Localizing Chemical Groups while Imaging Single Native Proteins by High-Resolution Atomic Force Microscopy
Abstract

Simultaneous high-resolution imaging and localization of chemical interaction sites on single native proteins is a pertinent biophysical, biochemical, and nanotechnological challenge. Such structural mapping and characterization of binding sites is of importance in understanding how proteins interact with their environment and in manipulating such interactions in a plethora of biotechnological applications. Thus far, this challenge remains to be tackled. Here, we introduce force–distance curve-based atomic force microscopy (FD-based AFM) for the high-resolution imaging of SAS-6, a protein that self-assembles into cartwheel-like structures. Using functionalized AFM tips bearing Ni2+-N-nitrilotriacetate groups, we locate specific interaction sites on SAS-6 at nanometer resolution and quantify the binding strength of the Ni2+-NTA groups to histidine residues. The FD-based AFM approach can readily be applied to image any other native protein and to locate and structurally map histidine residues. Moreover, the surface chemistry used to functionalize the AFM tip can be modified to map other chemical interaction sites.
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- Daniel J. Müller, Andra C. Dumitru, Cristina Lo Giudice, Hermann E. Gaub, Peter Hinterdorfer, Gerhard Hummer, James J. De Yoreo, Yves F. Dufrêne, David Alsteens. Atomic Force Microscopy-Based Force Spectroscopy and Multiparametric Imaging of Biomolecular and Cellular Systems. Chemical Reviews 2021, 121 (19) , 11701-11725. https://doi.org/10.1021/acs.chemrev.0c00617
- Jing Hu, Mingyan Gao, Ying Wang, Mengnan Liu, Jianfei Wang, Jiani Li, Zhengxun Song, Yujuan Chen, Zuobin Wang. Imaging the Substructures of Individual IgE Antibodies with Atomic Force Microscopy. Langmuir 2019, 35 (46) , 14896-14901. https://doi.org/10.1021/acs.langmuir.9b02631
- Estefania Mulvihill, Moritz Pfreundschuh, Johannes Thoma, Noah Ritzmann, Daniel J. Müller. High-Resolution Imaging of Maltoporin LamB while Quantifying the Free-Energy Landscape and Asymmetry of Sugar Binding. Nano Letters 2019, 19 (9) , 6442-6453. https://doi.org/10.1021/acs.nanolett.9b02674
- Wout Frederickx, Susana Rocha, Yasuhiko Fujita, Koen Kennes, Herlinde De Keersmaecker, Steven De Feyter, Hiroshi Uji-i, and Willem Vanderlinden . Orthogonal Probing of Single-Molecule Heterogeneity by Correlative Fluorescence and Force Microscopy. ACS Nano 2018, 12 (1) , 168-177. https://doi.org/10.1021/acsnano.7b05405
- Pawel R. Laskowski, Moritz Pfreundschuh, Mirko Stauffer, Zöhre Ucurum, Dimitrios Fotiadis, and Daniel J. Müller . High-Resolution Imaging and Multiparametric Characterization of Native Membranes by Combining Confocal Microscopy and an Atomic Force Microscopy-Based Toolbox. ACS Nano 2017, 11 (8) , 8292-8301. https://doi.org/10.1021/acsnano.7b03456
- David Alsteens, Daniel J. Müller, and Yves F. Dufrêne . Multiparametric Atomic Force Microscopy Imaging of Biomolecular and Cellular Systems. Accounts of Chemical Research 2017, 50 (4) , 924-931. https://doi.org/10.1021/acs.accounts.6b00638
- X Chang, S Hallais, S Roux, K Danas. Model reduction techniques for quantitative nano-mechanical AFM mode. Measurement Science and Technology 2021, 32 (7) , 075406. https://doi.org/10.1088/1361-6501/abf023
- Mi Li, Ning Xi, Lianqing Liu. Peak force tapping atomic force microscopy for advancing cell and molecular biology. Nanoscale 2021, 13 (18) , 8358-8375. https://doi.org/10.1039/D1NR01303C
