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Ångström- and Nano-scale Pore-Based Nucleic Acid Sequencing of Current and Emergent Pathogens

Published online by Cambridge University Press:  29 October 2020

Britney A Shepherd ,
Md Rubayat-E Tanjil ,
Yunjo Jeong ,
Bilgenur Baloğlu ,
Jingqiu Liao  and
Michael Cai Wang Open the ORCID record for Michael Cai Wang [Opens in a new window]
Britney A Shepherd
Affiliation:
Department of Medical Engineering, University of South Florida, 4202 E. Fowler Avenue, Tampa, Florida33620, USA.
Md Rubayat-E Tanjil
Affiliation:
Department of Mechanical Engineering, University of South Florida, 4202 E. Fowler Avenue, Tampa, Florida33620, USA.
Yunjo Jeong
Affiliation:
Department of Mechanical Engineering, University of South Florida, 4202 E. Fowler Avenue, Tampa, Florida33620, USA.
Bilgenur Baloğlu*
Affiliation:
Centre for Biodiversity Genomics, University of Guelph, 50 Stone Road East, Guelph, OntarioN1G2W1, Canada.
Jingqiu Liao*
Affiliation:
Department of Systems Biology, Columbia University, 1130 St. Nicholas Avenue, New York, New York10032, USA.
Michael Cai Wang*
Affiliation:
Department of Medical Engineering, University of South Florida, 4202 E. Fowler Avenue, Tampa, Florida33620, USA. Department of Mechanical Engineering, University of South Florida, 4202 E. Fowler Avenue, Tampa, Florida33620, USA.
*
†Author to whom correspondence should be addressed. MCW:mcwang@usf.eduBB:bbaloglu@uoguelph.caJL:jl5897@cumc.columbia.edu
†Author to whom correspondence should be addressed. MCW:mcwang@usf.eduBB:bbaloglu@uoguelph.caJL:jl5897@cumc.columbia.edu
†Author to whom correspondence should be addressed. MCW:mcwang@usf.eduBB:bbaloglu@uoguelph.caJL:jl5897@cumc.columbia.edu

Abstract

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State-of-the-art nanopore sequencing enables rapid and real-time identification of novel pathogens, which has wide application in various research areas and is an emerging diagnostic tool for infectious diseases including COVID-19. Nanopore translocation enables de novo sequencing with long reads (> 10 kb) of novel genomes, which has advantages over existing short-read sequencing technologies. Biological nanopore sequencing has already achieved success as a technology platform but it is sensitive to empirical factors such as pH and temperature. Alternatively, ångström- and nano-scale solid-state nanopores, especially those based on two-dimensional (2D) membranes, are promising next-generation technologies as they can surpass biological nanopores in the variety of membrane materials, ease of defining pore morphology, higher nucleotide detection sensitivity, and facilitation of novel and hybrid sequencing modalities. Since the discovery of graphene, atomically-thin 2D materials have shown immense potential for the fabrication of nanopores with well-defined geometry, rendering them viable candidates for nanopore sequencing membranes. Here, we review recent progress and future development trends of 2D materials and their ångström- and nano-scale pore-based nucleic acid (NA) sequencing including fabrication techniques and current and emerging sequencing modalities. In addition, we discuss the current challenges of translocation-based nanopore sequencing and provide an outlook on promising future research directions.

Type
Articles
Information
MRS Advances , Volume 5 , Issue 56: Materials advances in application to COVID-19 related challenges , 2020 , pp. 2889 - 2906
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
Copyright © The Author(s), 2020, published on behalf of Materials Research Society by Cambridge University Press

Footnotes

*

These authors contributed equally to this work.

