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Determination of protein–protein interactions at the single-molecule level using optical tweezers

Published online by Cambridge University Press:  10 August 2022

Wendy N. Sánchez Open the ORCID record for Wendy N. Sánchez [Opens in a new window] ,
Luka Robeson Open the ORCID record for Luka Robeson [Opens in a new window] ,
Valentina Carrasco Open the ORCID record for Valentina Carrasco [Opens in a new window] ,
Nataniel L. Figueroa Open the ORCID record for Nataniel L. Figueroa [Opens in a new window] ,
Francesca Burgos-Bravo Open the ORCID record for Francesca Burgos-Bravo [Opens in a new window] ,
Christian A. M. Wilson Open the ORCID record for Christian A. M. Wilson [Opens in a new window]  and
Nathalie Casanova-Morales Open the ORCID record for Nathalie Casanova-Morales [Opens in a new window]
Wendy N. Sánchez
Affiliation:
Biochemistry and Molecular Biology Department, Faculty of Chemistry and Pharmaceutical Sciences, Universidad de Chile, Santiago, Chile Department of Molecular Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, Faculty of Science and Engineering, University of Groningen, Groningen, The Netherlands
Luka Robeson
Affiliation:
Biochemistry and Molecular Biology Department, Faculty of Chemistry and Pharmaceutical Sciences, Universidad de Chile, Santiago, Chile
Valentina Carrasco
Affiliation:
Biochemistry and Molecular Biology Department, Faculty of Chemistry and Pharmaceutical Sciences, Universidad de Chile, Santiago, Chile
Nataniel L. Figueroa
Affiliation:
Johannes Gutenberg-Universität Mainz, 55128 Mainz, Germany Helmholtz-Institut Mainz, GSI Helmholtzzentrum für Schwerionenforschung, 55128 Mainz, Germany
Francesca Burgos-Bravo
Affiliation:
Institute for Quantitative Biosciences, University of California, Berkeley, CA 94720, USA
Christian A. M. Wilson*
Affiliation:
Biochemistry and Molecular Biology Department, Faculty of Chemistry and Pharmaceutical Sciences, Universidad de Chile, Santiago, Chile
Nathalie Casanova-Morales*
Affiliation:
Facultad de Artes Liberales, Universidad Adolfo Ibáñez, Santiago, Chile
*
Authors for correspondence: Christian A. M. Wilson, E-mail: [email protected]; Nathalie Casanova-Morales, E-mail: [email protected]
Authors for correspondence: Christian A. M. Wilson, E-mail: [email protected]; Nathalie Casanova-Morales, E-mail: [email protected]
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Abstract

Biomolecular interactions are at the base of all physical processes within living organisms; the study of these interactions has led to the development of a plethora of different methods. Among these, single-molecule (in singulo) experiments have become relevant in recent years because these studies can give insight into mechanisms and interactions that are hidden for ensemble-based (in multiplo) methods. The focus of this review is on optical tweezer (OT) experiments, which can be used to apply and measure mechanical forces in molecular systems. OTs are based on optical trapping, where a laser is used to exert a force on a dielectric bead; and optically trap the bead at a controllable position in all three dimensions. Different experimental approaches have been developed to study protein–protein interactions using OTs, such as: (1) refolding and unfolding in trans interaction where one protein is tethered between the beads and the other protein is in the solution; (2) constant force in cis interaction where each protein is bound to a bead, and the tension is suddenly increased. The interaction may break after some time, giving information about the lifetime of the binding at that tension. And (3) force ramp in cis interaction where each protein is attached to a bead and a ramp force is applied until the interaction breaks. With these experiments, parameters such as kinetic constants (koff, kon), affinity values (KD), energy to the transition state ΔG≠, distance to the transition state Δx≠ can be obtained. These parameters characterize the energy landscape of the interaction. Some parameters such as distance to the transition state can only be obtained from force spectroscopy experiments such as those described here.

