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Annual Review of Biochemistry

Volume 91, 2022

High-Resolution Single-Molecule Magnetic Tweezers

Abstract

Single-molecule magnetic tweezers deliver magnetic force and torque to single target molecules, permitting the study of dynamic changes in biomolecular structures and their interactions. Because the magnetic tweezer setups can generate magnetic fields that vary slowly over tens of millimeters—far larger than the nanometer scale of the single molecule events being observed—this technique can maintain essentially constant force levels during biochemical experiments while generating a biologically meaningful force on the order of 1–100 pN. When using bead–tether constructs to pull on single molecules, smaller magnetic beads and shorter submicrometer tethers improve dynamic response times and measurement precision. In addition, employing high-speed cameras, stronger light sources, and a graphics programming unit permits true high-resolution single-molecule magnetic tweezers that can track nanometer changes in target molecules on a millisecond or even submillisecond time scale. The unique force-clamping capacity of the magnetic tweezer technique provides a way to conduct measurements under near-equilibrium conditions and directly map the energy landscapes underlying various molecular phenomena. High-resolution single-molecule magnetic tweezerscan thus be used to monitor crucial conformational changes in single-protein molecules, including those involved in mechanotransduction and protein folding.

Keyword(s): high-resolution magnetic tweezers, magnetic tweezers, mechanotransduction, protein folding, single molecules, single-molecule force spectroscopy
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/content/journals/10.1146/annurev-biochem-032620-104637
2022-06-21
2024-04-30
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Literature Cited

  1. 1.
    Freundlich H, Seifriz W. 1923. Über die Elastizität von Solen und Gelen. Z. Phys. Chem. 104U:233–61
     [Google Scholar]
  2. 2.
    Crick FHC, Hughes AFW. 1950. The physical properties of cytoplasm. Exp. Cell Res. 1:37–80
     [Google Scholar]
  3. 3.
    Smith SB, Finzi L, Bustamante C. 1992. Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science 258:1122–26
     [Google Scholar]
  4. 4.
    Strick TR, Allemand JF, Bensimon D, Bensimon A, Croquette V. 1996. The elasticity of a single supercoiled DNA molecule. Science 271:1835–37
     [Google Scholar]
  5. 5.
    Haber C, Wirtz D. 2000. Magnetic tweezers for DNA micromanipulation. Rev. Sci. Instrum. 71:4561–70
     [Google Scholar]
  6. 6.
    Gosse C, Croquette V. 2002. Magnetic tweezers: micromanipulation and force measurement at the molecular level. Biophys. J. 82:3314–29
     [Google Scholar]
  7. 7.
    De Vlaminck I, Dekker C. 2012. Recent advances in magnetic tweezers. Annu. Rev. Biophys. 41:453–72
     [Google Scholar]
  8. 8.
    Block SM, Goldstein LS, Schnapp BJ. 1990. Bead movement by single kinesin molecules studied with optical tweezers. Nature 348:348–52
     [Google Scholar]
  9. 9.
    Svoboda K, Schmidt CF, Schnapp BJ, Block SM. 1993. Direct observation of kinesin stepping by optical trapping interferometry. Nature 365:721–27
     [Google Scholar]
  10. 10.
    Smith SB, Cui Y, Bustamante C. 1996. Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science 271:795–99
     [Google Scholar]
  11. 11.
    Simmons RM, Finer JT, Chu S, Spudich JA 1996. Quantitative measurements of force and displacement using an optical trap. Biophys. J. 70:1813–22
     [Google Scholar]
  12. 12.
    Moffitt JR, Chemla YR, Smith SB, Bustamante C. 2008. Recent advances in optical tweezers. Annu. Rev. Biochem. 77:205–28
     [Google Scholar]
  13. 13.
    Florin E-L, Moy VT, Gaub HE. 1994. Adhesion forces between individual ligand-receptor pairs. Science 264:415–17
     [Google Scholar]
  14. 14.
    Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE. 1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276:1109–12
     [Google Scholar]
  15. 15.
    Oberhauser AF, Marszalek PE, Erickson HP, Fernandez JM. 1998. The molecular elasticity of the extracellular matrix protein tenascin. Nature 393:181–85
     [Google Scholar]
  16. 16.
    Oesterhelt F, Oesterhelt D, Pfeiffer M, Engel A, Gaub HE, Muller DJ. 2000. Unfolding pathways of individual bacteriorhodopsins. Science 288:143–46
     [Google Scholar]
  17. 17.
    Neuman KC, Nagy A. 2008. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods 5:491–505
     [Google Scholar]
  18. 18.
