Nuclease resistance of DNA nanostructures.


Journal

Nature reviews. Chemistry
ISSN: 2397-3358
Titre abrégé: Nat Rev Chem
Pays: England
ID NLM: 101703631

Informations de publication

Date de publication:
Apr 2021
Historique:
accepted: 08 01 2021
medline: 1 4 2021
pubmed: 1 4 2021
entrez: 28 4 2023
Statut: ppublish

Résumé

DNA nanotechnology has progressed from proof-of-concept demonstrations of structural design towards application-oriented research. As a natural material with excellent self-assembling properties, DNA is an indomitable choice for various biological applications, including biosensing, cell modulation, bioimaging and drug delivery. However, a major impediment to the use of DNA nanostructures in biological applications is their susceptibility to attack by nucleases present in the physiological environment. Although several DNA nanostructures show enhanced resistance to nuclease attack compared with duplexes and plasmid DNA, this may be inadequate for practical application. Recently, several strategies have been developed to increase the nuclease resistance of DNA nanostructures while retaining their functions, and the stability of various DNA nanostructures has been studied in biological fluids, such as serum, urine and cell lysates. This Review discusses the approaches used to modulate nuclease resistance in DNA nanostructures and provides an overview of the techniques employed to evaluate resistance to degradation and quantify stability.

Identifiants

pubmed: 37117281
doi: 10.1038/s41570-021-00251-y
pii: 10.1038/s41570-021-00251-y
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

225-239

Informations de copyright

© 2021. Springer Nature Limited.

