Abstract
This review highlights operational principles, features, and modern aspects of the development of third-generation sequencing technology of biopolymers focusing on the nucleic acids analysis, namely the nanopore sequencing system. Basics of the method and technical solutions used for its realization are considered, from the first works showing the possibility of creation of these systems to the easy-to-handle procedure developed by Oxford Nanopore Technologies company. Moreover, this review focuses on applications, which were developed and realized using equipment developed by the Oxford Nanopore Technologies, including assembly of whole genomes, methagenomics, direct analysis of the presence of modified bases.
References
Deeb, K. K., Metcalf, J. D., Sesock, K. M., Shen, J., Wensel, Ch. A., Rippel, L. I., Smith, M., Chapman, M. S., and Zhang, S. (2015) The c.1364C>A (p.A455E) Mutation in the CFTR pseudogene results in an incorrectly assigned carrier status by a commonly used screening platform, J. Mol. Diagn., 17, 360-365, https://doi.org/10.1016/j.jmoldx.2015.02.005.
Topol, E. J. (2014) Individualized medicine from prewomb to tomb, Cell, 157, 241-253, https://doi.org/10.1016/j.cell.2014.02.012.
Sanger, F., and Coulson, A. R. (1975) Rapid method for determining sequences in DNA. by primed synthesis with DNA polymerase, J. Mol. Biol., 94, 441-448, https://doi.org/10.1016/0022-2836(75)90213-2.
Sanger, F., Air, G. M., Barrell, B. G., Brown, N. L., Coulson, A. R., Fiddes, C. A., Hutchison, C. A., Slocombe, P. M., and Smith, M. (1977) Nucleotide sequence of bacteriophage φX174 DNA, Nature, 265, 687-695, https://doi.org/10.1038/265687a0.
International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome, Nature, 409, 860-921, https://doi.org/10.1038/35057062.
Schadt, E. E., Turner, S., and Kasarskis, A. (2010) A window into third-generation sequencing, Hum. Mol. Genet., 19, R227-R240, https://doi.org/10.1093/hmg/ddq416.
Wang, Y., Yang, Q., and Wang, Zh. (2015) The evolution of nanopore sequencing, Front. Genet., 5, 449, https://doi.org/10.3389/fgene.2014.00449.
Bell, D. C., Thomas, W. K., Murtagh, K. M., Dionne, Ch. A., Graham, A. C., Anderson, J. E., Glover, W. R. (2012) DNA base identification by electron microscopy, Microsc. Microanal., 18, 1049-1053, https://doi.org/10.1017/S1431927612012615.
Cheng, P., Oliver, P. M., Barrett, M. J., and Vezenov, D. (2012) Progress toward the application of molecular force spectroscopy to DNA sequencing, Electrophoresis, 33, 3497-3505, https://doi.org/10.1002/elps.201200351.
Bailo, E., and Deckert, V. (2008) Tip-enhanced Raman spectroscopy of single RNA strands: towards a novel direct-sequencing method, Angewandte Chemie Int. Ed., 47, 1658-1661, https://doi.org/10.1002/anie.200704054.
Branton, D., Deamer, D. W., Marziali, A., Bayley, H., Benner, S. A., Butler, T., Di Ventra, M., Garaj, S., Hibbs, A., and Huang, X. (2008) The potential and challenges of nanopore sequencing, Nat. Biotechnol., 26, 1146-1153, https://doi.org/10.1038/nbt.1495.
Lu, H., Giordano, F., and Ning, Z. (2016) Oxford nanopore MinION sequencing and genome assembly, Genom. Proteom. Bioinform., 14, 265-279, https://doi.org/10.1016/j.gpb.2016.05.004.
Castro-Wallace, S. L., Chiu, C. Y., John, K. K., Stahl, S. E., Rubins, K. H., McIntyre, A. B. R., Dworkin, J. P., Lupisella, M. L., Smith, D. J., Botkin, D. J., Stephenson, T. A., Juul, S., Turner, D. J., Izquierdo, F., Federman, S., Stryke, D., Somasekar, S., Alexander, N., Yu, G., Mason, C. E., and Burton, A. S. (2017) Nanopore DNA sequencing and genome assembly on the international space station, Sci. Rep., 7, 18022, https://doi.org/10.1038/s41598-017-18364-0.
Heather, J. M., and Chain, B. (2016) The sequence of sequencers: the history of sequencing DNA, Genomics, 107, 1-8, https://doi.org/10.1016/j.ygeno.2015.11.003.