    Wang MD, Yin H, Landick R, Gelles J, Block SM. 1997. Stretching DNA with optical tweezers. Biophys. J. 72:1335–46
     [Google Scholar]
  19. 19.
    Strick TR, Allemand JF, Bensimon D, Croquette V. 1998. Behavior of supercoiled DNA. Biophys. J. 74:2016–28
     [Google Scholar]
  20. 20.
    Liphardt J, Onoa B, Smith SB, Tinoco I Jr., Bustamante C. 2001. Reversible unfolding of single RNA molecules by mechanical force. Science 292:733–37
     [Google Scholar]
  21. 21.
    Abels J, Moreno-Herrero F, Van der Heijden T, Dekker C, Dekker NH. 2005. Single-molecule measurements of the persistence length of double-stranded RNA. Biophys. J. 88:2737–44
     [Google Scholar]
  22. 22.
    Koster DA, Croquette V, Dekker C, Shuman S, Dekker NH. 2005. Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB. Nature 434:671–74
     [Google Scholar]
  23. 23.
    Lee G, Abdi K, Jiang Y, Michaely P, Bennett V, Marszalek PE. 2006. Nanospring behaviour of ankyrin repeats. Nature 440:246–49
     [Google Scholar]
  24. 24.
    Kishino A, Yanagida T. 1988. Force measurements by micromanipulation of a single actin filament by glass needles. Nature 334:74–76
     [Google Scholar]
  25. 25.
    Smith DE, Tans SJ, Smith SB, Grimes S, Anderson DL, Bustamante C. 2001. The bacteriophage 29 portal motor can package DNA against a large internal force. Nature 413:748–52
     [Google Scholar]
  26. 26.
    Asbury CL, Fehr AN, Block SM. 2003. Kinesin moves by an asymmetric hand-over-hand mechanism. Science 302:2130–34
     [Google Scholar]
  27. 27.
    Abbondanzieri EA, Greenleaf WJ, Shaevitz JW, Landick R, Block SM. 2005. Direct observation of base-pair stepping by RNA polymerase. Nature 438:460–65
     [Google Scholar]
  28. 28.
    Wen J-D, Lancaster L, Hodges C, Zeri A-C, Yoshimura SH et al. 2008. Following translation by single ribosomes one codon at a time. Nature 452:598–603
     [Google Scholar]
  29. 29.
    Kellermayer MS, Smith SB, Granzier HL, Bustamante C. 1997. Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science 276:1112–16
     [Google Scholar]
  30. 30.
    Marszalek PE, Lu H, Li H, Carrion-Vazquez M, Oberhauser AF et al. 1999. Mechanical unfolding intermediates in titin modules. Nature 402:100–3
     [Google Scholar]
  31. 31.
    Woodside MT, Block SM. 2014. Reconstructing folding energy landscapes by single-molecule force spectroscopy. Annu. Rev. Biophys. 43:19–39
     [Google Scholar]
  32. 32.
    Neupane K, Foster DA, Dee DR, Yu H, Wang F, Woodside MT 2016. Direct observation of transition paths during the folding of proteins and nucleic acids. Science 352:239–42
     [Google Scholar]
  33. 33.
    Yu H, Siewny MG, Edwards DT, Sanders AW, Perkins TT. 2017. Hidden dynamics in the unfolding of individual bacteriorhodopsin proteins. Science 355:945–50
     [Google Scholar]
  34. 34.
    Bustamante C, Alexander L, Maciuba K, Kaiser CM. 2020. Single-molecule studies of protein folding with optical tweezers. Annu. Rev. Biochem. 89:443–70
     [Google Scholar]
  35. 35.
    Danilowicz C, Greenfield D, Prentiss M 2005. Dissociation of ligand−receptor complexes using magnetic tweezers. Anal. Chem. 77:3023–28
     [Google Scholar]
  36. 36.
    Kim J, Zhang C-Z, Zhang X, Springer TA. 2010. A mechanically stabilized receptor–ligand flex-bond important in the vasculature. Nature 466:992–95
     [Google Scholar]
  37. 37.
    Kostrz D, Wayment-Steele HK, Wang JL, Follenfant M, Pande VS et al. 2019. A modular DNA scaffold to study protein–protein interactions at single-molecule resolution. Nat. Nanotechnol. 14:988–93
     [Google Scholar]
  38. 38.
    del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP. 2009. Stretching single talin rod molecules activates vinculin binding. Science 323:638–41
     [Google Scholar]
  39. 39.