- Ioannis Vakonakis. The centriolar cartwheel structure: symmetric, stacked, and polarized. Current Opinion in Structural Biology 2021, 66 , 1-7. https://doi.org/10.1016/j.sbi.2020.08.007
- Julia M.C. Busch, Minos-Timotheos Matsoukas, Maria Musgaard, Georgios A. Spyroulias, Philip C. Biggin, Ioannis Vakonakis. Identification of compounds that bind the centriolar protein SAS-6 and inhibit its oligomerization. Journal of Biological Chemistry 2020, 295 (52) , 17922-17934. https://doi.org/10.1074/jbc.RA120.014780
- Michael G. Ruppert, Ben S. Routley, Andrew J. Fleming, Yuen K. Yong, Georg E. Fantner. Model-based Q Factor Control for Photothermally Excited Microcantilevers. 2019,,, 1-6. https://doi.org/10.1109/MARSS.2019.8860969
- Adrian Nievergelt, Charlène Brillard, Haig Eskandarian, John McKinney, Georg Fantner. Photothermal Off-Resonance Tapping for Rapid and Gentle Atomic Force Imaging of Live Cells. International Journal of Molecular Sciences 2018, 19 (10) , 2984. https://doi.org/10.3390/ijms19102984
- Adrian P. Nievergelt, Niccolò Banterle, Santiago H. Andany, Pierre Gönczy, Georg E. Fantner. High-speed photothermal off-resonance atomic force microscopy reveals assembly routes of centriolar scaffold protein SAS-6. Nature Nanotechnology 2018, 13 (8) , 696-701. https://doi.org/10.1038/s41565-018-0149-4
- Anisha N. Patel, Christine Kranz. (Multi)functional Atomic Force Microscopy Imaging. Annual Review of Analytical Chemistry 2018, 11 (1) , 329-350. https://doi.org/10.1146/annurev-anchem-061417-125716
- Wanxin Sun. Principles of Atomic Force Microscopy. 2018,,, 1-28. https://doi.org/10.1007/978-981-13-1510-7_1
- Hao Sun, Ming Ye, Wanxin Sun. High Resolution AFM and Its Applications. 2018,,, 179-235. https://doi.org/10.1007/978-981-13-1510-7_10
- Alper D. Ozkan, Ahmet E. Topal, Fatma B. Dikecoglu, Mustafa O. Guler, Aykutlu Dana, Ayse B. Tekinay. Probe microscopy methods and applications in imaging of biological materials. Seminars in Cell & Developmental Biology 2018, 73 , 153-164. https://doi.org/10.1016/j.semcdb.2017.08.018
- Disha Mohan Bangalore, Ingrid Tessmer, . Unique insight into protein-DNA interactions from single molecule atomic force microscopy. AIMS Biophysics 2018, 5 (3) , 194-216. https://doi.org/10.3934/biophy.2018.3.194
- Byung Ho Lee, Sangjae Seo, Min Hyeok Kim, Youngjin Kim, Soojin Jo, Moon-ki Choi, Hoomin Lee, Jae Boong Choi, Moon Ki Kim, . Normal mode-guided transition pathway generation in proteins. PLOS ONE 2017, 12 (10) , e0185658. https://doi.org/10.1371/journal.pone.0185658
- David Alsteens, Hermann E. Gaub, Richard Newton, Moritz Pfreundschuh, Christoph Gerber, Daniel J. Müller. Atomic force microscopy-based characterization and design of biointerfaces. Nature Reviews Materials 2017, 2 (5) https://doi.org/10.1038/natrevmats.2017.8
- Jodie Ford, Phillip Stansfeld, Ioannis Vakonakis. Coupling Form and Function: How the Oligomerisation Symmetry of the SAS-6 Protein Contributes to the Architecture of Centriole Organelles. Symmetry 2017, 9 (5) , 74. https://doi.org/10.3390/sym9050074
- Wolfgang Ott, Markus A. Jobst, Constantin Schoeler, Hermann E. Gaub, Michael A. Nash. Single-molecule force spectroscopy on polyproteins and receptor–ligand complexes: The current toolbox. Journal of Structural Biology 2017, 197 (1) , 3-12. https://doi.org/10.1016/j.jsb.2016.02.011
- Nan Wang, Miaomiao Zhang, Xuejuan Chen, Xingxing Ma, Chen Li, Zhe Zhang, Jilin Tang. Mapping the interaction sites of Mucin 1 and DNA aptamer by atomic force microscopy. The Analyst 2017, 142 (20) , 3800-3804. https://doi.org/10.1039/C7AN01119A