Suspicyn, E. N., and Sokolenko, A. P. (2013) The Use of New Generation Molecular Technologies in Medical Genetics [in Russian], St. Petersburg, p. 22.
Suspicyn, E. N., Tyurin, V. I., and Imyanitov, E. N. (2016) Full excom sequencing: principles and diagnostic options [in Russian], Pediatrician, 7, 142-146, https://doi.org/10.17816/PED74142-146.
Suspicyn, E. N., Guseva, M. N., and Sokolenko, A. P. (2017) Next generation targeted sequencing (NGS) in diagnosing primary immunodeficiencies, Med. Immunol., 19, 174.
Barhatov, I. M., Predeus, A. V., and Chuhlovin, A. B. (2016) Sequencing of a new generation and its application in oncohematology [in Russian], Onkogematologiya, 11, 56-63.
Song, L., Hobaugh, M. R., Shustak, C., Cheley, S., Bayley, H., and Gouaux, J. E. (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore, Science, 274, 1859-1865, https://doi.org/10.1126/science.274.5294.1859.
Faller, M., Niederweis, M., and Schulz, G. E. (2004) The structure of a mycobacterial outer-membrane channel, Science, 303, 1189-1192, https://doi.org/10.1126/science.1094114.
Li, J., Stein, D., Mcmullan, C., Branton, D., Aziz, M. J., and Golovchenko, J. A. (2001) Ion-beam sculpting at nanometre length scales, Nature, 412, 166-169, https://doi.org/10.1038/35084037.
Yanagi, I., Akahori, R., Hatano, T., and Takeda, K.-I. (2014) Fabricating nanopores with diameters of sub-1 nm to 3 nm using multilevel pulse-voltage injection, Sci. Rep., 4, 5000, https://doi.org/10.1038/srep05000.
Wu, L., Liu, H., Zhao, W., Wang, L., Hou, C., Liu, Q., and Lu, Z. (2014) Electrically facilitated translocation of protein through solid nanopore, Nanoscale Res. Lett., 9, 140, https://doi.org/10.1186/1556-276X-9-140.
Hall, A., Scott, A., Rotem, D., Mehta, K. K., Bayley, H., and Dekker, C. (2010) Hybrid pore formation by directed insertion of α-haemolysin into solid-state nanopores, Nat. Nanotechnol., 5, 874-877, https://doi.org/10.1038/nnano.2010.237.
Cabello-Aguilar, S., Balme, S., Chaaya, A. A., Bechelany, M., Balanzat, E., Janot, J.-M., Pochat-Bohatier, C., Miele, P., and Dejardin, P. (2013) Slow translocation of polynucleotides and their discrimination by α-hemolysin inside a single track-etched nanopore designed by atomic layer deposition, Nanoscale, 5, 9582-9586, https://doi.org/10.1039/c3nr03683a.
Kasianowicz, J. J., Balijepalli, A. K., Ettedgui, J., Forstater, J. H., Wang, H., Zhang, H., and Robertson, J. W. (2016) Analytical applications for pore-forming proteins, Biochim. Biophys. Acta, 1858, 593-606, https://doi.org/10.1016/j.bbamem.2015.09.023.
Wendell, D., Jing, P., Geng, J., Subramaniam, V., Lee, T. J., Montemagno, C., and Guo, P. (2009) Translocation of double-stranded DNA through membrane-adapted ϕ29 motor protein nanopores, Nat. Nanotechnol., 4, 765-772, https://doi.org/10.1038/nnano.2009.259.
Laszlo, A. H., Derrington, I. M., and Gundlach, J. H. (2016) MspA nanopore as a single-molecule tool: from sequencing to SPRNT, Methods, 105, 75-89, https://doi.org/10.1016/j.ymeth.2016.03.026.
Kang, X. F., Gu, L. Q., Cheley, S., and Bayley, H. (2005) Single protein pores containing molecular adapters at high temperatures, Angewandte Chemie Int. Ed., 25, 44-54, https://doi.org/10.1002/anie.200461885.
Jing, P., Haque, F., Vonderheide, A. P., Montemagno, C., and Guo, P. (2010) Robust properties of membrane-embedded connector channel of bacterial virus phi29 DNA packaging motor, Mol. Biosystem, 6, 1844-1852, https://doi.org/10.1039/c003010d.
