1932

Abstract

The ability of cells to generate mechanical forces, but also to sense, adapt to, and respond to mechanical signals, is crucial for many developmental, postnatal homeostatic, and pathophysiological processes. However, the molecular mechanisms underlying cellular mechanotransduction have remained elusive for many decades, as techniques to visualize and quantify molecular forces across individual proteins in cells were missing. The development of genetically encoded molecular tension sensors now allows the quantification of piconewton-scale forces that act upon distinct molecules in living cells and even whole organisms. In this review, we discuss the physical principles, advantages, and limitations of this increasingly popular method. By highlighting current examples from the literature, we demonstrate how molecular tension sensors can be utilized to obtain access to previously unappreciated biophysical parameters that define the propagation of mechanical forces on molecular scales. We discuss how the methodology can be further developed and provide a perspective on how the technique could be applied to uncover entirely novel aspects of mechanobiology in the future.

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2021-05-06
2024-05-19
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Literature Cited

  1. 1. 
    Acharya BR, Wu SK, Lieu ZZ, Parton RG, Grill SW et al. 2017. Mammalian diaphanous 1 mediates a pathway for E-cadherin to stabilize epithelial barriers through junctional contractility. Cell Rep 18:122854–67
    [Google Scholar]
  2. 2. 
    Adli M. 2018. The CRISPR tool kit for genome editing and beyond. Nat. Commun. 9:1911
    [Google Scholar]
  3. 3. 
    Akula SM, Pramod NP, Wang FZ, Chandran B. 2002. Integrin alpha 3 beta 1 (CD 49c/29) is a cellular receptor for Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) entry into the target cells. Cell 108:3407–19
    [Google Scholar]
  4. 4. 
    Algar WR, Hildebrandt N, Vogel SS, Medintz IL. 2019. FRET as a biomolecular research tool—understanding its potential while avoiding pitfalls. Nat. Methods 16:9815–29
    [Google Scholar]
  5. 5. 
    Alsteens D, Newton R, Schubert R, Martinez-Martin D, Delguste M et al. 2017. Nanomechanical mapping of first binding steps of a virus to animal cells. Nat. Nanotechnol. 12:2177–83
    [Google Scholar]
  6. 6. 
    Antonacci G, Beck T, Bilenca A, Czarske J, Elsayad K et al. 2020. Recent progress and current opinions in Brillouin microscopy for life science applications. Biophys. Rev. 12:3615–24
    [Google Scholar]
  7. 7. 
    Antonacci G, Braakman S. 2016. Biomechanics of subcellular structures by non-invasive Brillouin microscopy. Sci. Rep. 6:37217
    [Google Scholar]
  8. 8. 
    Arbore C, Perego L, Sergides M, Capitanio M. 2019. Probing force in living cells with optical tweezers: from single-molecule mechanics to cell mechanotransduction. Biophys. Rev. 11:5765–82
    [Google Scholar]
  9. 9. 
    Arsenovic PT, Ramachandran I, Bathula K, Zhu RJ, Narang JD et al. 2016. Nesprin-2G, a component of the nuclear LINC complex, is subject to myosin-dependent tension. Biophys. J. 110:134–43
    [Google Scholar]
  10. 10. 
    Austen K, Kluger C, Freikamp A, Chrostek-Grashoff A, Grashoff C. 2013. Generation and analysis of biosensors to measure mechanical forces within cells. Methods Mol. Biol. 1066:169–84
    [Google Scholar]
  11. 11. 
    Austen K, Ringer P, Mehlich A, Chrostek-Grashoff A, Kluger C et al. 2015. Extracellular rigidity sensing by talin isoform-specific mechanical linkages. Nat. Cell Biol. 17:121597–606
    [Google Scholar]
  12. 12. 
    Batty P, Gerlich DW. 2019. Mitotic chromosome mechanics: how cells segregate their genome. Trends Cell Biol 29:9717–26
    [Google Scholar]
  13. 13. 
    Becker N, Oroudjev E, Mutz S, Cleveland JP, Hansma PK et al. 2003. Molecular nanosprings in spider capture-silk threads. Nat. Mater. 2:4278–83
    [Google Scholar]
  14. 14. 
    Blakely BL, Dumelin CE, Trappmann B, McGregor LM, Choi CK et al. 2014. A DNA-based molecular probe for optically reporting cellular traction forces. Nat. Methods 11:121229–32
    [Google Scholar]
  15. 15. 