Références

Seeman, N. C. Nucleic acid junctions and lattices. J. Theor. Biol. 99, 237–247 (1982).
pubmed: 6188926 doi: 10.1016/0022-5193(82)90002-9
Seeman, N. C. et al. New motifs in DNA nanotechnology. Nanotechnology 9, 257–273 (1998).
doi: 10.1088/0957-4484/9/3/018
Seeman, N. C. DNA in a material world. Nature 421, 427–431 (2003).
pubmed: 12540916 doi: 10.1038/nature01406
Chandrasekaran, A. R. & Zhuo, R. A ‘tile’ tale: hierarchical self-assembly of DNA lattices. Appl. Mater. Today 2, 7–16 (2016).
doi: 10.1016/j.apmt.2015.11.004
Seeman, N. C. DNA Nanotechnology at 40. Nano Lett. 20, 1477–1478 (2020).
pubmed: 32011893 doi: 10.1021/acs.nanolett.0c00325
Seeman, N. C. & Sleiman, H. F. DNA nanotechnology. Nat. Rev. Mater. 3, 17068 (2018).
doi: 10.1038/natrevmats.2017.68
Xavier, P. L. & Chandrasekaran, A. R. DNA-based construction at the nanoscale: emerging trends and applications. Nanotechnology 29, 062001 (2018).
pubmed: 29232197 doi: 10.1088/1361-6528/aaa120
Hong, F., Zhang, F., Liu, Y. & Yan, H. DNA origami: scaffolds for creating higher order structures. Chem. Rev. 117, 12584–12640 (2017).
pubmed: 28605177 doi: 10.1021/acs.chemrev.6b00825
Liu, L., Li, Z., Li, Y. & Mao, C. Rational design and self-assembly of two-dimensional, dodecagonal DNA quasicrystals. J. Am. Chem. Soc. 141, 4248–4251 (2019).
pubmed: 30827097 doi: 10.1021/jacs.9b00843
He, Y. et al. Hierarchical self-assembly of DNA into symmetric supramolecular polyhedra. Nature 452, 198–201 (2008).
pubmed: 18337818 doi: 10.1038/nature06597
Benson, E. et al. DNA rendering of polyhedral meshes at the nanoscale. Nature 523, 441–444 (2015).
pubmed: 26201596 doi: 10.1038/nature14586
Andersen, E. S. et al. Self-assembly of a nanoscale DNA box with a controllable lid. Nature 459, 73–76 (2009).
pubmed: 19424153 doi: 10.1038/nature07971
Gu, H., Chao, J., Xiao, S.-J. & Seeman, N. C. A proximity-based programmable DNA nanoscale assembly line. Nature 465, 202–205 (2010).
pubmed: 20463734 pmcid: 2872101 doi: 10.1038/nature09026
Tikhomirov, G., Petersen, P. & Qian, L. Fractal assembly of micrometre-scale DNA origami arrays with arbitrary patterns. Nature 552, 67–71 (2017).
pubmed: 29219965 doi: 10.1038/nature24655
Chandrasekaran, A. R., Anderson, N., Kizer, M., Halvorsen, K. & Wang, X. Beyond the fold: emerging biological applications of DNA origami. ChemBioChem 17, 1081–1089 (2016).
pubmed: 26928725 doi: 10.1002/cbic.201600038
Chandrasekaran, A. R. DNA origami and biotechnology applications: a perspective. J. Chem. Technol. Biotechnol. 91, 843–846 (2016).
doi: 10.1002/jctb.4826
Chandrasekaran, A. R. & Levchenko, O. DNA nanocages. Chem. Mater. 28, 5569–5581 (2016).
doi: 10.1021/acs.chemmater.6b02546
Li, S. et al. A DNA nanorobot functions as a cancer therapeutic in response to a molecular trigger in vivo. Nat. Biotechnol. 36, 258–264 (2018).
pubmed: 29431737 doi: 10.1038/nbt.4071
Chandrasekaran, A. R. et al. Cellular microRNA detection with miRacles: microRNA-activated conditional looping of engineered switches. Sci. Adv. 5, eaau9443 (2019).
pubmed: 30891499 pmcid: 6415953 doi: 10.1126/sciadv.aau9443
Bhatia, D., Surana, S., Chakraborty, S., Koushika, S. P. & Krishnan, Y. A synthetic icosahedral DNA-based host–cargo complex for functional in vivo imaging. Nat. Commun. 2, 339 (2011).
pubmed: 21654639 doi: 10.1038/ncomms1337
Shi, S. et al. Modulation of chondrocyte motility by tetrahedral DNA nanostructures. Cell Prolif. 50, e12368 (2017).
pmcid: 6529109 doi: 10.1111/cpr.12368
Xiao, M. et al. Rationally engineered nucleic acid architectures for biosensing applications. Chem. Rev. 119, 11631–11717 (2019).
pubmed: 31573184 doi: 10.1021/acs.chemrev.9b00121
Ye, D., Zuo, X. & Fan, C. DNA nanotechnology-enabled interfacial engineering for biosensor development. Annu. Rev. Anal. Chem. 11, 171–195 (2018).
doi: 10.1146/annurev-anchem-061417-010007
Chandrasekaran, A. R., Wady, H. & Subramanian, H. K. K. Nucleic acid nanostructures for chemical and biological sensing. Small 12, 2689–2700 (2016).