Keywords

Protein-protein interactionoptical tweezersDudko-Hummer-Szabo modelforce spectroscopybinding parameters
Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 55 , 2022 , e8
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Akasaka, K, Kitahara, R and Kamatari, YO (2013) Exploring the folding energy landscape with pressure. Archives of Biochemistry and Biophysics 531, 110–115.CrossRefGoogle ScholarPubMed
Akiyoshi, B, Sarangapani, KK, Powers, AF, Nelson, CR, Reichow, SL, Arellano-Santoyo, H, Gonen, T, Ranish, JA, Asbury, CL, and Biggins, S (2010) Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468, 576–579.CrossRefGoogle ScholarPubMed
Allen, S, Chen, X, Davies, J, Davies, MC, Dawkes, AC, Edwards, JC, Roberts, CJ, Sefton, J, Tendler, SJB, and Williams, PM (1997) Detection of antigen–antibody binding events with the atomic force microscope. Biochemistry 36, 7457–7463.CrossRefGoogle ScholarPubMed
Alon, R, Hammer, DA and Springer, TA (1995) Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature 374, 539–542.CrossRefGoogle ScholarPubMed
Ananthakrishnan, R and Ehrlicher, A (2007) The forces behind cell movement. International Journal of Biological Sciences 3, 303–317.CrossRefGoogle ScholarPubMed
Ashkin, A (1970) Acceleration and trapping of particles by radiation pressure. Physical Review Letters 24, 156–159.CrossRefGoogle Scholar
Aubin-Tam, M-E, Olivares, AO, Sauer, RT, Baker, TA and Lang, MJ (2011) Single-molecule protein unfolding and translocation by an ATP-fueled proteolytic machine. Cell 145, 257–267.CrossRefGoogle ScholarPubMed
Avellaneda, MJ, Koers, EJ, Minde, DP, Sunderlikova, V and Tans, SJ (2020) Simultaneous sensing and imaging of individual biomolecular complexes enabled by modular DNA–protein coupling. Communications Chemistry 3, 20.CrossRefGoogle Scholar
Baez, M, Wilson, CAM, Ramírez-Sarmiento, CA, Guixé, V and Babul, J (2012) Expanded monomeric intermediate upon cold and heat unfolding of phosphofructokinase-2 from Escherichia coli. Biophysical Journal 103, 2187–2194.CrossRefGoogle ScholarPubMed
Bartels, FW, Baumgarth, B, Anselmetti, D, Ros, R and Becker, A (2003) Specific binding of the regulatory protein ExpG to promoter regions of the galactoglucan biosynthesis gene cluster of Sinorhizobium meliloti – a combined molecular biology and force spectroscopy investigation. Journal of Structural Biology 143, 145–152.CrossRefGoogle ScholarPubMed
Bartels, FW, McIntosh, M, Fuhrmann, A, Metzendorf, C, Plattner, P, Sewald, N, Anselmetti, D, Ros, R and Becker, A (2007) Effector-stimulated single molecule protein–DNA interactions of a quorum-sensing system in Sinorhizobium meliloti. Biophysical Journal 92, 4391–4400.CrossRefGoogle ScholarPubMed
Baumgarth, B, Bartels, FW, Anselmetti, D, Becker, A and Ros, R (2005) Detailed studies of the binding mechanism of the Sinorhizobium meliloti transcriptional activator ExpG to DNA. Microbiology 151, 259–268.CrossRefGoogle Scholar
Bell, GI (1978) Models for the specific adhesion of cells to cells. Science 200, 618–627.CrossRefGoogle ScholarPubMed
Björnham, O and Schedin, S (2009) Methods and estimations of uncertainties in single-molecule dynamic force spectroscopy. European Biophysics Journal 38, 911–922.CrossRefGoogle ScholarPubMed
Block, SM, Goldstein, LSB and Schnapp, BJ (1990) Bead movement by single kinesin molecules studied with optical tweezers. Nature 348, 348–352.CrossRefGoogle ScholarPubMed
Bouchiat, C, Wang, MD, Allemand, JF, Strick, T, Block, SM and Croquette, V (1999) Estimating the persistence length of a worm-like chain molecule from force–extension measurements. Biophysical Journal 76, 409–413.CrossRefGoogle ScholarPubMed
Brampton, C, Wahab, O, Batchelor, MR, Allen, S and Williams, PM (2011) Biomembrane force probe investigation of RNA dissociation. European Biophysics Journal 40, 247–257.CrossRefGoogle ScholarPubMed
Bullerjahn, JT, Sturm, S and Kroy, K (2014) Theory of rapid force spectroscopy. Nature Communications 5, 4463.CrossRefGoogle ScholarPubMed
Burgos-Bravo, F, Figueroa, NL, Casanova-Morales, N, Quest, AFG, Wilson, CAM and Leyton, L (2018) Single-molecule measurements of the effect of force on Thy-1/αvβ3-integrin interaction using nonpurified proteins. Molecular Biology of the Cell 29, 326–338. doi: 10.1091/mbc.E17-03-0133.CrossRefGoogle ScholarPubMed
Burgos-Bravo, F, Martínez-Meza, S, Quest, AFG, Wilson, CAM and Leyton, L (2020) Application of force to a syndecan-4 containing complex with Thy-1–αVβ3 integrin accelerates neurite retraction. Frontiers in Molecular Biosciences 7. doi: 10.3389/fmolb.2020.582257CrossRefGoogle ScholarPubMed
