Noncontact Atomic Force Microscopy for Studying Biomolecules in Liquids

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Abstract

Noncontact atomic force microscopy, a type of scanning probe microscopy, has been actively used in the last two decades to study hydrated biomolecules. Analysis of modern literature shows that noncontact atomic force microscopy is a very promising method for studying adsorbed biomacromolecules and biomacromolecular complexes at the membrane interface or surfaces. This mini-review describes the foundations of this method, its application to biomolecules, discusses the requirements for the method and the possibility of its extension through additional processing of the obtained experimental data using theoretical analysis, molecular modeling or machine learning.

About the authors

T. Mamedov

Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences

Pushchino, Russia

A. Shvirst

Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences

Pushchino, Russia

M. V Fedotova

G.A. Krestov Institute of Solution Chemistry, Russian Academy of Sciences

Pushchino, Russia

G. N Chuev

Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences

Email: genchuev@rambler.ru
Pushchino, Russia

References

  1. Binnig G. and Rohrer H. Scanning tunneling microscopy. Helvetica Phys. Acta, 55, 726–735 (1982).
  2. Binnig G., Quate C. F., and Gerber C. Atomic force microscope. Phys. Rev. Lett., 56 (9), 930–933 (1986). doi: 10.1103/PhysRevLett.56.930
  3. Garcia R., Amplitude modulation atomic force microscopy (Wiley‐VCH Verlag GmbH & Co., 2010). doi: 10.1002/9783527632183
  4. Morris V. J., Kirby A. R., and Gunning A. P. Atomic force microscopy for biologists (Imperial College Press, 2009).
  5. Melitz W., Shen J., Kummel A. C., and Lee S. Kelvin probe force microscopy and its application. Surface Sci. Rep., 66 (1), 1–27 (2011). doi: 10.1016/j.surfrep.2010.10.001
  6. Chen X., Li B., Liao Z., Li J., Li X., Yin J., and Guo W. Principles and applications of liquid-environment atomic force microscopy. Adv. Mater. Interfaces, 9 (35), 2201864 (2022). doi: 10.1002/admi.202201864
  7. Baro A. M. and Reifenberger R. G. Atomic force microscopy in liquid (Wiley-VCH Verlag GmbH & Co., 2012). doi: 10.1002/9783527649808
  8. Kominami H., Kobayashi K., and Yamada H. Molecularscale visualization and surface charge density measurement of Z-DNA in aqueous solution. Sci. Rep., 9, 6851 (2019). doi: 10.1038/s41598-019-42394-5
  9. Kuchuk K. and Sivan U. Hydration structure of a single DNA molecule revealed by frequency-modulation atomic force microscopy. Nano Lett., 18 (4), 2733–2737 (2018). doi: 10.1021/acs.nanolett.8b00854
  10. Heenan P. R. and Perkins T. T. Imaging DNA Equilibrated onto mica in liquid using biochemically relevant deposition conditions. ACS Nano, 13 (4), 4220–4229 (2019). doi: 10.1021/acsnano.8b09234
  11. Sotres J. and Baro A. M. AFM imaging and analysis of electrostatic double layer forces on single DNA molecules. Biophys. J., 98 (9), 1995–2004 (2010). doi: 10.1016/j.bpj.2009.12.4330
  12. Sumikama T., Foster A. S., and Fukuma T. Computed atomic force microscopy images of chromosomes by calculating forces with oscillating probes. J. Phys. Chem. C., 124 (3), 2213–2218 (2020). doi: 10.1021/acs.jpcc.9b10263
  13. Ido S., Kobayashi K., Oyabu N., Hirata Y., Matsushige K., and Yamada H. Structured water molecules on membrane proteins resolved by atomic force microscopy. Nano Lett., 22 (6), 2391–2397 (2022). doi: 10.1021/acs.nanolett.2c00029
  14. Philippsen A., Im W., Engel A., Schirmer T., Roux B., and Muller D. J. Imaging the electrostatic potential of transmembrane channels: atomic probe microscopy of OmpF porin. Biophys. J., 82 (3), 1667–1676 (2003). doi: 10.1016/S0006-3495(02)75517-3