    Borghi N, Sorokina M, Shcherbakova OG, Weis WI, Pruitt BL et al. 2012. E-cadherin is under constitutive actomyosin-generated tension that is increased at cell-cell contacts upon externally applied stretch. PNAS 109:3112568–73
    [Google Scholar]
  16. 16. 
    Braam J. 2005. In touch: plant responses to mechanical stimuli. New Phytol 165:2373–89
    [Google Scholar]
  17. 17. 
    Brenner MD, Zhou R, Conway DE, Lanzano L, Gratton E et al. 2016. Spider silk peptide is a compact, linear nanospring ideal for intracellular tension sensing. Nano Lett 16:32096–102
    [Google Scholar]
  18. 18. 
    Brockman JM, Su H, Blanchard AT, Duan Y, Meyer T et al. 2020. Live-cell super-resolved PAINT imaging of piconewton cellular traction forces. Nat. Methods 17:101018–24
    [Google Scholar]
  19. 19. 
    Brodland GW, Veldhuis JH, Kim S, Perrone M, Mashburn D, Hutson MS. 2014. CellFIT: a cellular force-inference toolkit using curvilinear cell boundaries. PLOS ONE 9:6e99116
    [Google Scholar]
  20. 20. 
    Chang CW, Kumar S. 2013. Vinculin tension distributions of individual stress fibers within cell-matrix adhesions. J. Cell Sci. 126:Pt. 143021–30
    [Google Scholar]
  21. 21. 
    Cocco S, Monasson R, Marko JF 2001. Force and kinetic barriers to unzipping of the DNA double helix. PNAS 98:158608–13
    [Google Scholar]
  22. 22. 
    Colom A, Derivery E, Soleimanpour S, Tomba C, Dal Molin M et al. 2018. A fluorescent membrane tension probe. Nat. Chem. 10:111118–25
    [Google Scholar]
  23. 23. 
    Conway DE, Breckenridge MT, Hinde E, Gratton E, Chen CS, Schwartz MA. 2013. Fluid shear stress on endothelial cells modulates mechanical tension across VE-cadherin and PECAM-1. Curr. Biol. 23:111024–30
    [Google Scholar]
  24. 24. 
    Cost AL, Khalaji S, Grashoff C. 2019. Genetically encoded FRET-based tension sensors. Curr. Protoc. Cell Biol. 83:1e85
    [Google Scholar]
  25. 25. 
    Cost AL, Ringer P, Chrostek-Grashoff A, Grashoff C. 2015. How to measure molecular forces in cells: a guide to evaluating genetically-encoded FRET-based tension sensors. Cell Mol. Bioeng. 8:196–105
    [Google Scholar]
  26. 26. 
    Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:54181318–22
    [Google Scholar]
  27. 27. 
    Critchley DR. 2009. Biochemical and structural properties of the integrin-associated cytoskeletal protein talin. Annu. Rev. Biophys. 38:235–54
    [Google Scholar]
  28. 28. 
    Dahl-Jensen S, Grapin-Botton A. 2017. The physics of organoids: a biophysical approach to understanding organogenesis. Development 144:6946–51
    [Google Scholar]
  29. 29. 
    de Pascalis C, Etienne-Manneville S. 2017. Single and collective cell migration: the mechanics of adhesions. Mol. Biol. Cell 28:141833–46
    [Google Scholar]
  30. 30. 
    Déjardin T, Carollo PS, Sipieter F, Davidson PM, Seiler C et al. 2020. Nesprins are mechanotransducers that discriminate epithelial-mesenchymal transition programs. J. Cell Biol. 219:10e201908036
    [Google Scholar]
  31. 31. 
    Demeautis C, Sipieter F, Roul J, Chapuis C, Padilla-Parra S et al. 2017. Multiplexing PKA and ERK1&2 kinases FRET biosensors in living cells using single excitation wavelength dual colour FLIM. Sci. Rep. 7:41026
    [Google Scholar]
  32. 32. 
    Dietz H, Rief M 2004. Exploring the energy landscape of GFP by single-molecule mechanical experiments. PNAS 101:4616192–97
    [Google Scholar]
  33. 33. 
    Fang J, Mehlich A, Koga N, Huang J, Koga R et al. 2013. Forced protein unfolding leads to highly elastic and tough protein hydrogels. Nat. Commun. 4:2974
    [Google Scholar]
  34. 34. 