Bustamante, C (2008) In singulo biochemistry: when less is more. Annual Review of Biochemistry 77, 45–50.CrossRefGoogle ScholarPubMed
Bustamante, C and Smith, S (2007) Optical beam translation device and method utilizing a pivoting optical fiber. Patent No.: US 7,274,451 B2.Google Scholar
Bustamante, C, Bryant, Z and Smith, SB (2003) Ten years of tension: single-molecule DNA mechanics. Nature 421, 423–427.CrossRefGoogle ScholarPubMed
Bustamante, C, Chemla, YR, Forde, NR and Izhaky, D (2004) Mechanical processes in biochemistry. Annual Review of Biochemistry 73, 705–748.CrossRefGoogle ScholarPubMed
Bustamante, A, Sotelo-Campos, J, Guerra, DG, Wilson, CAM, Bustamante, C and Báez, M (2017) The energy cost of polypeptide knot formation and its folding consequences. Nature Communications 8, 1581.CrossRefGoogle ScholarPubMed
Cai, X-E and Yang, J (2003) The binding potential between the cholera toxin B-oligomer and Its receptor. Biochemistry 42, 4028–4034.CrossRefGoogle ScholarPubMed
Casanova-Morales, N, Alavi, Z, Wilson, CAM and Zocchi, G (2018 a) Identifying chaotropic and kosmotropic agents by nanorheology. Journal of Physical Chemistry B 122, 3754–3759. doi:10.1021/acs.jpcb.7b12782.CrossRefGoogle ScholarPubMed
Casanova-Morales, N, Quiroga-Roger, D, Alfaro-Valdés, HM, Alavi, Z, Lagos-Espinoza, MIA, Zocchi, G, Wilson, CAM (2018 b) Mechanical properties of BiP protein determined by nano-rheology. Protein Science 27, 1418–1426.CrossRefGoogle ScholarPubMed
Casanova-Morales, N, Figueroa, NL, Alfaro, K, Montenegro, F, Barrera, NP, Maze, JR, Wilson, CAM and Conejeros, P (2019) Structural characterization of the saxitoxin-targeting APTSTX1 aptamer using optical tweezers and molecular dynamics simulations. PLoS ONE 14, e0222468.CrossRefGoogle ScholarPubMed
Cecconi, C, Shank, EA, Dahlquist, FW, Marqusee, S and Bustamante, C (2008) Protein–DNA chimeras for single molecule mechanical folding studies with the optical tweezers. European Biophysics Journal 37, 729–738.CrossRefGoogle ScholarPubMed
Cecconi, C, Shank, EA, Marqusee, S and Bustamante, C (2011) DNA molecular handles for single-molecule protein-folding studies by optical tweezers, pp. 255–271.CrossRefGoogle Scholar
Chen, W, Lou, J and Zhu, C (2010) Forcing switch from short- to intermediate- and long-lived states of the αA domain generates LFA-1/ICAM-1 catch bonds. Journal of Biological Chemistry 285, 35967–35978.CrossRefGoogle ScholarPubMed
Chen, K, He, Y, Srinivasakannan, C, Li, S, Yin, S, Peng, J, Guo, S and Zhang, L (2019) Characterization of the interaction of rare earth elements with P507 in a microfluidic extraction system using spectroscopic analysis. Chemical Engineering Journal 356, 453–460.CrossRefGoogle Scholar
Claudia, D, Greenfield, D and Prentiss, M (2005) Dissociation of ligand–receptor complexes using magnetic tweezers. doi:10.1021/AC050057+.CrossRefGoogle Scholar
Comstock, MJ, Ha, T and Chemla, YR (2011) Ultrahigh-resolution optical trap with single-fluorophore sensitivity. Nature Methods 8, 335–340.CrossRefGoogle ScholarPubMed
Cossio, P, Hummer, G and Szabo, A (2016) Kinetic ductility and force-spike resistance of proteins from single-molecule force spectroscopy. Biophysical Journal 111, 832–840.CrossRefGoogle ScholarPubMed
Dague, E, Pons, V, Roland, A, Azaïs, JM, Arcucci, S, Lachaize, V, Velmont, S, Trevisiol, E, N’Guyen, D, Sénard, JM and Galés, C (2022) Atomic force microscopy-single-molecule force spectroscopy unveils GPCR cell surface architecture. Communications Biology 5, 1–13.CrossRefGoogle ScholarPubMed
Dammer, U, Popescu, O, Wagner, P, Anselmetti, D, Guntherodt, H and Misevic, G (1995) Binding strength between cell adhesion proteoglycans measured by atomic force microscopy. Science 267, 1173–1175.CrossRefGoogle ScholarPubMed
Danilowicz, C, Greenfield, D, Prentiss, M (2005) Dissociation of ligand–receptor complexes using magnetic tweezers. Analytical Chemistry 77, 3023–3028.CrossRefGoogle ScholarPubMed
de Lorenzo, S, Ribezzi-Crivellari, M, Arias-Gonzalez, JR, Smith, SB and Ritort, F (2015) A temperature-jump optical trap for single-molecule manipulation. Biophysical Journal 108, 2854–2864.CrossRefGoogle ScholarPubMed
Dembo, M, Torney, DC, Saxman, K and Hammer, D (1988) The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proceedings of the Royal Society of London. Series B. Biological Sciences 234, 55–83.Google ScholarPubMed
