The review considers the possibility of using atomic force microscopy (AFM) as a basic method for protein detection in solutions with low protein concentrations. The demand for new bioanalytical approaches is determined by the problem of insufficient sensitivity of systems used in routine practice for protein detection. Special attention is paid to demonstration of the use in bioanalysis of a combination of AFM and fishing methods as an approach of concentrating biomolecules from a large volume of the analyzed solution on a small surface area.
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Keywords: atomic force microscopy, biospecific fishing, protein detection
Citation:
Pleshakova T.O., Ershova M.O., Valueva A.A., Ivanova I.A., Ivanov Yu.D., Archakov A.I. (2024) AFM-fishing technology for protein detection in solutions. Biomeditsinskaya Khimiya, 70(5), 273-286.
Pleshakova T.O. et al. AFM-fishing technology for protein detection in solutions // Biomeditsinskaya Khimiya. - 2024. - V. 70. -N 5. - P. 273-286.
Pleshakova T.O. et al., "AFM-fishing technology for protein detection in solutions." Biomeditsinskaya Khimiya 70.5 (2024): 273-286.
Pleshakova, T. O., Ershova, M. O., Valueva, A. A., Ivanova, I. A., Ivanov, Yu. D., Archakov, A. I. (2024). AFM-fishing technology for protein detection in solutions. Biomeditsinskaya Khimiya, 70(5), 273-286.
References
Orekhovich V.N. (1952) Sovremennye predstavleniya o belkakh i ikh znachenie v biologii i meditsine, Znanie, Moscow, 2(60), 22 p. Scholar google search
Lisitsa A.V., Ponomarenko E.A., Lokhov P.G., Archakov A.A. (2016) Postgenomic medicine: Alternative to biomarkers. Annals of the Russian Academy of Medical Sciences, 71(3), 255–260. CrossRef Scholar google search
Archakov A.I., Ivanov Y.D., Lisitsa A.V., Zgoda V.G. (2007) AFM fishing nanotechnology is the way to reverse the Avogadro number in proteomics. Proteomics, 7(1), 4–9. CrossRef Scholar google search
Pleshakova T.O., Ivanov Y.D., Valueva A.A., Shumyantseva V.V., Ilgisonis E.V., Ponomarenko E.A., Lisitsa A.V., Chekhonin V.P., Archakov A.I. (2023) Analysis of single biomacromolecules and viruses: Is it a myth or reality? Int. J. Mol. Sci., 24(3), 1877. CrossRef Scholar google search
Lisitsa A., Poverennaya E., Ponomarenko E., Archakov A. (2015) The width of the human plasma proteome compared with a cancer cell line and bacteria. J. Biomol. Res. Ther., 4(3), 132. CrossRef Scholar google search
Ponomarenko E., Baranova A., Lisitsa A., Albar J.P., Archakov A. (2014) The chromosome-centric human proteome project at FEBS congress. Proteomics, 14(2–3), 147–152. CrossRef Scholar google search
Hori S.S., Gambhir S.S. (2011) Mathematical model identifies blood biomarker-based early cancer detection strategies and limitations. Sci. Transl. Med., 3(109), 109ra116. CrossRef Scholar google search
Rissin D.M., Kan C.W., Campbell T.G., Howes S.C., Fournier D.R., Song L., Piech T., Patel P.P., Chang L., Rivnak A.J., Ferrell E.P., Randall J.D., Provuncher G.K., Walt D.R., Duffy D.C. (2010) Single-molecule enzyme-linked immunosorbent assay detects serum proteins at subfemtomolar concentrations. Nat. Biotechnol., 28(6), 595–599. CrossRef Scholar google search
Bryukhovetskiy A.S., Shevchenko V.E., Chekhonin V.P., Bryukhovetskiy I.S., Kovalev S.V., Baklaushev V.P., Davydov M.I. (2013) Comparative proteome mapping of tumor stem cells isolated from U87 glioblastoma, neural stem and multipotent mesenchymal stromal cells of a human: From cataloguing of cell proteins to novel paradigm of proteome-based cell therapy of tumors. Genes and Cells, 8(2), 85–92. CrossRef Scholar google search