Pastoriza-Gallego, M., Rabah, L., Gibrat, G., Thiebot, B., van der Goot, F. G., Auvray, L., Betton, J.-M., and Pelta, J. (2011) Dynamics of unfolded protein transport through an aerolysin pore, J. Am. Chem. Soc., 133, 2923-2931, https://doi.org/10.1021/ja1073245.
Cressiot, B., Braselmann, E., Oukhaled, A., Elcock, A. H., Pelta, J., and Clark, P. L. (2015) Dynamics and energy contributions for transport of unfolded pertactin through a protein nanopore, ACS Nano, 9, 9050-9061, https://doi.org/10.1021/acsnano.5b03053.
Fennouri, A., Daniel, R., Pastoriza-Gallego, M., Auvray, L., Pelta, J., and Bacri, L. (2013) Kinetics of enzymatic degradation of high molecular weight polysaccharides through a nanopore: experiments and data-modeling, Anal. Chem., 85, 8488-8492, https://doi.org/10.1021/ac4020929.
Cao, C., Ying, Y. L., Hu, Z. L., Liao, D. F., Tian, H., and Long, Y. T. (2016) Discrimination of oligonucleotides of different lengths with a wild-type aerolysin nanopore, Nat. Nanotechnol., 11, 713-718, https://doi.org/10.1038/nnano.2016.66.
Butler, T. Z., Pavlenok, M., Derrington, I. M., Niederweis, M., and Gundlach, J. H. (2008) Single-molecule DNA detection with an engineered MspA protein nanopore, Proc. Natl. Acad. Sci. USA, 105, 20647, https://doi.org/10.1073/pnas.0807514106.
Heinz, C., Engelhardt, H., and Niederweis, M. (2003) The core of the tetrameric mycobacterial porin MspA is an extremely stable beta-sheet domain, J. Biol. Chem., 278, 8678-8685, https://doi.org/10.1074/jbc.M212280200.
Van den Hout, M., Hall, A. R., Wu, M. Y., Zandbergen, H. W., Dekker, C., and Dekker, N. H. (2010) Controlling nanopore size, shape and stability, Nanotechnology, 21, 115304, https://doi.org/10.1088/0957-4484/21/11/115304.
Yuan, J. H., He, F. Y., Sun, D. C., and Xia, X. H. (2004) A simple method for preparation of through-hole porous anodic alumina membrane, Chem. Mater., 16, 1841, https://doi.org/10.1021/cm049971u.
Siwi, Z., Gu, Y., Spohr, H. A., Baur, D., Wolf-Reber, A., Spohr, R., Apel, P., and Korchev, Y. E. (2002) Rectification and voltage gating of ion currents in a nanofabricated pore, Europhys. Lett., 60, 349, https://doi.org/10.1209/epl/i2002-00271-3.
Storm, A. J., Chen, J. H., Ling, X. S., Zandbergen, H. W., and Dekker, C. (2003) Fabrication of solid-state nanopores with single-nanometre precision, Nat. Materials, 2, 537-540, https://doi.org/10.1209/epl/i2002-00271-3.
Zhao, Q., Sigalov, G., Dimitrov, V., Dorvel, B., Mirsaidov, U., Sligar, S., Aksimentiev, A., and Timp, G. (2007) Detecting SNPs using a synthetic nanopore, Nano Lett., 7, 1680-1685, https://doi.org/10.1021/nl070668c.
Heng, J. B., Ho, C., Kim, T., Timp, R., Aksimentiev, A., Grinkova, Y. V., Sligar, S., Schulten, K., and Timp, G. (2004) Sizing DNA using a nanometer-diameter pore, Biophys. J., 87, 2905, https://doi.org/10.1529/biophysj.104.041814.
Cressiot, B., Greive, S. J., Mojtabavi, M., Antson, A. A., and Wanunu, M. (2018) Thermostable virus portal proteins as reprogrammable adapters for solid-state nanopore sensors, Nat. Commun., 9, 4652, https://doi.org/10.1038/s41467-018-07116-x.
Hall, A. R., Scott, A., Rotem, D., Mehta, K. K., Bayley, H., and Dekker, C. (2010) Hybrid pore formation by directed insertion of α-haemolysin into solid-state nanopores, Nat. Nanotechnol., 5, 874, https://doi.org/10.1038/nnano.2010.237.
Zvereva, M. E., Malyavko, A. N., Dontsova, O. A. (2012) DNA as a nanomaterial, Polymer Sci. Ser. A, 54, 531-539, https://doi.org/10.1134/S0965545X12040104.
