Abstract
Self-assembly, which is ubiquitous in living systems, also stimulates countless synthetic molecular self-assembling systems. Most synthetic self-assemblies are realized by passive processes, going from high-energy states to thermodynamic equilibrium. Conversely, living systems work out of equilibrium, meaning they are energy-consuming, dissipative and active. In recently years, chemists have made extensive efforts to design artificial active self-assembly systems, which will be pivotal to emulating and understanding life. Among various strategies, emerging approaches based on DNA nanotechnology have attracted a lot of attention. Structural- as well as dynamic-DNA-nanotechnology offer diverse tools with which to design building blocks and to shape their assembly behaviors. To achieve active self-assembly, a synergy of diverse DNA techniques is essential, including structural design, controllable assembly–disassembly, autonomous assembly, molecular circuits, biochemical oscillators, and so on. In this review, we introduce progress towards, or related to, active assembly via DNA nanotechnology. Dynamic DNA assembly systems ranging from passive assembly–disassembly systems, to autonomous assembly systems to sophisticated artificial metabolism and time-clocking oscillation systems will be discussed. We catalogue these systems from the perspective of free energy change with the reaction process. We end the review with a brief outlook and discussion.
Similar content being viewed by others
References
Gibson DG, Glass JI, Lartigue C, Noskov VN, Chuang RY, Algire MA, Benders GA, Montague MG, Ma L, Moodie MM, Merryman C, Vashee S, Krishnakumar R, Assad-Garcia N, Andrews-Pfannkoch C, Denisova EA, Young L, Qi ZQ, Segall-Shapiro TH, Calvey CH, Parmar PP, Hutchison CA 3rd, Smith HO, Venter JC (2010) Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329(5987):52–56. https://doi.org/10.1126/science.1190719
Des Marais DJ, Nuth JA 3rd, Allamandola LJ, Boss AP, Farmer JD, Hoehler TM, Jakosky BM, Meadows VS, Pohorille A, Runnegar B, Spormann AM (2008) The NASA astrobiology roadmap. Astrobiology 8(4):715–730. https://doi.org/10.1089/ast.2008.0819
Kaneko K (2006) Life: an introduction to complex systems biology. Springer, Berlin
Hess B, Mikhailov A (1994) Self-organization in living cells. Science 264(5156):223–225
Bhalla US, Iyengar R (1999) Emergent properties of networks of biological signaling pathways. Science 283(5400):381–387
Ashkenasy G, Hermans TM, Otto S, Taylor AF (2017) Systems chemistry. Chem Soc Rev 46(9):2543–2554. https://doi.org/10.1039/c7cs00117g
Merindol R, Walther A (2017) Materials learning from life: concepts for active, adaptive and autonomous molecular systems. Chem Soc Rev 46(18):5588–5619. https://doi.org/10.1039/c6cs00738d
van Roekel HW, Rosier BJ, Meijer LH, Hilbers PA, Markvoort AJ, Huck WT, de Greef TF (2015) Programmable chemical reaction networks: emulating regulatory functions in living cells using a bottom-up approach. Chem Soc Rev 44(21):7465–7483. https://doi.org/10.1039/c5cs00361j
Song J, Li Z, Wang P, Meyer T, Mao C, Ke Y (2017) Reconfiguration of DNA molecular arrays driven by information relay. Science 357:6349. https://doi.org/10.1126/science.aan3377
