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Dynamic DNA Nanotechnology: Toward Functional Nanoscale Devices Cite This: Nanoscale Horiz., 2020, 5,182 Marcello Deluca,A Ze Shi,B Carlos E

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Dynamic DNA Nanotechnology: Toward Functional Nanoscale Devices Cite This: Nanoscale Horiz., 2020, 5,182 Marcello Deluca,A Ze Shi,B Carlos E Nanoscale Horizons View Article Online REVIEW View Journal | View Issue Dynamic DNA nanotechnology: toward functional nanoscale devices Cite this: Nanoscale Horiz., 2020, 5,182 Marcello DeLuca,a Ze Shi,b Carlos E. Castrocd and Gaurav Arya *a Dynamic DNA nanotechnology involves the creation of nanoscale devices made of DNA whose primary function arises from their ability to undergo controlled motion or reconfiguration. In the past two Received 8th August 2019, decades, dynamic DNA nanotechnology has evolved to the point where it is now being employed in Accepted 15th October 2019 devices intended for applications in sensing, drug delivery, computation, nanorobotics, and more. In this DOI: 10.1039/c9nh00529c review article, we discuss the design of dynamic DNA nanodevices and the characterization and prediction of device behavior. We also identify a number of continuing challenges in dynamic DNA rsc.li/nanoscale-horizons nanotechnology and discuss potential solutions to those challenges. 1 Introduction DNA is highly programmable. Sequences of DNA bind specifi- cally to each other via strict base-pairing rules.1 This means DNA nanotechnology is a rapidly growing field that uses DNA as that the lengths, positions, and orientations of the hybridized, a material for creating nanoscale structures and devices. DNA is double-helical elements of the structure can be readily and an attractive candidate for this application for several reasons. rationally programmed into the DNA sequence. Lastly, DNA can Firstly, DNA is truly nanoscopic. Its smallest structural unit, the be readily synthesized at reasonable cost and its properties are nucleotide, occupies approximately the space of a 0.34 nm wide also generally well understood. and 1 nm long cylinder. One should thus be able to design In biology, one major role of DNA is encoding the structure structures at a similar resolution, which makes DNA one of the of proteins, many of which are quite complex, but as far as finest nanoscopic building blocks currently available. Secondly, DNA’s own structural form is concerned, it is mostly limited to Published on 15 October 2019. Downloaded 10/1/2021 2:52:37 AM. that of a linear double helix. This raises the natural question as a Department of Mechanical Engineering and Materials Science, Duke University, to whether DNA can encode its own structure in a manner that 2 Durham, North Carolina 27708, USA. E-mail: [email protected] produces geometry more complex than the double helix. Ned b Department of NanoEngineering, University of California San Diego, La Jolla, Seeman addressed this question in the early 1980s when he California 92093, USA proposed the design of an immobile four-way junction with c Department of Mechanical and Aerospace Engineering, The Ohio State University, sticky ends made from four different DNA sequences.3 This Columbus, Ohio 43210, USA d Biophysics Graduate Program, The Ohio State University, Columbus, Ohio 43210, concept represented the first major step towards synthetic DNA USA structures spanning two or even three dimensions, marking the Marcello DeLuca is a PhD student Ze Shi is working as a Bioinfor- in the Department of Mechanical matics Intern at BioLegend Inc. Engineering and Materials Science She obtained her PhD in Nano- at Duke University. He received his Engineering at the University of BS in Mechanical Engineering from California, San Diego in 2018 Rensselaer Polytechnic Institute and her BS in Materials Science in 2018. His graduate research from Fudan University in 2012. focuses on mesoscopic modeling Her PhD research focused on and simulation of dynamic DNA atomistic, coarse-grained, and nanodevices. statistical mechanics modeling of mechanically compliant DNA nanostructures. Marcello DeLuca Ze Shi 182 | Nanoscale Horiz., 2020, 5, 182--201 This journal is © The Royal Society of Chemistry 2020 View Article Online Review Nanoscale Horizons birth of structural DNA nanotechnology. However, structures into literal arabic numerals that can be read by atomic force created using junctions alone were not stiff enough to find microscopy.22 Whether simple or complex, the incorporation practical use except for simple shapes of small length scales. of dynamic mechanisms into DNA systems can dramatically This problem was solved in 1993 with the invention of the broaden their potential applications. For example, where a double-crossover motif,4 which allowed for 2D structures of static DNA device might have a unique plasmonic signature,39 large span to be created while maintaining stiffness. Ten years a dynamic one might be able to modify that