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DNA Nanotechnology from the Test Tube to the Cell Yuan-Jyue Chen1, Benjamin Groves1, Richard A

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DNA Nanotechnology from the Test Tube to the Cell Yuan-Jyue Chen1, Benjamin Groves1, Richard A REVIEW ARTICLE PUBLISHED ONLINE: 3 SEPTEMBER 2015!|!DOI: 10.1038/NNANO.2015.195 DNA nanotechnology from the test tube to the cell Yuan-Jyue Chen1, Benjamin Groves1, Richard A. Muscat1 and Georg Seelig1,2* The programmability of Watson–Crick base pairing, combined with a decrease in the cost of synthesis, has made DNA a widely used material for the assembly of molecular structures and dynamic molecular devices. Working in cell-free settings, research- ers in DNA nanotechnology have been able to scale up system complexity and quantitatively characterize reaction mecha- nisms to an extent that is infeasible for engineered gene circuits or other cell-based technologies. However, the most intriguing applications of DNA nanotechnology — applications that best take advantage of the small size, biocompatibility and program- mability of DNA-based systems — lie at the interface with biology. Here, we review recent progress in the transition of DNA nanotechnology from the test tube to the cell. We highlight key successes in the development of DNA-based imaging probes, prototypes of smart therapeutics and drug delivery systems, and explore the future challenges and opportunities for cellular DNA nanotechnology. NA nanotechnology is a purist’s approach to biomolecular several recent results that show how DNA nanodevices can be pro- engineering. Te feld aims to create molecular structures grammed to interact with cell surface proteins, before turning to Dand devices through the exclusive use of DNA as an engi- work on the delivery of DNA devices and structures into cells. We neering material. Te well-characterized nature of DNA base- reach devices that operate inside live cells and review initial work pairing provides an easy means to control DNA interactions; this towards using DNA sensors and logic gates to detect, analyse and ‘sequence programmability’ has allowed the rational design of pre- regulate cellular RNA levels. We put this work into context by high- cisely defned structures ranging in size from nanometres to milli- lighting design principles identifed in the development of live-cell metres, and of molecular motors or circuits that can autonomously RNA imaging probes, small interfering RNAs (siRNAs) or anti- move or process information. Tere is currently no other molecular sense oligonucleotides (ASOs), which could be used to improve the engineering technology that enables the fully de novo design of a performance of DNA devices in cells. Finally, we make connections similarly complex and diverse set of biomolecular systems. to RNA nanotechnology and RNA synthetic biology, which have Te success of DNA nanotechnology comes from three key broadly similar aims to DNA nanotechnology but typically rely on ingredients: 1) our quantitative understanding of DNA thermo- the use of genetically encoded and transcribed RNA. dynamics, which makes it possible to predict reliably how single- stranded DNA molecules fold and interact with one another1,2; Cell-free DNA nanotechnology 2) the rapidly falling cost and increasing quality of DNA synthe- To operate reliably in complex, wet environments, living organ- sis3; and 3) the focus on cell-free settings, where designed reaction isms use molecular sensors to detect changes in that environment, pathways can proceed without interference from DNA and RNA motors and actuators to adapt to the environment, computational processing enzymes and other confounding factors that might be control circuits to convert sensor information into motor activity, encountered in cells. and structural elements that protect and organize these components. DNA nanotechnology has long been motivated by the goal of Intriguingly, cell-free DNA nanotechnology has made progress building ‘smart therapeutics’, drug delivery systems, tools for molec- towards the construction of most of the functional components — ular biology and other devices that could interact with or operate both structures and dynamic devices — required for creating molec- within living cells4–7 (Fig. 1). Such applications play to the obvious ular ‘robots’ that can emulate some of the behavioural complexity strengths of nucleic acid nanostructures and devices, particularly observed in biology. Here we review a few key results from cell-free their small size, biocompatibility and straightforward manner in DNA nanotechnology and point out potential applications in the which they could be programmed to interact with cellular nucleic cellular environment. acids through hybridization. However, to realize such applica- tions using tools from DNA nanotechnology, it will be necessary Structural DNA nanotechnology. In the 1980s, Nadrian