Green LN, Subramanian HKK, Mardanlou V, Kim J, Hariadi RF, Franco E (2019) Autonomous dynamic control of DNA nanostructure self-assembly. Nat Chem 11(6):510–520. https://doi.org/10.1038/s41557-019-0251-8
Hamada S, Yancey KG, Pardo Y, Gan M, Vanatta M, An D, Hu Y, Derrien TL, Ruiz R, Liu P, Sabin J, Luo D (2019) Dynamic DNA material with emergent locomotion behavior powered by artificial metabolism. Sci Robot 4:29. https://doi.org/10.1126/scirobotics.aaw3512
Seeman NC (1982) Nucleic acid junctions and lattices. J Theor Biol 99(2):237–247. https://doi.org/10.1016/0022-5193(82)90002-9
Yan H, Park SH, Finkelstein G, Reif JH, LaBean TH (2003) DNA-templated self-assembly of protein arrays and highly conductive nanowires. Science 301(5641):1882–1884. https://doi.org/10.1126/science.1089389
Rothemund PW (2006) Folding DNA to create nanoscale shapes and patterns. Nature 440(7082):297–302. https://doi.org/10.1038/nature04586
Ong LL, Hanikel N, Yaghi OK, Grun C, Strauss MT, Bron P, Lai-Kee-Him J, Schueder F, Wang B, Wang P, Kishi JY, Myhrvold C, Zhu A, Jungmann R, Bellot G, Ke Y, Yin P (2017) Programmable self-assembly of three-dimensional nanostructures from 10,000 unique components. Nature 552(7683):72–77. https://doi.org/10.1038/nature24648
Wang W, Chen SL, An B, Huang K, Bai TX, Xu MY, Bellot G, Ke YG, Xiang Y, Wei B (2019) Complex wireframe DNA nanostructures from simple building blocks. Nat Commun 10(1):1067. https://doi.org/10.1038/s41467-019-08647-7
Zheng J, Birktoft JJ, Chen Y, Wang T, Sha R, Constantinou PE, Ginell SL, Mao C, Seeman NC (2009) From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal. Nature 461(7260):74–77. https://doi.org/10.1038/nature08274
Zhang T, Hartl C, Frank K, Heuer-Jungemann A, Fischer S, Nickels PC, Nickel B, Liedl T (2018) 3D DNA origami crystals. Adv Mater 30:e1800273. https://doi.org/10.1002/adma.201800273
Zhang Y, Pan V, Li X, Yang X, Li H, Wang P, Ke Y (2019) Dynamic DNA structures. Small 15(26):e1900228. https://doi.org/10.1002/smll.201900228
Simmel FC, Yurke B, Singh HR (2019) Principles and applications of nucleic acid strand displacement reactions. Chem Rev 119(10):6326–6369. https://doi.org/10.1021/acs.chemrev.8b00580
Zhang DY, Seelig G (2011) Dynamic DNA nanotechnology using strand-displacement reactions. Nat Chem 3(2):103–113. https://doi.org/10.1038/nchem.957
Tigges T, Heuser T, Tiwari R, Walther A (2016) 3D DNA origami cuboids as monodisperse patchy nanoparticles for switchable hierarchical self-assembly. Nano Lett 16(12):7870–7874. https://doi.org/10.1021/acs.nanolett.6b04146
Wagenbauer KF, Sigl C, Dietz H (2017) Gigadalton-scale shape-programmable DNA assemblies. Nature 552(7683):78–83. https://doi.org/10.1038/nature24651
Yang S, Liu W, Wang R (2019) Control of the stepwise assembly–disassembly of DNA origami nanoclusters by pH stimuli–responsive DNA triplexes. Nanoscale 11(39):18026–18030. https://doi.org/10.1039/C9NR05047G
Dong Y, Yang Z, Liu D (2014) DNA nanotechnology based on i-motif structures. Acc Chem Res 47(6):1853–1860. https://doi.org/10.1021/ar500073a
Yang S, Liu W, Nixon R, Wang R (2018) Metal-ion responsive reversible assembly of DNA origami dimers: G-quadruplex induced intermolecular interaction. Nanoscale 10(8):3626–3630. https://doi.org/10.1039/c7nr09458b