Bell, N. A. W., Engst, C. R., Ablay, M., Divitini, G., Ducati, C., Liedl, T., and Keyser, U. F. (2012) DNA origami nanopores, Nano Lett., 12, 512-517, https://doi.org/10.1021/nl204098n.
Bell, N. A. W., and Keyser, U. F. (2014) Nanopores formed by DNA origami: a review, FEBS Lett., 588, 3564-3570, https://doi.org/10.1016/j.febslet.2014.06.013.
Shenoy, D. K., Barger, W. R., Singh, A., Panchal, R. G., Misakian, M., Stanford, V. M., and Kasianowicz, J. J. (2005) Functional reconstitution of protein ion channels into planar polymerizable phospholipid membranes, Nano Lett., 5, 1181-1185, https://doi.org/10.1021/nl050481q.
Schiller, S. M., Naumann, R., Lovejoy, K., Kunz, H., and Knoll, W. (2003) Archaea analogue thiolipids for tethered bilayer lipid membranes on ultrasmooth gold surfaces, Angewandte Chemie Int. Ed., 42, 208-211, https://doi.org/10.1002/anie.200390080.
Holden, M. A., Needham, D., and Bayley, H. (2007) Functional bionetworks from nanoliter water droplets, J. Am. Chem. Soc., 129, 8650-8655, https://doi.org/10.1021/ja072292a.
Van der Verren, S. E., Van Gerven, N., Jonckheere, W., Hambley, R., Singh, P., Kilgour, J., Jordan, M., Wallace, E. J., Jayasinghe, L., and Remaut, H. (2020) A dual-constriction biological nanopore resolves homonucleotide sequences with high fidelity, Nat. Biotechnol., 38, 1415-1420, https://doi.org/10.1038/s41587-020-0570-8.
Deamer, D., Akeson, M., and Branton, D. (2016) Author response to John Kasianowicz and Sergey Bezrukov, Nat. Biotechnol., 34, 482-482, https://doi.org/10.1038/nbt.3561.
Goyal, P., Krasteva, P. V., Van Gerven, N., Gubellini, F., Van den Broeck, I., Troupiotis-Tsaïlaki, A., Jonckheere, W., Péhau-Arnaudet, G., Pinkner, J. S., Chapman, M. R., Hultgren, S. J., Howorka, S., Fronzes, R., and Remaut, H. (2014) Structural and mechanistic insights into the bacterial amyloid secretion channel CsgG, Nature, 516, 250-253, https://doi.org/10.1038/nature13768.
Minei, R., Hoshina, R., and Ogura, A. (2018) De novo assembly of middle-sized genome using MinION and Illumina sequencers, Genomics, 19, 700, https://doi.org/10.1186/s12864-018-5067-1.
Ashton, P. M., Nair, S., Dallman, T., Rubino, S., Rabsch, W., Mwaigwisya, S., Wain, J., and O’Grady, J. (2015) MinION nanopore sequencing identifies the position and structure of a bacterial antibiotic resistance island, Nat. Biotechnol., 33, 296-300, https://doi.org/10.1038/nbt.3103.
Carter, J. M., and Hussain, S. (2017) Robust long-read native DNA sequencing using the ONT CsgG Nanopore system, Wellcome Open Res., 2, 23, https://doi.org/10.12688/wellcomeopenres.11246.3.
Wick, R. R., Judd, L. M., and Holt, K. E. (2019) Performance of neural network basecalling tools for Oxford Nanopore sequencing, Genome Biol., 20, 129, https://doi.org/10.1186/s13059-019-1727-y.
Tytgat, O., Gansemans, Y., Weymaere, J., Rubben, K., Deforce, D., and Van Nieuwerburgh, F. (2020) Nanopore sequencing of a forensic STR multiplex reveals loci suitable for single-contributor STR profiling, Genes, 11, 381, https://doi.org/10.3390/genes11040381.
Huang, Y. T., Liu, P. Y., and Shih, P. W. (2021) Homopolish: a method for the removal of systematic errors in nanopore sequencing by homologous polishing, Genome Biol., 22, 95, https://doi.org/10.1186/s13059-021-02282-6.
Rhoads, A., and Au, K. F. (2015) PacBio sequencing and its applications, Genom. Proteom. Bioinform., 13, 278-289, https://doi.org/10.1016/j.gpb.2015.08.002.
