy images show contraction of DNA-modified di-block MTs/DNA origami complexes in the presence of kinesin linkers. See Supplementary Movie S1 for the real-time movement. Scale bars are 500 µm. (g) Change of radius of global microtubule network with time in the presence (blue circles) and absence (black circles) of 6HB DNA origami.


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SCHEMES

Scheme 1. Preparation of DNA-modified MTs.


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Scheme 2. Preparation of DNA-modified di-block MTs, and MTs/DNA origami complex.


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Scheme 3. Preparation of the contraction system.


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ASSOCIATED CONTENT Supporting Information. The following files are available free of charge. Materials and Methods, Table S1 (sequences of the staples), Figures S1–S4 (full structure of 6HB DNA origami, aster images with different concentrations of DNA origami, dependence of contraction on DNA origami concentrations) (PDF) Supplementary Movies S1 and S2 (contraction of microtubule network in the presence and absence of DNA origami) (.mov) AUTHOR INFORMATION Corresponding Authors *E-mails: [email protected] (A. Kuzuya), [email protected] (A. Kakugo). Author Contributions #These authors contributed equally. ACKNOWLEDGMENT We thank S. Kono for assisting in DNA synthesis. This work was financially supported by Future AI and Robot Technology Research and Development Project from New Energy and Industrial Technology Development Organization (NEDO), Japan; and Grant-in-Aid for Scientific Research on Innovative Areas "Molecular Engine" (18H05423 and 19H05407), Grant-in-Aid for Challenging Research (Pioneering) (17K19211), Grant-in-Aid for Challenging Exploratory Research (15K12135), and Private University Research Branding Project (2016-2021) from the Ministry of Education, Culture, Sports, Science and Technology, Japan.


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