Atomic force microscopy and force spectroscopy

Our lab is equipped with an atomic force microscopy (AFM) instrument which we use in various aspects of virus research and beyond. Our current applications include probing the interaction between virus particles and their cell-surface receptors and looking at morphological and mechanical changes occurring in cells upon viral infection.

AFM is a powerful and multipurpose imaging technique. The working principle of AFM is rather simple. It is based on “feeling” the surface using a very sharp cantilever tip. Deflection of the cantilever is directly related to the magnitude of the force applied to it (Figure A). This principle can be used in the context of (i) acquiring topographic images of surface-immobilized objects (including viruses or biomolecules) with atomic resolution, (ii) probing biomolecular forces, and (iii) determining the mechanical properties of the scanned material (e.g., a cell).

Left: visulazation of the concept of atomic force microscopy on a cell. Top right: Height image of a living cell. Bottom right: Young's modulus image of a living cell.
Figure A: Schematic representation of AFM imaging of cell operating in QI™ mode to simultaneously acquire height and elastic modulus images.

In our research, we are interested in understanding how the interactions of virus particles are modulated at the cell surface. In this context, AFM-based force spectroscopy is a great tool as it makes it possible to probe, on a single molecule level, the interaction between viral proteins and cell-surface receptors by the so-called force-distance curve (Figure B) [1]. It helps us quantify the association (kon) and dissociation (koff) rate constants of the monovalent interaction by probing the interaction as a function of contact time and pulling speed, respectively. Moreover, we can gain information on the mechanical stability of the bond (i.e., its resistance against an applied force), and in some cases determine the number of contacts or bonds formed, if the interaction is multivalent. Force spectroscopy is carried out by covalently immobilizing a viral particle or a viral protein on the AFM tip through a linker and probing its interaction with surface-immobilized biomolecules, e.g., a cell-surface mimic or the surface of a live cell. In a force spectroscopy experiment, the tip is first approached to the surface to allow for the formation of the bond and then retracted. The force needed to overcome the molecular interaction is then measured. (Figure B, inset).

Figure B: Schematic representation of AFM force spectroscopy to acquire force-distance curves to measure a range of binding properties of biomolecular interaction.

In addition to this, we use AFM-based force spectroscopy, together with imaging, to look at morphological or mechanical changes occurring within the cell upon infection or to characterize the cellular glycocalyx, for example when studying glycocalyx degradation.

Finally, AFM imaging is powerful in the context of characterizing lipid membranes. It can be used to look at the topography of a (supported) membrane, e.g., to ascertain the formation of microdomains [2] or to reveal the organization of membrane-binding proteins at lipid interfaces (Figure C). This is well-aligned with our research interests and the ones of our collaborators.

Figure C: AFM imaging in PeakForce Tapping mode allows the characterization of various organizations of membrane-binding proteins on supported lipid bilayers.

Key References

1. Site-specific sulfations regulate the physicochemical properties of papillomavirus–heparan sulfate interactions for entry
F. Bano, L. Soria-Martinez, D. van Bodegraven, K. Throsteinsson, A. M. Brown, I. Fels, N. L. Synder, M. Bally, M. Schelhaas
Sci. Adv., 2024, 10, eado8540.
2. Regulatory Mechanisms of the Mucin-Like Region on Herpes Simplex Virus during Cellular Attachment
M. Delguste, N. Peerboom, G. LeBrun, E. Trybala, S. Olofsson, T. Bergström, D. Alsteens, M. Bally
ACS Chem. Biol., 2019, 14(3), 534-542.
3. Norovirus GII.4 virus-like particles recognize galactosylceramides in microdomains of planar supported lipid bilayers
M. Bally, G. Rydell, R. Zahn, W. Nasir, M. Breimer, L. Svensson, F. Höök, G. Larson
Angewandte Chemie Int. Ed., 2012, 51(48) 12020-12024.