pubmed: 27040036 doi: 10.1002/smll.201503854
Hu, Q., Li, H., Wang, L., Gu, H. & Fan, C. DNA nanotechnology-enabled drug delivery systems. Chem. Rev. 119, 6459–6506 (2019).
pubmed: 29465222 doi: 10.1021/acs.chemrev.7b00663
Madhanagopal, B. R., Zhang, S., Demirel, E., Wady, H. & Chandrasekaran, A. R. DNA nanocarriers: programmed to deliver. Trends Biochem. Sci. 43, 997–1013 (2018).
pubmed: 30342801 doi: 10.1016/j.tibs.2018.09.010
Linko, V., Ora, A. & Kostiainen, M. A. DNA nanostructures as smart drug-delivery vehicles and molecular devices. Trends Biotechnol. 33, 586–594 (2015).
pubmed: 26409777 doi: 10.1016/j.tibtech.2015.08.001
Jiang, D., England, C. G. & Cai, W. DNA nanomaterials for preclinical imaging and drug delivery. J. Control. Release 239, 27–38 (2016).
pubmed: 27527555 pmcid: 5037045 doi: 10.1016/j.jconrel.2016.08.013
Mathur, D. & Medintz, I. L. The growing development of DNA nanostructures for potential healthcare-related applications. Adv. Healthc. Mater. 8, 1801546 (2019).
doi: 10.1002/adhm.201801546
Chakraborty, K., Veetil, A. T., Jaffrey, S. R. & Krishnan, Y. Nucleic acid–based nanodevices in biological imaging. Annu. Rev. Biochem. 85, 349–373 (2016).
pubmed: 27294440 pmcid: 5522603 doi: 10.1146/annurev-biochem-060815-014244
Rajwar, A., Kharbanda, S., Chandrasekaran, A. R., Gupta, S. & Bhatia, D. Designer, programmable 3D DNA nanodevices to probe biological systems. ACS Appl. Bio Mater. 3, 7265–7277 (2020).
pubmed: 35019470 doi: 10.1021/acsabm.0c00916
Zhao, N., Chen, Y., Chen, G. & Xiao, Z. Artificial cells based on DNA nanotechnology. ACS Appl. Bio Mater. 3, 3928–3934 (2020).
pubmed: 35025469 doi: 10.1021/acsabm.0c00149
Kuzuya, A. & Ohya, Y. DNA nanostructures as scaffolds for metal nanoparticles. Polym. J. 44, 452–460 (2012).
doi: 10.1038/pj.2012.38
Chandrasekaran, A. R. Programmable DNA scaffolds for spatially-ordered protein assembly. Nanoscale 8, 4436–4446 (2016).
pubmed: 26852879 doi: 10.1039/C5NR08685J
Bhatia, D. et al. Icosahedral DNA nanocapsules by modular assembly. Angew. Chem. Int. Ed. 48, 4134–4137 (2009).
doi: 10.1002/anie.200806000
He, Y., Chen, Y., Liu, H., Ribbe, A. E. & Mao, C. Self-assembly of hexagonal DNA two-dimensional (2D) arrays. J. Am. Chem. Soc. 127, 12202–12203 (2005).
pubmed: 16131180 doi: 10.1021/ja0541938
Rothemund, P. W. K. Folding DNA to create nanoscale shapes and patterns. Nature 440, 297–302 (2006).
pubmed: 16541064 doi: 10.1038/nature04586
Ke, Y., Ong, L. L., Shih, W. M. & Yin, P. Three-dimensional structures self-assembled from DNA bricks. Science 338, 1177–1183 (2012).
pubmed: 23197527 doi: 10.1126/science.1227268
Chandrasekaran, A. R. & Halvorsen, K. Controlled disassembly of a DNA tetrahedron using strand displacement. Nanoscale Adv. 1, 969–972 (2019).
pubmed: 31179419 doi: 10.1039/C8NA00340H
Pei, H. et al. Reconfigurable three-dimensional DNA nanostructures for the construction of intracellular logic sensors. Angew. Chem. Int. Ed. 51, 9020–9024 (2012).
doi: 10.1002/anie.201202356
Douglas, S. M., Bachelet, I. & Church, G. M. A logic-gated nanorobot for targeted transport of molecular payloads. Science 335, 831–834 (2012).
pubmed: 22344439 doi: 10.1126/science.1214081
Dittmer, W. U., Reuter, A. & Simmel, F. C. A DNA-based machine that can cyclically bind and release thrombin. Angew. Chem. Int. Ed. 43, 3550–3553 (2004).
doi: 10.1002/anie.200353537
Modi, S. et al. A DNA nanomachine that maps spatial and temporal pH changes inside living cells. Nat. Nanotechnol. 4, 325–330 (2009).
pubmed: 19421220 doi: 10.1038/nnano.2009.83
Idili, A., Vallée-Bélisle, A. & Ricci, F. Programmable pH-triggered DNA nanoswitches. J. Am. Chem. Soc. 136, 5836–5839 (2014).
pubmed: 24716858 doi: 10.1021/ja500619w
Juul, S. et al. Temperature-controlled encapsulation and release of an active enzyme in the cavity of a self-assembled DNA nanocage. ACS Nano 7, 9724–9734 (2013).