    Faure LM, Fiche J-B, Espinosa L, Ducret A, Anantharaman V et al. 2016. The mechanism of force transmission at bacterial focal adhesion complexes. Nature 539:7630530–35
    [Google Scholar]
  35. 35. 
    Ferrari A. 2019. Recent technological advancements in traction force microscopy. Biophys. Rev. 11:5679–81
    [Google Scholar]
  36. 36. 
    Fraley SI, Feng Y, Krishnamurthy R, Kim DH, Celedon A et al. 2010. A distinctive role for focal adhesion proteins in three-dimensional cell motility. Nat. Cell Biol. 12:6598–604
    [Google Scholar]
  37. 37. 
    Freikamp A, Cost AL, Grashoff C. 2016. The piconewton force awakens: quantifying mechanics in cells. Trends Cell Biol 26:11838–47
    [Google Scholar]
  38. 38. 
    Freikamp A, Mehlich A, Klingner C, Grashoff C. 2016. Investigating piconewton forces in cells by FRET-based molecular force microscopy. J. Struct. Biol. 197:137–42
    [Google Scholar]
  39. 39. 
    Galior K, Liu Y, Yehl K, Vivek S, Salaita K. 2016. Titin-based nanoparticle tension sensors map high-magnitude integrin forces within focal adhesions. Nano Lett 16:1341–48
    [Google Scholar]
  40. 40. 
    Ganim Z, Rief M 2017. Mechanically switching single-molecule fluorescence of GFP by unfolding and refolding. PNAS 114:4211052–56
    [Google Scholar]
  41. 41. 
    Gates EM, LaCroix AS, Rothenberg KE, Hoffman BD. 2019. Improving quality, reproducibility, and usability of FRET-based tension sensors. Cytom. A 95:2201–13
    [Google Scholar]
  42. 42. 
    Gayrard C, Bernaudin C, Dejardin T, Seiler C, Borghi N. 2018. Src- and confinement-dependent FAK activation causes E-cadherin relaxation and beta-catenin activity. J. Cell Biol. 217:31063–77
    [Google Scholar]
  43. 43. 
    Geitmann A, Ortega JKE. 2009. Mechanics and modeling of plant cell growth. Trends Plant Sci 14:9467–78
    [Google Scholar]
  44. 44. 
    Goldstein B, King N. 2016. The future of cell biology: emerging model organisms. Trends Cell Biol 26:11818–24
    [Google Scholar]
  45. 45. 
    Gotzke H, Kilisch M, Martinez-Carranza M, Sograte-Idrissi S, Rajavel A et al. 2019. The ALFA-tag is a highly versatile tool for nanobody-based bioscience applications. Nat. Commun. 10:4403
    [Google Scholar]
  46. 46. 
    Grashoff C, Hoffman BD, Brenner MD, Zhou R, Parsons M et al. 2010. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466:7303263–66
    [Google Scholar]
  47. 47. 
    Guilluy C, Osborne LD, van Landeghem L, Sharek L, Superfine R et al. 2014. Isolated nuclei adapt to force and reveal a mechanotransduction pathway within the nucleus. Nat. Cell Biol. 16:4376–81
    [Google Scholar]
  48. 48. 
    Gwosch KC, Pape JK, Balzarotti F, Hoess P, Ellenberg J et al. 2020. MINFLUX nanoscopy delivers 3D multicolor nanometer resolution in cells. Nat. Methods 17:2217–24
    [Google Scholar]
  49. 49. 
    Haining AWM, von Essen M, Attwood SJ, Hytonen VP, Hernandez AD. 2016. All subdomains of the talin rod are mechanically vulnerable and may contribute to cellular mechanosensing. ACS Nano 10:76648–58
    [Google Scholar]
  50. 50. 
    Hamant O, Haswell ES. 2017. Life behind the wall: sensing mechanical cues in plants. BMC Biol. 15:159
    [Google Scholar]
  51. 51. 
    Hamilton ES, Schlegel AM, Haswell ES. 2015. United in diversity: mechanosensitive ion channels in plants. Annu. Rev. Plant Biol. 66:113–37
    [Google Scholar]
  52. 52. 
    Hernández-Varas P, Berge U, Lock JG, Strömblad S. 2015. A plastic relationship between vinculin-mediated tension and adhesion complex area defines adhesion size and lifetime. Nat. Commun. 6:7524
    [Google Scholar]
  53. 53. 
