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Enzymology on an Electrode and in a Nanopore: Analysis Algorithms, Enzyme Kinetics, and Perspectives

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Abstract   

Enzymes are powerful and effective biological catalysts demanded in various areas of human activity, especially in medicinal area and as modem diagnostic tools. Enzymes-based electrode sensors (2D format) and nanopore sensors (3D format) represent modern, high-tech areas of bionanotechnology and bionanoscience. A comparative analysis of the catalytic activity of enzymes on flat electrode as a 2D sensor, on an electrode functionalized with a nanoporous material based on indium tin oxide as a transition from 2 to 3D model, and in a biological nanopore as a 3D sensor was carried out. Analysis of electrochemical properties of substrate or product/metabolite for the assessment of catalytic activity of enzymes was described. Comparative kinetic parameters of enzymes immobilized on an electrode and in a nanopore as sensors are given. The authors present the prospects of both electrochemical studies of enzymes using electrode sensor and studies of enzymes or substrates confined in a nanopore sensor.

Highlights

Enzyme-based electrodes (2D format) for analysis of ensemble of proteins were discussed.

A novel method was developed for analysis of cytochrome P450 confined in nanopores on electrode.

Nanopore sensors as 3D systems for analysis of single molecule catalytic activity were analyzed.

Comparative kinetic parameters of enzyme systems on an electrode and in a nanopore were augmented.

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References

  1. Singh, R. S., Singh, T., Singh, A. K. (2019). Enzymes as diagnostic tools. In: Singh RS, Singhania RR, Pandey A, Larroche C (eds) Biomass, biofuels, biochemicals, advances in enzyme technology. Elsevier, B.V., 225–271. https://doi.org/10.1016/B978-0-444-64114-4.00009-1.

  2. Kuddus, M. (2019). Enzymes in food biotechnology, production, applications, and future prospects. Elsevier B.V. https://doi.org/10.1016/C2016-0-04555-2

  3. Kuzikov, A., Masamrekh, R., Archakov, A., & Shumyantseva, V. (2018). Methods for determining of cytochrome P450 isozymes functional activity. Biochemistry (Moscow), 64, 149–168. https://doi.org/10.18097/PBMC20186402149

    Article  Google Scholar 

  4. Schneider, E., & Clark, D. S. (2013). Cytochrome P450 (CYP) enzymes and the development of CYP biosensors. Biosensors & Bioelectronics, 39, 1–13. https://doi.org/10.1016/j.bios.2012.05.043

    Article  Google Scholar 

  5. Shumyantseva, V. V., Kuzikov, A. V., Masamrekh, R. A., Bulko, T. V., & Archakov, A. I. (2018). From electrochemistry to enzyme kinetics of cytochrome P450. Biosensors & Bioelectronics, 121, 192–204. https://doi.org/10.1016/j.bios.2018.08.040

    Article  Google Scholar 

  6. Krishnan, S. (2020). Bioelectrodes for evaluating molecular therapeutic and toxicity properties. Current Opinion in Electrochemistry, 19, 20–26. https://doi.org/10.1016/j.coelec.2019.09.004

    Article  Google Scholar 

  7. Suprun, E. V., Saveliev, A. A., Evtugyn, G. A., Lisitsa, A. V., Bulko, T., Shumyantseva, V. V., & Archakov, A. I. (2012). Electrochemical approach for acute myocardial infarction diagnosis based on direct antibodies-free analysis of human blood plasma. Biosensors & Bioelectronics, 33, 158–164. https://doi.org/10.1016/j.bios.2011.12.045

    Article  Google Scholar 

  8. Shumyantseva, V. V., Bulko, T. V., Sigolaeva, L. V., Kuzikov, A. V., Pogodin, P. V., & Archakov, A. I. (2018). Molecular imprinting coupled with electrochemical analysis for plasma samples classification in acute myocardial infarction diagnostic. Biosensors & Bioelectronics, 99, 216–222. https://doi.org/10.1016/j.bios.2017.07.026

    Article  Google Scholar 

  9. Archakov, A. I., & Bachmanova, G. I. (1990). Cytochrome P-450 and active oxygen. Taylor & Francis Group.

    Google Scholar 

  10. Guengerich, F. P. (2001). Common and uncommon cytochrome P450 reactions related to metabolism and chemical toxicity. Chemical Research in Toxicology, 14, 611–650. https://doi.org/10.1021/tx0002583

    Article  Google Scholar 

  11. Bernhardt, R. (2006). Cytochromes P450 as versatile biocatalysts. Journal of Biotechnology, 124, 128–145. https://doi.org/10.1016/j.jbiotec.2006.01.026

    Article  Google Scholar 

  12. Ortiz de Montellano, P. R. (2015). Substrate oxidation. In: Cytochrome P450. Structure, mechanism, and biochemistry. 4th edn, pp. 111–176.