    Yao M, Qiu W, Liu R, Efremov AK, Cong P et al. 2014. Force-dependent conformational switch of α-catenin controls vinculin binding. Nat. Commun. 5:4525
     [Google Scholar]
  40. 40.
    Buckley CD, Tan J, Anderson KL, Hanein D, Volkmann N et al. 2014. The minimal cadherin-catenin complex binds to actin filaments under force. Science 346:1254211
     [Google Scholar]
  41. 41.
    Seo D, Southard KM, Kim JW, Lee HJ, Farlow J et al. 2016. A mechanogenetic toolkit for interrogating cell signaling in space and time. Cell 165:1507–18
     [Google Scholar]
  42. 42.
    Harris AR, Jreij P, Fletcher DA. 2018. Mechanotransduction by the actin cytoskeleton: converting mechanical stimuli into biochemical signals. Annu. Rev. Biophys. 47:617–31
     [Google Scholar]
  43. 43.
    Ashkin A, Dziedzic JM, Bjorkholm JE, Chu S 1986. Observation of a single-beam gradient force optical trap for dielectric particles. Opt. Lett. 11:288–90
     [Google Scholar]
  44. 44.
    Shaevitz JW, Abbondanzieri EA, Landick R, Block SM. 2003. Backtracking by single RNA polymerase molecules observed at near-base-pair resolution. Nature 426:684–87
     [Google Scholar]
  45. 45.
    Peterman EJ, Gittes F, Schmidt CF. 2003. Laser-induced heating in optical traps. Biophys. J. 84:1308–16
     [Google Scholar]
  46. 46.
    Čižmár T, Mazilu M, Dholakia K. 2010. In situ wavefront correction and its application to micromanipulation. Nat. Photon. 4:388–94
     [Google Scholar]
  47. 47.
    Park J-H, Yu Z, Lee K, Lai P, Park Y. 2018. Wavefront shaping techniques for controlling multiple light scattering in biological tissues: toward in vivo applications. APL Photon. 3:100901
     [Google Scholar]
  48. 48.
    Favre-Bulle IA, Stilgoe AB, Scott EK, Rubinsztein-Dunlop H. 2019. Optical trapping in vivo: theory, practice, and applications. Nanophotonics 8:1023–40
     [Google Scholar]
  49. 49.
    Hughes ML, Dougan L. 2016. The physics of pulling polyproteins: a review of single molecule force spectroscopy using the AFM to study protein unfolding. Rep. Prog. Phys. 79:076601
     [Google Scholar]
  50. 50.
    Edwards DT, Faulk JK, Sanders AW, Bull MS, Walder R et al. 2015. Optimizing 1-μs-resolution single-molecule force spectroscopy on a commercial atomic force microscope. Nano Lett 15:7091–98
     [Google Scholar]
  51. 51.
    Churnside AB, Sullan RM, Nguyen DM, Case SO, Bull MS et al. 2012. Routine and timely sub-picoNewton force stability and precision for biological applications of atomic force microscopy. Nano Lett 12:3557–61
     [Google Scholar]
  52. 52.
    Edwards DT, Faulk JK, LeBlanc MA, Perkins TT. 2017. Force spectroscopy with 9-μs resolution and sub-pN stability by tailoring AFM cantilever geometry. Biophys. J. 113:2595–600
     [Google Scholar]
  53. 53.
    Edwards DT, LeBlanc MA, Perkins TT. 2021. Modulation of a protein-folding landscape revealed by AFM-based force spectroscopy notwithstanding instrumental limitations. PNAS 118:e2015728118
     [Google Scholar]
  54. 54.
    Vilfan ID, Lipfert J, Koster D, Lemay S, Dekker N 2009. Magnetic tweezers for single-molecule experiments. Handbook of Single-Molecule Biophysics P Hinterdorfer, A Oijen 371–95 New York: Springer
     [Google Scholar]
  55. 55.
    Lipfert J, Hao X, Dekker NH. 2009. Quantitative modeling and optimization of magnetic tweezers. Biophys. J. 96:5040–49
     [Google Scholar]
  56. 56.
    te Velthuis AJ, Kerssemakers JW, Lipfert J, Dekker NH. 2010. Quantitative guidelines for force calibration through spectral analysis of magnetic tweezers data. Biophys. J. 99:1292–302
     [Google Scholar]
  57. 57.
    Lansdorp BM, Tabrizi SJ, Dittmore A, Saleh OA. 2013. A high-speed magnetic tweezer beyond 10,000 frames per second. Rev. Sci. Instrum. 84:044301
     [Google Scholar]
  58. 58.