signature between later, the introduction of DNA origami5 democratized the multiple states for applications in sensing35,36,40 or optics;40,41 design process and enabled the creation of larger and more and while a static DNA box might be designed to hold mole- complex structures. Further breakthroughs in the design of 3D cular cargo, a dynamic one can be designed to open and release shapes6 and curved structures,7 along with technologies that cargo once the device enters a specific microenvironment focused on creating larger structures8,9 have enabled the design or detects a particular molecule, enabling important functions of even more complex DNA geometries of sizes ranging from like targeted drug delivery.28,29,42 10 nm up to microns.8,10 In general, artificial molecular machines and devices can be Fairly early on in the development of the field, there was designed using two different approaches. One approach treats interest in mechanizing DNA nanostructures.11,12 These these devices as macroscopic machines, which are designed so-called ‘‘dynamic’’ structures are defined as structures whose according to the principles of mechanical engineering, and, functions rely upon changing of their conformations. Despite consequently, input to a device will produce a single deterministic early interest in the topic of dynamic mechanisms, a vast response. Devices can also be designed to mimic biomolecular majority of progress in DNA nanotechnology focused on enhancing machines like enzymes and molecular motors which are inherently the size and geometric complexity of static objects, namely, flexible and incorporate some degree of stochasticity into their structural DNA nanotechnology. The past decade, however, has function. DNA nanodevices exist at the interface of macroscopic witnessed a tremendous surge of interest toward dynamic DNA and biomolecular machines; specifically, these devices can exhibit nanotechnology and DNA-based nanoscale devices,13 resulting many macroscopic device behaviours, but flexibility and thermal in diverse applications including but not limited to sensors,14–20 motion are critical to the function of most DNA devices and cannot molecular algorithms,18,21–23 biological assays,24–26 cargo sorting27 be ignored. and delivery28–31 devices, tunable plasmonic devices,32–36 and Many of the dynamic DNA devices developed so far have nanoscale robotic arms.37,38 A pictorial timeline of the progression been inspired by macroscopic machines. In general, machines of dynamic DNA nanotechnology toward increasingly complex and are made up of a collection of structural elements connected by useful devices is presented in Fig. 1. kinematic mechanisms such as hinges, sliders, and gears to At the macroscale, devices as simple as a pair of tweezers produce precise and complex motions. Machines also typically or as complicated as a gasoline-powered automobile engine employ actuation mechanisms to convert an energy source into qualify as dynamic. A large span of complexity also exists in useful mechanical work, e.g., the internal combustion chamber DNA devices, from the first dynamic mechanism which in automobiles that converts the chemical energy stored in Published on 15 October 2019. Downloaded 10/1/2021 2:52:37 AM. induced a simple twist in a connected pair of double-crossover gasoline into translational motion and force of the pistons. molecules11 to a recent device which performs calculations Furthermore, many modern machines carry sophisticated con- given an input and then produces output by conforming DNA trol elements including sensors and computer chips to sense Carlos Castro is an Associate Gaurav Arya is an Associate Professor in the Department of Professor in the Department Mechanical and Aerospace of Mechanical Engineering and Engineering at the Ohio State Materials Science at Duke Univer- University. He received his BS sity. He received his BTech from and MS from the Ohio State IIT Bombay in 1998 and his PhD University in 2005 and his PhD from the University of Notre from MIT in 2009, all in mechanical Dame in 2003, all in chemical engineering. He carried out post- engineering. He carried out post- doctoral research at the Technische doctoral research at Princeton Universita¨tMu¨nchen. His research University and New York Univer- group develops dynamic DNA sity. His research group uses Carlos E. Castro nanodevices for applications in Gaurav Arya multi-scale simulation methods nanorobotics, biophysics, and to study various biomolecular bioengineering. and nanoscale systems of interest, including DNA nanostructures, chromatin, polymer nanocomposites, and viral DNA packaging motors. This journal is © The Royal Society of Chemistry 2020 Nanoscale Horiz., 2020, 5,182--201| 183 View Article Online Nanoscale Horizons Review Fig. 1 Timeline of the increasing complexity of dynamic DNA nanostructures over the past two decades. (a) Paired double crossover structure actuated by the
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