journal article·2024Open access

Variable gain DNA nanostructure charge amplifiers for biosensing

Jacob M. Majikes, Seulki Cho, Thomas E. Cleveland, J. Alexander Liddle, Arvind Balijepalli

Nanoscale· Volume 16· Issue 45

Abstract

Electronic measurements of engineered nanostructures comprised solely of DNA (DNA origami) enable new signal conditioning modalities for use in biosensing. DNA origami, designed to take on arbitrary shapes and allow programmable motion triggered by conjugated biomolecules, have sufficient mass and charge to generate a large electrochemical signal. Here, we demonstrate the ability to electrostatically control the DNA origami conformation, and thereby the resulting signal amplification, when the structure binds a nucleic acid analyte. Critically, unlike previous studies that employ DNA origami to amplify an electrical signal, we show that the conformation changes under an applied field are reversible. This applied field also simultaneously accelerates structural transitions above the rate determined by thermal motion. We tuned this property of the structures to achieve a response that was ≈2 × 104 times greater (i.e., a gain or amplification) than the value from DNA hybridization under similar conditions. Because this signal amplification is independent of DNA origami-analyte interactions, our approach is agnostic of the end application. Furthermore, since large signal changes are only triggered in response to desirable interactions, we minimize the deleterious effects of non-specific binding. The above benefits of self-assembled DNA origami make them ideally suited for multiplexed biosensing when paired with highly parallel electronic readout.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Advanced biosensing and bioanalysis techniques · Plasmonic and Surface Plasmon Research · Microfluidic and Bio-sensing Technologies

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Microsystems and Nanotechnology Division, National Institute of Standards and Technology, Gaithersburg, MD 20899, USA

Biomolecular Measurement Division, National Institute of Standards and Technology, Gaithersburg, MD 20899, USA

Institute for Bioscience and Biotechnology Research, University of Maryland, Rockville, MD 20850, USA

Funding

National Institute of Standards and Technology

References (43)

Show source-provided references
1. Rothemund · Nature · 2006 · 440 · 29710.1038/nature04586 ↗
2. Marras · Proc. Natl. Acad. Sci. U. S. A. · 2015 · 112 · 71310.1073/pnas.1408869112 ↗
3. Dey · Nat. Rev. Methods Primers · 2021 · 1 · 110.1038/s43586-020-00009-8 ↗
4. Wang · Sensors · 2020 · 20 · 689910.3390/s20236899 ↗
5. Chandrasekaran · Nucleic Acids Res. · 2019 · 47 · 1048910.1093/nar/gkz580 ↗
6. Funck · Angew. Chem., Int. Ed. · 2018 · 57 · 1349510.1002/anie.201807029 ↗
7. Thacker · Nat. Commun. · 2014 · 5 · 344810.1038/ncomms4448 ↗
8. Trofymchuk · ACS Nano · 2023 · 17 · 132710.1021/acsnano.2c09577 ↗
9. Minev · Nat. Commun. · 2021 · 12 · 174110.1038/s41467-021-21755-7 ↗
10. Majikes · Bioconjugate Chem. · 2017 · 28 · 182110.1021/acs.bioconjchem.7b00288 ↗
11. Julin · ACS Nano · 2023 · 17 · 1101410.1021/acsnano.3c03438 ↗
12. Kroener · J. Am. Chem. Soc. · 2017 · 139 · 1651010.1021/jacs.7b10862 ↗
13. Chang · Anal. Chem. · 2021 · 93 · 1207510.1021/acs.analchem.1c02343 ↗
14. Williamson · ACS Sens. · 2023 · 8 · 147110.1021/acssensors.2c02469 ↗
15. Tayyab · Sci. Adv. · 2023 · 9 · eadi499710.1126/sciadv.adi4997 ↗
16. Liu · Anal. Chem. · 2023 · 96 · 82810.1021/acs.analchem.3c04340 ↗
17. V.Walawalkar , M. S.Sajal , Y.Gilpin , M.Dandin and R. E.Taylor , bioRxiv , 2023 , preprint, 2023.03.02.530881, 10.1101/2023.03.02.53088110.1101/2023.03.02.530881 ↗
18. Robinson · Biosensors · 2019 · 9 · 5410.3390/bios9020054 ↗
19. Xiao · Nat. Protoc. · 2007 · 2 · 287510.1038/nprot.2007.413 ↗
20. Lin · Nat. Protoc. · 2016 · 11 · 124410.1038/nprot.2016.071 ↗
21. Qing · Sci. Adv. · 2023 · 9 · eadf140210.1126/sciadv.adf1402 ↗
22. Ortega · Annu. Rev. Biophys. · 2023 · 52 · 31910.1146/annurev-biophys-091222-082247 ↗
23. Ye · Nat. Nanotechnol. · 2024 · 19 · 33010.1038/s41565-023-01513-0 ↗
24. Majikes · Nanoscale · 2022 · 14 · 1558610.1039/D2NR04040A ↗
25. Liu · Front. Bioeng. Biotechnol. · 2021 · 70761510.3389/fbioe.2021.707615 ↗
26. Wang · Sci Rep · 2023 · 13 · 1519610.1038/s41598-023-41459-w ↗
27. Darcy · ACS Nano · 2022 · 16 · 568210.1021/acsnano.1c10698 ↗
28. Wang · Nucleic Acids Res. · 2021 · 49 · 898710.1093/nar/gkab656 ↗
29. Liu · IEEE Sens. J. · 2022 · 22 · 1246010.1109/JSEN.2022.3176601 ↗
30. A. J.Bard and L. R.Faulkner , Electrochemical Methods: Fundamentals and Applications , Wiley , 2nd edn, 2000
31. Josephs · J. Am. Chem. Soc. · 2012 · 134 · 1002110.1021/ja3010946 ↗
32. Kelley · Langmuir · 1998 · 14 · 678110.1021/la980874n ↗
33. Modi · J. Phys. Chem. Lett. · 2010 · 1 · 199410.1021/jz1004957 ↗
34. Steel · Anal. Chem. · 1998 · 70 · 467010.1021/ac980037q ↗
35. S.Cho , A.Zaslavsky , C. A.Richter , J. M.Majikes , J. A.Liddle , F.Andrieu , S.Barraud and A.Balijepalli , in 2022 International Electron Devices Meeting (IEDM) , 2022 , pp. 24.2.1–24.2.4
36. Le · Nanoscale · 2019 · 11 · 1562210.1039/C9NR03171E ↗
37. Thévenot · Biosens. Bioelectron. · 2001 · 16 · 12110.1016/S0956-5663(01)00115-4 ↗
38. B.Jeon , M. M.Guareschi , J. M.Stewart , E.Wu , A.Gopinath , N.Arroyo-Currás , P.Dauphin-Ducharme , P. S.Lukeman , K. W.Plaxco and P. W. K.Rothemund , arXiv , 2023 , preprint, arXiv:2312.06554, 10.48550/arXiv.2312.0655410.48550/arXiv.2312.06554 ↗
39. Park · Sensors · 2009 · 9 · 951310.3390/s91209513 ↗
40. Arnaout · Clin. Infect. Dis. · 2021 · 73 · e304210.1093/cid/ciaa1382 ↗
41. Baranwal · Chemosensors · 2022 · 10 · 36310.3390/chemosensors10090363 ↗
42. Duan · Nat. Nanotechnol. · 2012 · 7 · 40110.1038/nnano.2012.82 ↗
43. Yin · Chem. Res. Chin. Univ. · 2020 · 36 · 21910.1007/s40242-020-9086-5 ↗