    Dulin D, Cui TJ, Cnossen J, Docter MW, Lipfert J, Dekker NH. 2015. High spatiotemporal-resolution magnetic tweezers: calibration and applications for DNA dynamics. Biophys. J. 109:2113–25
     [Google Scholar]
  59. 59.
    Huhle A, Klaue D, Brutzer H, Daldrop P, Joo S et al. 2015. Camera-based three-dimensional real-time particle tracking at kHz rates and Ångström accuracy. Nat. Commun. 6:5885
     [Google Scholar]
  60. 60.
    Kirby TJ, Lammerding J. 2018. Emerging views of the nucleus as a cellular mechanosensor. Nat. Cell Biol. 20:373–81
     [Google Scholar]
  61. 61.
    Romani P, Valcarcel-Jimenez L, Frezza C, Dupont S. 2021. Crosstalk between mechanotransduction and metabolism. Nat. Rev. Mol. Cell Biol. 22:22–38
     [Google Scholar]
  62. 62.
    Purcell EM. 1977. Life at low Reynolds number. Am. J. Phys. 45:3–11
     [Google Scholar]
  63. 63.
    Dill KA, Ghosh K, Schmit JD. 2011. Physical limits of cells and proteomes. PNAS 108:17876–82
     [Google Scholar]
  64. 64.
    Sawle L, Ghosh K. 2011. How do thermophilic proteins and proteomes withstand high temperature?. Biophys. J. 101:217–27
     [Google Scholar]
  65. 65.
    Woodside MT, Behnke-Parks WM, Larizadeh K, Travers K, Herschlag D, Block SM. 2006. Nanomechanical measurements of the sequence-dependent folding landscapes of single nucleic acid hairpins. PNAS 103:6190–95
     [Google Scholar]
  66. 66.
    Krebs MD, Erb RM, Yellen BB, Samanta B, Bajaj A et al. 2009. Formation of ordered cellular structures in suspension via label-free negative magnetophoresis. Nano Lett 9:1812–17
     [Google Scholar]
  67. 67.
    Kose AR, Fischer B, Mao L, Koser H. 2009. Label-free cellular manipulation and sorting via biocompatible ferrofluids. PNAS 106:21478–83
     [Google Scholar]
  68. 68.
    Zeng J, Deng YX, Vedantam P, Tzeng TR, Xuan XC. 2013. Magnetic separation of particles and cells in ferrofluid flow through a straight microchannel using two offset magnets. J. Magn. Magn. Mater. 346:118–23
     [Google Scholar]
  69. 69.
    Furlani EP. 2006. Analysis of particle transport in a magnetophoretic microsystem. J. Appl. Phys. 99:024912
     [Google Scholar]
  70. 70.
    Timonen JVI, Grzybowski BA. 2017. Tweezing of magnetic and non-magnetic objects with magnetic fields. Adv. Mater. 29:1603516
     [Google Scholar]
  71. 71.
    Chen H, Fu H, Zhu X, Cong P, Nakamura F, Yan J 2011. Improved high-force magnetic tweezers for stretching and refolding of proteins and short DNA. Biophys. J. 100:517–23
     [Google Scholar]
  72. 72.
    Liu R, Garcia-Manyes S, Sarkar A, Badilla CL, Fernandez JM. 2009. Mechanical characterization of protein L in the low-force regime by electromagnetic tweezers/evanescent nanometry. Biophys. J. 96:3810–21
     [Google Scholar]
  73. 73.
    Choi HK, Min D, Kang H, Shon MJ, Rah SH et al. 2019. Watching helical membrane proteins fold reveals a common N-to-C-terminal folding pathway. Science 366:1150–56
     [Google Scholar]
  74. 74.
    Fonnum G, Johansson C, Molteberg A, Morup S, Aksnes E. 2005. Characterisation of Dynabeads® by magnetization measurements and Mossbauer spectroscopy. J. Magn. Magn. Mater. 293:41–47
     [Google Scholar]
  75. 75.
    De Vlaminck I, Henighan T, van Loenhout MT, Burnham DR, Dekker C. 2012. Magnetic forces and DNA mechanics in multiplexed magnetic tweezers. PLOS ONE 7:e41432
     [Google Scholar]
  76. 76.
    van Oene MM, Dickinson LE, Pedaci F, Kober M, Dulin D et al. 2015. Biological magnetometry: torque on superparamagnetic beads in magnetic fields. Phys. Rev. Lett. 114:218301
     [Google Scholar]
  77. 77.
    Yan J, Skoko D, Marko JF. 2004. Near-field-magnetic-tweezer manipulation of single DNA molecules. Phys. Rev. E Stat. Nonlin. Soft. Matter Phys. 70:011905
     [Google Scholar]
  78. 78.