  13. Gomez, L., Kovac, J. R., & Lamb, D. J. (2015). CYP17A1 inhibitors in castration-resistant prostate cancer. Steroids, 95, 80–87. https://doi.org/10.1016/j.steroids.2014.12.021

    Article  Google Scholar 

  14. Hargrove, T. Y., Friggeri, L., Wawrzak, Z., Sivakumaran, S., Yazlovitskaya, E. M., Hiebert, S. W., Guengerich, F. P., Waterman, M. R., & Lepesheva, G. I. (2016). Human sterol 14α-demethylase (CYP51) as a target for anticancer chemotherapy: Towards structure-aided drug design. Journal of Lipid Research, 57, 1552–1563. https://doi.org/10.1194/jlr.M069229

    Article  Google Scholar 

  15. Estabrook, R. W., Shet, M. S., Faulkner, K., & Fisher, C. W. (1996). The use of electrochemistry for the synthesis of 17 alpha-hydroxyprogesterone by a fusion protein containing P450c17. Endocrine Research, 22, 665–671. https://doi.org/10.1080/07435809609043761

    Article  Google Scholar 

  16. Hagen, K. D., Gillan, J. M., Im, S.-C., Landefeld, S., Mead, G., Hiley, M., Waskell, L. A., Hill, M. G., & Udita, A. K. (2013). Electrochemistry of mammalian cytochrome P450 2B4 indicates tunable thermodynamic parameters in surfactant films. Journal of Inorganic Biochemistry, 129, 30–34. https://doi.org/10.1016/j.jinorgbio.2013.07.039

    Article  Google Scholar 

  17. Carrara, S., Baj-Rossi, C., Boero, C., & De Micheli, G. (2014). Do carbon nanotubes contribute to electrochemical biosensing? Electrochimica Acta, 128, 102–112. https://doi.org/10.1016/j.electacta.2013.12.123

    Article  Google Scholar 

  18. Cui, D., Mi, L., Xu, X., Lu, J., Qian, J., & Liu, S. (2014). Nanocomposites of graphene and cytochrome P450 2D6 isozyme for electrochemical-driven tramadol metabolism. Langmuir, 30, 11833–11840. https://doi.org/10.1021/la502699m

    Article  Google Scholar 

  19. Shumyantseva, V. V., Makhova, A. A., Bulko, T. V., Kuzikov, A. V., Masamrekh, R. A., Shkel, T., Usanov, S., Gilep, A., & Archakov, A. I. (2019). Bioelectrochemical systems as technologies for studying drug interactions related to cytochrome P450. Bio Nano Science, 9, 79–86. https://doi.org/10.1007/s12668-018-0567-7

    Article  Google Scholar 

  20. Mi, L., He, F., Jiang, L., Shangguan, L., Zhang, X., Ding, T., Liu, A., Zhang, Y., & Liu, S. (2017). Electrochemically-driven benzo [a] pyrene metabolism via human cytochrome P450 1A1 with reductase coated nitrogen-doped graphene nano-composites. Journal of Electroanalytical Chemistry, 804, 23–28. https://doi.org/10.1016/j.jelechem.2017.09.035

    Article  Google Scholar 

  21. Mie, Y., Tateyama, E., & Komatsu, Y. (2014). P-Aminothiophenol modification on gold surface improves stability for electrochemically driven cytochrome P450 microsome activity. Electrochimica Acta, 115, 364–369. https://doi.org/10.1016/j.electacta.2013.10.170

    Article  Google Scholar 

  22. Panicco, P., Castrignanò, S., Sadeghi, S. J., Di Nardo, G., & Gilardi, G. (2021). Engineered human CYP2C9 and its main polymorphic variants for bioelectrochemical measurements of catalytic response. Bioelectrochem, 138, 107729. https://doi.org/10.1016/j.bioelechem.2020.107729

    Article  Google Scholar 

  23. Jensen, S. B., Thodberg, S., Parween, Sh., Moses, M. E., Hansen, C. C., Thomsen, J., Sletfjerding, M. B., Knudsen, C., Del Giudice, R., Lund, P. M., Castaño, P. R., Bustamante, Y. G., Velazquez, M. N. R., Jørgensen, F. S., Pandey, A. V., Laursen, T., Møller, B. L., & Hatzakis, N. S. (2021). Biased cytochrome P450-mediated metabolism via small-molecule ligands binding P450 oxidoreductase. Nature Communications, 12, 2260. https://doi.org/10.1038/s41467-021-22562-w

