Quantifying forces in cell biology

Nature Cell Biology

Volumn 19, Issue 7, 2017, Pages 742-751

  Roca Cusachs, Pere ^a,b   Conte, Vito ^a   Trepat, Xavier ^a,b,c,d  

^a INSTITUTE FOR BIOENGINEERING OF CATALONIA IBEC   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^d BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSENSOR; CANTILEVER; CELL FUNCTION; CELL STRUCTURE; CELL SURFACE; CYTOLOGY; DATA ANALYSIS SOFTWARE; EXTRACELLULAR MATRIX; FLUORESCENCE RESONANCE ENERGY TRANSFER; GEOMETRIC FORCE INFERENCE; LASER; MICROPILLAR; MICROSCOPY; MONOLAYER STRESS MICROSCOPY; PRIORITY JOURNAL; REVIEW; SIGNAL NOISE RATIO; TRACTION MICROSCOPY; ANIMAL; BIOLOGICAL MODEL; BIOMECHANICS; CELL MEMBRANE; CYTOSKELETON; GENETIC PROCEDURES; HUMAN; MECHANICAL STRESS; MECHANOTRANSDUCTION; PHYSIOLOGY; PROCEDURES; SINGLE CELL ANALYSIS;

ANIMALS; BIOMECHANICAL PHENOMENA; BIOSENSING TECHNIQUES; CELL BIOLOGY; CELL MEMBRANE; CYTOSKELETON; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MICROSCOPY; MODELS, BIOLOGICAL; SINGLE-CELL ANALYSIS; STRESS, MECHANICAL;

EID: 85021775122     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3564     Document Type: Review

References (152)

1. Thompson, D. A. W. On Growth and Form 2nd edn (Cambridge Univ. Press, 1942).
2. Murray, C. D. The physiological principle of minimum work: II. Oxygen exchange in capillaries. Proc. Natl Acad. Sci. USA 12, 299-304 (1926).
3. Wolff, J. The Law of Bone Remodeling (Springer, 1986).
4. Chambers, R. Microdissection studies. II. The cell aster: a reversible gelation phenomenon. J. Exp. Zool. 23, 483-505 (1917).
5. Crick, F. H. C. & Hughes, A . F. W. The physical properties of cytoplasm. Exp. Cell. Res. 1, 37-80 (1950).
6. Paluch, E. K. et al. Mechanotransduction: use the force(s). BMC Biol. 13, 47 (2015).
7. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006).
8. Farge, E. Mechanical induction of Twist in the Drosophila foregut/stomodeal primordium. Curr. Biol. 13, 1365-1377 (2003).
9. Bosveld, F. et al. Mechanical control of morphogenesis by Fat/Dachsous/Four-jointed planar cell polarity pathway. Science 336, 724-727 (2012).
10. Sunyer, R. et al. Collective cell durotaxis emerges from long-range intercellular force transmission. Science 353, 1157-1161 (2016).
11. Miroshnikova, Y. A. et al. Tissue mechanics promote IDH1-dependent HIF1-tenascin C feedback to regulate glioblastoma aggression. Nat. Cell Biol. 18, 1336-1345 (2016).
12. Riveline, D. et al. Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J. Cell Biol. 153, 1175-1186 (2001).
13. Yonemura, S., Wada, Y., Watanabe, T., Nagafuchi, A. & Shibata, M.-Catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 12, 533-542 (2010).
14. Sinha, B. et al. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 144, 402-413 (2011).
15. Swift, J. et al. Nuclear laminA scales with tissue stiffness and enhances matrix-directed differentiation. Science 341, 1240104 (2013).
16. Elosegui-Artola, A. et al. Mechanical regulation of a molecular clutch defines force transmission and transduction in response to matrix rigidity. Nat. Cell Biol. 18, 540-548 (2016).
17. Schwarz, U. S. & Gardel, M. L. United we stand: integrating the actin cytoskeleton and cell-matrix adhesions in cellular mechanotransduction. J. Cell Sci. 125, 3051-3060 (2012).
18. Polacheck, W. J. & Chen, C. S. Measuring cell-generated forces: a guide to the available tools. Nat. Methods 13, 415-423 (2016).
19. Sugimura, K., Lenne, P. F. & Graner, F. Measuring forces and stresses in situ in living tissues. Development 143, 186-196 (2016).
20. Campas, O. A toolbox to explore the mechanics of living embryonic tissues. Semin. Cell Dev. Biol. 55, 119-130 (2016).