pubmed: 24168393 doi: 10.1021/nn4030543
Kohman, R. E. & Han, X. Light sensitization of DNA nanostructures via incorporation of photo-cleavable spacers. Chem. Commun. 51, 5747–5750 (2015).
doi: 10.1039/C5CC00082C
Chandrasekaran, A. R., Punnoose, J. A., Valsangkar, V., Sheng, J. & Halvorsen, K. Integration of a photocleavable element into DNA nanoswitches. Chem. Commun. 55, 6587–6590 (2019).
doi: 10.1039/C9CC03069G
Pinheiro, A. V., Han, D., Shih, W. M. & Yan, H. Challenges and opportunities for structural DNA nanotechnology. Nat. Nanotechnol. 6, 763–772 (2011).
pubmed: 22056726 pmcid: 3334823 doi: 10.1038/nnano.2011.187
Jones, M. R., Seeman, N. C. & Mirkin, C. A. Programmable materials and the nature of the DNA bond. Science 347, 1260901 (2015).
pubmed: 25700524 doi: 10.1126/science.1260901
Dunn, K. E. The business of DNA nanotechnology: commercialization of origami and other technologies. Molecules 25, 377 (2020).
pmcid: 7024392 doi: 10.3390/molecules25020377
Linko, V. & Dietz, H. The enabled state of DNA nanotechnology. Curr. Opin. Biotechnol. 24, 555–561 (2013).
pubmed: 23566376 doi: 10.1016/j.copbio.2013.02.001
Kershner, R. J. et al. Placement and orientation of individual DNA shapes on lithographically patterned surfaces. Nat. Nanotechnol. 4, 557–561 (2009).
pubmed: 19734926 doi: 10.1038/nnano.2009.220
Takabayashi, S. et al. Boron-implanted silicon substrates for physical adsorption of DNA origami. Int. J. Mol. Sci. 19, 2513 (2018).
pmcid: 6165417 doi: 10.3390/ijms19092513
Qian, L. & Winfree, E. Scaling up digital circuit computation with DNA strand displacement cascades. Science 332, 1196–1201 (2011).
pubmed: 21636773 doi: 10.1126/science.1200520
Erlich, Y. & Zielinski, D. DNA fountain enables a robust and efficient storage architecture. Science 355, 950–954 (2017).
pubmed: 28254941 doi: 10.1126/science.aaj2038
Sun, W. et al. Casting inorganic structures with DNA molds. Science 346, 1258361 (2014).
pubmed: 25301973 pmcid: 4260265 doi: 10.1126/science.1258361
Weichelt, R., Ye, J., Banin, U., Eychmüller, A. & Seidel, R. DNA-mediated self-assembly and metallization of semiconductor nanorods for the fabrication of nanoelectronic interfaces. Chem. Eur. J. 25, 9012–9016 (2019).
pubmed: 31081977 doi: 10.1002/chem.201902148
Liao, S. & Seeman, N. C. Translation of DNA signals into polymer assembly instructions. Science 306, 2072–2074 (2004).
pubmed: 15604403 pmcid: 3470904 doi: 10.1126/science.1104299
Chen, Y. & Mao, C. Reprogramming DNA-directed reactions on the basis of a DNA conformational change. J. Am. Chem. Soc. 126, 13240–13241 (2004).
pubmed: 15479075 doi: 10.1021/ja045718j
Martin, T. G. et al. Design of a molecular support for cryo-EM structure determination. Proc. Natl Acad. Sci. USA 113, E7456–E7463 (2016).
pubmed: 27821763 pmcid: 5127339 doi: 10.1073/pnas.1612720113
Douglas, S. M., Chou, J. J. & Shih, W. M. DNA-nanotube-induced alignment of membrane proteins for NMR structure determination. Proc. Natl Acad. Sci. USA 104, 6644–6648 (2007).
pubmed: 17404217 pmcid: 1871839 doi: 10.1073/pnas.0700930104
Hernandez, C. et al. Self-assembly of 3D DNA crystals containing a torsionally stressed component. Cell Chem. Biol. 24, 1401–1406.e2 (2017).
pubmed: 28988948 doi: 10.1016/j.chembiol.2017.08.018
Chandrasekaran, A. R. et al. DNA nanotechnology approaches for microRNA detection and diagnosis. Nucleic Acids Res. 47, 10489–10505 (2019).
pubmed: 31287874 pmcid: 6847506 doi: 10.1093/nar/gkz580
Coleridge, E. L. & Dunn, K. E. Assessing the cost-effectiveness of DNA origami nanostructures for targeted delivery of anti-cancer drugs to tumours. Biomed. Phys. Eng. Express 6, 065030 (2020).
doi: 10.1088/2057-1976/abbe73
Zhou, L. et al. Programmable low-cost DNA-based platform for viral RNA detection. Sci. Adv. 6, eabc6246 (2020).
pubmed: 32978154 pmcid: 7518872 doi: 10.1126/sciadv.abc6246
Li, Y., Cu, Y. T. H. & Luo, D. Multiplexed detection of pathogen DNA with DNA-based fluorescence nanobarcodes. Nat. Biotechnol. 23, 885–889 (2005).