  15. MacKerell A. D., Bashford D., Bellott M., Dunbrack R. L., Evanseck J. D., Field M. J., Fischer S., Gao J., Guo H., Ha S., Joseph-McCarthy D., Kuchnir L., Kuczera K., Lau F. T., Mattos C., Michnick S., Ngo T., Nguyen D. T., Prodhom B., Reiher W. E., Roux B., Schlenkrich M., Smith J. C., Stote R., Straub J., Watanabe M., Wiorkiewicz-Kuczera J., Yin D., and Karplus M. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B., 102 (18), 3586–3616 (1998). doi: 10.1021/jp973084f
  16. Hernando-Perez M., Cartagena-Rivera A. X., Lošdorfer Božič A., Carrillo P. J., San Martin C., Mateu M. G., Raman A., Podgornik R., and Pablo P. Quantitative nanoscale electrostatics of viruses. J. Nanoscale, 7 (41), 17289–17298 (2015). doi: 10.1039/C5NR04274G
  17. Heldt C. L., Areo O., Joshi P. U., Mi X., Ivanova Y., and Berrill A. Empty and full AAV capsid charge and hydrophobicity differences measured with single-particle AFM. Langmuir, 39 (16), 5641–5648 (2023). doi: 10.1021/acs.langmuir.2c02643
  18. Дерягин Б. В., Чураев Н. В., и Муллер В. М. Поверхностные силы (Наука, М., 1985).
  19. van Oss C. J. The extended DLVO theory. Interface Sci. Technol., 16, 31–48 (2008). doi: 10.1016/S1573-4285(08)00203-2
  20. Sharma P. K. and Hanumantha R. K. Adhesion of paenibacillus polymyxa on chalcopyrite and pyrite: surface thermodynamics and extended DLVO theory. Colloids and Surfaces B: Biointerfaces, 29 (1), 21–38 (2003). doi: 10.1016/S0927-7765(02)00180-7
  21. Liang Y., Hilal N., Langston P., and Starov V. Interaction forces between colloidal particles in liquid: theory and experiment. J. Adv. Colloid Interface Sci., 134–135, 151–166 (2007). doi: 10.1016/j.cis.2007.04.003
  22. Klaassen A., Liu F., Mugele F., and Siretanu I. Correlation between electrostatic and hydration forces on silica and gibbsite surfaces: an atomic force microscopy study. Langmuir, 38 (3), 914–926 (2022). doi: 10.1021/acs.langmuir.1c02077
  23. Li L., Eppell S., and Zypman F. Method to quantify nanoscale surface charge in liquid with atomic force microscopy. Langmuir, 36 (15), 4123–4134 (2020). doi: 10.1021/acs.langmuir.9b03602
  24. Li L., Steinmetz N., Eppell S., and Zypman F. Charge calibration standard for atomic force microscope tips in liquids. Langmuir, 36 (45), 13621–13632 (2020). doi: 10.1021/acs.langmuir.0c02455
  25. Blum L. J. Invariant Expansion for two‐body correlations: thermodynamic functions, scattering, and the Ornstein–Zernike equation. J. Chem. Phys., 56, 303–310 (1972). doi: 10.1063/1.1676864
  26. Ikeguchi M. and Doi J. Direct numerical solution of the Ornstein–Zernike integral equation and spatial distribution of water around hydrophobic molecules. J. Chem. Phys., 103 (12), 5011–5017 (1995). doi: 10.1063/1.470587
  27. Ishizuka R. and Yoshida N. Extended molecular Ornstein−Zernike integral equation for fully anisotropic solute molecules: formulation in a rectangular coordinate system. J. Chem. Phys., 139 (8), 084119 (2013). doi: 10.1063/1.4819211
  28. Fedotova M. V. and Kruchinin S. E. Ion-binding of glycine zwitterion with inorganic ions in biologically relevant aqueous electrolyte solutions. Biophys. Chem., 190–191, 25–31 (2014). doi: 10.1016/j.bpc.2014.04.001
  29. Dmitrieva O. A. and Fedotova M. V. Characterization of selective binding of biologically relevant inorganic ions with the proline zwitterion by 3D-RISM theory. New J. Chem., 39 (11), 8594–8601 (2015). doi: 10.1039/C5NJ01559F
  30. Fedotova M. V. and Dmitrieva O. A. Proline hydration at low temperatures: its role in the protection of cell from freeze-induced stress. Amino Acids, 48 (7), 1685–1694 (2016). doi: 10.1007/s00726-016-2232-1
  31. Fedotova M. V., Kruchinin S. E., and Chuev G. N. Hydration structure of osmolyte TMAO: concentration/pressure-induced response. New J. Chem., 41 (3), 1219–1228 (2017). doi: 10.1039/C6NJ03296F
  32. Fedotova M. V. and Kruchinin S. E. Hydration and ion-binding of glycine betaine: How they may be involved into protection of proteins under abiotic stresses. J. Mol. Liq., 244, 489–498 (2017). doi: 10.1016/j.molliq.2017.08.117