References

Baloğlu, B., Chen, Z., Elbrecht, V., Braukmann, T., MacDonald, S., and Steinke, D., “A workflow for accurate metabarcoding using nanopore MinION sequencing 1,” bioRxiv, p. 2020.05.21.108852, May 2020, doi: 10.1101/2020.05.21.108852.Google Scholar
Dao Thi, V. L. et al. , “A colorimetric RT-LAMP assay and LAMP-sequencing for detecting SARS-CoV-2 RNA in clinical samples,” Sci. Transl. Med., vol. 12, no. 556, p. eabc7075, Aug. 2020, doi: 10.1126/scitranslmed.abc7075.CrossRefGoogle ScholarPubMed
Chen, Q. and Liu, Z., “Fabrication and applications of solid-state nanopores,” Sensors (Switzerland), vol. 19, no. 8. MDPI AG, Apr. 02, 2019, doi: 10.3390/s19081886.Google ScholarPubMed
Mirsaidov, U. M., Wang, D., Timp, W., and Timp, G., “Molecular diagnostics for personal medicine using a nanopore,” Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, vol. 2, no. 4. NIH Public Access, pp. 367–381, Jul. 2010, doi: 10.1002/wnan.86.Google ScholarPubMed
Guglielmi, G., “The explosion of new coronavirus tests that could help to end the pandemic,” Nature, vol. 583, no. 7817, pp. 506–509, Jul. 2020, doi: 10.1038/d41586-020-02140-8.Google ScholarPubMed
George, S. et al. , “DNA Thermo-Protection Facilitates Whole Genome Sequencing of Mycobacteria Direct from Clinical Samples by the Nanopore Platform,” bioRxiv, p. 2020.04.05.026864, Apr. 2020, doi: 10.1101/2020.04.05.026864.Google Scholar
UK Government, “Roll-out of 2 new rapid coronavirus tests ahead of winter - GOV.UK,” 2020. https://www.gov.uk/government/news/roll-out-of-2-new-rapid-coronavirus-tests-ahead-of-winter (accessed Aug. 10, 2020).Google Scholar
“Novel Coronavirus (COVID-19) Overview.” https://nanoporetech.com/covid-19/overview (accessed Sep. 16, 2020).Google Scholar
James, P. et al. , “LamPORE: rapid, accurate and highly scalable molecular screening for SARS-CoV-2 infection, based on nanopore sequencing,” medRxiv, vol. 2020, no. January, p. 2020.08.07.20161737, 2020, doi: 10.1101/2020.08.07.20161737.Google Scholar
Sutton, M. A. et al. , “Radiation Tolerance of Nanopore Sequencing Technology for Life Detection on Mars and Europa,” Sci. Rep., vol. 9, no. 1, pp. 1–10, Dec. 2019, doi: 10.1038/s41598-019-41488-4.CrossRefGoogle ScholarPubMed
Tucker, T., Marra, M., and Friedman, J. M., “Massively Parallel Sequencing: The Next Big Thing in Genetic Medicine,” American Journal of Human Genetics, vol. 85, no. 2. Am J Hum Genet, pp. 142–154, Aug. 14, 2009, doi: 10.1016/j.ajhg.2009.06.022.CrossRefGoogle ScholarPubMed
Yang, J. et al. , “Photo-induced ultrafast active ion transport through graphene oxide membranes,” 2019. doi: 10.1038/s41467-019-09178-x.CrossRefGoogle Scholar
Johnson, S. S., Zaikova, E., Goerlitz, D. S., Bai, Y., and Tighe, S. W., “Real-time DNA sequencing in the antarctic dry valleys using the Oxford nanopore sequencer,” J. Biomol. Tech., vol. 28, no. 1, pp. 2–7, Apr. 2017, doi: 10.7171/jbt.17-2801-009.CrossRefGoogle ScholarPubMed
Meier, R., Wong, W., Srivathsan, A., and Foo, M., “$1 DNA barcodes for reconstructing complex phenomes and finding rare species in specimen-rich samples,” Cladistics, vol. 32, no. 1, pp. 100–110, Feb. 2016, doi: 10.1111/cla.12115.Google Scholar
Viehweger, A. et al. , “Direct RNA nanopore sequencing of full-length coronavirus genomes provides novel insights into structural variants and enables modification analysis,” bioRxiv, p. 483693, Aug. 2018, doi: 10.1101/483693.Google Scholar