Desai, VP, Frank, F, Lee, A, Righini, M, Lancaster, L, Noller, HF, Tinoco, I and Bustamante, C (2019) Co-temporal force and fluorescence measurements reveal a ribosomal gear shift mechanism of translation regulation by structured mRNAs. Molecular Cell 75, 1007–1019.e5.CrossRefGoogle ScholarPubMed
Dudko, OK, Hummer, G and Szabo, A (2008) Theory, analysis, and interpretation of single-molecule force spectroscopy experiments. Proceedings of the National Academy of Sciences 105, 15755–15760.CrossRefGoogle ScholarPubMed
Eckel, R, Ros, R, Decker, B, Mattay, J and Anselmetti, D (2005 a) Supramolecular chemistry at the single-molecule level. Angewandte Chemie International Edition 44, 484–488.CrossRefGoogle ScholarPubMed
Eckel, R, Wilking, SD, Becker, A, Sewald, N, Ros, R and Anselmetti, D (2005 b) Single-molecule experiments in synthetic biology: an approach to the affinity ranking of DNA-binding peptides. Angewandte Chemie International Edition 44, 3921–3924.CrossRefGoogle Scholar
Evans, E. and Kinoshita, K. (2007). Using force to probe single-molecule receptor–cytoskeletal anchoring beneath the surface of a living cell, pp. 373–396.CrossRefGoogle Scholar
Evans, E, Ritchie, K and Merkel, R (1995) Sensitive force technique to probe molecular adhesion and structural linkages at biological interfaces. Biophysical Journal 68, 2580–2587.CrossRefGoogle ScholarPubMed
Evans, E, Leung, A, Heinrich, V and Zhu, C (2004) Mechanical switching and coupling between two dissociation pathways in a P-selectin adhesion bond. Proceedings of the National Academy of Sciences 101, 11281–11286.CrossRefGoogle Scholar
Evans, E, Heinrich, V, Leung, A and Kinoshita, K (2005) Nano- to microscale dynamics of P-selectin detachment from leukocyte interfaces. I. Membrane Separation from the Cytoskeleton. Biophysical Journal 88, 2288–2298.CrossRefGoogle ScholarPubMed
Evans, E, Kinoshita, K, Simon, S and Leung, A (2010) Long-lived, high-strength states of ICAM-1 bonds to β2 integrin, I: lifetimes of bonds to recombinant αLβ2 under force. Biophysical Journal 98, 1458–1466.CrossRefGoogle ScholarPubMed
Fillebeen, C, Wilkinson, N and Pantopoulos, K (2014) Electrophoretic mobility shift assay (EMSA) for the study of RNA–protein interactions: the IRE/IRP example. Journal of Visualized Experiments. doi: 10.3791/52230CrossRefGoogle Scholar
Fiore, VF, Ju, L, Chen, Y, Zhu, C and Barker, TH (2014) Dynamic catch of a Thy-1–α5β1 + syndecan-4 trimolecular complex. Nature Communications 5, 4886.CrossRefGoogle ScholarPubMed
Florin, E, Moy, V and Gaub, H (1994) Adhesion forces between individual ligand–receptor pairs. Science 264, 415–417.CrossRefGoogle ScholarPubMed
Forns, N, de Lorenzo, S, Manosas, M, Hayashi, K, Huguet, JM and Ritort, F (2011) Improving signal/noise resolution in single-molecule experiments using molecular constructs with short handles. Biophysical Journal 100, 1765–1774.CrossRefGoogle ScholarPubMed
Fournier, MF, Sauser, R, Ambrosi, D, Meister, J-J and Verkhovsky, AB (2010) Force transmission in migrating cells. Journal of Cell Biology 188, 287–297.CrossRefGoogle ScholarPubMed
Fritz, J, Katopodis, AG, Kolbinger, F and Anselmetti, D (1998) Force-mediated kinetics of single P-selectin/ligand complexes observed by atomic force microscopy. Proceedings of the National Academy of Sciences 95, 12283–12288.CrossRefGoogle ScholarPubMed
Fuhrmann, A and Ros, R (2010) Single-molecule force spectroscopy: a method for quantitative analysis of ligand–receptor interactions. Nanomedicine: Nanotechnology, Biology, and Medicine 5, 657–666.CrossRefGoogle ScholarPubMed
Fuhrmann, A, Schoening, JC, Anselmetti, D, Staiger, D and Ros, R (2009) Quantitative analysis of single-molecule RNA–protein interaction. Biophysical Journal 96, 5030–5039.CrossRefGoogle ScholarPubMed
Fukuda, S, Yan, S, Komi, Y, Sun, M, Gabizon, R and Bustamante, C (2020) The biogenesis of SRP RNA is modulated by an RNA folding intermediate attained during transcription. Molecular Cell 77, 241–250.e8.CrossRefGoogle ScholarPubMed
Ghisaidoobe, A and Chung, S (2014) Intrinsic tryptophan fluorescence in the detection and analysis of proteins: a focus on Förster resonance energy transfer techniques. International Journal of Molecular Sciences 15, 22518–22538.CrossRefGoogle ScholarPubMed
Gourier, C, Jegou, A, Husson, J and Pincet, F (2008) A nanospring named erythrocyte. The biomembrane force probe. Cellular and Molecular Bioengineering 1, 263–275.CrossRefGoogle Scholar