Ip, C. L. C., Loose, M., Tyson, J. R., de Cesare, M., Brown, B. L., Jain, M., Leggett, R. M., Eccles, D. A., Zalunin, V., Urban, J. M., Piazza, P., Bowden, R. J., Paten, B., Mwaigwisya, S., Batty, E. M., Simpson, J. T., Snutch, T. P., Birney, E., Buck, D., Goodwin, S., Jansen, H. J., O’Grady, J., and Olsen, H. E. (2015) MinION analysis and reference consortium. MinION analysis and reference consortium: Phase 1 data release and analysis, F1000Res., 15, 1075, https://doi.org/10.12688/f1000research.7201.1.
Gong, L., Wong, C. H., Cheng, W. C., Tjong, H., Menghi, F., Ngan, C. Y., Liu, E. T., and Wei, C. L. (2018) Picky comprehensively detects high-resolution structural variants in nanopore long reads, Nat. Methods, 15, 455-460, https://doi.org/10.1038/s41592-018-0002-6.
Seki, M., Katsumata, E., Suzuki, A., Sereewattanawoot, S., Sakamoto, Y., Mizushima-Sugano, J., Sugano, S., Kohno, T., Frith, M. C., Tsuchihara, K., and Suzuki, Y. (2019) Evaluation and application of RNA-Seq by MinION, DNA Res., 26, 55-65, https://doi.org/10.1093/dnares/dsy038.
Rang, F. J., Kloosterman, W. P., and de Ridder, J. (2018) From squiggle to basepair: computational approaches for improving nanopore sequencing read accuracy, Genome Biol., 19, 90, https://doi.org/10.1186/s13059-018-1462-9.
Lee, I., Razaghi, R., Gilpatrick, T., Molnar, M., Gershman, A., Sadowski, N., Sedlazeck, F. J., Hansen, K. D., Simpson, J. T., and Timp, W. (2020) Simultaneous profiling of chromatin accessibility and methylation on human cell lines with nanopore sequencing, Nat. Methods, 17, 1191-1199, https://doi.org/10.1038/s41592-020-01000-7.
Norris, A. L., Workman, R. E., Fan, Y. F., Eshleman, J. R., and Timp, W. (2016) Nanopore sequencing detects structural variants in cancer, Cancer Biol. Ther., 17, 246-253, https://doi.org/10.1080/15384047.2016.1139236.
Squires, A., Atas, E., and Meller, A. (2015) Nanopore sensing of individual transcription factors bound to DNA, Sci. Rep., 5, 1-11, https://doi.org/10.1038/srep11643.
Lyko, F. (2018) The DNA methyltransferase family: a versatile toolkit for epigenetic regulation, Nat. Rev. Genet., 19, 81-92, https://doi.org/10.1038/nrg.2017.80.
Chan, W. M., Ip, J. D., Chu, A. W. H., Yip, C. C. Y., Lo, L. S., Chan, K. H., Ng, A. C. K., Poon, R. W. S., To, W. K., Tsang, O. T. Y., et al. (2020) Identification of nsp1 gene as the target of SARS-CoV-2 real-time RT-PCR using nanopore whole-genome sequencing, J. Med. Virol., 92, 2725-2734, https://doi.org/10.1002/jmv.26140.
Wang, M., Fu, A. S., Hu, B., Tong, Y. Q., Liu, R., Liu, Z., Gu, J. S., Xiang, B., Liu, J. H., Jiang, W., et al. (2020) Nanopore targeted sequencing for the accurate and comprehensive detection of SARS-CoV-2 and other respiratory viruses, Small, 16, 15, https://doi.org/10.1002/smll.202002169.
Amoutzias, G. D., Nikolaidis, M., and Hesketh, A. (2022) The notable achievements and the prospects of bacterial pathogen genomics, Microorganisms, 10, 1040, https://doi.org/10.3390/microorganisms10051040.
Athanasopoulou, K., Boti, M. A., Adamopoulos, P. G., Skourou, P. C., and Scorilas, A. (2021) Third-generation sequencing: the spearhead towards the radical transformation of modern genomics, Life, 12, 30, https://doi.org/10.3390/life12010030.
Khrenova, M. G., Panova, T. V., Rodin, V. A., Kryakvin, M. A., Lukyanov, D. A., Osterman, I. A., and Zvereva, M. I. (2022) Nanopore sequencing for de novo bacterial genome assembly and search for single-nucleotide polymorphism, Int. J. Mol. Sci., 23, 8569, https://doi.org/10.3390/ijms23158569.