21. Dembo, M. & Wang, Y. L. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys. J. 76, 2307-2316 (1999).
22. Polio, S. R. et al. Topographical control of multiple cell adhesion molecules for traction force microscopy. Integr. Biol. (Camb.) 6, 357-365 (2014).
23. Bergert, M. et al. Confocal reference free traction force microscopy. Nat. Commun. 7, 12814 (2016).
24. Han, S. J., Oak, Y., Groisman, A. & Danuser, G. Traction microscopy to identify force modulation in subresolution adhesions. Nat. Methods 12, 653-656 (2015).
25. Ribeiro, A. J., Denisin, A. K., Wilson, R. E. & Pruitt, B. L. For whom the cells pull: hydrogel and micropost devices for measuring traction forces. Methods 94, 51-64 (2016).
26. Butler, J. P., Tolic-Norrelykke, I. M., Fabry, B. & Fredberg, J. J. Traction fields, moments, and strain energy that cells exert on their surroundings. Am. J. Physiol. Cell Physiol. 282, C595-C605 (2002).
27. Del Alamo, J. C. et al. Spatio-temporal analysis of eukaryotic cell motility by improved force cytometry. Proc. Natl Acad. Sci. USA 104, 13343-13348 (2007).
28. Trepat, X. et al. Physical forces during collective cell migration. Nat. Phys. 5, 426 (2009).
29. Ambrosi, D., Duperray, A., Peschetola, V. & Verdier, C. Traction patterns of tumor cells. J. Math. Biol. 58, 163-181 (2009).
30. Munoz, J. J. Non-regularised inverse finite element analysis for 3D traction force microscopy. Int. J. Numer. Anal. Model. 13, 763-781 (2016).
31. Sabass, B., Gardel, M. L., Waterman, C. M. & Schwarz, U. S. High resolution traction force microscopy based on experimental and computational advances. Biophys. J. 94, 207-220 (2008).
32. Brask, J. B., Singla-Buxarrais, G., Uroz, M., Vincent, R. & Trepat, X. Compressed sensing traction force microscopy. Acta Biomater. 26, 286-294 (2015).
33. Colin-York, H. et al. Super-resolved traction force microscopy (STFM). Nano Lett. 16, 2633-2638 (2016).
34. Bastounis, E. et al. Both contractile axial and lateral traction force dynamics drive amoeboid cell motility. J. Cell Biol. 204, 1045-1061 (2014).
35. Hur, S. S., Zhao, Y., Li, Y. S., Botvinick, E. & Chien, S. Live cells exert 3dimensional traction forces on their substrata. Cell Mol. Bioeng. 2, 425-436 (2009).
36. Toyjanova, J. et al. High resolution, large deformation 3D traction force microscopy. PLoS ONE 9, e90976 (2014).
37. Maskarinec, S. A., Franck, C., Tirrell, D. A. & Ravichandran, G. Quantifying cellular traction forces in three dimensions. Proc. Natl Acad. Sci. USA 106, 22108-22113 (2009).
38. Legant, W. R. et al. Measurement of mechanical tractions exerted by cells in three-dimensional matrices. Nat. Methods 7, 969-971 (2010).
39. Steinwachs, J. et al. Three-dimensional force microscopy of cells in biopolymer networks. Nat. Methods 13, 171-176 (2016).
40. Martiel, J. L. et al. Measurement of cell traction forces with ImageJ. Methods Cell Biol. 125, 269-287 (2015).
41. Style, R. W. et al. Traction force microscopy in physics and biology. Soft Matter 10, 4047-4055 (2014).
42. Schwarz, U. S. & Soine, J. R. Traction force microscopy on soft elastic substrates: a guide to recent computational advances. Biochim. Biophys. Acta 1853, 3095-3104 (2015).
43. Hutter, J. L. & Bechhoefer, J. Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 64, 1868-1873 (1993).
44. Tan, J. L. et al. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc. Natl Acad. Sci. USA 100, 1484-1489 (2003).
45. du Roure, O. et al. Force mapping in epithelial cell migration. Proc. Natl Acad. Sci. USA 102, 2390-2395 (2005).
46. Gupta, M. et al. Adaptive rheology and ordering of cell cytoskeleton govern matrix rigidity sensing. Nat. Commun. 6, 7525 (2015).
47. Ghassemi, S. et al. Cells test substrate rigidity by local contractions on sub-micrometer pillars. Proc. Natl Acad. Sci. USA 109, 5328-5333 (2012).