Guo, H and Li, Z (2013) Optical tweezers technique and its applications. Science China Physics, Mechanics and Astronomy 56, 2351–2360.CrossRefGoogle Scholar
Hackl, M, Contrada, EV, Ash, JE and Chundawat, SPS (2021) Acoustic force spectroscopy reveals subtle differences in cellulose unbinding behavior of carbohydrate-binding modules. BioRxiv, 2021.09.20.461102.CrossRefGoogle Scholar
Halvorsen, K, Schaak, D and Wong, WP (2011) Nanoengineering a single-molecule mechanical switch using DNA self-assembly. Nanotechnology 22, 494005. doi:10.1088/0957-4484/22/49/494005.CrossRefGoogle ScholarPubMed
Hinterdorfer, P, Baumgartner, W, Gruber, HJ, Schilcher, K and Schindler, H (1996) Detection and localization of individual antibody-antigen recognition events by atomic force microscopy. Proceedings of the National Academy of Sciences 93, 3477–3481.CrossRefGoogle ScholarPubMed
Jarzynski, C (1997) Nonequilibrium equality for free energy differences. Physical Review Letters 78, 2690–2693.CrossRefGoogle Scholar
Kada, G, Blayney, L, Jeyakumar, L, Kienberger, F, Pastushenko, VPh, Fleischer, S, Schindler, H, Lai, FA and Hinterdorfer, P (2001) Recognition force microscopy/spectroscopy of ion channels: applications to the skeletal muscle Ca2+ release channel (RYR1). Ultramicroscopy 86, 129–137.CrossRefGoogle Scholar
Kaiser, CM, Goldman, DH, Chodera, JD, Tinoco, I and Bustamante, C (2011) The ribosome modulates nascent protein folding. Science 334, 1723–1727.CrossRefGoogle ScholarPubMed
Kamsma, D and Wuite, GJL (2018) single-molecule measurements using acoustic force spectroscopy (AFS), pp. 341–351.CrossRefGoogle Scholar
Kamsma, D, Bochet, P, Oswald, F, Alblas, N, Goyard, S, Wuite, GJL, Peterman, EJG and Rose, T (2018) Single-cell acoustic force spectroscopy: resolving kinetics and strength of T cell adhesion to fibronectin. Cell Reports 24, 3008–3016.CrossRefGoogle ScholarPubMed
Kienberger, F, Kada, G, Mueller, H and Hinterdorfer, P (2005) Single molecule studies of antibody–antigen interaction strength versus intra-molecular antigen stability. Journal of Molecular Biology 347, 597–606.CrossRefGoogle ScholarPubMed
Kilinc, D, Blasiak, A, O'Mahony, JJ, Suter, DM and Lee, GU (2012) Magnetic tweezers-based force clamp reveals mechanically distinct apCAM domain interactions. Biophysical Journal 103, 1120–1129.CrossRefGoogle ScholarPubMed
Kim, J, Zhang, C-Z, Zhang, X and Springer, TA (2010) A mechanically stabilized receptor–ligand flex-bond important in the vasculature. Nature 466, 992–995.CrossRefGoogle ScholarPubMed
Kim, J, Hudson, NE and Springer, TA (2015) Force-induced on-rate switching and modulation by mutations in gain-of-function von Willebrand diseases. Proceedings of the National Academy of Sciences 112, 4648–4653.CrossRefGoogle ScholarPubMed
Kokkoli, E, Ochsenhirt, SE and Tirrell, M (2004) Collective and single-molecule interactions of α5β1 integrins. Langmuir 20, 2397–2404.CrossRefGoogle ScholarPubMed
Kühner, F, Costa, LT, Bisch, PM, Thalhammer, S, Heckl, WM and Gaub, HE (2004) LexA–DNA bond strength by single molecule force spectroscopy. Biophysical Journal 87, 2683–2690.CrossRefGoogle ScholarPubMed
Lavoisier, A (1790) Elements of chemistry: in a new systematic order, containing all the modern discoveries.Google Scholar
Lee, I and Marchant, RE (2001) Force measurements on the molecular interactions between ligand (RGD) and human platelet αIIbβ3 receptor system. Surface Science 491, 433–443.CrossRefGoogle Scholar
Lee, I and Marchant, RE (2003) Molecular interaction studies of hemostasis: fibrinogen ligand–human platelet receptor interactions. Ultramicroscopy 97, 341–352.CrossRefGoogle ScholarPubMed
Lee, G, Chrisey, L and Colton, R (1994 a) Direct measurement of the forces between complementary strands of DNA. Science 266, 771–773.CrossRefGoogle ScholarPubMed
Lee, GU, Kidwell, DA and Colton, RJ (1994 b) Sensing discrete streptavidin-biotin interactions with atomic force microscopy. Langmuir 10, 354–357.CrossRefGoogle Scholar
Lee, C-Y, Lou, J, Wen, K-K,McKane M, Eskin S G, Ono S, Chien S, Rubenstein PA, Zhu C, McIntire, LV (2013) Actin depolymerization under force is governed by lysine 113:glutamic acid 195-mediated catch-slip bonds. Proceedings of the National Academy of Sciences 110, 5022–5027.CrossRefGoogle ScholarPubMed
Li, P, Jiang, N, Nagarajan, S, Wohlhueter, R, Selvaraj, P and Zhu, C (2007) Affinity and kinetic analysis of Fcγ receptor IIIa (CD16a) binding to IgG ligands. Journal of Biological Chemistry 282, 6210–6221.CrossRefGoogle ScholarPubMed