    Article  Google Scholar 

  24. Shumyantseva, V. V., Makhova, A. A., Bulko, T. V., Kuzikov, A. V., Shich, E. V., Suprun, E., Kukes, V., Usanov, S. A., & Archakov, A. (2013). The dose-dependent influence of antioxidant vitamins on electrochemically-driven cytochrome P450 3A4 catalysis. Oxid Antioxid Med Sci, 2, 113–117. https://doi.org/10.5455/oams.010413.or.034

    Article  Google Scholar 

  25. Shumyantseva, V. V., Makhova, A. A., Bulko, T. V., Kuzikov, A. V., Shich, E. V., Kukes, V., & Archakov, A. I. (2015). Electrocatalytic cycle of P450 cytochromes: The protective and stimulating roles of antioxidants. RSC Advances, 5, 71306. https://doi.org/10.1039/c5ra09998f

    Article  Google Scholar 

  26. Makhova, A. A., Shikh, E. V., Bulko, T. V., Sizova, Z. M., & Shumyantseva, V. V. (2019). The influence of taurine and L-carnitine on 6 β-hydroxycortisol/cortisol ratio in human urine of healthy volunteers. Drug Metabol. Personal. Ther., 34, 20190013. https://doi.org/10.1515/dmpt-2019-0013

    Article  Google Scholar 

  27. Sun, P., & Wu, Y. (2013). An amperometric biosensor based on human cytochrome P450 2C9 in polyacrylamide hydrogel films for bisphenol A determination. Sensors and Actuators, B: Chemical Sensors and Materials, 178, 113–118. https://doi.org/10.1016/j.snb.2012.12.055

    Article  Google Scholar 

  28. Hrycay, E. G., & Bandiera, S. M. (2015). Monooxygenase, peroxygenase and peroxidase properties and reaction mechanism of cytochrome P450 enzymes. Advances in Experimental Medicine and Biology, 851, 1–61. https://doi.org/10.1007/978-3-319-16009-2_1

    Article  Google Scholar 

  29. Veith, A., & Moorthy, B. (2018). Role of cytochrome P450s in the generation and metabolism of reactive oxygen species. Curr Opin Toxicol, 7, 44–51. https://doi.org/10.1016/j.cotox.2017.10.003

    Article  Google Scholar 

  30. Ferrari, A.G.-M., Rowley-Neale, S. J., & Banks, C. E. (2021). Screen-printed electrodes: Transitioning the laboratory in-to-the field. Talanta Open, 3, 100032. https://doi.org/10.1016/j.talo.2021.100032

    Article  Google Scholar 

  31. Sadeghi, S. J., Fantuzzi, A., & Gilardi, G. (2011). Breakthrough in P450 bioelectrochemistry and future perspectives. Biochim Biophys Acta - Proteins Proteomics, 1814, 237–248. https://doi.org/10.1016/j.bbapap.2010.07.010

    Article  Google Scholar 

  32. Jalalvand, A. R. (2020). A study originated from combination of electrochemistry and chemometrics for investigation of the inhibitory effects of ciprofloxacin as a potent inhibitor on cytochrome P450. Microchemical Journal, 57, 105104. https://doi.org/10.1016/j.microc.2020.105104

    Article  Google Scholar 

  33. Agafonova, L. E., Bulko, T. V., Kuzikov, A. V., Masamrekh, R. A., & Shumyantseva, V. V. (2022). Sensors for analysis of drugs, drug-drug interactions, and catalytic activity of enzymes. Bulletin of RSMU, 1, 60–65. https://doi.org/10.24075/brsmu.2022.009

    Article  Google Scholar 

  34. Shumyantseva, V., Bulko, T., Sigolaeva, L., Kuzikov, A., & Archakov, A. (2016). Electrosynthesis and binding properties of molecularly imprinted poly-o-phenylenediamine for selective recognition and direct electrochemical detection of myoglobin. Biosensors & Bioelectronics, 86, 330–336. https://doi.org/10.1016/j.bios.2016.05.101

    Article  Google Scholar 

  35. Shumyantseva, V., Koroleva, P., Bulko, T., Sergeev, G., & Usanov, S. (2021). Predicting drug–drug interactions by electrochemically driven cytochrome P450 3A4 reactions. Drug metabolism and Personalized Therapy. https://doi.org/10.1515/dmpt-2021-0116

    Article  Google Scholar 

  36. Kuzikov, A. V., Dugin, N. O., Stulov, S. V., Shcherbinin, D. S., Zharkova, M. S., Tkachev, Y. V., Timofeev, V. P., Veselovsky, A. V., Shumyantseva, V. V., & Misharin, A. Y. (2014). Novel oxazolinyl derivatives of pregna-5, 17 (20)-diene as 17α-hydroxylase/17, 20-lyase (CYP17A1) inhibitors. Steroids, 88, 66–71. https://doi.org/10.1016/j.steroids.2014.06.014