Howorka, S., “Building membrane nanopores,” Nature Nanotechnology, vol. 12, no. 7. Nature Publishing Group, pp. 619–630, Jul. 01, 2017, doi: 10.1038/nnano.2017.99.CrossRefGoogle ScholarPubMed
Liu, Y. and Yobas, L., “Slowing DNA Translocation in a Nanofluidic Field-Effect Transistor,” ACS Nano, vol. 10, no. 4, pp. 3985–3994, 2016, doi: 10.1021/acsnano.6b00610.Google Scholar
Kowalczyk, S. W., Grosberg, A. Y., Rabin, Y., and Dekker, C., “Modeling the conductance and DNA blockade of solid-state nanopores,” Nanotechnology, vol. 22, no. 31, 2011, doi: 10.1088/0957-4484/22/31/315101.Google ScholarPubMed
Liang, L., Shen, J. W., Zhang, Z., and Wang, Q., “DNA sequencing by two-dimensional materials: As theoretical modeling meets experiments,” Biosensors and Bioelectronics, vol. 89. Elsevier Ltd, pp. 280–292, Mar. 15, 2017, doi: 10.1016/j.bios.2015.12.037.CrossRefGoogle ScholarPubMed
Heerema, S. J., Schneider, G. F., Rozemuller, M., Vicarelli, L., Zandbergen, H. W., and Dekker, C., “1/F Noise in Graphene Nanopores,” Nanotechnology, vol. 26, no. 7, p. 074001, Feb. 2015, doi: 10.1088/0957-4484/26/7/074001.CrossRefGoogle ScholarPubMed
Sarkar, D., Liu, W., Xie, X., Anselmo, A. C., Mitragotri, S., and Banerjee, K., “MoS2 field-effect transistor for next-generation label-free biosensors,” ACS Nano, vol. 8, no. 4, pp. 3992–4003, 2014, doi: 10.1021/nn5009148.CrossRefGoogle ScholarPubMed
Mojtabavi, M., VahidMohammadi, A., Liang, W., Beidaghi, M., and Wanunu, M., “Single-Molecule Sensing Using Nanopores in Two-Dimensional Transition Metal Carbide (MXene) Membranes,” ACS Nano, p. acsnano.8b08017, 2019, doi: 10.1021/acsnano.8b08017.Google Scholar
Tanjil, M. R.-E., Jeong, Y., Yin, Z., Panaccione, W., and Wang, M. C., “Ångstrom-Scale, Atomically Thin 2D Materials for Corrosion Mitigation and Passivation,” Coatings, vol. 9, no. 2, p. 133, Feb. 2019, doi: 10.3390/coatings9020133.CrossRefGoogle Scholar
Liu, K., Feng, J., Kis, A., and Radenovic, A., “Atomically Thin Molybdenum Disulfide Nanopores with High Sensitivity for DNA Translocation,” 2014, doi: 10.1021/nn406102h.CrossRefGoogle Scholar
Garaj, S., Hubbard, W., Reina, A., Kong, J., Branton, D., and Golovchenko, J. A., “Graphene as a subnanometre trans-electrode membrane,” Nature, vol. 467, no. 7312, pp. 190–193, Sep. 2010, doi: 10.1038/nature09379.CrossRefGoogle ScholarPubMed
Thomas, S., Rajan, A. C., Rezapour, M. R., and Kim, K. S., “In search of a two-dimensional material for DNA sequencing,” J. Phys. Chem. C, vol. 118, no. 20, pp. 10855–10858, 2014, doi: 10.1021/jp501711d.Google Scholar
Garaj, S., Hubbard, W., Reina, A., Kong, J., Branton, D., and Golovchenko, J. A., “Graphene as a subnanometre trans-electrode membrane,” Nature, vol. 467, no. 7312, pp. 190–193, Sep. 2010, doi: 10.1038/nature09379.CrossRefGoogle ScholarPubMed
Su, S., Guo, X., Fu, Y., Xie, Y., Wang, X., and Xue, J., “Origin of nonequilibrium 1/: F noise in solid-state nanopores,” Nanoscale, vol. 12, no. 16, pp. 8975–8981, Apr. 2020, doi: 10.1039/c9nr09829a.CrossRefGoogle Scholar
Robertson, A. W. et al. , “Spatial control of defect creation in graphene at the nanoscale,” Nat. Commun., vol. 3, no. 1, p. 1144, Jan. 2012, doi: 10.1038/ncomms2141.CrossRefGoogle ScholarPubMed
Rochman, C. M., “The complex mixture, fate and toxicity of chemicals associated with plastic debris in the marine environment,” in Marine Anthropogenic Litter, Cham: Springer International Publishing, 2015, pp. 117–140.CrossRefGoogle Scholar