Lin, S-N, Qin, L, Wuite, GJL and Dame, RT (2018) Unraveling the biophysical properties of chromatin proteins and DNA using acoustic force spectroscopy, 1837, 301–316.Google ScholarPubMed
Litvinov, RI, Bennett, JS, Weisel, JW and Shuman, H (2005) Multi-step fibrinogen binding to the integrin αIIbβ3 detected using force spectroscopy. Biophysical Journal 89, 2824–2834.CrossRefGoogle Scholar
Lo, Y-S, Zhu, Y-J and Beebe, TP (2001) Loading-Rate dependence of individual ligand–receptor bond-rupture forces studied by atomic force microscopy. Langmuir 17, 3741–3748.CrossRefGoogle Scholar
Lynch, S, Baker, H, Byker, SG, Zhou, D and Sinniah, K (2009) Single molecule force spectroscopy on G-quadruplex DNA. Chemistry – A European Journal 15, 8113–8116.CrossRefGoogle ScholarPubMed
Marshall, BT, Long, M, Piper, JW, Yago, T, McEver, RP and Zhu, C (2003) Direct observation of catch bonds involving cell-adhesion molecules. Nature 423, 190–193.CrossRefGoogle ScholarPubMed
Mateluna, C, Torres, P, Rodriguez–Peña, M, Silva, P, Matthies, DJ, Criollo, A, Bikker, FJ, Bolscher, JGM, Wilson, CAM, Zapata–Torres, G and Torres, VA (2022) Identification of VEGFR2 as the histatin-1 receptor in endothelial cells. Biochemical Pharmacology 201, 115079.CrossRefGoogle ScholarPubMed
Mejean, CO, Schaefer, AW, Millman, EA, Forscher, P and Dufresne, ER (2009) Multiplexed force measurements on live cells with holographic optical tweezers. Optics Express 17, 6209.CrossRefGoogle ScholarPubMed
Merkel, R, Nassoy, P, Leung, A, Ritchie, K and Evans, E (1999) Energy landscapes of receptor–ligand bonds explored with dynamic force spectroscopy. Nature 397, 50–53.CrossRefGoogle ScholarPubMed
Meyer, G and Amer, NM (1988) Novel optical approach to atomic force microscopy. Applied Physics Letters 53, 1045–1047.CrossRefGoogle Scholar
Misselwitz, B, Staeck, O and Rapoport, TA (1998) J proteins catalytically activate Hsp70 molecules to trap a wide range of peptide sequences. Molecular Cell 2, 593–603.CrossRefGoogle Scholar
Molloy, JE and Padgett, MJ (2002) Lights, action: optical tweezers. Contemporary Physics 43, 241–258.CrossRefGoogle Scholar
Morfill, J, Blank, K, Zahnd, C, Luginbühl, B, Kühner, F, Gottschalk, K-E, Plückthun, A and Gaub, HE (2007) Affinity-matured recombinant antibody fragments analyzed by single-molecule force spectroscopy. Biophysical Journal 93, 3583–3590.CrossRefGoogle ScholarPubMed
Muñoz, R, Aguilar Sandoval, F, Wilson, CAM and Melo, F (2015) Pulling on super paramagnetic beads with micro cantilevers: single molecule mechanical assay application. Physical Biology 12, 046011.CrossRefGoogle ScholarPubMed
Neuman, KC and Nagy, A (2008) Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nature Methods 5, 491–505.CrossRefGoogle ScholarPubMed
Nicholas, MP, Rao, L and Gennerich, A (2014) An improved optical tweezers assay for measuring the force generation of single kinesin molecules. Methods in Molecular Biology 1136, 171–246.CrossRefGoogle ScholarPubMed
Nieminen, TA, Knöner, G, Heckenberg, NR and Rubinsztein-Dunlop, H (2007) Physics of Optical Tweezers, pp. 207–236.CrossRefGoogle Scholar
Nishizaka, T, Tadakuma, H, Kato, H, Miyata, H and Kinosita, KSI (1996) Lifetime of a single actomyosin rigor bond measured using optical tweezers.Google Scholar
Nobel Prize (2021) Arthur Ashkin. Available at https://www.nobelprize.org/prizes/physics/2018/ashkin/.Google Scholar
O'Shannessy, DJ (1994) Determination of kinetic rate and equilibrium binding constants for macromolecular interactions: a critique of the surface plasmon resonance literature. Current Opinion in Biotechnology 5, 65–71.CrossRefGoogle ScholarPubMed
Peña-Oyarzun, D, Rodriguez-Peña, M, Burgos-Bravo, F,Vergara A, Kretschmar C, Sotomayor-Flores C, Ramirez-Sarmiento CA, De Smedt H, Reyes M, Perez W, Torres V A, Morselli E, Altamirano F, Wilson C AM, Hill J A, Lavandero S, Criollo, A (2020) PKD2/polycystin-2 induces autophagy by forming a complex with BECN1. Autophagy 17(7), 1714–1728.CrossRefGoogle ScholarPubMed
Perret, E, Leung, A, Feracci, H and Evans, E (2004) Trans-bonded pairs of E-cadherin exhibit a remarkable hierarchy of mechanical strengths. Proceedings of the National Academy of Sciences 101, 16472–16477.CrossRefGoogle ScholarPubMed
Pierres, A, Touchard, D, Benoliel, A-M and Bongrand, P (2002) Dissecting streptavidin–biotin interaction with a laminar flow chamber. Biophysical Journal 82, 3214–3223.CrossRefGoogle ScholarPubMed