    Article  Google Scholar 

  37. Gray, J. J. (2004). The interaction of proteins with solid surfaces. Curr Opin Structur Biol, 14, 110–115. https://doi.org/10.1016/j.sbi.2003.12.001

    Article  Google Scholar 

  38. Kuzikov, A. V., Bulko, T. V., Koroleva, P. I., Masamrekh, R. A., Babkina, S. S., Gilep, A. A., & Shumyantseva, V. V. (2020). Electroanalytical and electrocatalytical characteristics of cytochrome P450 3A4 using electrodes modified with nanocomposite carbon nanomaterials. Biochemistry (Moscow) Supplement Series B Biomedical Chemistry, 66(1), 64–70. https://doi.org/10.18097/PBMC20206601064

    Article  Google Scholar 

  39. Kuzikov, A. V., Masamrekh, R. A., Khatri, Y., Zavialova, M. G., Bernhardt, R., Archakov, A. I., & Shumyantseva, V. V. (2016). Scrutiny of electrochemically-driven electrocatalysis of C-19 steroid 1 α -hydroxylase (CYP260A1) from Sorangium cellulosum So ce56. Analytical Biochemistry, 513, 28–35. https://doi.org/10.1016/j.ab.2016.08.016

    Article  Google Scholar 

  40. Frank, R., Klenner, M., Azendorf, R., Bartz, M., Jahnke, H. G., & Robitzki, A. A. (2017). Novel 96-well quantitative bioelectrocatalytic analysis platform reveals highly efficient direct electrode regeneration of cytochrome P450 BM3 on indium tin oxide. Biosensors & Bioelectronics, 93, 322–329. https://doi.org/10.1016/j.bios.2016.08.059

    Article  Google Scholar 

  41. Herold, R., Reinbold, R., Megarity, C., Abboud, M., Schofield, C., & Armstrong, F. A. (2021). Exploiting electrode nanoconfinement to investigate the catalytic properties of isocitrate dehydrogenase (IDH1) and a cancer-associated variant. Journal of Physical Chemistry Letters, 12, 6095–6101. https://doi.org/10.1021/acs.jpclett.1c01517

    Article  Google Scholar 

  42. Yen, K., Travins, J., Wang, F., David, M., Artin, E., et al. (2017). AG-221, a first-in-class therapy targeting acute myeloid leukemia harboring oncogenic IDH2 mutations. Cancer Discovery, 7, 478–493. https://doi.org/10.1158/2159-8290.CD-16-1034

    Article  Google Scholar 

  43. Davis, C., Wang, S., & Sepunaru, L. (2021). What can electrochemistry tell us about individual enzymes? Current Opinion in Electrochemistry, 25, 100643. https://doi.org/10.1016/j.coelec.2020.100643

    Article  Google Scholar 

  44. Gaus, K., & Gooding, J. J. (2016). Single-molecule sensors: Challenges and opportunities for quantitative analysis. Angewandte Chemie International Edition, 55, 11354–11366. https://doi.org/10.1002/anie.201600495

    Article  Google Scholar 

  45. Shumyantseva, V. V., Bulko, T. V., Kuzikov, A. V., Masamrekh, R. A., Konyakhina, A. Y., Romanenko, I., Max, J. B., Köhler, M., Gilep, A. A., Usanov, S. A., Pergushov, D. V., Schacher, F. H., & Sigolaeva, L. V. (2020). All-electrochemical nanocomposite two-electrode setup for quantification of drugs and study of their electrocatalytical conversion by cytochromes P450. Electrochimica Acta, 336, 135579. https://doi.org/10.1016/j.electacta.2019.135579

    Article  Google Scholar 

  46. Shumyantseva, V. V., Bulko, T. V., Koroleva, P. I., Shikh, E. V., Makhova, A. A., Kisel, M. S., Haidukevich, I. V., & Gilep, A. A. (2022). Human cytochrome P450 2C9 and its polymorphic modifications: Electroanalysis, catalytic properties, and approaches to the regulation of enzymatic activity. Processes, 10(2), 383. https://doi.org/10.3390/pr10020383

    Article  Google Scholar 

  47. Zanger, U. M., & Schwab, M. (2013). Cytochrome P450 enzymes in drug metabolism: Regulation of gene expression, enzyme activities, and impact of genetic variation. Pharmacology & Therapeutics, 138, 103–141. https://doi.org/10.1016/j.pharmthera.2012.12.007