pubmed: 15951805 pmcid: 7097058 doi: 10.1038/nbt1106
Chandrasekaran, A. R. et al. DNA nanoswitch barcodes for multiplexed biomarker profiling. Nano Lett. 21, 469–475 (2021).
pubmed: 33395311 pmcid: 8059342 doi: 10.1021/acs.nanolett.0c03929
Porchetta, A. et al. Programmable nucleic acid nanoswitches for the rapid, single-step detection of antibodies in bodily fluids. J. Am. Chem. Soc. 140, 947–953 (2018).
pubmed: 29313682 doi: 10.1021/jacs.7b09347
Liang, L. et al. Single-particle tracking and modulation of cell entry pathways of a tetrahedral DNA nanostructure in live cells. Angew. Chem. Int. Ed. 53, 7745–7750 (2014).
doi: 10.1002/anie.201403236
Hu, R. et al. DNA nanoflowers for multiplexed cellular imaging and traceable targeted drug delivery. Angew. Chem. Int. Ed. 53, 5821–5826 (2014).
doi: 10.1002/anie.201400323
Valsangkar, V. A. et al. Click and photo-release dual-functional nucleic acid nanostructures. Chem. Commun. 55, 9709–9712 (2019).
doi: 10.1039/C9CC03806J
Messaoudi, S., Greschner, A. A. & Gauthier, M. A. Progress toward absorption, distribution, metabolism, elimination, and toxicity of DNA nanostructures. Adv. Ther. 2, 1900144 (2019).
doi: 10.1002/adtp.201900144
Schüller, V. J. et al. Cellular immunostimulation by CpG-sequence-coated DNA origami structures. ACS Nano 5, 9696–9702 (2011).
pubmed: 22092186 doi: 10.1021/nn203161y
Rosier, B. J. H. M. et al. Incorporation of native antibodies and Fc-fusion proteins on DNA nanostructures via a modular conjugation strategy. Chem. Commun. 53, 7393–7396 (2017).
doi: 10.1039/C7CC04178K
Stewart, J. M. et al. Programmable RNA microstructures for coordinated delivery of siRNAs. Nanoscale 8, 17542–17550 (2016).
pubmed: 27714127 pmcid: 5510167 doi: 10.1039/C6NR05085A
Fakhoury, J. J., McLaughlin, C. K., Edwardson, T. W., Conway, J. W. & Sleiman, H. F. Development and characterization of gene silencing DNA cages. Biomacromolecules 15, 276–282 (2014).
pubmed: 24328173 doi: 10.1021/bm401532n
Liu, X. et al. A DNA nanostructure platform for directed assembly of synthetic vaccines. Nano Lett. 12, 4254–4259 (2012).
pubmed: 22746330 doi: 10.1021/nl301877k
Song, L. et al. DNA origami/gold nanorod hybrid nanostructures for the circumvention of drug resistance. Nanoscale 9, 7750–7754 (2017).
pubmed: 28581004 doi: 10.1039/C7NR02222K
Aldaye, F. A., Senapedis, W. T., Silver, P. A. & Way, J. C. A structurally tunable DNA-based extracellular matrix. J. Am. Chem. Soc. 132, 14727–14729 (2010).
pubmed: 20925350 pmcid: 3092387 doi: 10.1021/ja105431h
Zhou, M. et al. Effect of tetrahedral DNA nanostructures on proliferation and osteo/odontogenic differentiation of dental pulp stem cells via activation of the notch signaling pathway. Nanomed. Nanotechnol. Biol. Med. 14, 1227–1236 (2018).
doi: 10.1016/j.nano.2018.02.004
Stephanopoulos, N. et al. Bioactive DNA-peptide nanotubes enhance the differentiation of neural stem cells into neurons. Nano Lett. 15, 603–609 (2015).
pubmed: 25546084 doi: 10.1021/nl504079q
Zhang, Q. et al. Anti-inflammatory and antioxidative effects of tetrahedral DNA nanostructures via the modulation of macrophage responses. ACS Appl. Mater. Interfaces 10, 3421–3430 (2018).
pubmed: 29300456 doi: 10.1021/acsami.7b17928
Peng, Q. et al. Understanding the biomedical effects of the self-assembled tetrahedral DNA nanostructure on living cells. ACS Appl. Mater. Interfaces 8, 12733–12739 (2016).
pubmed: 27153101 doi: 10.1021/acsami.6b03786
Jia, R. et al. Aptamer-functionalized activatable DNA tetrahedron nanoprobe for PIWI-interacting RNA imaging and regulating in cancer cells. Anal. Chem. 91, 15107–15113 (2019).
pubmed: 31691558 doi: 10.1021/acs.analchem.9b03819
Wang, S., Xia, M., Liu, J., Zhang, S. & Zhang, X. Simultaneous imaging of three tumor-related mRNAs in living cells with a DNA tetrahedron-based multicolor nanoprobe. ACS Sens. 2, 735–739 (2017).
pubmed: 28723114 doi: 10.1021/acssensors.7b00290