Russo, C. J. and Golovchenko, J. A., “Atom-by-atom nucleation and growth of graphene nanopores.,” Proc. Natl. Acad. Sci. U. S. A., vol. 109, no. 16, pp. 5953–7, Apr. 2012, doi: 10.1073/pnas.1119827109.CrossRefGoogle ScholarPubMed
Danda, G. et al. , “Monolayer WS2 Nanopores for DNA Translocation with Light-Adjustable Sizes,” ACS Nano, vol. 11, no. 2, pp. 1937–1945, Feb. 2017, doi: 10.1021/acsnano.6b08028.CrossRefGoogle ScholarPubMed
Feng, J. et al. , “Electrochemical reaction in single layer MoS2: Nanopores opened atom by atom,” Nano Lett., vol. 15, no. 5, pp. 3431–3438, 2015, doi: 10.1021/acs.nanolett.5b00768.CrossRefGoogle ScholarPubMed
Kuan, A. T., Lu, B., Xie, P., Szalay, T., and Golovchenko, J. A., “Electrical pulse fabrication of graphene nanopores in electrolyte solution,” Appl. Phys. Lett., vol. 106, no. 20, May 2015, doi: 10.1063/1.4921620.CrossRefGoogle ScholarPubMed
Jain, M., Olsen, H. E., Paten, B., and Akeson, M., “The Oxford Nanopore MinION: delivery of nanopore sequencing to the genomics community,” Genome Biol., vol. 17, no. 1, pp. 1–11, Dec. 2016, doi: 10.1186/s13059-016-1103-0.Google ScholarPubMed
Wloka, C., Mutter, N. L., Soskine, M., and Maglia, G., “Alpha-Helical Fragaceatoxin C Nanopore Engineered for Double-Stranded and Single-Stranded Nucleic Acid Analysis,” Angew. Chemie - Int. Ed., vol. 55, no. 40, pp. 12494–12498, Sep. 2016, doi: 10.1002/anie.201606742.CrossRefGoogle ScholarPubMed
Larkin, J., Henley, R., Bell, D. C., Cohen-Karni, T., Rosenstein, J. K., and Wanunu, M., “Slow DNA transport through nanopores in hafnium oxide membranes,” ACS Nano, vol. 7, no. 11, pp. 10121–10128, Nov. 2013, doi: 10.1021/nn404326f.CrossRefGoogle ScholarPubMed
Qiu, H., Sarathy, A., Schulten, K., and Leburton, J. P., “Detection and mapping of DNA methylation with 2D material nanopores,” npj 2D Mater. Appl., vol. 1, no. 1, p. 3, Dec. 2017, doi: 10.1038/s41699-017-0005-7.CrossRefGoogle ScholarPubMed
Belkin, M., Chao, S. H., Jonsson, M. P., Dekker, C., and Aksimentiev, A., “Plasmonic Nanopores for Trapping, Controlling Displacement, and Sequencing of DNA,” ACS Nano, vol. 9, no. 11, pp. 10598–10611, Nov. 2015, doi: 10.1021/acsnano.5b04173.CrossRefGoogle ScholarPubMed
Yang, J. M. et al. , “Surface-Enhanced Raman Scattering Probing the Translocation of DNA and Amino Acid through Plasmonic Nanopores,” Anal. Chem., vol. 91, no. 9, pp. 6275–6280, May 2019, doi: 10.1021/acs.analchem.9b01045.CrossRefGoogle ScholarPubMed
Wanunu, M., Morrison, W., Rabin, Y., Grosberg, A. Y., and Meller, A., “Electrostatic focusing of unlabelled DNA into nanoscale pores using a salt gradient,” Nat. Nanotechnol., vol. 5, no. 2, pp. 160–165, Dec. 2010, doi: 10.1038/nnano.2009.379.CrossRefGoogle ScholarPubMed
Kowalczyk, S. W., Wells, D. B., Aksimentiev, A., and Dekker, C., “Slowing down DNA translocation through a nanopore in lithium chloride,” Nano Lett., vol. 12, no. 2, pp. 1038–1044, 2012, doi: 10.1021/nl204273h.CrossRefGoogle ScholarPubMed
Wanunu, M., Sutin, J., McNally, B., Chow, A., and Meller, A., “DNA translocation governed by interactions with solid-state nanopores,” Biophys. J., vol. 95, no. 10, pp. 4716–4725, Nov. 2008, doi: 10.1529/biophysj.108.140475.Google ScholarPubMed