Curry, K. D., Wang, Q., Nute, M. G., Tyshaieva, A., Reeves, E., Soriano, S., Wu, Q., Graeber, E., Finzer, P., Mendling, W., Savidge, T., Villapol, S., Dilthey, A., and Treangen, T. J. (2022) Emu: species-level microbial community profiling of full-length 16S rRNA Oxford Nanopore sequencing data, Nat. Methods, 19, 845-853, https://doi.org/10.1038/s41592-022-01520-4.
Clarke, J., Wu, H.-C., Jayasinghe, L., Patel, A., Reid, S., and Bayley, H. (2009) Continuous base identification for single-molecule nanopore DNA sequencing, Nat. Nanotechnol., 4, 265-270, https://doi.org/10.1038/s41592-022-01520-4.
Manrao, E. A., Derrington, I. M., Laszlo, A. H., Langford, K. W., Hopper, M. K., Gillgren, N., Pavlenok, M., Niederweis, M., and Gundlach, J. H. (2012) Reading DNA at single-nucleotide resolution with a mutant MspA nanopore and phi29 DNA polymerase, Nat. Biotechnol., 30, 349-353, https://doi.org/10.1038/nbt.2171.
Cherf, G. M., Lieberman, K. R., Rashid, H., Lam, C. E., Karplus, K., and Akeson, M. (2012) Automated forward and reverse ratcheting of DNA in a nanopore at 5-A precision, Nat. Biotechnol., 30, 344-348, https://doi.org/10.1038/nbt.2147.
Steen, H., and Mann, M. (2004) The abc’s (and xyz’s) of peptide sequencing, Nat. Rev. Mol. Cell Biol., 5, 699-711, https://doi.org/10.1038/nrm1468.
Yates, J. R., III (2011) A century of mass spectrometry: from atoms to proteomes, Nat. Methods, 8, 633-637, https://doi.org/10.1038/nmeth.1659.
Aebersold, R., and Mann, M. (2016) Mass-spectrometric exploration of proteome structure and function, Nature, 537, 347-355, https://doi.org/10.1038/nature19949.
Walther, T. C., and Mann, M. (2010) Mass spectrometry-based proteomics in cell biology, J. Cell Biol., 190, 491-500, https://doi.org/10.1083/jcb.201004052.
Domon, B., and Aebersold, R. (2010) Options and considerations when selecting a quantitative proteomics strategy, Nat. Biotechnol., 28, 710-721, https://doi.org/10.1038/nbt.1661.
Oukhaled, G., Mathe, J., Biance, A., Bacri, L., Betton, J., Lairez, D., Pelta, J., and Auvray, L. (2007) Unfolding of proteins and long transient conformations detected by single nanopore recording, Phys. Rev. Lett., 98, 158101, https://doi.org/10.1103/PhysRevLett.98.158101.
Talaga, D., and Li, J. (2009) Single-molecule protein unfolding in solid state nanopores, J. Am. Chem. Soc., 131, 9287-9297, https://doi.org/10.1021/ja901088b.
Van Meervelt, V., Soskine, M., Singh, S., Schuurman-Wolters, G. K., Wijma, H. J., Poolman, B., and Maglia, G. (2017) Real-time conformational changes and controlled orientation of native proteins inside a protein nanoreactor, J. Am. Chem. Soc., 139, 18640-18646, https://doi.org/10.1021/jacs.7b10106.
Varongchayakul, N., Huttner, D., Grinstaff, M. W., and Meller, A. (2018) Sensing native protein solution structures using a solid-state nanopore: unraveling the states of VEGF, Sci. Rep., 8, 1017, https://doi.org/10.1038/s41598-018-19332-y.
Waduge, P., Hu, R., Bandarkar, P., Yamazaki, H., Cressiot, B., Zhao, Q., Whitford, P. C., and Wanunu, M. (2017) Nanopore- based measurements of protein size, fluctuations, and conformational changes, ACS Nano, 11, 5706-5716, https://doi.org/10.1021/acsnano.7b01212.
Martyushenko, N., Bell, N. A., Lamboll, R. D., and Keyser, U. F. (2015) Nanopore analysis of amyloid fibrils formed by lysozyme aggregation, Analyst, 140, 4882-4886, https://doi.org/10.1039/c5an00530b.