Liu, X., Wu, L., Wang, L. & Jiang, W. A dual-targeting DNA tetrahedron nanocarrier for breast cancer cell imaging and drug delivery. Talanta 179, 356–363 (2018).
pubmed: 29310244 doi: 10.1016/j.talanta.2017.11.034
Schmied, J. J. et al. DNA origami–based standards for quantitative fluorescence microscopy. Nat. Protoc. 9, 1367–1391 (2014).
pubmed: 24833175 doi: 10.1038/nprot.2014.079
Jungmann, R. et al. Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and exchange-PAINT. Nat. Methods 11, 313–318 (2014).
pubmed: 24487583 pmcid: 4153392 doi: 10.1038/nmeth.2835
Allentoft, M. E. et al. The half-life of DNA in bone: measuring decay kinetics in 158 dated fossils. Proc. R. Soc. B Biol. Sci. 279, 4724–4733 (2012).
doi: 10.1098/rspb.2012.1745
Rajendran, A., Endo, M., Katsuda, Y., Hidaka, K. & Sugiyama, H. Photo-cross-linking-assisted thermal stability of DNA origami structures and its application for higher-temperature self-assembly. J. Am. Chem. Soc. 133, 14488–14491 (2011).
pubmed: 21859143 doi: 10.1021/ja204546h
Kielar, C. et al. On the stability of DNA origami nanostructures in low-magnesium buffers. Angew. Chem. Int. Ed. 57, 9470–9474 (2018).
doi: 10.1002/anie.201802890
Chandrasekaran, A. R. et al. Exceptional nuclease resistance of paranemic crossover (PX) DNA and crossover-dependent biostability of DNA motifs. J. Am. Chem. Soc. 142, 6814–6821 (2020).
pubmed: 32208657 pmcid: 7315441 doi: 10.1021/jacs.0c02211
Ramakrishnan, S., Krainer, G., Grundmeier, G., Schlierf, M. & Keller, A. Structural stability of DNA origami nanostructures in the presence of chaotropic agents. Nanoscale 8, 10398–10405 (2016).
pubmed: 27142120 doi: 10.1039/C6NR00835F
Myhrvold, C., Dai, M., Silver, P. A. & Yin, P. Isothermal self-assembly of complex DNA structures under diverse and biocompatible conditions. Nano Lett. 13, 4242–4248 (2013).
pubmed: 23978049 doi: 10.1021/nl4019512
Salvati, A. et al. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat. Nanotechnol. 8, 137–143 (2013).
pubmed: 23334168 doi: 10.1038/nnano.2012.237
Yang, W. Nucleases: diversity of structure, function and mechanism. Q. Rev. Biophys. 44, 1–93 (2011).
pubmed: 20854710 doi: 10.1017/S0033583510000181
Champoux, J. J. DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70, 369–413 (2001).
pubmed: 11395412 doi: 10.1146/annurev.biochem.70.1.369
Grindley, N. D. F., Whiteson, K. L. & Rice, P. A. Mechanisms of site-specific recombination. Annu. Rev. Biochem. 75, 567–605 (2006).
pubmed: 16756503 doi: 10.1146/annurev.biochem.73.011303.073908
Patel, A. A. & Steitz, J. A. Splicing double: insights from the second spliceosome. Nat. Rev. Mol. Cell Biol. 4, 960–970 (2003).
pubmed: 14685174 doi: 10.1038/nrm1259
Barry, M. E. et al. Role of endogenous endonucleases and tissue site in transfection and CpG-mediated immune activation after naked DNA injection. Hum. Gene Ther. 10, 2461–2480 (1999).
pubmed: 10543612 doi: 10.1089/10430349950016816
Samejima, K. & Earnshaw, W. C. Trashing the genome: the role of nucleases during apoptosis. Nat. Rev. Mol. Cell Biol. 6, 677–688 (2005).
pubmed: 16103871 doi: 10.1038/nrm1715
Koizumi, T. Deoxyribonuclease II (DNase II) activity in mouse tissues and body fluids. Exp. Anim. 44, 169–171 (1995).
pubmed: 7601228 doi: 10.1538/expanim.44.169
Dietz, H., Douglas, S. M. & Shih, W. M. Folding DNA into twisted and curved nanoscale shapes. Science 325, 725–730 (2009).
pubmed: 19661424 pmcid: 2737683 doi: 10.1126/science.1174251
Castro, C. E. et al. A primer to scaffolded DNA origami. Nat. Methods 8, 221–229 (2011).
pubmed: 21358626 doi: 10.1038/nmeth.1570
Keum, J.-W. & Bermudez, H. Enhanced resistance of DNA nanostructures to enzymatic digestion. Chem. Commun. 7036–7038 (2009).
Goltry, S. et al. DNA topology influences molecular machine lifetime in human serum. Nanoscale 7, 10382–10390 (2015).
pubmed: 25959862 pmcid: 4457601 doi: 10.1039/C5NR02283E