Wu N, Willner I (2016) DNAzyme-controlled cleavage of dimer and trimer origami tiles. Nano Lett 16(4):2867–2872. https://doi.org/10.1021/acs.nanolett.6b00789
Green LN, Amodio A, Subramanian HKK, Ricci F, Franco E (2017) pH-driven reversible self-assembly of micron-scale DNA scaffolds. Nano Lett 17(12):7283–7288. https://doi.org/10.1021/acs.nanolett.7b02787
Rothemund PWK, Ekani-Nkodo A, Papadakis N, Kumar A, Fygenson DK, Winfree E (2004) Design and characterization of programmable DNA nanotubes. J Am Chem Soc 126(50):16344–16352. https://doi.org/10.1021/ja0443191
Suzuki Y, Endo M, Yang Y, Sugiyama H (2014) Dynamic assembly/disassembly processes of photoresponsive DNA origami nanostructures directly visualized on a lipid membrane surface. J Am Chem Soc 136(5):1714–1717. https://doi.org/10.1021/ja4109819
Peng RZ, Wang HJ, Lyu YF, Xu LJ, Liu H, Kuai HL, Liu Q, Tan WH (2017) Facile assembly/disassembly of DNA nanostructures anchored on cell-mimicking giant vesicles. J Am Chem Soc 139(36):12410–12413. https://doi.org/10.1021/jacs.7b07485
Li H, Wang M, Shi T, Yang S, Zhang J, Wang HH, Nie Z (2018) A DNA-mediated chemically induced dimerization (D-CID) nanodevice for nongenetic receptor engineering to control cell behavior. Angew Chem Int Ed 57(32):10226–10230. https://doi.org/10.1002/anie.201806155
Dirks RM, Pierce NA (2004) Triggered amplification by hybridization chain reaction. Proc Natl Acad Sci USA 101(43):15275–15278. https://doi.org/10.1073/pnas.0407024101
Choi HMT, Chang JY, Trinh LA, Padilla JE, Fraser SE, Pierce NA (2010) Programmable in situ amplification for multiplexed imaging of mrna expression. Nat Biotechnol 28(11):1208–1212. https://doi.org/10.1038/nbt.1692
Zhu G, Zheng J, Song E, Donovan M, Zhang K, Liu C, Tan W (2013) Self-assembled, aptamer-tethered DNA nanotrains for targeted transport of molecular drugs in cancer theranostics. Proc Natl Acad Sci USA 110(20):7998–8003. https://doi.org/10.1073/pnas.1220817110
Venkataraman S, Dirks RM, Rothemund PW, Winfree E, Pierce NA (2007) An autonomous polymerization motor powered by DNA hybridization. Nat Nanotechnol 2(8):490–494. https://doi.org/10.1038/nnano.2007.225
Cangialosi A, Yoon C, Liu J, Huang Q, Guo J, Nguyen TD, Gracias DH, Schulman R (2017) DNA sequence-directed shape change of photopatterned hydrogels via high-degree swelling. Science 357(6356):1126–1130. https://doi.org/10.1126/science.aan3925
Zhang H, Wang Y, Zhang H, Liu X, Lee A, Huang Q, Wang F, Chao J, Liu H, Li J, Shi J, Zuo X, Wang L, Wang L, Cao X, Bustamante C, Tian Z, Fan C (2019) Programming chain-growth copolymerization of DNA hairpin tiles for in-vitro hierarchical supramolecular organization. Nat Commun 10(1):1006. https://doi.org/10.1038/s41467-019-09004-4
Nie Z, Wang P, Tian C, Mao C (2014) Synchronization of two assembly processes to build responsive DNA nanostructures. Angew Chem Int Ed 53(32):8402–8405. https://doi.org/10.1002/anie.201404307
Zhang DY, Turberfield AJ, Yurke B, Winfree E (2007) Engineering entropy-driven reactions and networks catalyzed by DNA. Science 318(5853):1121–1125. https://doi.org/10.1126/science.1148532
Yin P, Choi HM, Calvert CR, Pierce NA (2008) Programming biomolecular self-assembly pathways. Nature 451(7176):318–322. https://doi.org/10.1038/nature06451