- Hagen Söngen, Martin Nalbach, Holger Adam, Angelika Kühnle. Three-dimensional atomic force microscopy mapping at the solid-liquid interface with fast and flexible data acquisition. Review of Scientific Instruments 2016, 87 (6) , 063704. https://doi.org/10.1063/1.4952954
- Chrystal R. Quisenberry, Arshan Nazempour, Bernard J. Van Wie, Nehal I. Abu-Lail. Evaluation of β1-integrin expression on chondrogenically differentiating human adipose-derived stem cells using atomic force microscopy. Biointerphases 2016, 11 (2) , 021005. https://doi.org/10.1116/1.4947049
- David Alsteens. Étude des récepteurs membranaires par microscopie à force atomique. médecine/sciences 2016, 32 (5) , 433-435. https://doi.org/10.1051/medsci/20163205002
- Manuel Hilbert, Akira Noga, Daniel Frey, Virginie Hamel, Paul Guichard, Sebastian H. W. Kraatz, Moritz Pfreundschuh, Sarah Hosner, Isabelle Flückiger, Rolf Jaussi, Mara M. Wieser, Katherine M. Thieltges, Xavier Deupi, Daniel J. Müller, Richard A. Kammerer, Pierre Gönczy, Masafumi Hirono, Michel O. Steinmetz. SAS-6 engineering reveals interdependence between cartwheel and microtubules in determining centriole architecture. Nature Cell Biology 2016, 18 (4) , 393-403. https://doi.org/10.1038/ncb3329
- Nehal I Abu-Lail. Expression of N-Cadherins on Chondrogenically Differentiating Human Adipose Derived Stem Cells Using Single-Molecule Force Spectroscopy. Journal of Nanomedicine Research 2016, 3 (1) https://doi.org/10.15406/jnmr.2016.03.00045
- Alma P. Perrino, Ricardo Garcia. How soft is a single protein? The stress–strain curve of antibody pentamers with 5 pN and 50 pm resolutions. Nanoscale 2016, 8 (17) , 9151-9158. https://doi.org/10.1039/C5NR07957H
- Moritz Pfreundschuh, David Alsteens, Ralph Wieneke, Cheng Zhang, Shaun R. Coughlin, Robert Tampé, Brian K. Kobilka, Daniel J. Müller. Identifying and quantifying two ligand-binding sites while imaging native human membrane receptors by AFM. Nature Communications 2015, 6 (1) https://doi.org/10.1038/ncomms9857
- David Alsteens, Moritz Pfreundschuh, Cheng Zhang, Patrizia M Spoerri, Shaun R Coughlin, Brian K Kobilka, Daniel J Müller. Imaging G protein–coupled receptors while quantifying their ligand-binding free-energy landscape. Nature Methods 2015, 12 (9) , 845-851. https://doi.org/10.1038/nmeth.3479
- Mi Li, Lianqing Liu, Ning Xi, Yuechao Wang. Biological Applications of a Nanomanipulator Based on AFM: In situ visualization and quantification of cellular behaviors at the single-molecule level.. IEEE Nanotechnology Magazine 2015, 9 (3) , 25-35. https://doi.org/10.1109/MNANO.2015.2441110
- Congzhou Wang, Christopher J. Ehrhardt, Vamsi K. Yadavalli. Single cell profiling of surface carbohydrates on Bacillus cereus. Journal of The Royal Society Interface 2015, 12 (103) , 20141109. https://doi.org/10.1098/rsif.2014.1109
- Yuping Shan, Hongda Wang. The structure and function of cell membranes examined by atomic force microscopy and single-molecule force spectroscopy. Chemical Society Reviews 2015, 44 (11) , 3617-3638. https://doi.org/10.1039/C4CS00508B
- Christian Marlière, Samia Dhahri. An in vivo study of electrical charge distribution on the bacterial cell wall by atomic force microscopy in vibrating force mode. Nanoscale 2015, 7 (19) , 8843-8857. https://doi.org/10.1039/C5NR00968E
- Shuai Zhang, Hüsnü Aslan, Flemming Besenbacher, Mingdong Dong. Quantitative biomolecular imaging by dynamic nanomechanical mapping. Chem. Soc. Rev. 2014, 43 (21) , 7412-7429. https://doi.org/10.1039/C4CS00176A