Yurke, B., Turberfield, A. J., Mills, A. P. Jr, Simmel, F. C. & Neumann, J. L. A DNA-fuelled molecular machine made of DNA. Nature 406, 605–608 (2000).
pubmed: 10949296 doi: 10.1038/35020524
Wang, X. et al. Paranemic crossover DNA: there and back again. Chem. Rev. 119, 6273–6289 (2019).
pubmed: 29911864 doi: 10.1021/acs.chemrev.8b00207
Hahn, J., Wickham, S. F. J., Shih, W. M. & Perrault, S. D. Addressing the instability of DNA nanostructures in tissue culture. ACS Nano 8, 8765–8775 (2014).
pubmed: 25136758 pmcid: 4174095 doi: 10.1021/nn503513p
Wamhoff, E.-C. et al. Controlling wireframe DNA origami nuclease degradation with minor groove binders. Preprint at bioRxiv https://www.biorxiv.org/content/10.1101/2020.05.24.110783v1.full (2020).
Li, Y. et al. Universal pH-responsive and metal-ion-free self-assembly of DNA nanostructures. Angew. Chem. Int. Ed. 57, 6892–6895 (2018).
doi: 10.1002/anie.201804054
Li, Y. & Schulman, R. DNA nanostructures that self-heal in serum. Nano Lett. 19, 3751–3760 (2019).
pubmed: 31140279 doi: 10.1021/acs.nanolett.9b00888
Conway, J. W., McLaughlin, C. K., Castor, K. J. & Sleiman, H. DNA nanostructure serum stability: greater than the sum of its parts. Chem. Commun. 49, 1172–1174 (2013).
doi: 10.1039/c2cc37556g
Cassinelli, V. et al. One-step formation of “chain-armor”-stabilized DNA nanostructures. Angew. Chem. Int. Ed. 54, 7795–7798 (2015).
doi: 10.1002/anie.201500561
Gerling, T., Kube, M., Kick, B. & Dietz, H. Sequence-programmable covalent bonding of designed DNA assemblies. Sci. Adv. 4, eaau1157 (2018).
pubmed: 30128357 pmcid: 6097813 doi: 10.1126/sciadv.aau1157
Lacroix, A., Vengut-Climent, E., de Rochambeau, D. & Sleiman, H. F. Uptake and fate of fluorescently labeled DNA nanostructures in cellular environments: a cautionary tale. ACS Cent. Sci. 5, 882–891 (2019).
pubmed: 31139724 pmcid: 6535766 doi: 10.1021/acscentsci.9b00174
Lin, C. et al. Mirror image DNA nanostructures for chiral supramolecular assemblies. Nano Lett. 9, 433–436 (2009).
pubmed: 19063615 pmcid: 2669104 doi: 10.1021/nl803328v
Liu, Q. et al. Enhanced stability of DNA nanostructures by incorporation of unnatural base pairs. ChemPhysChem 18, 2977–2980 (2017).
pubmed: 28856771 doi: 10.1002/cphc.201700809
Chandrasekaran, A. R. et al. Hybrid DNA/RNA nanostructures with 2′-5′ linkages. Nanoscale 12, 21583–21590 (2020).
pubmed: 33089274 pmcid: 7644649 doi: 10.1039/D0NR05846G
Lacroix, A., Edwardson, T. G. W., Hancock, M. A., Dore, M. D. & Sleiman, H. F. Development of DNA nanostructures for high-affinity binding to human serum albumin. J. Am. Chem. Soc. 139, 7355–7362 (2017).
pubmed: 28475327 doi: 10.1021/jacs.7b02917
Kim, Y. & Yin, P. Enhancing biocompatible stability of DNA nanostructures using dendritic oligonucleotides and brick motifs. Angew. Chem. Int. Ed. 59, 700–703 (2020).
doi: 10.1002/anie.201911664
Perrault, S. D. & Shih, W. M. Virus-inspired membrane encapsulation of DNA nanostructures to achieve in vivo stability. ACS Nano 8, 5132–5140 (2014).
pubmed: 24694301 pmcid: 4046785 doi: 10.1021/nn5011914
Ahmadi, Y., Llano, E. D. & Barišić, I. (Poly)cation-induced protection of conventional and wireframe DNA origami nanostructures. Nanoscale 10, 7494–7504 (2018).
pubmed: 29637957 doi: 10.1039/C7NR09461B
Ponnuswamy, N. et al. Oligolysine-based coating protects DNA nanostructures from low-salt denaturation and nuclease degradation. Nat. Commun. 8, 15654 (2017).
pubmed: 28561045 pmcid: 5460023 doi: 10.1038/ncomms15654
Anastassacos, F. M., Zhao, Z., Zeng, Y. & Shih, W. M. Glutaraldehyde cross-linking of oligolysines coating DNA origami greatly reduces susceptibility to nuclease degradation. J. Am. Chem. Soc. 142, 3311–3315 (2020).
pubmed: 32011869 doi: 10.1021/jacs.9b11698
Agarwal, N. P., Matthies, M., Gür, F. N., Osada, K. & Schmidt, T. L. Block copolymer micellization as a protection strategy for DNA origami. Angew. Chem. Int. Ed. 56, 5460–5464 (2017).
doi: 10.1002/anie.201608873