    Ribeck N, Saleh OA. 2008. Multiplexed single-molecule measurements with magnetic tweezers. Rev. Sci. Instrum. 79:094301
     [Google Scholar]
  79. 79.
    Tapia-Rojo R, Eckels EC, Fernandez JM. 2019. Ephemeral states in protein folding under force captured with a magnetic tweezers design. PNAS 116:7873–78
     [Google Scholar]
  80. 80.
    Lansdorp BM, Saleh OA. 2012. Power spectrum and Allan variance methods for calibrating single-molecule video-tracking instruments. Rev. Sci. Instrum. 83:025115
     [Google Scholar]
  81. 81.
    Yu Z, Dulin D, Cnossen J, Kober M, van Oene MM et al. 2014. A force calibration standard for magnetic tweezers. Rev. Sci. Instrum. 85:123114
     [Google Scholar]
  82. 82.
    Daldrop P, Brutzer H, Huhle A, Kauert DJ, Seidel R. 2015. Extending the range for force calibration in magnetic tweezers. Biophys. J. 108:2550–61
     [Google Scholar]
  83. 83.
    Barbic M, Mock JJ, Gray AP, Schultz S. 2001. Scanning probe electromagnetic tweezers. Appl. Phys. Lett. 79:1897–99
     [Google Scholar]
  84. 84.
    Jiang C, Lionberger TA, Wiener DM, Meyhofer E. 2016. Electromagnetic tweezers with independent force and torque control. Rev. Sci. Instrum. 87:084304
     [Google Scholar]
  85. 85.
    Matthews BD, LaVan DA, Overby DR, Karavitis J, Ingber DE. 2004. Electromagnetic needles with submicron pole tip radii for nanomanipulation of biomolecules and living cells. Appl. Phys. Lett. 85:2968–70
     [Google Scholar]
  86. 86.
    Chiou C-H, Lee G-B. 2005. A micromachined DNA manipulation platform for the stretching and rotation of a single DNA molecule. J. Micromech. Microeng. 15:109–17
     [Google Scholar]
  87. 87.
    Chiou CH, Huang YY, Chiang MH, Lee HH, Lee GB. 2006. New magnetic tweezers for investigation of the mechanical properties of single DNA molecules. Nanotechnology 17:1217–24
     [Google Scholar]
  88. 88.
    Wang X, Ho C, Tsatskis Y, Law J, Zhang Z et al. 2019. Intracellular manipulation and measurement with multipole magnetic tweezers. Sci. Robot. 4:eaav6180
     [Google Scholar]
  89. 89.
    Kim JW, Jeong HK, Southard KM, Jun YW, Cheon J. 2018. Magnetic nanotweezers for interrogating biological processes in space and time. Acc. Chem. Res. 51:839–49
     [Google Scholar]
  90. 90.
    Greenleaf WJ, Woodside MT, Abbondanzieri EA, Block SM. 2005. Passive all-optical force clamp for high-resolution laser trapping. Phys. Rev. Lett. 95:208102
     [Google Scholar]
  91. 91.
    Romano G, Sacconi L, Capitanio M, Pavone FS. 2003. Force and torque measurements using magnetic micro beads for single molecule biophysics. Opt. Commun. 215:323–31
     [Google Scholar]
  92. 92.
    Lee JU, Shin W, Lim Y, Kim J, Kim WR et al. 2021. Non-contact long-range magnetic stimulation of mechanosensitive ion channels in freely moving animals. Nat. Mater. 20:1029–36
     [Google Scholar]
  93. 93.
    van Reenen A, Gutierrez-Mejia F, van IJzendoorn LJ, Prins MWJ. 2013. Torsion profiling of proteins using magnetic particles. Biophys. J. 104:1073–80
     [Google Scholar]
  94. 94.
    Maier B, Bensimon D, Croquette V. 2000. Replication by a single DNA polymerase of a stretched single-stranded DNA. PNAS 97:12002–7
     [Google Scholar]
  95. 95.
    Manosas M, Xi XG, Bensimon D, Croquette V. 2010. Active and passive mechanisms of helicases. Nucleic Acids Res. 38:5518–26
     [Google Scholar]
  96. 96.
    Dekker NH, Rybenkov VV, Duguet M, Crisona NJ, Cozzarelli NR et al. 2002. The mechanism of type IA topoisomerases. PNAS 99:12126–31
     [Google Scholar]
  97. 97.