Ponomarenko E.A., Zgoda V.G., Kopylov A.T., Poverennaya E.V., Ilgisonis E.V., Lisitsa A.V., Archakov A.I. (2015) The Russian part of the human proteome project: First results and prospects. Biomeditsinskaya Khimiya, 61(2), 169–175. CrossRef Scholar google search
Archakov A.I., Ivanov Yu.D. (2007) Analytical nanobiotechnology for medicine diagnostics. Mol. BioSyst., 3, 336–342. CrossRef Scholar google search
Anderson N.L. (2010) The clinical plasma proteome: A survey of clinical assays for proteins in plasma and serum. Clin. Chem., 56(2), 177–185. CrossRef Scholar google search
Geyer P.E., Holdt L.M., Teupser D., Mann M. (2017) Revisiting biomarker discovery by plasma proteomics. Mol. Syst. Biol., 13(9), 942. CrossRef Scholar google search
Naryzhny S.N., Zgoda V.G., Maynskova M.A., Ronzhina N.L., Belyakova N.V., Legina O.K., Archakov A.I. (2015) Experimental estimation of proteome size for cells and human plasma. Biomeditsinskaya Khimiya, 61(2), 279–285. CrossRef Scholar google search
Archakov A., Ivanov Y., Lisitsa A., Zgoda V. (2009) Biospecific irreversible fishing coupled with atomic force microscopy for detection of extremely low-abundant proteins. Proteomics, 9(5), 1326–1343. CrossRef Scholar google search
Serdyuk I., Zaccai N., Zaccai J. (2009) Metody v molekulyarnoi biofizike: struktura, funktsiya, dinamika Methods in molecular biophysics: Structure, Function, Dynamics. KDU, Moscow 568 p. Scholar google search
Pleshakova T.O., Shumov I.D., Ivanov Yu.D., Malsagova K.A., Kaysheva A.L., Archakov A.I. (2015) AFM-based technologies as the way towards the reverse Avogadro number. Biomeditsinskaya Khimiya, 61(2), 239–253. CrossRef Scholar google search
Eftimov T., Genova-Kalou P., Dyankov G., Bock W.J., Mankov V., Shoar Ghaffari S., Veselinov P., Arapova A., Makouei S. (2023) Capabilities of double-resonance LPG and SPR methods for hypersensitive detection of SARS-CoV-2 structural proteins: A comparative study. Biosensors, 13(3), 318. CrossRef Scholar google search
Ahmadivand A., Gerislioglu B., Ramezani Z., Kaushik A., Manickam P., Ghoreishi S.A. (2021) Functionalized terahertz plasmonic metasensors: Femtomolar-level detection of SARS-CoV-2 spike proteins. Biosens. Bioelectron., 177, 112971. CrossRef Scholar google search
Bodily T.A., Ramanathan A., Wei S., Karkisaval A., Bhatt N., Jerez C., Haque M.A., Ramil A., Heda P., Wang Y., Kumar S., Leite M., Li T., Zhao J., Lal R. (2023) In pursuit of degenerative disease diagnosis: Dementia biomarkers detected by DNA aptamer-attached portable graphene biosensor. Proc. Natl. Acad. Sci. USA, 120(47), e2311565120. CrossRef Scholar google search
Allison D.P., Mortensen N.P., Sullivan C.J., Doktycz M.J. (2010) Atomic force microscopy of biological samples. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol., 2(6), 618–634. CrossRef Scholar google search
Pleshakova T., Bukharina N., Archakov A., Ivanov Y. (2018) Atomic force microscopy for protein detection and their physicochemical characterization. Int. J. Mol. Sci., 19(4), 1142. CrossRef Scholar google search
Sheiko S.S., da Silva M., Shirvaniants D., LaRu, I., Prokhorova S., Moeller M., Matyjaszewski K. (2003) Measuring molecular weight by atomic force microscopy. J. Am. Chem. Soc., 125(22), 6725–6728. CrossRef Scholar google search