Luan, B., Stolovitzky, G., and Martyna, G., “Slowing and controlling the translocation of DNA in a solid-state nanopore,” Nanoscale, vol. 4, no. 4, pp. 1068–1077, Feb. 2012, doi: 10.1039/c1nr11201e.CrossRefGoogle Scholar
Peng, H. and Ling, X. S., “Reverse DNA translocation through a solid-state nanopore by magnetic tweezers,” Nanotechnology, vol. 20, no. 18, p. 185101, Apr. 2009, doi: 10.1088/0957-4484/20/18/185101.CrossRefGoogle ScholarPubMed
Van Dorp, S., Keyser, U. F., Dekker, N. H., Dekker, C., and Lemay, S. G., “Origin of the electrophoretic force on DNA in solid-state nanopores,” Nat. Phys., vol. 5, no. 5, pp. 347–351, Mar. 2009, doi: 10.1038/nphys1230.CrossRefGoogle Scholar
Balasubramanian, R. et al. , “DNA Translocation through Hybrid Bilayer Nanopores,” J. Phys. Chem. C, vol. 123, no. 18, pp. 11908–11916, May 2019, doi: 10.1021/acs.jpcc.9b00399.CrossRefGoogle ScholarPubMed
Lee, M. H. et al. , “A low-noise solid-state nanopore platform based on a highly insulating substrate,” Sci. Rep., vol. 4, Dec. 2014, doi: 10.1038/srep07448.Google ScholarPubMed
Schneider, G. F. et al. , “DNA translocation through graphene nanopores,” Nano Lett., vol. 10, no. 8, pp. 3163–3167, 2010, doi: 10.1021/nl102069z.CrossRefGoogle ScholarPubMed
Heerema, S. J., Vicarelli, L., Pud, S., Schouten, R. N., Zandbergen, H. W., and Dekker, C., “Probing DNA Translocations with Inplane Current Signals in a Graphene Nanoribbon with a Nanopore,” ACS Nano, vol. 12, no. 3, pp. 2623–2633, Mar. 2018, doi: 10.1021/acsnano.7b08635.CrossRefGoogle Scholar
Haynes, T., Smith, I. P. S., Wallace, E. J., Trick, J. L., Sansom, M. S. P., and Khalid, S., “Electric-field-driven translocation of ssDNA through hydrophobic nanopores,” ACS Nano, vol. 12, no. 8, pp. 8208–8213, 2018, doi: 10.1021/acsnano.8b03365.Google ScholarPubMed
Graf, M., Lihter, M., Altus, D., Marion, S., and Radenovic, A., “Transverse Detection of DNA Using a MoS2 Nanopore,” Nano Lett., vol. 19, no. 12, pp. 9075–9083, 2019, doi: 10.1021/acs.nanolett.9b04180.CrossRefGoogle ScholarPubMed
“SERS/TERS.” https://www.renishaw.com/en/sers-ters--25811 (accessed Sep. 18, 2020).Google Scholar
Cao, J. et al. , “SERS Detection of Nucleobases in Single Silver Plasmonic Nanopores,” ACS sensors, vol. 5, no. 7, pp. 2198–2204, Jul. 2020, doi: 10.1021/acssensors.0c00844.CrossRefGoogle ScholarPubMed
Huang, J. A. et al. , “SERS discrimination of single DNA bases in single oligonucleotides by electro-plasmonic trapping,” Nat. Commun., vol. 10, no. 1, pp. 1–10, Dec. 2019, doi: 10.1038/s41467-019-13242-x.CrossRefGoogle ScholarPubMed
Chen, C. et al. , “High spatial resolution nanoslit SERS for single-molecule nucleobase sensing,” Nat. Commun., vol. 9, no. 1, pp. 1–9, Dec. 2018, doi: 10.1038/s41467-018-04118-7.Google ScholarPubMed
He, Z. et al. , “Tip-Enhanced Raman Imaging of Single-Stranded DNA with Single Base Resolution,” J. Am. Chem. Soc., vol. 141, no. 2, pp. 753–757, 2019, doi: 10.1021/jacs.8b11506.CrossRefGoogle ScholarPubMed
Spitzberg, J. D., Zrehen, A., van Kooten, X. F., and Meller, A., “Plasmonic-Nanopore Biosensors for Superior Single-Molecule Detection,” Adv. Mater., vol. 31, no. 23, p. 1900422, Jun. 2019, doi: 10.1002/adma.201900422.Google ScholarPubMed
Garoli, D. et al. , “Hybrid plasmonic nanostructures based on controlled integration of MoS2 flakes on metallic nanoholes,” Nanoscale, vol. 10, no. 36, pp. 17105–17111, Sep. 2018, doi: 10.1039/c8nr05026k.CrossRefGoogle ScholarPubMed