    Hirano S, Yamamoto T, Michiue T. 2018. FRET-based tension measurement across actin-associated mechanotransductive structures using Lima1. Int. J. Dev. Biol. 62:9–10631–36
    [Google Scholar]
  54. 54. 
    Hoffman BD, Grashoff C, Schwartz MA. 2011. Dynamic molecular processes mediate cellular mechanotransduction. Nature 475:7356316–23
    [Google Scholar]
  55. 55. 
    Huang DL, Bax NA, Buckley CD, Weis WI, Dunn AR. 2017. Vinculin forms a directionally asymmetric catch bond with F-actin. Science 357:6352703–6
    [Google Scholar]
  56. 56. 
    Hussein HA, Walker LR, Abdel-Raouf UM, Desouky SA, Montasser AK, Akula SM. 2015. Beyond RGD: virus interactions with integrins. Arch. Virol. 160:112669–81
    [Google Scholar]
  57. 57. 
    Ichimura T, Fujita H, Yoshizawa K, Watanabe TM. 2012. Engineering strain-sensitive yellow fluorescent protein. Chem. Commun. 48:637871–73
    [Google Scholar]
  58. 58. 
    Jaalouk DE, Lammerding J. 2009. Mechanotransduction gone awry. Nat. Rev. Mol. Cell Biol. 10:163–73
    [Google Scholar]
  59. 59. 
    Jagannathan B, Marqusee S. 2013. Protein folding and unfolding under force. Biopolymers 99:11860–69
    [Google Scholar]
  60. 60. 
    Jares-Erijman EA, Jovin TM 2003. FRET imaging. Nat. Biotechnol. 21:111387–95
    [Google Scholar]
  61. 61. 
    Julicher F, Grill SW, Salbreux G. 2018. Hydrodynamic theory of active matter. Rep. Prog. Phys. 81:7076601
    [Google Scholar]
  62. 62. 
    Jungmann R, Avendano MS, Dai M, Woehrstein JB, Agasti SS et al. 2016. Quantitative super-resolution imaging with qPAINT. Nat. Methods 13:5439–42
    [Google Scholar]
  63. 63. 
    Kambe Y, Kojima K, Tomita N, Tamada Y, Yamaoka T. 2016. Development of a FRET-based recombinant tension sensor to visualize cell-material interactions. J. Mater. Chem. B 4:4649–55
    [Google Scholar]
  64. 64. 
    Kanoldt V, Fischer L, Grashoff C. 2019. Unforgettable force—crosstalk and memory of mechanosensitive structures. Biol. Chem. 400:6687–98
    [Google Scholar]
  65. 65. 
    Krieg M, Dunn AR, Goodman MB. 2014. Mechanical control of the sense of touch by β-spectrin. Nat. Cell Biol. 16:3224–33
    [Google Scholar]
  66. 66. 
    Krieg M, Fläschner G, Alsteens D, Gaub BM, Roos WH et al. 2019. Atomic force microscopy-based mechanobiology. Nat. Rev. Phys. 1:141–57
    [Google Scholar]
  67. 67. 
    Kronenberg NM, Liehm P, Steude A, Knipper JA, Borger JG et al. 2017. Long-term imaging of cellular forces with high precision by elastic resonator interference stress microscopy. Nat. Cell Biol. 19:7864–72
    [Google Scholar]
  68. 68. 
    Kubow KE, Horwitz AR. 2011. Reducing background fluorescence reveals adhesions in 3D matrices. Nat. Cell Biol. 13:1 3–5; author reply 5–7
    [Google Scholar]
  69. 69. 
    Kumar A, Ouyang M, van den Dries K, McGhee EJ, Tanaka K et al. 2016. Talin tension sensor reveals novel features of focal adhesion force transmission and mechanosensitivity. J. Cell Biol. 213:3371–83
    [Google Scholar]
  70. 70. 
    LaCroix AS, Lynch AD, Berginski ME, Hoffman BD. 2018. Tunable molecular tension sensors reveal extension-based control of vinculin loading. eLife 7:e33927
    [Google Scholar]
  71. 71. 
    Ladoux B, Mege RM. 2017. Mechanobiology of collective cell behaviours. Nat. Rev. Mol. Cell Biol. 18:12743–57
    [Google Scholar]
  72. 72. 
