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Digitally encoded DNA nanostructures for multiplexed, single-molecule protein sensing with nanopores
Abstract
The simultaneous detection of a large number of different analytes is important in bionanotechnology research and in diagnostic applications. Nanopore sensing is an attractive method in this regard as the approach can be integrated into small, portable device architectures, and there is significant potential for detecting multiple sub-populations in a sample. Here, we show that highly multiplexed sensing of single molecules can be achieved with solid-state nanopores by using digitally encoded DNA nanostructures. Based on the principles of DNA origami, we designed a library of DNA nanostructures in which each member contains a unique barcode; each bit in the barcode is signalled by the presence or absence of multiple DNA dumbbell hairpins. We show that a 3-bit barcode can be assigned with 94% accuracy by electrophoretically driving the DNA structures through a solid-state nanopore. Select members of the library were then functionalized to detect a single, specific antibody through antigen presentation at designed positions on the DNA. This allows us to simultaneously detect four different antibodies of the same isotype at nanomolar concentration levels.
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“Conversely, in regards to nanopore reads of labeled DNA, each label is read in [10–1; 101] ms.”
From Emerging Approaches to DNA Data Storage: Challenges and Prospects (2022) · cites this paper as [21]
In the citing paper
“The authors used conical quartz nanopores with diameters of ∼14 nm for a 3-bit barcode that could be assigned with 94% accuracy.”
From Emerging Approaches to DNA Data Storage: Challenges and Prospects (2022) · cites this paper as [21]
In the citing paper
“The use of nanopores to read out digital information encoded in DNA nanostructures was demonstrated by Bell and Keyser, who fabricated “DNA barcodes” to capture proteins.21”
From Emerging Approaches to DNA Data Storage: Challenges and Prospects (2022) · cites this paper as [21]
In the citing paper
“More recently, through the use of long DNA backbones as in DNA origami, the organization of DNA protrusions has been used to produce three-dimensional DNA barcodes21 or hard drives that may be read using solid-state nanopores.”
From Emerging Approaches to DNA Data Storage: Challenges and Prospects (2022) · cites this paper as [21]
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Replication‐induced DNA secondary structures drive fork uncoupling and breakage
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“The linear ssDNA scaffold for our designs as the positive control and negative control was obtained by cutting circular M13mp18 DNA (New England Biolabs) at BamHI-HF and EcoRI-HF (New England Biolabs, 100 units/ μ l) restriction sites following our published protocol (Bell & Keyser, 2016).”
BackgroundMethodInfluentialSelf-citationSuper‐Resolution Detection of DNA Nanostructures Using a Nanopore
Chen, K., Choudhary, A., Sandler, S. E., Maffeo, C., Ducati, C., Aksimentiev, A., & Keyser, U. F. (2023) · Advanced Materials · doi:10.1002/adma.202207434 · Cited by 51
Self-citationPromoting single-file DNA translocations through nanopores using electro-osmotic flow
Ermann, N., Hanikel, N., Wang, V., Chen, K., Weckman, N. E., & Keyser, U. F. (2018) · The Journal of Chemical Physics · doi:10.1063/1.5031010 · Cited by 50
Self-citationSpecific Biosensing Using DNA Aptamers and Nanopores
Kong, J., Zhu, J., Chen, K., & Keyser, U. F. (2018) · Advanced Functional Materials · doi:10.1002/adfm.201807555 · Cited by 50
Self-citationSingle Molecule DNA Resensing Using a Two‐Pore Device
Zhang, Y., Liu, X., Zhao, Y., Yu, J., Reisner, W., & Dunbar, W. B. (2018) · Small · doi:10.1002/smll.201801890 · Cited by 49
Zhu, Z., Wu, R., & Li, B. (2018) · Chemical Science · doi:10.1039/c8sc04875d · Cited by 49
Shot noise sets the limit of quantification in electrochemical measurements