48. Wolfenson, H. et al. Tropomyosin controls sarcomere-like contractions for rigidity sensing and suppressing growth on soft matrices. Nat. Cell Biol. 18, 33-42 (2016).
49. Moore, S. W., Biais, N. & Sheetz, M. P. Traction on immobilized netrin1 is sufficient to reorient axons. Science 325, 166 (2009).
50. Biais, N., Higashi, D., So, M. & Ladoux, B. Techniques to measure pilus retraction forces. Methods Mol. Biol. 799, 197-216 (2012).
51. Saez, A., Ghibaudo, M., Buguin, A., Silberzan, P. & Ladoux, B. Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates. Proc. Natl Acad. Sci. USA 104, 8281-8286 (2007).
52. Lee, S., Hong, J. & Lee, J. Cell motility regulation on a stepped micro pillar array device (SMPAD) with a discrete stiffness gradient. Soft Matter 12, 2325-2333 (2016).
53. le Digabel, J. et al. Magnetic micropillars as a tool to govern substrate deformations. Lab Chip 11, 2630-2636 (2011).
54. Sniadecki, N. J. et al. Magnetic microposts as an approach to apply forces to living cells. Proc. Natl Acad. Sci. USA 104, 14553-14558 (2007).
55. Ghibaudo, M. et al. Traction forces and rigidity sensing regulate cell functions. Soft Matter 4, 1836-1843 (2008).
56. Taubenberger, A. V., Hutmacher, D. W. & Muller, D. J. Single-cell force spectroscopy, an emerging tool to quantify cell adhesion to biomaterials. Tissue Eng. Part B Rev. 20, 40-55 (2014).
57. Bufi, N., Durand-Smet, P. & Asnacios, A. Single-cell mechanics: the parallel plates technique. Methods Cell Biol. 125, 187-209 (2015).
58. Harris, A. R. et al. Characterizing the mechanics of cultured cell monolayers. Proc. Natl Acad. Sci. USA 109, 16449-16454 (2012).
59. Rajagopalan, J. & Saif, M. T. MEMS sensors and microsystems for cell mechanobiology. J. Micromech. Microeng. 21, 54002-54012 (2011).
60. Campas, O. et al. Quantifying cell-generated mechanical forces within living embryonic tissues. Nat. Methods 11, 183-189 (2014).
61. Serwane, F. et al. In vivo quantification of spatially varying mechanical properties in developing tissues. Nat. Methods 14, 181-186 (2017).
62. Dolega, M. E. et al. Cell-like pressure sensors reveal increase of mechanical stress towards the core of multicellular spheroids under compression. Nat. Commun. 8, 14056 (2017).
63. Jurchenko, C. & Salaita, K. S. Lighting up the force: investigating mechanisms of mechanotransduction using fluorescent tension probes. Mol. Cell Biol. 35, 2570-2582 (2015).
64. Meng, F., Suchyna, T. M. & Sachs, F. A fluorescence energy transfer-based mechanical stress sensor for specific proteins in situ. FEBS J. 275, 3072-3087 (2008).
65. Iwai, S. & Uyeda, T. Q. Visualizing myosin-actin interaction with a genetically-encoded fluorescent strain sensor. Proc. Natl Acad. Sci. USA 105, 16882-16887 (2008).
66. Grashoff, C. et al. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466, 263266 (2010).
67. Austen, K. et al. Extracellular rigidity sensing by talin isoform-specific mechanical linkages. Nat. Cell Biol. 17, 1597-1606 (2015).
68. Borghi, N. et al. Ecadherin is under constitutive actomyosin-generated tension that is increased at cell-cell contacts upon externally applied stretch. Proc. Natl Acad. Sci. USA 109, 12568-12573 (2012).
69. Cai, D. et al. Mechanical feedback through Ecadherin promotes direction sensing during collective cell migration. Cell 157, 1146-1159.
70. Conway, D. E. et al. Fluid shear stress on endothelial cells modulates mechanical tension across VEcadherin and PECAM1. Curr. Biol. 23, 1024-1030 (2013).
71. Morimatsu, M., Mekhdjian, A. H., Adhikari, A. S. & Dunn, A. R. Molecular tension sensors report forces generated by single integrin molecules in living cells. Nano Lett. 13, 3985-3989 (2013).
72. Zhang, Y., Ge, C., Zhu, C. & Salaita, K. DNA-based digital tension probes reveal integrin forces during early cell adhesion. Nat. Commun. 5, 5167 (2014).
