Comparative Evaluation of Interaction Force Characteristics for the Lipopolysaccharide of Yersinia pseudotuberculosis and Antibodies by Optical Trapping and Atomic Force Microscopy

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Abstract

Optical tweezers and atomic force microscopy were used for comparative evaluation of the interaction force between the lipopolysaccharide of Yersinia pseudotuberculosis and monoclonal antibodies. This paper discusses the peculiarities of two methods which allow determining significant differences in the values of the measured force required to rupture the interaction of probe sensitized by lipopolysaccharide (polystyrene microsphere for optical tweezers and silicon nitride cantilever for atomic force microscopy) with substrate (glass and mica, respectively) covered with monoclonal antibodies. In atomic force microscopy, the cantilever slides along the substrate for some time after the piezo stage is brought to a stop, causing changes in the spatial structure of sensitins and, therefore, redistribution of multiple bonds between the lipopolysaccharide agglomerate and antibodies. No significant displacement of the microsphere along the substrate occurs when an optical tweezers setup is used, and, unlike atomic force microscopy, the breaking of a complex bond between lipopolysaccharide and complementary antibodies is recorded in the form of a single and short-term (1–2 ms) leap of the photodetector signal employing optical tweezers. The recorded values of the force required to rupture the interaction measured by both methods are relative and vary depending on the chosen experimental conditions. It is shown that the non-specific component of the force needed to break the interaction measured by atomic force microscopy is significantly higher than that determined with optical tweezers.

About the authors

A. A Byvalov

Vyatka State University; nstitute of Physiology, Кomi Science Centre of the Ural Branch of the Russian Academy of Sciences

Email: byvalov@nextmail.ru
Kirov, 610000 Russia; Syktyvkar, 167982 Russia

V. S Belozerov

Vyatka State University; nstitute of Physiology, Кomi Science Centre of the Ural Branch of the Russian Academy of Sciences

Kirov, 610000 Russia; Syktyvkar, 167982 Russia

I. V Konyshev

Vyatka State University; nstitute of Physiology, Кomi Science Centre of the Ural Branch of the Russian Academy of Sciences