    Crut A, Koster DA, Seidel R, Wiggins CH, Dekker NH. 2007. Fast dynamics of supercoiled DNA revealed by single-molecule experiments. PNAS 104:11957–62
     [Google Scholar]
  98. 98.
    Bell GI. 1978. Models for the specific adhesion of cells to cells. Science 200:618–27
     [Google Scholar]
  99. 99.
    Evans E, Ritchie K 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541–55
     [Google Scholar]
  100. 100.
    Dudko OK, Hummer G, Szabo A. 2008. Theory, analysis, and interpretation of single-molecule force spectroscopy experiments. PNAS 105:15755–60
     [Google Scholar]
  101. 101.
    Lof A, Walker PU, Sedlak SM, Gruber S, Obser T et al. 2019. Multiplexed protein force spectroscopy reveals equilibrium protein folding dynamics and the low-force response of von Willebrand factor. PNAS 116:18798–807
     [Google Scholar]
  102. 102.
    Chen H, Yuan G, Winardhi RS, Yao M, Popa I et al. 2015. Dynamics of equilibrium folding and unfolding transitions of titin immunoglobulin domain under constant forces. J. Am. Chem. Soc. 137:3540–46
     [Google Scholar]
  103. 103.
    Neuman KC, Lionnet T, Allemand JF. 2007. Single-molecule micromanipulation techniques. Annu. Rev. Mater. Res. 37:33–67
     [Google Scholar]
  104. 104.
    Bouchiat C, Wang MD, Allemand J, Strick T, Block SM, Croquette V. 1999. Estimating the persistence length of a worm-like chain molecule from force-extension measurements. Biophys. J. 76:409–13
     [Google Scholar]
  105. 105.
    Schaffer E, Norrelykke SF, Howard J. 2007. Surface forces and drag coefficients of microspheres near a plane surface measured with optical tweezers. Langmuir 23:3654–65
     [Google Scholar]
  106. 106.
    Wong WP, Halvorsen K. 2006. The effect of integration time on fluctuation measurements: calibrating an optical trap in the presence of motion blur. Opt. Express 14:12517–31
     [Google Scholar]
  107. 107.
    Ostrofet E, Papini FS, Dulin D. 2018. Correction-free force calibration for magnetic tweezers experiments. Sci. Rep. 8:15920
     [Google Scholar]
  108. 108.
    Klaue D, Seidel R. 2009. Torsional stiffness of single superparamagnetic microspheres in an external magnetic field. Phys. Rev. Lett. 102:028302
     [Google Scholar]
  109. 109.
    Otto O, Gutsche C, Kremer F, Keyser UF. 2008. Optical tweezers with 2.5 kHz bandwidth video detection for single-colloid electrophoresis. Rev. Sci. Instrum. 79:023710
     [Google Scholar]
  110. 110.
    Gibson GM, Leach J, Keen S, Wright AJ, Padgett MJ. 2008. Measuring the accuracy of particle position and force in optical tweezers using high-speed video microscopy. Opt. Express 16:14561–70
     [Google Scholar]
  111. 111.
    Otto O, Czerwinski F, Gornall JL, Stober G, Oddershede LB et al. 2010. Real-time particle tracking at 10,000 fps using optical fiber illumination. Opt. Express 18:22722–33
     [Google Scholar]
  112. 112.
    El-Desouki M, Deen MJ, Fang Q, Liu L, Tse F, Armstrong D 2009. CMOS image sensors for high speed applications. Sensors 9:430–44
     [Google Scholar]
  113. 113.
    Shon MJ, Rah SH, Yoon TY. 2019. Submicrometer elasticity of double-stranded DNA revealed by precision force-extension measurements with magnetic tweezers. Sci. Adv. 5:eaav1697
     [Google Scholar]
  114. 114.
    Dulin D, Barland S, Hachair X, Pedaci F. 2014. Efficient illumination for microsecond tracking microscopy. PLOS ONE 9:e107335
     [Google Scholar]
  115. 115.
    Cnossen JP, Dulin D, Dekker NH. 2014. An optimized software framework for real-time, high-throughput tracking of spherical beads. Rev. Sci. Instrum. 85:103712
     [Google Scholar]
  116. 116.
    De Vlaminck I, Henighan T, van Loenhout MT, Pfeiffer I, Huijts J et al. 2011. Highly parallel magnetic tweezers by targeted DNA tethering. Nano Lett 11:5489–93
     [Google Scholar]
  117. 117.
    Allan DW. 1966. Statistics of atomic frequency standards. Proc. IEEE 54:221–30
     [Google Scholar]
  118. 118.