Pierres, A, Benoliel, A-M and Bongrand, P (2008) Studying molecular interactions at the single bond level with a laminar flow chamber. Cellular and Molecular Bioengineering 1, 247–262.CrossRefGoogle ScholarPubMed
Polacheck, WJ, Charest, JL and Kamm, RD (2011) Interstitial flow influences direction of tumor cell migration through competing mechanisms. Proceedings of the National Academy of Sciences 108, 11115–11120.CrossRefGoogle ScholarPubMed
Polimeno, P, Magazzù, A, Iatì, MA, Patti F, Saija R, Esposti B C D, Donato M G, Gucciardi P G, Jones P H, Volpe G,Maragò, OM (2018) Optical tweezers and their applications. Journal of Quantitative Spectroscopy and Radiative Transfer 218, 131–150.CrossRefGoogle Scholar
Pollard, TD and Borisy, GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453–465.CrossRefGoogle ScholarPubMed
Porter-Peden, L, Kamper, SG, Vander Wal, M, Blankespoor, R and Sinniah, K (2008) Estimating kinetic and thermodynamic parameters from single molecule enzyme–inhibitor interactions. Langmuir 24, 11556–11561.CrossRefGoogle ScholarPubMed
Rakshit, S, Zhang, Y, Manibog, K, Shafraz, O and Sivasankar, S (2012) Ideal, catch, and slip bonds in cadherin adhesion. Proceedings of the National Academy of Sciences 109, 18815–18820.CrossRefGoogle ScholarPubMed
Raman, S, Utzig, T, Baimpos, T, Ratna Shrestha, B and Valtiner, M (2014) Deciphering the scaling of single-molecule interactions using Jarzynski's equality. Nature Communications 5, 5539.CrossRefGoogle ScholarPubMed
Ramírez, MP (2016) Studying the role of BiP as a chaperone through single, Universidad de Chile.Google Scholar
Ramírez, MP, Rivera, M, Quiroga-Roger, D, Bustamante A, Vega M, Baez M, Puchner E M,Wilson, CAM (2017) Single molecule force spectroscopy reveals the effect of BiP chaperone on protein folding. Protein Science 26, 1404–1412.CrossRefGoogle ScholarPubMed
Rinko, LJ, Lawrence, MB and Guilford, WH (2004) The molecular mechanics of P- and L-selectin lectin domains binding to PSGL-1. Biophysical Journal 86, 544–554.CrossRefGoogle ScholarPubMed
Robert, P, Benoliel, A-M, Pierres, A and Bongrand, P (2007) What is the biological relevance of the specific bond properties revealed by single-molecule studies? Journal of Molecular Recognition 20, 432–447.CrossRefGoogle ScholarPubMed
Rognoni, L, Stigler, J, Pelz, B, Ylanne, J and Rief, M (2012) Dynamic force sensing of filamin revealed in single-molecule experiments. Proceedings of the National Academy of Sciences 109, 19679–19684.CrossRefGoogle ScholarPubMed
Schlierf, M and Rief, M (2005) Temperature softening of a protein in single-molecule experiments. Journal of Molecular Biology 354, 497–503.CrossRefGoogle ScholarPubMed
Schmid, D, Baici, A, Gehring, H and Christen, P (1994) Kinetics of molecular chaperone action. Science 263, 971–973.CrossRefGoogle ScholarPubMed
Shang, H and Lee, GU (2007) Magnetic tweezers measurement of the bond lifetime–force behavior of the IgG – protein A specific molecular interaction. Journal of the American Chemical Society 129, 6640–6646.CrossRefGoogle ScholarPubMed
Shao, J-Y (2004) Quantifying cell-adhesion strength with micropipette manipulation: principle and application. Frontiers in Bioscience 9, 2183.CrossRefGoogle ScholarPubMed
Shemesh, J, Jalilian, I, Shi, A, Heng Yeoh, G, Knothe Tate, ML and Ebrahimi Warkiani, M (2015) Flow-induced stress on adherent cells in microfluidic devices. Lab on a Chip 15, 4114–4127.CrossRefGoogle ScholarPubMed
Singha Roy, A, Dinda, AK, Chaudhury, S and Dasgupta, S (2014) Binding of antioxidant flavonol morin to the native state of bovine serum albumin: effects of urea and metal ions on the binding. Journal of Luminescence 145, 741–751.CrossRefGoogle Scholar
Sitters, G, Kamsma, D, Thalhammer, G, Ritsch-Marte, M, Peterman, EJG and Wuite, GJL (2014) Acoustic force spectroscopy. Nature Methods 12, 47–50.CrossRefGoogle ScholarPubMed
Smith, SB, Cui, Y and Bustamante, C (2003) Optical-trap force transducer that operates by direct measurement of light momentum. Methods Enzymol 361, 134–162. doi:10.1016/s0076-6879(03)61009-8.CrossRefGoogle ScholarPubMed
Sorkin, R, Bergamaschi, G, Kamsma, D, Brand G, Dekel E, Ofir-Birin Y, Rudik A, Gironella M, Ritort F, Regev-Rudzki N, Roos W H, Wuite, GJL (2018) Probing cellular mechanics with acoustic force spectroscopy. Molecular Biology of the Cell 29, 2005–2011.CrossRefGoogle ScholarPubMed