Giamblanco, N., Coglitore, D., Janot, J.-M., Coulon, P. E., Charlot, B., and Balme, S. (2018) Detection of protein aggregate morphology through single antifouling nanopore, Sens. Actuators B, 260, 736-745, https://doi.org/10.1016/j.snb.2018.01.094.
Iacovache, I., De Carlo, S., Cirauqui, N., Dal Peraro, M., van der Goot, F. G., and Zuber, B. (2016) Cryo-EM structure of aerolysin variants reveals a novel protein fold and the pore-formation process, Nat. Commun., 7, 12062, https://doi.org/10.1038/ncomms12062.
Tanaka, K., Caaveiro, J. M. M., Morante, K., González-Mañas, J. M., and Tsumoto, K. (2015) Structural basis for self-assembly of a cytolytic pore lined by protein and lipid, Nat. Commun., 6, 6337, https://doi.org/10.1038/ncomms7337.
Gu, Z., Ying, Y. L., and Long, Y. T. (2018) Nanopore sensing system for high-throughput single molecular analysis, Sci. China Chem., 61, 1483-1485, https://doi.org/10.1007/s11426-018-9312-3.
Kasianowicz, J. J., Balijepalli, A. K., Ettedgui, J., Forstater, J. H., Wang, H., Zhang, H., and Robertson, J. W. F., (2016) Analytical applications for pore-forming proteins, Biochim. Biophys. Acta Biomembr., 1858, 593-606, https://doi.org/10.1016/j.bbamem.2015.09.023.
Ayub, M., Hardwick, S. W., Luisi, B. F., and Bayley, H. (2013) Nanopore-based identification of individual nucleotides for direct RNA sequencing, Nano Lett., 12, 6144-6150, https://doi.org/10.1021/nl403469r.
Khrenova, M., Nikiforova, L., Grabovenko, F., Orlova, N., Sinegubova, M., Kolesov, D., Zavyalova, E., Spiridonova, V., Zatsepin, T., and Zvereva, M. (2022) In vitro selection of an aptamer targeting SARS-CoV-2 Spike protein with nanopore sequence identification reveals discrimination between the authentic strain and Omicron, ChemRxiv. Cambridge: Cambridge Open Engage, https://doi.org/10.26434/chemrxiv-2022-d9gcs.
Xi, D., Shang, J., Fan, E., You, J., Zhang, S., and Wang, H. (2016) Nanopore-based selective discrimination of microRNAs with single-nucleotide difference using locked nucleic acid-modified probes, Anal. Chem., 21, 10540-10546, https://doi.org/10.1021/acs.analchem.6b02620.
Zahid, O. K., Wang, F., Ruzicka, J. A., Taylor, E. W., and Hall, A. R. (2016) Sequence-specific recognition of microRNAs and other short nucleic acids with solid-state nanopores, Nano Lett., 3, 2033-2039, https://doi.org/10.1021/acs.nanolett.6b00001.
Riedl, J., Ding, Y., Fleming, A. M., and Burrows, C. J. (2015) Identification of DNA lesions using a third base pair for amplification and nanopore sequencing, Nat. Commun., 1, 8807, https://doi.org/10.1038/ncomms9807.
Shang, J., Li, Z., Liu, L., Xi, D., and Wang, H. (2018) Label-free sensing of human 8-oxoguanine DNA glycosylase activity with a nanopore, ACS Sensors, 2, 512-518, https://doi.org/10.1021/acssensors.7b00954.
Wang, Y., Tian, K., Shi, R., Gu, A., Pennella, M., Alberts, L., Gates, K. S., Li, G., Fan, H., Wang, M. X., and Gu, L. Q. (2017) Nanolock-nanopore facilitated digital diagnostics of cancer driver mutation in tumor tissue, ACS Sensors, 7, 975-981, https://doi.org/10.1021/acssensors.7b00235.
Zhang, Sh., Cao, Z., Fan, P., Wang, Y., Jia, W., Wang, L., Wang, K., Liu, Y., Du, X., Hu, C., Zhang, P., Chen, H.-Y., and Huang, S. (2022) A nanopore-based saccharide sensor, Angewandte Chemie Int. Ed., 61, e202203769, https://doi.org/10.1002/anie.202203769.
Wang, H.-Y., Song, Z.-Y., Zhang, H.-S., and Chen, S.-P. (2016) Single-molecule analysis of lead(II)-binding aptamer conformational changes in an α-hemolysin nanopore, and sensitive detection of lead(II), Microchim. Acta, 183, 1003-1010, https://doi.org/10.1007/s00604-015-1699-x.