    Czerwinski F, Richardson AC, Oddershede LB. 2009. Quantifying noise in optical tweezers by Allan variance. Opt. Express 17:13255–69
     [Google Scholar]
  119. 119.
    Rico F, Gonzalez L, Casuso I, Puig-Vidal M, Scheuring S. 2013. High-speed force spectroscopy unfolds titin at the velocity of molecular dynamics simulations. Science 342:741–43
     [Google Scholar]
  120. 120.
    Seol Y, Li J, Nelson PC, Perkins TT, Betterton MD. 2007. Elasticity of short DNA molecules: theory and experiment for contour lengths of 0.6–7 μm. Biophys. J. 93:4360–73
     [Google Scholar]
  121. 121.
    Shon MJ, Kim H, Yoon TY. 2018. Focused clamping of a single neuronal SNARE complex by complexin under high mechanical tension. Nat. Commun. 9:3639
     [Google Scholar]
  122. 122.
    Kim C, Shon MJ, Kim SH, Eun GS, Ryu JK et al. 2021. Extreme parsimony in ATP consumption by 20S complexes in the global disassembly of single SNARE complexes. Nat. Commun. 12:3206
     [Google Scholar]
  123. 123.
    Janissen R, Berghuis BA, Dulin D, Wink M, van Laar T, Dekker NH. 2014. Invincible DNA tethers: covalent DNA anchoring for enhanced temporal and force stability in magnetic tweezers experiments. Nucleic Acids Res 42:e137
     [Google Scholar]
  124. 124.
    Dietz H, Berkemeier F, Bertz M, Rief M. 2006. Anisotropic deformation response of single protein molecules. PNAS 103:12724–28
     [Google Scholar]
  125. 125.
    van Noort SJ, van der Werf KO, Eker AP, Wyman C, de Grooth BG et al. 1998. Direct visualization of dynamic protein-DNA interactions with a dedicated atomic force microscope. Biophys. J. 74:2840–49
     [Google Scholar]
  126. 126.
    Synakewicz M, Bauer D, Rief M, Itzhaki LS. 2019. Bioorthogonal protein-DNA conjugation methods for force spectroscopy. Sci. Rep. 9:13820
     [Google Scholar]
  127. 127.
    England CG, Luo H, Cai W. 2015. HaloTag technology: a versatile platform for biomedical applications. Bioconjug. Chem. 26:975–86
     [Google Scholar]
  128. 128.
    Popa I, Rivas-Pardo JA, Eckels EC, Echelman DJ, Badilla CL et al. 2016. A HaloTag anchored ruler for week-long studies of protein dynamics. J. Am. Chem. Soc. 138:10546–53
     [Google Scholar]
  129. 129.
    Rivas-Pardo JA, Eckels EC, Popa I, Kosuri P, Linke WA, Fernandez JM. 2016. Work done by titin protein folding assists muscle contraction. Cell Rep 14:1339–47
     [Google Scholar]
  130. 130.
    Tapia-Rojo R, Alonso-Caballero A, Fernandez JM 2020. Talin folding as the tuning fork of cellular mechanotransduction. PNAS 117:21346–53
     [Google Scholar]
  131. 131.
    Tapia-Rojo R, Alonso-Caballero A, Fernandez JM 2020. Direct observation of a coil-to-helix contraction triggered by vinculin binding to talin. Sci. Adv. 6:eaaz4707
     [Google Scholar]
  132. 132.
    Spadaro D, Le S, Laroche T, Mean I, Jond L et al. 2017. Tension-dependent stretching activates ZO-1 to control the junctional localization of its interactors. Curr. Biol. 27:3783–95.e8
     [Google Scholar]
  133. 133.
    Le S, Hu X, Yao M, Chen H, Yu M et al. 2017. Mechanotransmission and mechanosensing of human alpha-actinin 1. Cell Rep. 21:2714–23
     [Google Scholar]
  134. 134.
    Yu M, Zhao Z, Chen Z, Le S, Yan J 2020. Modulating mechanical stability of heterodimerization between engineered orthogonal helical domains. Nat. Commun. 11:4476
     [Google Scholar]
  135. 135.
    Zakeri B, Fierer JO, Celik E, Chittock EC, Schwarz-Linek U et al. 2012. Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. PNAS 109:E690–97
     [Google Scholar]
  136. 136.
    Min D, Arbing MA, Jefferson RE, Bowie JU. 2016. A simple DNA handle attachment method for single molecule mechanical manipulation experiments. Protein Sci 25:1535–44
     [Google Scholar]
  137. 137.