Sinyakov A.N. (2007) Biochips: Diagnosis is a matter of technique! Science First Hand, 5(17), 40-49. Scholar google search
Nettikadan S.R., Johnson J.C., Vengasandra S.G., Muys J., Henderson E. (2004) ViriChip: A solid phase assay for detection and identification of viruses by atomic force microscopy. Nanotechnology, 15, 383. CrossRef Scholar google search
Dubrovin E.V., Yaminsky I.V., Presnova G.V., Rubtsova M.Y., Egorov A.M., Grigorenko V.G. (2015) The use of atomic force microscopy for 3D analysis of nucleic acid hybridization on microarrays. Acta Naturae, 7(2), 108–114. CrossRef Scholar google search
Talapatra A., Rouse R., Hardiman G. (2002) Protein microarrays: Challenges and promises. Pharmacogenomics, 3(4), 527–536. CrossRef Scholar google search
Maercker C. (2005) Protein arrays in functional genome research. Biosci. Rep., 25(1-2), 57–70. CrossRef Scholar google search
Janovjak H., Kessler M., Oesterhelt D., Gaub H., Müller D.J. (2003) Unfolding pathways of native bacteriorhodopsin depend on temperature. EMBO J., 22(19), 5220–5229. CrossRef Scholar google search
Valueva A.A., Shumov I.D., Kaysheva A.L., Ivanova I.A., Ziborov V.S., Ivanov Y.D., Pleshakova T.O. (2020) Covalent protein immobilization onto muscovite mica surface with a photocrosslinker. Minerals, 10(5), 464. CrossRef Scholar google search
Ivanov Yu.D., Pleshakova T.O., Malsagova K.A., Kaysheva A.L., Kopylov A.T., Izotov A.A., Tatur V.Yu., Vesnin S.G., Ivanova N.D., Ziborov V.S., Archakov A.I. (2016) AFM fishing of proteins under impulse electric field. Biomeditsinskaya Khimiya, 62(4), 439–446. CrossRef Scholar google search
Gold L., Walker J.J., Wilcox S.K., Williams S. (2012) Advances in human proteomics at high scale with the SOMAscan proteomics platform. New Biotechnol., 29(5), 543–549. CrossRef Scholar google search
Rohloff J.C., Gelinas A.D., Jarvis T.C., Ochsner U.A., Schneider D.J., Gold L., Janjic N. (2014) Nucleic acid ligands with protein-like side chains: Modified aptamers and their use as diagnostic and therapeutic agents. Mol. Ther. Nucleic Acids, 3(10), e201. CrossRef Scholar google search
Ivanov Y.D., Pleshakova T., Malsagova K., Kozlov A., Kaysheva A., Kopylov A., Izotov A., Andreeva E., Kanashenko S., Usanov S., Archakov A. (2014) Highly sensitive protein detection by combination of atomic force microscopy fishing with charge generation and mass spectrometry analysis. FEBS J., 281(20), 4705–4717. CrossRef Scholar google search
Ivanov Yu.D., Danichev V.V., Pleshakova T.O., Shumov I.D., Ziborov V.S., Krokhin N.V., Zagumenniy M.N., Ustinov V.S., Smirnov L.P., Shironin A.V., Archakov A.I. (2014) Irreversible chemical afm-fishing for the detection of low-copied proteins. Biomeditsinskaya Khimiya, 60(1), 28–50. CrossRef Scholar google search
Frantsuzov P.A. (2010) Atomic force microscopy chips for the revelation of markers of viral hepatitis B and C diseases. Diss. kand. nauk, Institute of Biomedical Chemistry, Moscow. Scholar google search
Pleshakova T.O., Kaysheva A.L., Bayzyanova J.M., Anashkina A.S., Uchaikin V.F., Shumov I.D., Ziborov V.S., Konev V.A., Archakov A.I., Ivanov Yu.D. (2017) Advantages of aptamers as ligands upon protein detection by AFM-based fishing. Anal. Methods, 9, 6049–6060. CrossRef Scholar google search