73. Blakely, B. L. et al. A DNA-based molecular probe for optically reporting cellular traction forces. Nat. Methods 11, 1229-1232 (2014).
74. Chang, A. C. et al. Single molecule force measurements in living cells reveal a minimally tensioned integrin state. ACS Nano 10, 10745-10752 (2016).
75. Woodside, M. T. et al. Nanomechanical measurements of the sequence-dependent folding landscapes of single nucleic acid hairpins. Proc. Natl Acad. Sci. USA 103, 6190-6195 (2006).
76. Wang, X. & Ha, T. Defining single molecular forces required to activate integrin and notch signaling. Science 340, 991-994 (2013).
77. Rahil, Z. et al. Nanoscale mechanics guides cellular decision making. Integr. Biol. 8, 929-935 (2016).
78. Galior, K., Liu, Y., Yehl, K., Vivek, S. & Salaita, K. Titin-based nanoparticle tension sensors map high-magnitude integrin forces within focal adhesions. Nano Lett. 16, 341-348 (2016).
79. Wang, N. et al. Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am. J. Physiol. Cell Physiol. 282, C606-C616 (2002).
80. Liu, Z. et al. Mechanical tugging force regulates the size of cell-cell junctions. Proc. Natl Acad. Sci. USA 107, 9944-9949 (2010).
81. Maruthamuthu, V., Sabass, B., Schwarz, U. S. & Gardel, M. L. Cell-ECM traction force modulates endogenous tension at cell-cell contacts. Proc. Natl Acad. Sci. USA 108, 4708-4713 (2011).
82. Ng, M. R., Besser, A., Brugge, J. S. & Danuser, G. Mapping the dynamics of force transduction at cell-cell junctions of epithelial clusters. eLife 3, e03282 (2014).
83. Tambe, D. T. et al. Collective cell guidance by cooperative intercellular forces. Nat. Mater. 10, 469-475 (2011).
84. Lamason, R. L. et al. Rickettsia Sca4 reduces vinculin-mediated intercellular tension to promote spread. Cell 167, 670-683. e10 (2016).
85. Das, T. et al. A molecular mechanotransduction pathway regulates collective migration of epithelial cells. Nat. Cell Biol. 17, 276-287 (2015).
86. Trepat, X. & Fredberg, J. J. Plithotaxis and emergent dynamics in collective cellular migration. Trends Cell Biol. 21, 638-646 (2011).
87. Tambe, D. T. et al. Monolayer stress microscopy: limitations, artifacts, and accuracy of recovered intercellular stresses. PLoS ONE 8, e55172 (2013).
88. Zimmermann, J. et al. Intercellular stress reconstitution from traction force data. Biophys. J. 107, 548-554 (2014).
89. Nier, V. et al. Inference of internal stress in a cell monolayer. Biophys. J. 110, 1625-1635 (2016).
90. Serra-Picamal, X., Conte, V., Sunyer, R., Muñoz, J. J. & Trepat, X. in Biophysical Methods in Cell Biology Vol. 125. (ed. Paluch, E. K.) 309-330 (Academic Press, 2015).
91. Serra-Picamal, X. et al. Mechanical waves during tissue expansion. Nat. Phys. 8, 628-634 (2012).
92. Soine, J. R. et al. Model-based traction force microscopy reveals differential tension in cellular actin bundles. PLoS Comput. Biol. 11, e1004076 (2015).
93. Colombelli, J. et al. Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization. J. Cell Sci. 122, 1665-1679 (2009).
94. Grill, S. W., Gonczy, P., Stelzer, E. H. K. & Hyman, A. A. Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409, 630-633 (2001).
95. Kumar, S. et al. Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys. J. 90, 3762-3773 (2006).
96. Fernandez-Gonzalez, R., Simoes, S. d. M., Röper, J. C., Eaton, S. & Zallen, J. A. Myosin II dynamics are regulated by tension in intercalating cells. Dev. Cell 17, 736-743 (2009).
97. Kasza, K. E., Farrell, D. L. & Zallen, J. A. Spatiotemporal control of epithelial remodeling by regulated myosin phosphorylation. Proc. Natl Acad. Sci. USA 111, 11732-11737 (2014).
98. Landsberg, K. P. et al. Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary. Curr. Biol. 19, 1950-1955 (2009).
99. LeGoff, L., Rouault, H. & Lecuit, T. A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila. Development 140, 4051-4059 (2013).