    Lagendijk AK, Gomez GA, Baek S, Hesselson D, Hughes WE et al. 2017. Live imaging molecular changes in junctional tension upon VE-cadherin in zebrafish. Nat. Commun. 8:1402
    [Google Scholar]
  73. 73. 
    Legant WR, Miller JS, Blakely BL, Cohen DM, Genin GM, Chen CS. 2010. Measurement of mechanical tractions exerted by cells in three-dimensional matrices. Nat. Methods 7:12969–71
    [Google Scholar]
  74. 74. 
    Lemke SB, Weidemann T, Cost AL, Grashoff C, Schnorrer F. 2019. A small proportion of talin molecules transmit forces at developing muscle attachments in vivo. PLOS Biol 17:3e3000057
    [Google Scholar]
  75. 75. 
    Li FJ, Chen A, Reeser A, Wang Y, Fan Y et al. 2019. Vinculin force sensor detects tumor-osteocyte interactions. Sci. Rep. 9:5615
    [Google Scholar]
  76. 76. 
    Li Q, Guan XH, Wu P, Wang XY, Zhou L et al. 2020. Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia. N. Engl. J. Med. 382:131199–207
    [Google Scholar]
  77. 77. 
    Li WH, Moore MJ, Vasilieva N, Sui JH, Wong SK et al. 2003. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:6965450–54
    [Google Scholar]
  78. 78. 
    Liehm P, Kronenberg NM, Gather MC. 2018. Analysis of the precision, robustness, and speed of elastic resonator interference stress microscopy. Biophys. J. 114:92180–93
    [Google Scholar]
  79. 79. 
    Lin YC, Guo YR, Miyagi A, Levring J, MacKinnon R, Scheuring S. 2019. Force-induced conformational changes in PIEZO1. Nature 573:7773230–34
    [Google Scholar]
  80. 80. 
    Liu Y, Yehl K, Narui Y, Salaita K. 2013. Tension sensing nanoparticles for mechano-imaging at the living/nonliving interface. J. Am. Chem. Soc. 135:145320–23
    [Google Scholar]
  81. 81. 
    Meng F, Sachs F. 2011. Visualizing dynamic cytoplasmic forces with a compliance-matched FRET sensor. J. Cell Sci. 124:Pt. 2261–69
    [Google Scholar]
  82. 82. 
    Meng F, Sachs F. 2012. Orientation-based FRET sensor for real-time imaging of cellular forces. J. Cell Sci. 125:Pt. 3743–50
    [Google Scholar]
  83. 83. 
    Meng F, Suchyna TM, Sachs F. 2008. A fluorescence energy transfer-based mechanical stress sensor for specific proteins in situ. FEBS J 275:123072–87
    [Google Scholar]
  84. 84. 
    Milles LF, Schulten K, Gaub HE, Bernardi RC. 2018. Molecular mechanism of extreme mechanostability in a pathogen adhesin. Science 359:63831527–33
    [Google Scholar]
  85. 85. 
    Mongera A, Rowghanian P, Gustafson HJ, Shelton E, Kealhofer DA et al. 2018. A fluid-to-solid jamming transition underlies vertebrate body axis elongation. Nature 561:7723401–5
    [Google Scholar]
  86. 86. 
    Morimatsu M, Mekhdjian AH, Adhikari AS, Dunn AR. 2013. Molecular tension sensors report forces generated by single integrin molecules in living cells. Nano Lett 13:93985–89
    [Google Scholar]
  87. 87. 
    Morimatsu M, Mekhdjian AH, Chang AC, Tan SJ, Dunn AR. 2015. Visualizing the interior architecture of focal adhesions with high-resolution traction maps. Nano Lett 15:42220–28
    [Google Scholar]
  88. 88. 
    Mosayebi M, Louis AA, Doye JPK, Ouldridge TE. 2015. Force-induced rupture of a DNA duplex: from fundamentals to force sensors. ACS Nano 9:1211993–2003
    [Google Scholar]
  89. 89. 
    Mueller DJ, Dufrene YF. 2011. Atomic force microscopy: a nanoscopic window on the cell surface. Trends Cell Biol 21:8461–69
    [Google Scholar]
  90. 90. 
    Murakoshi H, Shibata ACE, Nakahata Y, Nabekura J. 2015. A dark green fluorescent protein as an acceptor for measurement of Förster resonance energy transfer. Sci. Rep. 5:15334
    [Google Scholar]
  91. 91. 