Roozbahani, G. M., Chen, X., Zhang, Y., Xie, R., Ma, R., Li, D., Li, H., and Guan, X. (2017) Peptide-mediated nanopore detection of uranyl ions in aqueous media, ACS Sensors, 5, 703-709, https://doi.org/10.1021/acssensors.7b00210.
Roozbahani, G. M., Chen, X., Zhang, Y., Wang, L., and Guan, X. (2020) Nanopore detection of metal ions: current status and future directions, Small Methods, 4, 2000266, https://doi.org/10.1002/smtd.202000266.
Tsutsui, M., Yokota, K., Yoshida, T., Hotehama, C., Kowada, H., Esaki, Y., Taniguchi, M., Washio, T., and Kawai, T. (2019) ‘Identifying single particles in air using a 3D-integrated solid-state pore’, ACS Sensors, 4, 748-755, https://doi.org/10.1021/acssensors.9b00113.
Goyal, G., Mulero, R., Ali, J., Darvish, A., and Kim, M. J. (2015) Low aspect ratio micropores for single-particle and single-cell analysis: nanoanalysis, Electrophoresis, 36, 1164-1171, https://doi.org/10.1002/elps.201400570.
Tsutsui, M., Yoshida, T., Yokota, K., Yasaki, H., Yasui, T., Arima, A., Tonomura, W., Nagashima, K., Yanagida, T., Kaji, N., Taniguchi, M., Washio, T., Baba, Y., and Kawai, T. (2017) Discriminating single-bacterial shape using low-aspect-ratio pores, Sci. Rep., 7, 17371, https://doi.org/10.1038/s41598-017-17443-6.
Tsutsui, M., Hongo, S., He, Y., Taniguchi, M., Gemma, N., and Kawai, T., (2012) Single-nanoparticle detection using a low-aspect-ratio pore, ACS Nano, 6, 3499-3505, https://doi.org/10.1021/nn300530b.
Taniguchi, M., Takei, H., Tomiyasu, K., Sakamoto, O., and Naono, N. (2022) Sensing the performance of artificially intelligent nanopores developed by integrating solid-state nanopores with machine learning methods, J. Phys. Chem. C, 126, 12197-12209, https://doi.org/10.1021/acs.jpcc.2c02674.
Darvish, A., Goyal, G., Aneja, R., Sundaram, R. V. K., Lee, K., Ahn, C. W., Kim, K.-B., Vlahovskaf, P. M., and Kim, M. J. (2016) Nanoparticle mechanics: deformation detection via nanopore resistive pulse sensing, Nanoscale, 8, 14420-14431, https://doi.org/10.1039/c6nr03371g.
Gu, Z., Ying, Y.-L., Cao, C., He, P., and Long, Y.-T. (2015) Accurate data process for nanopore analysis, Anal. Chem., 87, 907-913, https://doi.org/10.1021/ac5028758.
Misiunas, K., Ermann, N., and Keyser, U. F. (2018) QuipuNet: convolutional neural network for single-molecule nanopore sensing, Nano Lett., 18, 4040-4045, https://doi.org/10.1021/acs.nanolett.8b01709.
Shekar, S., Chien, C. C., Hartel, A., Ong, P., Clarke, O. B., Marks, A., Drndic, M., and Shepard, K. L. (2019) wavelet denoising of high-bandwidth nanopore and ion-channel signals, Nano Lett., 19, 1090-1097, https://doi.org/10.1021/acs.nanolett.8b04388.
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This work was financially supported by the Ministry of Science and Higher Education of the Russian Federation, grant no. 075-15-2021-1396, October 26, 2021.
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M.E.Z. and V.K.S. concept and supervision of the study; O.A.P. analysis of the literature on the structure and organization of nanopores; A.A.Z. and V.A.R analysis of the literature on the history of method development and preparation of illustrations; T.V.P. information on the technology applications; A.K.B preparation of the text and editing the paper.
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Translated from Uspekhi Biologicheskoi Khimii, 2024, Vol. 64, pp. 449-478.
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Berkovich, A.K., Pyshkina, O.A., Zorina, A.A. et al. Direct Determination of the Structure of Single Biopolymer Molecules Using Nanopore Sequencing. Biochemistry Moscow 89 (Suppl 1), S234–S248 (2024). https://doi.org/10.1134/S000629792414013X
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DOI: https://doi.org/10.1134/S000629792414013X