    Article  Google Scholar 

  48. Nouri-Nigjeh, E., Bischoff, R., Permentier, B. A. P., & HP,. (2011). Electrochemistry in the mimicry of oxidative drug metabolism by cytochrome P450s. Current Drug Metabolism, 12, 359–371. https://doi.org/10.2174/138920011795202929

    Article  Google Scholar 

  49. Suckow, R. F., Cooper, T. B., Quitkin, F. M., & Stewart, J. W. (1982). Determination of mianserin and metabolites in plasma by liquid chromatography with electrochemical detection. Journal of Pharmaceutical Sciences, 71, 889–892. https://doi.org/10.1002/jps.2600710812

    Article  Google Scholar 

  50. Tang, W. (2003). The metabolism of diclofenac–enzymology and toxicology perspectives. Current Drug Metabolism, 4, 319–329. https://doi.org/10.2174/1389200033489398

    Article  Google Scholar 

  51. Rajendra, G., Sanghamitra, C., & Bharati, A. (2010). Electrochemical investigations of diclofenac at edge plane pyrolytic graphite electrode and its determination in human urine. Sensors and Actuators, B: Chemical Sensors and Materials, 145(2), 743–748. https://doi.org/10.1016/j.snb.2010.01.038

    Article  Google Scholar 

  52. Cid-Cerón, M. M., Guzmán-Hernández, D. S., Ramírez-Silva, M. T., Galano, A., Romero-Romo, M., & Palomar-Pardavé, M. (2016). New insigths on the kinetics and mechanism of the electrochemical oxidation of diclofenac in neutral aqueous medium. Electrochimica Acta, 199, 92–98. https://doi.org/10.1016/j.electacta.2016.03.094

    Article  Google Scholar 

  53. Aguilar-Lira, G. Y., Álvarez-Romero, G. A., Zamora-Suárez, A., Palomar-Pardavé, M., Rojas-Hernández, A., Rodríguez-Ávila, J. A., & Páez-Hernández, M. E. (2017). New insights on diclofenac electrochemistry using graphite as working electrode. Journal of Electroanalytical Chemistry, 794, 182–188. https://doi.org/10.1016/j.jelechem.2017.03.050

    Article  Google Scholar 

  54. Madsen, K. G., Skonberg, C., Jurva, U., Cornett, C., Hansen, S. H., Johansen, T. N., & Olsen, J. (2008). Bioactivation of diclofenac in vitro and in vivo: Correlation to electrochemical studies. Chemical Research in Toxicology, 21(5), 1107–1119. https://doi.org/10.1021/tx700419d

    Article  Google Scholar 

  55. Kaminsky, L. S., & Zhang, Z.-Y. (1997). Human P450 metabolism of warfarin. Pharmacology & Therapeutics, 73(1), 67–74. https://doi.org/10.1016/S0163-7258(96)00140-4

    Article  Google Scholar 

  56. Kuzikov, A. V., Filippova, T. A., Masamrekh, R. A., & Shumyantseva, V. V. (2022). Electrochemical determination of (S)-7-hydroxywarfarin for analysis of CYP2C9 catalytic activity. Journal of Electroanalytical Chemistry, 904, 115937. https://doi.org/10.1016/j.jelechem.2021.115937

    Article  Google Scholar 

  57. Mosher, C. M., Hummel, M. A., Tracy, T. S., & Rettie, A. E. (2008). Functional analysis of phenylalanine residues in the active site of cytochrome P450 2C9. Biochemistry, 47, 11725–11734. https://doi.org/10.1021/bi801231m

    Article  Google Scholar 

  58. Sohl, C. D., & Guengerich, F. P. (2010). Kinetic analysis of the three-step steroid aromatase reaction of human cytochrome P450 19A1. Journal of Biological Chemistry, 285(23), 17734–17743. https://doi.org/10.1074/jbc.M110.123711

    Article  Google Scholar 

  59. Zhu, Y., Liu, X., & Jia, J. (2015). Electrochemical detection of natural estrogens using a graphene/ordered mesoporous carbon modified carbon paste electrode. Analytical Methods, 7(20), 8626–8631. https://doi.org/10.1039/C5AY01833A

    Article  Google Scholar 

  60. Moraes, F. C., Rossi, B., Donatoni, M. C., de Oliveira, K. T., & Pereira, E. C. (2015). Sensitive determination of 17β-estradiol in river water using a graphene based electrochemical sensor. Analytica Chimica Acta, 881, 37–43. https://doi.org/10.1016/j.aca.2015.04.043