Li B, Ellington AD, Chen X (2011) Rational, modular adaptation of enzyme-free DNA circuits to multiple detection methods. Nucleic Acids Res 39(16):e110. https://doi.org/10.1093/nar/gkr504
Zhang DY, Hariadi RF, Choi HMT, Winfree E (2013) Integrating DNA strand-displacement circuitry with DNA tile self-assembly. Nat Commun 4:1965. https://doi.org/10.1038/ncomms2965
Amodio A, Zhao B, Porchetta A, Idili A, Castronovo M, Fan CH, Ricci F (2014) Rational design of pH-controlled DNA strand displacement. J Am Chem Soc 136(47):16469–16472. https://doi.org/10.1021/ja508213d
Xing C, Dai J, Huang Y, Lin Y, Zhang KL, Lu C, Yang H (2019) Active self-assembly of train-shaped DNA nanostructures via catalytic hairpin assembly reactions. Small 15(27):e1901795. https://doi.org/10.1002/smll.201901795
Barish RD, Schulman R, Rothemund PWK, Winfree E (2009) An information-bearing seed for nucleating algorithmic self-assembly. Proc Natl Acad Sci USA 106(15):6054–6059. https://doi.org/10.1073/pnas.0808736106
Agrawal DK, Jiang R, Reinhart S, Mohammed AM, Jorgenson TD, Schulman R (2017) Terminating DNA tile assembly with nanostructured caps. ACS Nano 11(10):9770–9779. https://doi.org/10.1021/acsnano.7b02256
Mohammed AM, Sulc P, Zenk J, Schulman R (2017) Self-assembling DNA nanotubes to connect molecular landmarks. Nat Nanotechnol 12(4):312–316. https://doi.org/10.1038/nnano.2016.277
Kirschner M, Mitchison T (1986) Beyond self-assembly: From microtubules to morphogenesis. Cell 45(3):329–342. https://doi.org/10.1016/0092-8674(86)90318-1
Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112(4):453–465. https://doi.org/10.1016/s0092-8674(03)00120-x
Lazarides E (1980) Intermediate filaments as mechanical integrators of cellular space. Nature 283(5744):249–256. https://doi.org/10.1038/283249a0
Zaikin AN, Zhabotinsky AM (1970) Concentration wave propagation in two-dimensional liquid-phase self-oscillating system. Nature 225(5232):535–537. https://doi.org/10.1038/225535b0
Epstein IR, Showalter K (1996) Nonlinear chemical dynamics: oscillations, patterns, and chaos. J Phys Chem 100(31):13132–13147. https://doi.org/10.1021/jp953547m
Kim J, Winfree E (2011) Synthetic in vitro transcriptional oscillators. Mol Syst Biol 7:465. https://doi.org/10.1038/msb.2010.119
Franco E, Friedrichs E, Kim J, Jungmann R, Murray R, Winfree E, Simmel FC (2011) Timing molecular motion and production with a synthetic transcriptional clock. Proc Natl Acad Sci USA 108(40):E784–793. https://doi.org/10.1073/pnas.1100060108
Acknowledgements
The authors acknowledge the financial support of the National Natural Science Foundation of China (no. 21977112), Natural Science Foundation of Jiangsu Province (BK20190227) and Chinese Academy of Sciences (Y9BES11, Y9AAS110).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
On behalf of all authors, Chao Zhou and Qiangbin Wang states that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is part of the Topical Collection “DNA Nanotechnology: From Structure to Functionality”; edited by Chunhai Fan, Yonggang Ke.
Rights and permissions
About this article
Cite this article
Dong, J., Zhou, C. & Wang, Q. Towards Active Self-Assembly Through DNA Nanotechnology. Top Curr Chem (Z) 378, 33 (2020). https://doi.org/10.1007/s41061-020-0297-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s41061-020-0297-5