Gao, R., Edwards, M. A., Harris, J. M., & White, H. S. (2020) · Current Opinion in Electrochemistry · doi:10.1016/j.coelec.2020.05.010 · Cited by 49
Single‐Molecule Binding Assay Using Nanopores and Dimeric NP Conjugates
Ren, R., Sun, M., Goel, P., Cai, S., Kotov, N. A., Kuang, H., Xu, C., Ivanov, A. P., & Edel, J. B. (2021) · Advanced Materials · doi:10.1002/adma.202103067 · Cited by 48
Promoting single-file DNA translocations through nanopores using electro-osmotic flow
Ermann, N., Hanikel, N., Wang, V, Chen, K., Weckman, N., Keyser, U. F., et al. (2018) · Cambridge University Engineering Department Publications Database · Cited by 48
Self-citationOptical Nanopore Sensors for Quantitative Analysis
Fried, J. P., Wu, Y., Tilley, R. D., & Gooding, J. J. (2022) · Nano Letters · doi:10.1021/acs.nanolett.1c03976 · Cited by 48
Nanopores: a versatile tool to study protein dynamics
Schmid, S., & Dekker, C. (2020) · Essays in Biochemistry · doi:10.1042/ebc20200020 · Cited by 51
“…protein interaction has been studied using DNA carriers and solid-state nanopores: e.g. directly for dCas9 interactions [113,114], or using epitope [115] or aptamer [116] functionalized DNA constructs as designed by the Keyser and Edel labs to specifically detect antibodies, avidin, etc. Lastly,…”
Method3D nanopore shape control by current-stimulus dielectric breakdown
Ying, C., Zhang, Y., Feng, Y., Zhou, D., Wang, D., Xiang, Y., Zhou, W., Chen, Y., Du, C., & Tian, J. (2016) · Applied Physics Letters · doi:10.1063/1.4960636 · Cited by 46
Autonomously Assembled Synthetic Transmembrane Peptide Pore
Smrithi Krishnan, R., Satheesan, R., Puthumadathil, N., Kumar, K. S., Jayasree, P., & Mahendran, K. R. (2019) · Journal of the American Chemical Society · doi:10.1021/jacs.8b09973 · Cited by 45
High-throughput cell and spheroid mechanics in virtual fluidic channels
Panhwar, M. H., Czerwinski, F., Dabbiru, V. A. S., Komaragiri, Y., Fregin, B., Biedenweg, D., Nestler, P., Pires, R. H., & Otto, O. (2020) · Nature Communications · doi:10.1038/s41467-020-15813-9 · Cited by 45
Advanced DNA Nanopore Technologies
Shen, B., Piskunen, P., Nummelin, S., Liu, Q., Kostiainen, M. A., & Linko, V. (2020) · ACS Applied Bio Materials · doi:10.1021/acsabm.0c00879 · Cited by 45
Label-Free, Multiplexed, Single-Molecule Analysis of Protein–DNA Complexes with Nanopores
Celaya, G., Perales-Calvo, J., Muga, A., Moro, F., & Rodríguez‐Larrea, D. (2017) · ACS Nano · doi:10.1021/acsnano.7b01434 · Cited by 43
Zhu, Z., Zhou, Y., Xu, X., Wu, R., Jin, Y., & Li, B. (2017) · Analytical Chemistry · doi:10.1021/acs.analchem.7b03442 · Cited by 43
Metadata
- Authors
- Bell, N. A. W., & Keyser, U. F.
- Affiliations
- University of Cambridge (GB)
- Corresponding author
- Bell, Nicholas A. W.
- Keyser, Ulrich F.
- Venue
- Nature Nanotechnology
- Published
- 2016-04-04
- Volume
- 11
- Issue
- 7
- Pages
- 645-651
- ISSN
- 1748-3387 (ISSN-L)
- 1748-3395
- OpenAlex
- W2329887558
- Cited by
- 345
- References
- 45
- Citations by year
- 2026: 28 · 2025: 37 · 2024: 24 · 2023: 38 · 2022: 39 · 2021: 30 · 2020: 34 · 2019: 39 · 2018: 40 · 2017: 25 · 2016: 10
- FWCI
- 18.29
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Nanotechnology (publishedVersion)
- PubMed (publishedVersion)
- Apollo (University of Cambridge) (acceptedVersion)
- Funders
- Engineering and Physical Sciences Research Council
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › Nanopore and Nanochannel Transport Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Advanced biosensing and bioanalysis techniques
- Physical Sciences › Chemistry › Analytical Chemistry › Electrochemical sensors and biosensors
- Keywords
- DNA nanostructures, DNA origami, solid-state nanopores, nanopore sensing, multiplexed protein detection, single-molecule detection, DNA barcodes, antibody detection, antigen presentation
- MeSH terms
- Binding Sites, DNA, Proteins, Nanotechnology, Nanostructures, Nanopores
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