    Article  Google Scholar 

  61. Lin, X., & Li, Y. (2006). A sensitive determination of estrogens with a Pt nano-clusters/multi-walled carbon nanotubes modified glassy carbon electrode. Biosensors & Bioelectronics, 22(2), 253–259. https://doi.org/10.1016/j.bios.2006.01.005

    Article  Google Scholar 

  62. Hu, S., Wu, K., Yi, H., & Cui, D. (2002). Voltammetric behavior and determination of estrogens at Nafion-modified glassy carbon electrode in the presence of cetyltrimethylammonium bromide. Analytica Chimica Acta, 464, 209–216. https://doi.org/10.1016/S0003-2670(02)00496-8

    Article  Google Scholar 

  63. Musa, A. M., Kiely, J., Luxton, R., & Honeychurch, K. C. (2021). Recent progress in screen-printed electrochemical sensors and biosensors for the detection of estrogens. Trends in Analytical Chemistry, 139, 116254. https://doi.org/10.1016/j.trac.2021.116254

    Article  Google Scholar 

  64. Kuzikov, A. V., Masamrekh, R. A., Filippova, T. A., Haurychenka, Y. I., Gilep, A. A., Shkel, T. V., Strushkevich, N. V., Usanov, S. A., & Shumyantseva, V. V. (2020). Electrochemical oxidation of estrogens as a method for CYP19A1 (aromatase) electrocatalytic activity determination. Electrochimica Acta, 333, 135539. https://doi.org/10.1016/j.electacta.2019.135539

    Article  Google Scholar 

  65. Sheng, Y., Zhang, S., Liu, L., & Wu, H.-C. (2020). Measuring enzymatic activities with nanopores. ChemBioChem, 21(15), 2089–2097. https://doi.org/10.1002/cbic.202000079

    Article  Google Scholar 

  66. Fahie, M. A. V. (2021). Nanopore technology: Methods and protocols. Springer Protocols, Science+Business Media, LLC, part of Springer Nature. https://doi.org/10.1007/2F978-1-0716-0806-7.pdf

  67. Haque, F., Li, J., Wu, H.-C., Liang, X.-J., & Guo, P. (2013). Solid-state and biological nanopore for real-time sensing of single chemical and sequencing of DNA. Nano Today, 8(1), 56–74. https://doi.org/10.1016/j.nantod.2012.12.008

    Article  Google Scholar 

  68. Robertson, J., Ghimire, M. L., & Reiner, J. (2021). Nanopore sensing: A physical-chemical approach. BBA-Biomembranes, 1863(9), 183644. https://doi.org/10.1016/j.bbamem.2021.183644

    Article  Google Scholar 

  69. Wanunu, M. (2012). Nanopores: A journey towards DNA sequencing. Physics of Life Reviews, 9(2), 125–158. https://doi.org/10.1016/j.plrev.2012.05.010

    Article  Google Scholar 

  70. Haque, F., Lunn, J., Fang, H., Smithrud, D., & Guo, P. (2012). Real-time sensing and discrimination of single chemicals using the channel of phi29 DNA packaging nanomotor. ACS Nano, 6(4), 3251–3261. https://doi.org/10.1007/978-1-4939-8556-2_21

    Article  Google Scholar 

  71. Wang, S., Haque, F., Rychahou, P. G., Evers, B. M., & Guo, P. (2013). Engineered nanopore of Phi29 DNA-packaging motor for real-time detection of single colon cancer specific antibody in serum. ACS Nano, 7(11), 9814–9822. https://doi.org/10.1021/nn404435v

    Article  Google Scholar 

  72. Yu, R.-J., Chen, K.-L., Ying, Y.-L., & Long, Y.-T. (2022). Nanopore electrochemical measurement for single molecular interactions and beyond. Current Opinion in Electrochemistry, in press. https://doi.org/10.1016/j.coelec.2022.101063

    Article  Google Scholar 

  73. Chen, H., Lin, Y., Long, Y.-T., Minteer, S. D., & Ying, Y.-L. (2022). Nanopore-based measurement of the interaction of P450cam monooxygenase and putidaredoxin at the single-molecule level. Faraday Discussions, 233, 295–302. https://doi.org/10.1039/D1FD00042J

    Article  Google Scholar 

  74. Jain, M., Olsen, H. E., Paten, B., & Akeson, M. (2016). The Oxford Nanopore MinION: Delivery of nanopore sequencing to the genomics community. Genome Biology, 17, 1146. https://doi.org/10.1186/s13059-016-1103-0

    Article  Google Scholar 

  75. Lu, H., Giordano, F., & Ning, Z. (2016). Oxford Nanopore MinION sequencing and genome assembly. Genomics, Proteomics & Bioinformatics, 14(5), 265–279. https://doi.org/10.1016/j.gpb.2016.05.004