Stangner, T, Wagner, C, Singer, D,Angioletti-Uberti S, Gutsche C, Dzubiella J, Hoffmann R, Kremer, F (2013) Determining the specificity of monoclonal antibody HPT-101 to tau-peptides with optical tweezers. ACS Nano 7, 11388–11396.CrossRefGoogle ScholarPubMed
Stigler, J and Rief, M (2015) Ligand-induced changes of the apparent transition-state position in mechanical protein unfolding. Biophysical Journal 109, 365–372.CrossRefGoogle ScholarPubMed
Stout, AL (2001) Detection and characterization of individual intermolecular bonds using optical tweezers. Biophysical Journal 80, 2976–2986.CrossRefGoogle ScholarPubMed
Sudhakar, S, Abdosamadi, MK, Jachowski, TJ, Bugiel, M, Jannasch, A and Schäffer, E (2021) Germanium nanospheres for ultraresolution picotensiometry of kinesin motors. Science 371(6530). doi:10.1126/science.abd9944.CrossRefGoogle ScholarPubMed
Sung, K, Sung, L, Crimmins, M, Burakoff, S and Chien, S (1986) Determination of junction avidity of cytolytic T cell and target cell. Science 234, 1405–1408.CrossRefGoogle ScholarPubMed
Szili, EJ, Al-Bataineh, SA, Ruschitzka, P,Desmet G, Priest C, Griesser HJ, Voelcker NH, Harding FJ, Steele DA, Short, RD (2012) Microplasma arrays: a new approach for maskless and localized patterning of materials surfaces. RSC Advances 2, 12007.CrossRefGoogle Scholar
Thoumine, O, Bard, L, Saint-Michel, E, Dequidt, C and Choquet, D (2008) Optical tweezers and fluorescence recovery after photo-bleaching to measure molecular interactions at the cell surface. Cellular and Molecular Bioengineering 1, 301–311.CrossRefGoogle Scholar
Tinoco, I (2004) Force as a useful variable in reactions: unfolding RNA. Annual Review of Biophysics and Biomolecular Structure 33, 363–385.CrossRefGoogle ScholarPubMed
Tinoco, I, Sauer, K, Wang, JC, Puglisi, JD, Harbison, G and Rovnyak, D (2013) Physical Chemistry: Principles and Applications in Biological Sciences.Google Scholar
Tych, KM, Hoffmann, T, Brockwell, DJ and Dougan, L (2013) Single molecule force spectroscopy reveals the temperature-dependent robustness and malleability of a hyperthermophilic protein. Soft Matter 9, 9016.CrossRefGoogle Scholar
Ungai-Salánki, R, Peter, B, Gerecsei, T, Orgovan, N, Horvath, R and Szabó, B (2019) A practical review on the measurement tools for cellular adhesion force. Advances in Colloid and Interface Science 269, 309–333.CrossRefGoogle Scholar
Van Rosmalen, MGM, Kamsma, D, Biebricher, AS, Li, C, Zlotnick, A, Roos, WH and Wuite, GJL (2020) Revealing in real-time a multistep assembly mechanism for SV40 virus-like particles. Science Advances 6. doi:10.1126/sciadv.aaz1639.CrossRefGoogle ScholarPubMed
Weisel, J (2003) Protein–protein unbinding induced by force: single-molecule studies. Current Opinion in Structural Biology 13, 227–235.CrossRefGoogle ScholarPubMed
Whitley, KD, Comstock, MJ and Chemla, YR (2017) High-Resolution ‘Fleezers’: Dual-Trap Optical Tweezers Combined with Single-Molecule Fluorescence Detection, pp. 183–256.CrossRefGoogle Scholar
Willemsen, OH, Snel, MME, Cambi, A, Greve, J, De Grooth, BG and Figdor, CG (2000) Biomolecular interactions measured by atomic force microscopy. Biophysical Journal 79, 3267–3281.CrossRefGoogle ScholarPubMed
Wilson, C (2011) Single Molecule Studies by Optical Tweezers: Folding and Unfolding of Glucokinase from Thermococcus litoralis. Santiago, Chile: Universidad de Chile.Google Scholar
Yuan, C, Chen, A, Kolb, P and Moy, VT (2000) Energy landscape of streptavidin–biotin complexes measured by atomic force microscopy. Biochemistry 39, 10219–10223.CrossRefGoogle ScholarPubMed
Zaltron, A, Merano, M, Mistura, G, Sada, C and Seno, F (2020) Optical tweezers in single-molecule experiments. The European Physical Journal Plus 135, 896.CrossRefGoogle Scholar
Zhang, H and Liu, K-K (2008) Optical tweezers for single cells. Journal of the Royal Society Interface 5, 671–690.CrossRefGoogle ScholarPubMed
Zhang, X, Wojcikiewicz, E and Moy, VT (2002) Force spectroscopy of the leukocyte function-associated antigen-1/intercellular adhesion molecule-1 interaction. Biophysical Journal 83, 2270–2279.CrossRefGoogle ScholarPubMed
Zhu, C (2014) Mechanochemitry: a molecular biomechanics view of mechanosensing. Annals of Biomedical Engineering 42, 388–404.CrossRefGoogle ScholarPubMed
Zohra, FT (2021) Using single-molecule DNA flow-stretching experiments to see the effects of temperature and viscosity, The University of Texas Rio Grande Valley. Available at https://www.proquest.com/docview/2595580864?pq-origsite=gscholar&fromopenview=true.Google Scholar