100. Rauzi, M., Verant, P., Lecuit, T. & Lenne, P. F. Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat. Cell Biol. 10, 1401-1410 (2008).
101. Porazinski, S. et al. YAP is essential for tissue tension to ensure vertebrate 3D body shape. Nature 521, 217-221 (2015).
102. Campinho, P. et al. Tension-oriented cell divisions limit anisotropic tissue tension in epithelial spreading during zebrafish epiboly. Nat. Cell Biol. 15, 1405-1414 (2013).
103. Davis, J. R. et al. Inter-cellular forces orchestrate contact inhibition of locomotion. Cell 161, 361-373 (2015).
104. Samarage, C. R. et al. Cortical tension allocates the first inner cells of the mammalian embryo. Dev. Cell 34, 435-447 (2015).
105. Bonnet, I. et al. Mechanical state, material properties and continuous description of an epithelial tissue. J. R. Soc. Interface 9, 2614-2623 (2012).
106. Hutson, M. S. et al. Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300, 145-149 (2003).
107. Hutson, M. S. et al. Combining laser microsurgery and finite element modeling to assess cell-level epithelial mechanics. Biophys. J. 97, 3075-3085 (2009).
108. Kiehart, D. P., Galbraith, C. G., Edwards, K. A., Rickoll, W. L. & Montague, R. A. Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J. Cell Biol. 149, 471-490 (2000).
109. Martin, A. C., Gelbart, M., Fernandez-Gonzalez, R., Kaschube, M. & Wieschaus, E. F. Integration of contractile forces during tissue invagination. J. Cell Biol. 188, 735-749 (2010).
110. Scarcelli, G. et al. Noncontact three-dimensional mapping of intracellular hydromechanical properties by Brillouin microscopy. Nat. Methods 12, 1132-1134 (2015).
111. Moeendarbary, E. et al. The cytoplasm of living cells behaves as a poroelastic material. Nat. Mater. 12, 253-261 (2013).
112. Brodland, G. W. et al. CellFIT: a cellular force-inference toolkit using curvilinear cell boundaries. PLoS ONE 9, e99116 (2014).
113. Chiou, K. K., Hufnagel, L. & Shraiman, B. I. Mechanical stress inference for two dimensional cell arrays. PLoS Comput. Biol. 8, e1002512 (2012).
114. Guirao, B. et al. Unified quantitative characterization of epithelial tissue development. eLife 4, e08519 (2015).
115. Ishihara, S. & Sugimura, K. Bayesian inference of force dynamics during morphogenesis. J. Theor. Biol. 313, 201-211 (2012).
116. Sugimura, K. & Ishihara, S. The mechanical anisotropy in a tissue promotes ordering in hexagonal cell packing. Development 140, 4091-4101 (2013).
117. Veldhuis, J. H. et al. Inferring cellular forces from image stacks. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372, 20160261 (2017).
118. Etournay, R. et al. TissueMiner: a multiscale analysis toolkit to quantify how cellular processes create tissue dynamics. eLife 5, e14334 (2016).
119. Maitre, J. L. et al. Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 338, 253-256 (2012).
120. Brodland, G. W. et al. Video force microscopy reveals the mechanics of ventral furrow invagination in Drosophila. Proc. Natl Acad. Sci. USA 107, 22111-22116 (2010).
121. Mayer, M., Depken, M., Bois, J. S., Julicher, F. & Grill, S. W. Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 467, 617-621 (2010).
122. Sedzinski, J. et al. Polar actomyosin contractility destabilizes the position of the cytokinetic furrow. Nature 476, 462-466 (2011).
123. Roca-Cusachs, P., Iskratsch, T. & Sheetz, M. P. Finding the weakest link-exploring integrin-mediated mechanical molecular pathways. J. Cell Sci. 125, 30253038 (2012).
124. Alam, S., Lovett, D. B., Dickinson, R. B., Roux, K. J. & Lele, T. P. Nuclear forces and cell mechanosensing. Prog. Mol. Biol. Transl. Sci. 126, 205-215 (2014).
125. Han, M. K. & de Rooij, J. Converging and unique mechanisms of mechanotransduction at adhesion sites. Trends Cell Biol. 26, 612-623 (2016).
126. Chen, Y., Lee, H., Tong, H., Schwartz, M. & Zhu, C. Force regulated conformational change of integrin V3. Matrix Biol. 60-61, 70-85 (2016).
127. Ehrlicher, A. J., Nakamura, F., Hartwig, J. H., Weitz, D. A. & Stossel, T. P. Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A. Nature 478, 260-263 (2011).