Auvinen, H. et al. Protein coating of DNA nanostructures for enhanced stability and immunocompatibility. Adv. Healthc. Mater. 6, 1700692 (2017).
doi: 10.1002/adhm.201700692
Wang, S.-T. et al. DNA origami protection and molecular interfacing through engineered sequence-defined peptoids. Proc. Natl Acad. Sci. USA 117, 6339–6348 (2020).
pubmed: 32165539 pmcid: 7104344 doi: 10.1073/pnas.1919749117
Miller, S. M. et al. Proteolytic studies of homologous peptide and N-substituted glycine peptoid oligomers. Bioorg. Med. Chem. Lett. 4, 2657–2662 (1994).
doi: 10.1016/S0960-894X(01)80691-0
Nguyen, M.-K. et al. Ultrathin silica coating of DNA origami nanostructures. Chem. Mater. 32, 6657–6665 (2020).
doi: 10.1021/acs.chemmater.0c02111
Chandrasekaran, A. R. & Halvorsen, K. Nuclease degradation analysis of DNA nanostructures using gel electrophoresis. Curr. Protoc. Nucleic Acid. Chem. 82, e115 (2020).
pubmed: 32931657 pmcid: 8034824 doi: 10.1002/cpnc.115
Zagorovsky, K., Chou, L. Y. T. & Chan, W. C. W. Controlling DNA–nanoparticle serum interactions. Proc. Natl. Acad. Sci. USA 113, 13600–13605 (2016).
pubmed: 27856755 pmcid: 5137734 doi: 10.1073/pnas.1610028113
Ramakrishnan, S. et al. Real-time observation of superstructure-dependent DNA origami digestion by DNase I using high-speed atomic force microscopy. ChemBioChem 20, 2818–2823 (2019).
pubmed: 31163091 doi: 10.1002/cbic.201900369
Suck, D. DNA recognition by structure-selective nucleases. Biopolymers 44, 405–421 (1997).
pubmed: 9782777 doi: 10.1002/(SICI)1097-0282(1997)44:4<405::AID-BIP5>3.0.CO;2-L
Hogan, M. E., Roberson, M. W. & Austin, R. H. DNA flexibility variation may dominate DNase I cleavage. Proc. Natl. Acad. Sci. USA 86, 9273–9277 (1989).
pubmed: 2594767 pmcid: 298476 doi: 10.1073/pnas.86.23.9273
Stopar, A., Coral, L., Di Giacomo, S., Adedeji, A. F. & Castronovo, M. Binary control of enzymatic cleavage of DNA origami by structural antideterminants. Nucleic Acids Res. 46, 995–1006 (2018).
pubmed: 29216375 doi: 10.1093/nar/gkx1204
Suma, A., Stopar, A., Nicholson, A. W., Castronovo, M. & Carnevale, V. Global and local mechanical properties control endonuclease reactivity of a DNA origami nanostructure. Nucleic Acids Res. 48, 4672–4680 (2020).
pubmed: 32043111 pmcid: 7229852 doi: 10.1093/nar/gkaa080
Shaw, J.-P., Kent, K., Bird, J., Fishback, J. & Froehler, B. Modified deoxyoligonucleotides stable to exonuclease degradation in serum. Nucleic Acids Res. 19, 747–750 (1991).
pubmed: 1850122 pmcid: 333706 doi: 10.1093/nar/19.4.747
Kurnick, N. B. Desoxyribonuclease activity of sera of man and some other species. Arch. Biochem. Biophys. 43, 97–107 (1953).
pubmed: 13031664 doi: 10.1016/0003-9861(53)90088-5
Osada, K. Development of functional polyplex micelles for systemic gene therapy. Polym. J. 46, 469–475 (2014).
doi: 10.1038/pj.2014.49
Kiviaho, J. K. et al. Cationic polymers for DNA origami coating – examining their binding efficiency and tuning the enzymatic reaction rates. Nanoscale 8, 11674–11680 (2016).
pubmed: 27219684 doi: 10.1039/C5NR08355A
Kizer, M. E. et al. Hydroporator: a hydrodynamic cell membrane perforator for high-throughput vector-free nanomaterial intracellular delivery and DNA origami biostability evaluation. Lab Chip 19, 1747–1754 (2019).
pubmed: 30964485 doi: 10.1039/C9LC00041K
Jun, H. et al. Autonomously designed free-form 2D DNA origami. Sci. Adv. 5, eaav0655 (2019).
pubmed: 30613779 pmcid: 6314877 doi: 10.1126/sciadv.aav0655
Goodman, R. P. et al. Rapid chiral assembly of rigid DNA building blocks for molecular nanofabrication. Science 310, 1661–1665 (2005).
pubmed: 16339440 doi: 10.1126/science.1120367
Winfree, E., Liu, F., Wenzler, L. A. & Seeman, N. C. Design and self-assembly of two-dimensional DNA crystals. Nature 394, 539–544 (1998).
pubmed: 9707114 doi: 10.1038/28998

Auteurs

Arun Richard Chandrasekaran (AR)

The RNA Institute, University at Albany, State University of New York, Albany, NY, USA. arun@albany.edu.

Classifications MeSH