  33. Fedotova M. V. Compatible osmolytes – bioprotectants: Is there a common link between their hydration and their protective action under abiotic stresses? J. Mol. Liq., 292, 111339 (2019). doi: 10.1016/j.molliq.2019.111339
  34. Fedotova M. V., Kruchinin S. E., and Chuev G. N. Hydration features of the neurotransmitter acetylcholine. J. Mol. Liq., 304, 112757 (2020). doi: 10.1016/j.molliq.2020.112757
  35. Kumawat N., Tucs A., Bera S., Chuev G. N., Valiev M., Fedotova M. V., Kruchinin S. E., Tsuda K., Sljoka A., and Chakraborty A. Site density functional theory and structural bioinformatics analysis of the SARS-CoV spike protein and hACE2 complex. Molecules, 27 (3), 799 (2022). doi: 10.3390/molecules27030799
  36. Kruchinin S. E., Kislinskaya E. E., Chuev G. N., and Fedotova M. V. Protein 3D hydration: a case of bovine pancreatic trypsin inhibitor. Int. J. Mol. Sci., 23 (23), 14785 (2022). doi: 10.3390/ijms232314785
  37. Kruchinin S. E., Chuev G. N., and Fedotova M. V. Molecular insight on hydration of protein tyrosine phosphatase 1B and its complexes with ligands. J. Mol. Liq., 384, 122281 (2023). doi: 10.1016/j.molliq.2023.122281
  38. Кручинин С. Е., Федотова М. В., Кислинская Е. Е. и Чуев Г. Н. In silico исследование сольватационных эффектов в растворах биомолекул: возможности подхода, основанного на 3D-распределении атомной плотности растворителя. Биофизика, 68 (5), 837–849 (2023). doi: 10.31857/S0006302923050010
  39. Chandler D. and Andersen H. C. Optimized cluster expansions for classical fluids. II. Theory of molecular liquids. J. Chem. Phys., 57 (5), 1930 (1972). doi: 10.1063/1.1678513
  40. Hirata F., Rossky P. J., and Pettitt B. M. The interionic potential of mean force in a molecular polar solvent from an extended RISM equation. J. Chem. Phys., 78 (6), 4133–4144 (1983). doi: 10.1063/1.445090
  41. Perkyns J. and Pettitt B. M. A site–site theory for finite concentration saline solutions. J. Chem. Phys., 97 (10), 7656–7666 (1992). doi: 10.1063/1.463485
  42. Harada M. and Tsukada M. Tip-sample interaction force mediated by water molecules for AFM in water: Three-dimensional reference interaction site model theory. J. Physical Review B., 82 (3), 035414 (2010). doi: 10.1103/PhysRevB.82.035414
  43. Watkins M. and Reischl B. A simple approximation for forces exerted on an AFM tip in liquid. J. Chem. Phys., 138 (15), 154703 (2013). doi: 10.1063/1.4800770
  44. Miyazawa K., Kobayashi N., Watkins M., Shluger A., Amano K., and Fukuma T. A relationship between three-dimensional surface hydration structures and force distribution measured by atomic force microscopy. J. Nanoscale, 8, 7334–7342 (2016). doi: 10.1039/C5NR08092D
  45. Trabuco L. G., Villa E., Mitra K., Frank J., and Schulten K. Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. J. Structure, 16 (5), 673–683 (2008). doi: 10.1016/j.str.2008.03.005
  46. Fuchigami S. and Takada S. Inferring conformational state of myosin motor in an atomic force microscopy image via flexible fitting molecular simulations. J. Frontiers in Molecular Biosciences, 9, 882989 (2022). doi: 10.3389/fmolb.2022.882989
  47. LeCun Y., Boser B., Denker J. S., Henderson D., Howard R. E., Hubbard W., and Jackel L. D. Backpropagation applied to handwritten zip code recognition. J. Neural Computation, 1 (4), 541–551 (1989). doi: 10.1162/neco.1989.1.4.541
  48. Oinonen N., Xu C., Alldritt B., Canova F. F., Urtev F., Cai S., Krejci O., Kannala J., Liljeroth P., and Foster A. S. Correction to electrostatic discovery atomic force microscopy. J. ACS Nano, 16, 89 (2022). doi: 10.1021/acsnano.2c08130
  49. Fukuma T., Ueda Y., Yoshioka Sh., and Asakawa H. Atomic-scale distribution of water molecules at the micawater interface visualized by three-dimensional scanning force microscopy. Phys. Rev. Lett., 104 (1), 016101 (2010). doi: 10.1103/PhysRevLett.104.016101

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