    Nordenfelt P, Elliott HL, Springer TA. 2016. Coordinated integrin activation by actin-dependent force during T-cell migration. Nat. Commun. 7:13119
    [Google Scholar]
  92. 92. 
    Ossola D, Amarouch M-Y, Behr P, Vörös J, Abriel H, Zambelli T. 2015. Force-controlled patch clamp of beating cardiac cells. Nano Lett 15:31743–50
    [Google Scholar]
  93. 93. 
    Pasapera AM, Schneider IC, Rericha E, Schlaepfer DD, Waterman CM. 2010. Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation. J. Cell Biol. 188:6877–90
    [Google Scholar]
  94. 94. 
    Perez-Jimenez R, Alonso-Caballero A, Berkovich R, Franco D, Chen M-W et al. 2014. Probing the effect of force on HIV-1 receptor CD4. ACS Nano 8:1010313–20
    [Google Scholar]
  95. 95. 
    Petridou NI, Spiro Z, Heisenberg CP. 2017. Multiscale force sensing in development. Nat. Cell Biol. 19:6581–88
    [Google Scholar]
  96. 96. 
    Plotnikov SV, Pasapera AM, Sabass B, Waterman CM. 2012. Force fluctuations within focal adhesions mediate ECM-rigidity sensing to guide directed cell migration. Cell 151:71513–27
    [Google Scholar]
  97. 97. 
    Polacheck WJ, Chen CS. 2016. Measuring cell-generated forces: a guide to the available tools. Nat. Methods 13:5415–23
    [Google Scholar]
  98. 98. 
    Prevedel R, Diz-Munoz A, Ruocco G, Antonacci G. 2019. Brillouin microscopy: an emerging tool for mechanobiology. Nat. Methods 16:10969–77
    [Google Scholar]
  99. 99. 
    Price AJ, Cost AL, Ungewiss H, Waschke J, Dunn AR, Grashoff C. 2018. Mechanical loading of desmosomes depends on the magnitude and orientation of external stress. Nat. Commun. 9:5284
    [Google Scholar]
  100. 100. 
    Rakshit S, Zhang Y, Manibog K, Shafraz O, Sivasankar S 2012. Ideal, catch, and slip bonds in cadherin adhesion. PNAS 109:4618815–20
    [Google Scholar]
  101. 101. 
    Ringer P, Weissl A, Cost AL, Freikamp A, Sabass B et al. 2017. Multiplexing molecular tension sensors reveals piconewton force gradient across talin-1. Nat. Methods 14:111090–96
    [Google Scholar]
  102. 102. 
    Roca-Cusachs P, Conte V, Trepat X. 2017. Quantifying forces in cell biology. Nat. Cell Biol. 19:7742–51
    [Google Scholar]
  103. 103. 
    Rossier O, Octeau V, Sibarita JB, Leduc C, Tessier B et al. 2012. Integrins beta1 and beta3 exhibit distinct dynamic nanoscale organizations inside focal adhesions. Nat. Cell Biol. 14:101057–67
    [Google Scholar]
  104. 104. 
    Rothenberg KE, Scott DW, Christoforou N, Hoffman BD. 2018. Vinculin force-sensitive dynamics at focal adhesions enable effective directed cell migration. Biophys. J. 114:71680–94
    [Google Scholar]
  105. 105. 
    Sabass B, Gardel ML, Waterman CM, Schwarz US. 2008. High resolution traction force microscopy based on experimental and computational advances. Biophys. J. 94:1207–20
    [Google Scholar]
  106. 106. 
    Sarangi BR, Gupta M, Doss BL, Tissot N, Lam F et al. 2017. Coordination between intra- and extracellular forces regulates focal adhesion dynamics. Nano Lett 17:1399–406
    [Google Scholar]
  107. 107. 
    Schierbaum N, Rheinlaender J, Schaffer TE. 2019. Combined atomic force microscopy (AFM) and traction force microscopy (TFM) reveals a correlation between viscoelastic material properties and contractile prestress of living cells. Soft Matter 15:81721–29
    [Google Scholar]
  108. 108. 
    Shang J, Ye G, Shi K, Wan YS, Luo CM et al. 2020. Structural basis of receptor recognition by SARS-CoV-2. Nature 581:7807221–24
    [Google Scholar]
  109. 109. 