Guo L., Kim D.-H. (2012) LSPR biomolecular assay with high sensitivity induced by aptamer-antigen-antibody sandwich complex. Biosens. Bioelectron., 31(1), 567–570. CrossRef Scholar google search
Horton M., Charras G., Lehenkari P. (2002) Analysis of ligand-receptor interactions in cells by atomic force microscopy. J. Recept. Signal Transduct. Res., 22(1–4), 169–190. CrossRef Scholar google search
Chtcheglova L.A., Shubeita G.T., Sekatskii S.K., Dietler G. (2004) Force spectroscopy with a small dithering of AFM tip: Amethod of direct and continuous measurement of the spring constant of single molecules and molecular complexes. Biophys. J., 86(2), 1177–1184. CrossRef Scholar google search
Zapotoczny S., Auletta T., de Jong M.R., Schönherr H., Huskens J., van Veggel F.C.J.M., Reinhoudt D.N., Vancso G.J. (2002) Chain length and concentration dependence of β-cyclodextrin-ferrocene host-guest complex rupture forces probed by dynamic force spectroscopy. Langmuir, 18(18), 6988–6994. CrossRef Scholar google search
Ivanov Y.D., Bukharina N.S., Pleshakova T.O., Frantsuzov P.A., Andreeva E.Y., Kaysheva A.L., Zgoda V.G., Izotov A.A., Pavlova T.I., Ziborov V.S., Radko S.P., Moshkovskii S.A., Archakov A.I. (2014) Atomic force microscopy fishing and mass spectrometry identification of gp120 on immobilized aptamers. Int. J. Nanomedicine, 9, 4659–4670. CrossRef Scholar google search
Allen S., Chen X., Davies J., Davies M.C., Dawkes A.C., Edwards J.C., Roberts C.J., Sefton J., Tendler S.J.B., Williams P.M. (1997) Detection of antigen-antibody binding events with the atomic force microscope. Biochemistry, 36(24), 7457–7463. CrossRef Scholar google search
Bukharina N.S., Ivanov Yu.D., Pleshakova T.O., Frantsuzov P.A., Andreeva E.Yu., Kaysheva A.L., Izotov A.A., Pavlova T.I., Ziborov V.S., Radko S.P., Archakov A.I. (2014) Atomic force microscopy fishing of gp120 on immobilized aptamers and its mass spectrometry identification. Biomeditsinskaya Khimiya, 61(3), 363–372. CrossRef Scholar google search
Pleshakova T.O., Kaysheva A.L., Bayzyanova J.M., Anashkina A.S., Uchaikin V.F., Ziborov V.S., Konev V.A., Archakov A.I., Ivanov Y.D. (2018) The detection of hepatitis C virus core antigen using AFM chips with immobolized aptamers. J. Virol. Methods, 251, 99–105. CrossRef Scholar google search
Pleshakova T., Kaysheva A., Shumov I., Ziborov V., Bayzyanova J., Konev V., Uchaikin V., Archakov A., Ivanov Y. (2019) Detection of hepatitis C virus core protein in serum using aptamer-functionalized AFM chips. Micromachines, 10(2), 129. CrossRef Scholar google search
Islam M.S., Lee H.G., Choo J., Song J.M., Kang S.H. (2010) High sensitive detection of C-reactive protein by total internal reflection fluorescence microscopy on rapidly making nanoarray protein chip. Talanta, 81(4–5), 1402–1408. CrossRef Scholar google search
Lee S., Cho N.-P., Kim J.D., Jung H., Kang S.H. (2009) An ultra-sensitive nanoarray chip based on single-molecule sandwich immunoassay and TIRFM for protein detection in biologic fluids. Analyst, 134(5), 933–938. CrossRef Scholar google search
Zhang B., Xu G., Evans J.S. (1999) A kinetic molecular model of the reversible unfolding and refolding of titin under force extension. Biophys. J., 77(3), 1306–1315. CrossRef Scholar google search
Choi H.S., Huh J., Jo W.H. (2003) Similarity of force-induced unfolding of apomyoglobin to its chemical-induced unfolding: An atomistic molecular dynamics simulation approach. Biophys. J., 85(3), 1492–1502. CrossRef Scholar google search