Kirov, 610000 Russia; Syktyvkar, 167982 Russia

B. A Ananchenko

Vyatka State University

Kirov, 610000 Russia

References

  1. Konyshev I., Byvalov A., Ananchenko B., Fakhrullin R., Danilushkina A., and Dudina L. Force interactions between Yersiniae lipopolysaccharides and monoclonal antibodies: An optical tweezers study. J. Biomech., 99, 109504 (2020). doi: 10.1016/j.jbiomech.2019.109504
  2. Ananchenko B., Belozerov V., Byvalov A., Konyshev I., Korzhavina A., and Dudina L. Evaluation of intermolecular forces between lipopolysaccharides and monoclonal antibodies using atomic force microscopy. Int. J. Biol. Macromol., 156, 841–850 (2020). doi: 10.1016/j.ijbiomac.2020.04.055
  3. Neuman K. C. and Nagy A. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods, 5 (6), 491–505 (2008). doi: 10.1038/nmeth.1218
  4. Zhang Q., Li S., Yang Y., Shan Y., and Wang H. Studying structure and functions of cell membranes by single molecule biophysical techniques. Biophys. Rep., 7 (5), 384–398 (2021). doi: 10.52601/bpr.2021.210018
  5. Skurnik M. Molecular genetics, biochemistry and biological role of Yersinia lipopolysaccharide. Adv. Exp. Med. Biol., 529, 187–197 (2003).
  6. Бывалов А. А., Кононенко В. Л. и Конышев И. В. Влияние О-боковых цепей липополисахарида на адгезивность Yersinia pseudotuberculosis к макрофагам J774, установленное методом оптической ловушки. Прикл. биохимия и микробиология, 53 (2), 234–243 (2017).
  7. Vashist S. K., Lam E., Hrapovic S., Male K. B., and Luong J. H. Immobilization of antibodies and enzymes on 3aminopropyltriethoxysilane-functionalized bioanalytical platforms for biosensors and diagnostics. Chem. Rev., 114 (21), 11083–11130 (2014). doi: 10.1021/cr5000943
  8. Ebner A., Wildling L., and Gruber H. J. Functionalization of AFM tips and supports for molecular recognition force spectroscopy and recognition imaging. Methods Mol. Biol., 1886, 117–151 (2019). doi: 10.1007/978-1-4939-8894-5_7
  9. Gleńska-Olender J., Sęk S., Dworecki K., and Kaca W. A total internal reflection ellipsometry and atomic force microscopy study of interactions between Proteus mirabilis lipopolysaccharides and antibodies. Eur. Biophys J., 44 (5), 301–307 (2015). doi: 10.1007/s00249-015-1022-0
  10. Rodríguez C. and Hardy E. Lipopolysaccharide aggregates in native agarose gels detected by reversible negative staining with imidazole and zinc salts. Anal. Biochem., 485, 72–80 (2015). doi: 10.1016/j.ab.2015.06.020
  11. Zhou Z. L., Tang B., Ngan A. H., Dong Z. N., and WuY. S. Hepatitis B surface antigen-antibody interactions studied by optical tweezers. IET Nanobiotechnol., 6 (1), 9– 15 (2012). doi: 10.1049/iet-nbt.2010.0023
  12. Witt H. and Janshoff A. Using force spectroscopy to probe coiled-coil assembly and membrane fusion. Methods Mol. Biol., 1860, 145–159 (2019). doi: 10.1007/978-1-4939-8760-3_8
  13. Dorobantu L. S. and Gray M. R. Application of atomic force microscopy in bacterial research. Scanning, 32 (2), 74–96 (2010). doi: 10.1002/sca.20177
  14. Rankl C., Kienberger F., Wildling L., Wruss J., Gruber H. J., Blaas D., and Hinterdorfer P. Multiple receptors involved in human rhinovirus attachment to live cells. Proc. Natl. Acad. Sci. USA, 105 (46), 17778–17783 (2008). doi: 10.1073/pnas.0806451105
  15. Бывалов А. А., Белозёров В. С., Ананченко Б. А. и Конышев И. В. Специфические и неспецифические взаимодействия липополисахарида Yersinia pseudotuberculosis с моноклональными антителами, охарактеризованные методом атомно-силовой микроскопии. Биофизика, 67 (6), 1056–1067 (2022). doi: 10.31857/S0006302922050023
  16. Бывалов А. А., Кононенко В. Л. и Конышев И. В. Исследование взаимодействия липополисахаридов Yersinia pseudotuberculosis и Yersinia pestis с мембраной макрофага J774 методом силовой спектроскопии с использованием оптического пинцета. Биол. мембраны, 35 (2), 115–130 (2018). doi: 10.7868/S0233475518020032
  17. Formosa-Dague C., Castelain M., Martin-Yken H., Dunker K., Dague E., and Sletmoen M. The role of glycans in bacterial adhesion to mucosal surfaces: how can single-molecule techniques advance our understanding? Microorganisms, 6 (2), 39 (2018). doi: 10.3390/microorganisms6020039
  18. Elmahdy M. M., Drechsler A., Gutsche C., Synytska A., Uhlmann P., Kremer F., and Stamm M. Forces between blank surfaces as measured by the colloidal probe technique and by optical tweezers--a comparison. Langmuir, 25 (22), 12894–12898 (2009). doi: 10.1021/la901804a
  19. Arnal L., Longo G., Stupar P., Castez M. F., Cattelan N., Salvarezza R. C., Yantorno O. M., Kasas S., and Vela M. E. Localization of adhesins on the surface of a pathogenic bacterial envelope through atomic force microscopy. Nanoscale, 7 (41), 17563–17572 (2015). doi: 10.1039/c5nr04644k
  20. Zhang H. and Liu K. K. Optical tweezers for single cells. J. R. Soc. Interface, 5 (24), 671–690 (2008). doi: 10.1098/rsif.2008.0052
  21. Haugstad K. E., Hadjialirezaei S., Stokke B. T., Brewer C. F., Gerken T. A., Burchell J., Picco G., and Sletmoen M. Interactions of mucins with the Tn or sialyl Tn cancer antigens including MUC1 are due to GalNAcGalNAc interactions. Glycobiology, 26 (12), 1338–1350 (2016). doi: 10.1093/glycob/cww065
  22. Haugstad K. E., Gerken T. A., Stokke B. T., Dam T. K., Brewer C. F., and Sletmoen M. Enhanced self-association of mucins possessing the T and Tn carbohydrate cancer antigens at the single-molecule level. Biomacromolecules, 13 (5), 1400–1409 (2012). doi: 10.1021/bm300135h
  23. Chaves R. C., Teulon J. M., Odorico M., Parot P., Chen S. W., and Pellequer J. L. Conformational dynamics of individual antibodies using computational docking and AFM. J. Mol. Recognit., 26 (11), 596–604 (2013). doi: 10.1002/jmr.2310
  24. Zhang Z., Orski S., Woys A. M., Yuan G., Zarraga I. E., Wagner N. J., and Liu Y. Adsorption of polysorbate 20 and proteins on hydrophobic polystyrene surfaces studied by neutron reflectometry. Colloids Surf. B. Biointerfaces, 168, 94–102 (2018). doi: 10.1016/j.colsurfb.2018.04.036
  25. Tsapikouni T. S. and Missirlis Y. F. Measuring the force of single protein molecule detachment from surfaces with AFM. Colloids Surf. B. Biointerfaces, 75 (1), 252–259 (2010). doi: 10.1016/j.colsurfb.2009.08.041

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