    Shcherbakova DM, Hink MA, Joosen L, Gadella TWJ, Verkhusha VV. 2012. An orange fluorescent protein with a large Stokes shift for single-excitation multicolor FCCS and FRET imaging. J. Am. Chem. Soc. 134:187913–23
    [Google Scholar]
  110. 110. 
    Shih H-W, Miller ND, Dai C, Spalding EP, Monshausen GB. 2014. The receptor-like kinase FERONIA is required for mechanical signal transduction in Arabidopsis seedlings. Curr. Biol. 24:161887–92
    [Google Scholar]
  111. 111. 
    Sim JY, Moeller J, Hart KC, Ramallo D, Vogel V et al. 2015. Spatial distribution of cell-cell and cell-ECM adhesions regulates force balance while maintaining E-cadherin molecular tension in cell pairs. Mol. Biol. Cell 26:132456–65
    [Google Scholar]
  112. 112. 
    Smith AE, Helenius A. 2004. How viruses enter animal cells. Science 304:5668237–42
    [Google Scholar]
  113. 113. 
    Smith JT, Yao R, Sinsuebphon N, Rudkouskaya A, Un N et al. 2019. Fast fit-free analysis of fluorescence lifetime imaging via deep learning. PNAS 116:4824019–30
    [Google Scholar]
  114. 114. 
    Staufer O, Schröter M, Platzman I, Spatz JP. 2020. Bottom-up assembly of functional intracellular synthetic organelles by droplet-based microfluidics. Small 16:27e1906424
    [Google Scholar]
  115. 115. 
    Steinwachs J, Metzner C, Skodzek K, Lang N, Thievessen I et al. 2016. Three-dimensional force microscopy of cells in biopolymer networks. Nat. Methods 13:2171–76
    [Google Scholar]
  116. 116. 
    Stigler J, Ziegler F, Gieseke A, Gebhardt JC, Rief M. 2011. The complex folding network of single calmodulin molecules. Science 334:6055512–16
    [Google Scholar]
  117. 117. 
    Sugimura K, Lenne PF, Graner F. 2016. Measuring forces and stresses in situ in living tissues. Development 143:2186–96
    [Google Scholar]
  118. 118. 
    Tao H, Zhu M, Lau K, Whitley OKW, Samani M et al. 2019. Oscillatory cortical forces promote three dimensional cell intercalations that shape the murine mandibular arch. Nat. Commun. 10:1703
    [Google Scholar]
  119. 119. 
    van Helvert S, Storm C, Friedl P. 2018. Mechanoreciprocity in cell migration. Nat. Cell Biol. 20:8–20
    [Google Scholar]
  120. 120. 
    Wang H, La Russa M, Qi LS 2016. CRISPR/Cas9 in genome editing and beyond. Annu. Rev. Biochem. 85:227–64
    [Google Scholar]
  121. 121. 
    Wang X, Ha T. 2013. Defining single molecular forces required to activate integrin and Notch signaling. Science 340:6135991–94
    [Google Scholar]
  122. 122. 
    Weitkunat M, Kaya-Copur A, Grill SW, Schnorrer F. 2014. Tension and force-resistant attachment are essential for myofibrillogenesis in Drosophila flight muscle. Curr. Biol. 24:7705–16
    [Google Scholar]
  123. 123. 
    Wiegand T, Fratini M, Frey F, Yserentant K, Liu Y et al. 2020. Forces during cellular uptake of viruses and nanoparticles at the ventral side. Nat. Commun. 11:32
    [Google Scholar]
  124. 124. 
    Woolfenden HC, Baillie AL, Gray JE, Hobbs JK, Morris RJ, Fleming AJ. 2018. Models and mechanisms of stomatal mechanics. Trends Plant Sci 23:9822–32
    [Google Scholar]
  125. 125. 
    Yao M, Goult BT, Klapholz B, Hu X, Toseland CP et al. 2016. The mechanical response of talin. Nat. Commun. 7:11966
    [Google Scholar]
  126. 126. 
    Zhang Y, Ge C, Zhu C, Salaita K. 2014. DNA-based digital tension probes reveal integrin forces during early cell adhesion. Nat. Commun. 5:5167
    [Google Scholar]
  127. 127. 
    Zoldak G, Stigler J, Pelz B, Li H, Rief M 2013. Ultrafast folding kinetics and cooperativity of villin headpiece in single-molecule force spectroscopy. PNAS 110:4518156–61
    [Google Scholar]
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