    Article  Google Scholar 

  76. Hu, F., Angelov, B., Li, N., Lin, X., & Zou, A. (2020). Single-molecule study of peptides with the same amino acid composition but different sequences using an aerolysin nanopore. ChemBioChem, 21(17), 2467–2473. https://doi.org/10.1002/cbic.202000119

    Article  Google Scholar 

  77. Willems, K., Van Meervelt, V., Wloka, C., & Maglia, G. (2017). Single-molecule nanopore enzymology. Phil Trans R Soc B, 372(1726), 20160230. https://doi.org/10.1098/rstb.2016.0230

    Article  Google Scholar 

  78. Talaga, D. S., & Li, J. (2009). Single-molecule protein unfolding in solid state nanopores. Journal of the American Chemical Society, 131(26), 9287–9297. https://doi.org/10.1021/ja901088b

    Article  Google Scholar 

  79. Kasianowicz, J. J., Brandin, E., Branton, D., & Deamer, D. W. (1996). Characterization of individual polynucleotide molecules using a membrane channel. Proceedings of the National academy of Sciences of the United States of America, 93(24), 13770–13773. https://doi.org/10.1073/pnas.93.24.13770

    Article  Google Scholar 

  80. Soskine, M., Biesemans, A., De Maeyer, M., & Maglia, G. (2013). Tuning the size and properties of ClyA nanopores assisted by directed evolution. Journal of the American Chemical Society, 135(36), 13456–13463. https://doi.org/10.1021/ja4053398

    Article  Google Scholar 

  81. Van Meervelt, V., Soskine, M., & Maglia, G. (2014). Detection of two isomeric binding configurations in a protein–aptamer complex with a biological nanopore. ACS Nano, 8(12), 12826–12835. https://doi.org/10.1021/nn506077e

    Article  Google Scholar 

  82. Meyer, N., Abrao-Nemeir, I., Janot, J.-M., Torrent, J., Lepoitevin, M., & Balme, S. (2021). Solid-state and polymer nanopores for protein sensing. Advances in Colloid and Interface Science, 298, 102561. https://doi.org/10.1016/j.cis.2021.102561

    Article  Google Scholar 

  83. Wloka, C., Galenkamp, N. S., van der Heide, N. J., Lucas, F. L. R., & Maglia, G. (2021). Strategies for enzymological studies and measurements of biological molecules with the cytolysin A nanopore. Methods in Enzymol, 649, 567–585. https://doi.org/10.1016/bs.mie.2021.01.007

    Article  Google Scholar 

  84. Wang, S., Zhao, Z., Haque, F., & Guo, P. (2018). Engineering of protein nanopores for sequencing, chemical or protein sensing and disease diagnosis. Current Opinion in Biotechnology, 51, 80–89. https://doi.org/10.1016/j.copbio.2017.11.006

    Article  Google Scholar 

  85. Galenkamp, N. S., Van Meervelt, V., Mutter, N. L., van der Heide, N. J., Wloka, C., & Maglia, G. (2021). Preparation of cytolysin A (ClyA) nanopores. Methods in Molecular Biology, 2186, 11–18. https://doi.org/10.1007/978-1-0716-0806-7_2

    Article  Google Scholar 

  86. Maglia, G., Heron, A. J., Stoddart, D., Japrung, D., & Bayley, H. (2010). Analysis of single nucleic acid molecules with protein nanopores. Methods in Enzymology, 475, 591–623. https://doi.org/10.1016/S0076-6879(10)75022-9

    Article  Google Scholar 

  87. Montal, M., & Mueller, P. (1972). Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proceedings of the National academy of Sciences of the United States of America, 69(12), 3561–3566. https://doi.org/10.1073/pnas.69.12.3561

    Article  Google Scholar 

  88. Zakharian, E. (2013). Recording of ion channel activity in planar lipid bilayer experiments. Methods in Molecular Biology, 998, 109–118. https://doi.org/10.1007/978-1-62703-351-0_8

    Article  Google Scholar 

  89. Zakharian, E. (2021). Ion channel reconstitution in lipid bilayers. Methods in Enzymology, 652, 273–291. https://doi.org/10.1016/bs.mie.2021.03.001

    Article  Google Scholar 

  90. Soskine, M., Biesemans, A., & Maglia, G. (2015). Single-molecule analyte recognition with ClyA nanopores equipped with internal protein adaptors. Journal of the American Chemical Society, 137(17), 5793–5797. https://doi.org/10.1021/jacs.5b01520

    Article  Google Scholar 

  91. Wloka, C., Meervelt, V. V., Gelder, D. V., Danda, N., Jager, N., Williams, C. P., & Maglia, G. (2017). Label-free and real-time detection of protein ubiquitination with a biological nanopore. ACS Nano, 11(5), 4387–4394. https://doi.org/10.1021/acsnano.6b07760