128. Yao, M. et al. The mechanical response of talin. Nat. Commun. 7, 11966 (2016).
129. Kong, F., Garcia, A. J., Mould, A. P., Humphries, M. J. & Zhu, C. Demonstration of catch bonds between an integrin and its ligand. J. Cell Biol. 185, 1275-1284 (2009).
130. Coste, B. et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330, 55-60 (2010).
131. Wu, J., Goyal, R. & Grandl, J. Localized force application reveals mechanically sensitive domains of Piezo1. Nat. Commun. 7, 12939 (2016).
132. del Rio, A. et al. Stretching single talin rod molecules activates vinculin binding. Science 323, 638-641 (2009).
133. Yao, M. et al. Force-dependent conformational switch of ?-catenin controls vinculin binding. Nat. Commun. 5, 4525 (2014).
134. Rivas-Pardo, J. A. et al. Work done by titin protein folding assists muscle contraction. Cell Rep. 14, 1339-1347 (2016).
135. Kinoshita, K., Leung, A., Simon, S. & Evans, E. Long-lived, high-strength states of ICAM1 bonds to 2 integrin, II: lifetimes of LFA1 bonds under force in leukocyte signaling. Biophys. J. 98, 1467-1475 (2010).
136. Ju, L., Chen, Y., Xue, L., Du, X. & Zhu, C. Cooperative unfolding of distinctive mechanoreceptor domains transduces force into signals. eLife 5, e15447 (2016).
137. Margadant, F. et al. Mechanotransduction in vivo by repeated talin stretch-relaxation events depends upon vinculin. PLoS Biol. 9, e1001223 (2011).
138. Klotzsch, E. et al. Fibronectin forms the most extensible biological fibers displaying switchable force-exposed cryptic binding sites. Proc. Natl Acad. Sci. USA 106, 1826718272 (2009).
139. Kubow, K. E. et al. Mechanical forces regulate the interactions of fibronectin and collagen I in extracellular matrix. Nat. Commun. 6, 8026 (2015).
140. Krieger, C. C. et al. Cysteine shotgun-mass spectrometry (CS-MS) reveals dynamic sequence of protein structure changes within mutant and stressed cells. Proc. Natl Acad. Sci. USA 108, 8269-8274 (2011).
141. Yao, M. et al. Mechanical activation of vinculin binding to talin locks talin in an unfolded conformation. Sci. Rep. 4, 4610 (2014).
142. Plotnikov, S. V., Pasapera, A. M., Sabass, B. & Waterman, C. M. Force fluctuations within focal adhesions mediate ECM-rigidity sensing to guide directed cell migration. Cell 151, 1513-1527 (2012).
143. Elosegui-Artola, A. et al. Rigidity sensing and adaptation through regulation of integrin types. Nat. Mater. 13, 631-637 (2014).
144. Lewis, A. H. & Grandl, J. Mechanical sensitivity of Piezo1 ion channels can be tuned by cellular membrane tension. eLife 4, e12088 (2015).
145. Na, S. et al. Rapid signal transduction in living cells is a unique feature of mechanotransduction. Proc. Natl Acad. Sci. USA 105, 6626-6631 (2008).
146. Case, L. B. et al. Molecular mechanism of vinculin activation and nanoscale spatial organization in focal adhesions. Nat. Cell Biol. 17, 880-892 (2015).
147. Dupont, S. et al. Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183 (2011).
148. Roca-Cusachs, P., Gauthier, N. C., del Rio, A. & Sheetz, M. P. Clustering of 51 integrins determines adhesion strength whereas v3 and talin enable mechanotransduction. Proc. Natl Acad. Sci. USA 106, 16245-16250 (2009).
149. Jiang, G. Y., Giannone, G., Critchley, D. R., Fukumoto, E. & Sheetz, M. P. Two-piconewton slip bond between fibronectin and the cytoskeleton depends on talin. Nature 424, 334-337 (2003).
150. Seo, D. et al. A mechanogenetic toolkit for interrogating cell signaling in space and time. Cell 165, 1507-1518 (2016).
151. Mitrossilis, D. et al. Single-cell response to stiffness exhibits muscle-like behavior. Proc. Natl Acad. Sci. USA 106, 18243-18248 (2009).
152. Veldhuis, J. H., Mashburn, D., Hutson, M. S. & Brodland, G. W. Practical aspects of the cellular force inference toolkit (CellFIT). Methods Cell Biol. 125, 331-351 (2015).