Seeman to bridge the gap between performing experiments in well-mixed developed the notion that DNA could be used as a structural reaction bufers and spatially structured, densely packed cellular engineering material8–10. In 1998, Winfree et al. provided the frst environments (Box 1). experimental demonstration of large-scale structure formation: In this Review, we summarize recent progress towards the goal they showed that micrometre-sized periodic DNA lattices could of bringing DNA nanotechnology into the cell. We focus on nucleic self-assemble from nanoscale DNA tiles that are themselves assem- acid nanodevices and nanostructures that are rationally designed, blies of multiple oligonucleotides11. Subsequently, tile assembly and chemically synthesized and then delivered to mammalian cells. We related techniques were successfully used to create a wide variety of begin with a brief overview of DNA nanotechnology in cell-free lattices and wireframe DNA structures11–19. settings, and then move to more cell-like environments, such as Rothemund further advanced structural DNA self-assembly cell lysates and fxed cells — settings that capture some, but not by developing DNA origami, a technique that is easy to use, fex- all, of the complexity of cellular environments. Next, we discuss ible enough to accommodate almost any two-dimensional (2D) 1Department of Electrical Engineering, University of Washington, Seattle, Washington 98195, USA. 2Department of Computer Science and Engineering, University of Washington, Seattle, Washington 98195, USA. *e-mail: [email protected] 748 NATURE NANOTECHNOLOGY | VOL 10 | SEPTEMBER 2015 | www.nature.com/naturenanotechnology © 2015 Macmillan Publishers Limited. All rights reserved NATURE NANOTECHNOLOGY DOI: 10.1038/NNANO.2015.195 REVIEW ARTICLE structure of interest, and reliably results in a high yield of the target a Smart therapeutics b Drug delivery structure20. DNA origami relies on the use of a long single-stranded scafold strand that is folded into a target structure through hybridi- zation with a large number of short staple strands. Tis technology was rapidly and broadly adopted, and was soon generalized to the AND self-assembly of three-dimensional (3D) structures21–24. DNA nano- structures are beginning to be investigated as tools for drug delivery and similar applications because they provide precisely programm- able scafolds for the attachment of functional groups including drug and targeting moieties, and because 3D structures can be designed to act as protective enclosures for a cargo of interest. Dynamic DNA nanotechnology. Dynamic DNA nanotechnology combines self-assembly through programmed hybridization with c Imaging d Cell biology DNAzyme catalysis or DNA strand displacement reactions — a form of competitive hybridization — to create devices with moving parts and time-varying behaviours. Dynamic DNA nano technology can Cell be traced to multiple sources, including Adleman’s work on DNA computation and research on the directed evolution and characteri- zation of functional nucleic acids25. However, Yurke and co-workers d truly launched the feld by demonstrating that a functional molecu- lar ‘motor’ could be rationally designed and driven through its work cycle using only hybridization and strand displacement reactions26. Subsequently, the Winfree and Pierce groups demonstrated that multiple strand displacement reactions could be chained together to create complex reaction cascades27,28. Owing to their simplicity, Figure 1 | Applications of DNA nanotechnology at the interface with DNA strand displacement cascades have since been used widely and biology. a, Smart therapeutics could combine structural elements with efectively for molecular engineering and provide the mechanism molecular logic to target therapeutic actions to a specific cell or tissue that drives most dynamic DNA devices. type, thus minimizing side efects60. b, DNA nanostructures can serve as Dynamic DNA nanotechnology has resulted in molecular programmable scafolds for attaching drugs, targeting ligands and other motors29,30, including walking motors that autonomously move along modifications, such as lipid bilayers78. c, A novel class of sensitive and a track31–34, molecular circuits that can analyse information encoded specific imaging probes that takes advantage of DNA-based amplification in complex mixtures of molecules27,35–39, and catalytic amplifers that mechanisms can be programmed to sequence-specifically interact with can sense and amplify signals40–44. Many of these systems have obvi- cellular RNA52. d, DNA origami and other structures provide precise control ous potential for biotechnological applications: for example, Shapiro over the spatial organization of functional molecular groups, which makes and collaborators used DNA and a restriction enzyme to build a them intriguing tools for quantitative measurements
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