    Kriegel F, Ermann N, Lipfert J. 2017. Probing the mechanical properties, conformational changes, and interactions of nucleic acids with magnetic tweezers. J. Struct. Biol. 197:26–36
     [Google Scholar]
  138. 138.
    Shi Z, Graber ZT, Baumgart T, Stone HA, Cohen AE. 2018. Cell membranes resist flow. Cell 175:1769–79.e13
     [Google Scholar]
  139. 139.
    Linke WA. 2018. Titin gene and protein functions in passive and active muscle. Annu. Rev. Physiol. 80:389–411
     [Google Scholar]
  140. 140.
    Leake MC, Wilson D, Gautel M, Simmons RM. 2004. The elasticity of single titin molecules using a two-bead optical tweezers assay. Biophys. J. 87:1112–35
     [Google Scholar]
  141. 141.
    Eckels EC, Tapia-Rojo R, Rivas-Pardo JA, Fernández JM. 2018. The work of titin protein folding as a major driver in muscle contraction. Annu. Rev. Physiol. 80:327–51
     [Google Scholar]
  142. 142.
    Parsons JT, Horwitz AR, Schwartz MA. 2010. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 11:633–43
     [Google Scholar]
  143. 143.
    Yu M, Yuan X, Lu C, Le S, Kawamura R et al. 2017. mDia1 senses both force and torque during F-actin filament polymerization. Nat. Commun. 8:1650
     [Google Scholar]
  144. 144.
    Le S, Yu M, Hovan L, Zhao Z, Ervasti J et al. 2018. Dystrophin as a molecular shock absorber. ACS Nano 12:12140–48
     [Google Scholar]
  145. 145.
    Plaxco KW, Dobson CM. 1996. Time-resolved biophysical methods in the study of protein folding. Curr. Opin. Struct. Biol. 6:630–36
     [Google Scholar]
  146. 146.
    Feng H, Vu ND, Zhou Z, Bai Y. 2004. Structural examination of Φ-value analysis in protein folding. Biochemistry 43:14325–31
     [Google Scholar]
  147. 147.
    Oesterhelt F, Oesterhelt D, Pfeiffer M, Engel A, Gaub HE, Müller DJ. 2000. Unfolding pathways of individual bacteriorhodopsins. Science 288:143–46
     [Google Scholar]
  148. 148.
    Hoffmann A, Neupane K, Woodside MT. 2013. Single-molecule assays for investigating protein misfolding and aggregation. Phys. Chem. Chem. Phys. 15:7934–48
     [Google Scholar]
  149. 149.
    Guttula D, Yao M, Baker K, Yang L, Goult BT et al. 2019. Calcium-mediated protein folding and stabilization of Salmonella biofilm-associated protein A. J. Mol. Biol. 431:433–43
     [Google Scholar]
  150. 150.
    Haldar S, Tapia-Rojo R, Eckels EC, Valle-Orero J, Fernandez JM. 2017. Trigger factor chaperone acts as a mechanical foldase. Nat. Commun. 8:668
     [Google Scholar]
  151. 151.
    Cheng Y. 2018. Membrane protein structural biology in the era of single particle cryo-EM. Curr. Opin. Struct. Biol. 52:58–63
     [Google Scholar]
  152. 152.
    Quistgaard EM, Low C, Guettou F, Nordlund P. 2016. Understanding transport by the major facilitator superfamily (MFS): structures pave the way. Nat. Rev. Mol. Cell Biol. 17:123–32
     [Google Scholar]
  153. 153.
    Locher KP. 2016. Mechanistic diversity in ATP-binding cassette (ABC) transporters. Nat. Struct. Mol. Biol. 23:487–93
     [Google Scholar]
  154. 154.
    Guna A, Hegde RS. 2018. Transmembrane domain recognition during membrane protein biogenesis and quality control. Curr. Biol. 28:R498–511
     [Google Scholar]
  155. 155.
    Jumper J, Evans R, Pritzel A, Green T, Figurnov M et al. 2021. Highly accurate protein structure prediction with AlphaFold. Nature 596:583–89
     [Google Scholar]
  156. 156.
    Baek M, DiMaio F, Anishchenko I, Dauparas J, Ovchinnikov S et al. 2021. Accurate prediction of protein structures and interactions using a three-track neural network. Science 373:871–76
     [Google Scholar]
/content/journals/10.1146/annurev-biochem-032620-104637
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High-Resolution Single-Molecule Magnetic Tweezers
Annual Review of Biochemistry 91, 33 (2022); https://doi.org/10.1146/annurev-biochem-032620-104637
/content/journals/10.1146/annurev-biochem-032620-104637
/content/journals/10.1146/annurev-biochem-032620-104637
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