    Article  Google Scholar 

  92. Shorkey, S. A., Du, J., Pham, R., Strieter, E., & Chen, M. (2021). Real-time and label-free measurement of deubiquitinase activity with a MspA nanopore. ChemBioChem, 22(17), 2688–2692. https://doi.org/10.1002/cbic.202100092

    Article  Google Scholar 

  93. Galenkamp, N. S., Biesemans, A., & Maglia, G. (2020). Directional conformer exchange in dihydrofolate reductase revealed by single-molecule nanopore recordings. Nature Chem, 12(5), 481–488. https://doi.org/10.1038/s41557-020-0437-0

    Article  Google Scholar 

  94. Trewick, S. C., Henshaw, T. F., Hausinger, R. P., Lindahl, T., & Sedgwick, B. (2002). Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature, 419, 174–178. https://doi.org/10.1038/nature00908

    Article  Google Scholar 

  95. Zhao, Q., de Zoysa, R. S. S., Wang, D., Jayawardhana, D. A., & Guan, X. (2009). Real-time monitoring of peptide cleavage using a nanopore probe. Journal of the American Chemical Society, 131(18), 6324–6325. https://doi.org/10.1021/ja9004893

    Article  Google Scholar 

  96. Sahasrabudhe, S. R., Brown, A. M., Hulmes, J. D., Vitek, M. P., Blume, A. J., & Sonnenberg, J. L. (1996). Enzymatic generation of the amino terminus of the beta-amyloid peptide. Journal of Biological Chemistry, 268(22), 16699–16705. https://doi.org/10.1016/S0021-9258(19)85474-1

    Article  Google Scholar 

  97. Li, M., Li, W., Xiao, Y., Liu, Q., Liang, L., Wang, D., Huang, W., & Wang, L. (2021). Nanopore detects γ-radiation inhibited HIV-1 protease activity. Biosensors & Bioelectronics, 194, 113602. https://doi.org/10.1016/j.bios.2021.113602

    Article  Google Scholar 

  98. Pham, B., Eron, S. J., Hill, M. E., Li, X., Fahie, M. A., Hardy, J. A., & Chen, M. (2019). A nanopore approach for analysis of caspase-7 activity in cell lysates. Biophysical Journal, 117(5), 844–855. https://doi.org/10.1016/j.bpj.2019.07.045

    Article  Google Scholar 

  99. Fahie, M. A., Pham, B., Li, F., & Chen, M. (2021). A selective activity-based approach for analysis of enzymes with an OmpG nanopore. Methods in Molecular Biology, 2186, 115–133. https://doi.org/10.1007/978-1-0716-0806-7_9

    Article  Google Scholar 

  100. Cao, M., Wang, H., Tang, H., Zhao, D., & Li, Y. (2021). Enzyme-encapsulated zeolitic imidazolate frameworks formed inside the single glass nanopore: Catalytic performance and sensing application. Analytical Chemistry, 93(36), 12257–12264. https://doi.org/10.1021/acs.analchem.1c01790

    Article  Google Scholar 

  101. Pérez, V. G., & Sánchez-Sánchez, M. (2020). Environmentally friendly enzyme immobilization on MOF materials. Methods in Molecular Biology, 2100, 271–296. https://doi.org/10.1007/978-1-0716-0215-7_18

    Article  Google Scholar 

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Acknowledgements

The study was performed employing “Avogadro” large-scale research facilities.

Funding

The study was financially supported by the Ministry of Education and Science of the Russian Federation, Agreement No. 075–15-2021–933, unique project ID: RF00121X0004. The work was performed within the framework of the Program for Basic Research in the Russian Federation for a long-term period (2021-2030) (No. 122030100168-2).

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VVS, developed the concept, conceptualization, and methodology, supervision and manuscript editing, manuscript writing; AVK, designed the experiments and analyzed the data obtained; RAM, designed the experiments with drugs; TAF, performed the electrochemical experiments; PIK, performed the electrochemical experiments; LEA and TVB, designed the experiments and analyzed the data obtained; AIA, idea, supervision, and manuscript editing. All authors have read and agreed to the published version of the manuscript.

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Correspondence to V. V. Shumyantseva.

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Shumyantseva, V.V., Kuzikov, A.V., Masamrekh, R.A. et al. Enzymology on an Electrode and in a Nanopore: Analysis Algorithms, Enzyme Kinetics, and Perspectives. BioNanoSci. 12, 1341–1355 (2022). https://doi.org/10.1007/s12668-022-01037-2

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