Garoli, D., Yamazaki, H., MacCaferri, N., and Wanunu, M., “Plasmonic Nanopores for Single-Molecule Detection and Manipulation: Toward Sequencing Applications,” Nano Lett., vol. 19, no. 11, pp. 7553–7562, 2019, doi: 10.1021/acs.nanolett.9b02759.CrossRefGoogle ScholarPubMed
Restrepo-Pérez, L., Joo, C., and Dekker, C., “Paving the way to single-molecule protein sequencing,” Nature Nanotechnology, vol. 13, no. 9. Nature Publishing Group, pp. 786–796, Sep. 01, 2018, doi: 10.1038/s41565-018-0236-6.CrossRefGoogle Scholar
Srivathsan, A. et al. , “A MinIONTM-based pipeline for fast and cost-effective DNA barcoding,” Mol. Ecol. Resour., vol. 18, no. 5, pp. 1035–1049, Sep. 2018, doi: 10.1111/1755-0998.12890.CrossRefGoogle Scholar
Hoogerheide, D. P., Garaj, S., and Golovchenko, J. A., “Probing surface charge fluctuations with solid-state nanopores,” Phys. Rev. Lett., vol. 102, no. 25, 2009, doi: 10.1103/PhysRevLett.102.256804.CrossRefGoogle ScholarPubMed
Powell, M. R. et al. , “Noise properties of rectifying nanopores,” J. Phys. Chem. C, vol. 115, no. 17, pp. 8775–8783, May 2011, doi: 10.1021/jp2016038.CrossRefGoogle Scholar
Zhang, Z. Y., Deng, Y. S., Tian, H. B., Yan, H., Cui, H. L., and Wang, D. Q., “Noise analysis of monolayer graphene nanopores,” Int. J. Mol. Sci., vol. 19, no. 9, p. 2639, Sep. 2018, doi: 10.3390/ijms19092639.CrossRefGoogle ScholarPubMed
Fragasso, A., Schmid, S., and Dekker, C., “Comparing Current Noise in Biological and Solid-State Nanopores,” ACS Nano, vol. 14, no. 2, pp. 1338–1349, 2020, doi: 10.1021/acsnano.9b09353.CrossRefGoogle ScholarPubMed
Hall, A. R., Scott, A., Rotem, D., Mehta, K. K., Bayley, H., and Dekker, C., “Hybrid pore formation by directed insertion of α-haemolysin into solid-state nanopores,” Nat. Nanotechnol., vol. 5, no. 12, pp. 874–877, 2010, doi: 10.1038/nnano.2010.237.CrossRefGoogle ScholarPubMed
Nelson, E. M., Li, H., and Timp, G., “Direct, concurrent measurements of the forces and currents affecting DNA in a nanopore with comparable topography,” ACS Nano, vol. 8, no. 6, pp. 5484–5493, Jun. 2014, doi: 10.1021/nn405331t.CrossRefGoogle Scholar
Keyser, U. F. et al. , “Direct force measurements on DNA in a solid-state nanopore,” Nat. Phys., vol. 2, no. 7, pp. 473–477, Jul. 2006, doi: 10.1038/nphys344.CrossRefGoogle Scholar
Farimani, A. B., Dibaeinia, P., and Aluru, N. R., “DNA origami-graphene hybrid nanopore for DNA detection,” ACS Appl. Mater. Interfaces, vol. 9, no. 1, pp. 92–100, 2017, doi: 10.1021/acsami.6b11001.CrossRefGoogle Scholar
Hwang, M. T. et al. , “Ultrasensitive detection of nucleic acids using deformed graphene channel field effect biosensors,” Nat. Commun., vol. 11, no. 1, 2020, doi: 10.1038/s41467-020-15330-9.CrossRefGoogle ScholarPubMed
Shukla, V., Jena, N. K., Grigoriev, A., and Ahuja, R., “Prospects of Graphene-hBN Heterostructure Nanogap for DNA Sequencing,” ACS Appl. Mater. Interfaces, vol. 9, no. 46, pp. 39945–39952, 2017, doi: 10.1021/acsami.7b06827.CrossRefGoogle ScholarPubMed
Min, S. K., Kim, W. Y., Cho, Y., and Kim, K. S., “Fast DNA sequencing with a graphene-based nanochannel device,” Nat. Nanotechnol., vol. 6, no. 3, pp. 162–165, 2011, doi: 10.1038/nnano.2010.283.CrossRefGoogle ScholarPubMed
Luan, B. and Zhou, R., “Single-File Protein Translocations through Graphene-MoS2 Heterostructure Nanopores,” J. Phys. Chem. Lett., vol. 9, no. 12, pp. 3409–3415, Jun. 2018, doi: 10.1021/acs.jpclett.8b01340.CrossRefGoogle ScholarPubMed