Molecular force spectroscopy on cells

Annual Review of Physical Chemistry

Volumn 66, Issue , 2015, Pages 427-451

  Liu, Baoyu ^a   Chen, Wei ^d,e   Zhu, Cheng ^a,b,c  

^a Wallace H Coulter Department of Biomedical Engineering   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^d School of Medicine   (United States)

^e ZHEJIANG UNIVERSITY   (China)

Author keywords

binding kinetics; catch bond; cell adhesion; cyclic mechanical reinforcement; force clamp; force ramp

Indexed keywords

BIOLOGICAL SYSTEMS; CELL ENGINEERING; MECHANISMS; MOLECULAR INTERACTIONS; MOLECULAR STRUCTURE; PHYSICAL CHEMISTRY;

BINDING KINETICS; CATCH BOND; CELLS ADHESION; CELLULAR FUNCTION; CYCLIC MECHANICAL REINFORCEMENT; FORCE CLAMP; FORCE RAMP; MECHANICAL; MECHANICAL REINFORCEMENT; MOLECULAR FORCE SPECTROSCOPY;

CELL ADHESION;

INTEGRIN;

ANIMAL; BIOMECHANICS; CELL ADHESION; CHEMISTRY; CYTOLOGY; HUMAN; MECHANOTRANSDUCTION; MICROTUBULE; PROCEDURES; SPECTROSCOPY;

ANIMALS; BIOMECHANICAL PHENOMENA; CELL ADHESION; CYTOLOGICAL TECHNIQUES; HUMANS; INTEGRINS; MECHANOTRANSDUCTION, CELLULAR; MICROTUBULES; SPECTRUM ANALYSIS;

EID: 84926454018     PISSN: 0066426X     EISSN: 15451593     Source Type: Book Series    
DOI: 10.1146/annurev-physchem-040214-121742     Document Type: Article

References (157)

1. Malmqvist M. 1993. Surface plasmon resonance for detection and measurement of antibody-antigen affinity and kinetics. Curr. Opin. Immunol. 5:282-86
2. Li P, Jiang N, Nagarajan S, Wohlhueter R, Selvaraj P, Zhu C. 2007. Affinity and kinetic analysis of Fc receptor IIIa (CD16a) binding to IgG ligands. J. Biol. Chem. 282:6210-21
3. O'Shannessy DJ. 1994. Determination of kinetic rate and equilibrium binding constants for macromolecular interactions: a critique of the surface plasmon resonance literature. Curr. Opin. Biotechnol. 5:65-71
4. Marshall BT, Long M, Piper JW, Yago T, McEver RP, Zhu C. 2003. Direct observation of catch bonds involving cell-adhesion molecules. Nature 423:190-93
5. Kong F, Li Z, Parks WM, Dumbauld DW, Garca AJ, et al. 2013. Cyclic mechanical reinforcement of integrin-ligand interactions. Mol. Cell 49:1060-68
6. Alon R, Hammer DA, Springer TA. 1995. Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature 374:539-42
7. Bell G. 1978. Models for the specific adhesion of cells to cells. Science 200:618-27
8. Dembo M, Torney DC, Saxman K, Hammer D. 1988. The reaction-limited kinetics of membrane-tosurface adhesion and detachment. Proc. R. Soc. Lond. B 234:55-83
9. Rakshit S, Zhang Y, Manibog K, Shafraz O, Sivasankar S. 2012. Ideal, catch, and slip bonds in cadherin adhesion. Proc. Natl. Acad. Sci. USA 109:18815-20
10. Marshall BT, Sarangapani KK, Lou JH, McEver RP, Zhu C. 2005. Force history dependence of receptorligand dissociation. Biophys. J. 88:1458-66
11. Guo B, Guilford WH. 2006. Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. Proc. Natl. Acad. Sci. USA 103:9844-49
12. Sarangapani KK, Qian J, Chen W, Zarnitsyna VI, Mehta P, et al. 2011. Regulation of catch bonds by rate of force application. J. Biol. Chem. 286:32749-61
13. Fiore VF, Ju L, Zhu C, Barker TH. 2014. Dynamic catch of a Thy-1-51 + syndecan-4 trimolecular complex. Nat. Commun. 5:4886
14. Kim J, Zhang CZ, Zhang X, Springer TA. 2010. A mechanically stabilized receptor-ligand flex-bond important in the vasculature. Nature 466:992-95
15. Binnig G, Quate CF, Gerber C. 1986. Atomic force microscope. Phys. Rev. Lett. 56:930-33
16. Evans E, Ritchie K, Merkel R. 1995. Sensitive force technique to probe molecular adhesion and structural linkages at biological interfaces. Biophys. J. 68:2580-87
17. 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
18. Neuman KC, Nagy A. 2008. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods 5:491-505
19. Evans E. 2001. Probing the relation between force-lifetime-and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 30:105-28
20. Chen W, Zarnitsyna VI, Sarangapani KK, Huang J, Zhu C. 2008. Measuring receptor-ligand binding kinetics on cell surfaces: from adhesion frequency to thermal fluctuation methods. Cell. Mol. Bioeng. 1:276-88
21. Evans E, Leung A, Hammer D, Simon S. 2001. Chemically distinct transition states govern rapid dissociation of single L-selectin bonds under force. Proc. Natl. Acad. Sci. USA 98:3784-89
22. Liu B, Chen W, Evavold BD, Zhu C. 2014. Accumulation of dynamic catch bonds between TCR and agonist peptide-MHC triggers T cell signaling. Cell 157:357-68
23. Zhu C, Long M, Chesla SE, Bongrand P. 2002. Measuring receptor/ligand interaction at the single-bond level: experimental and interpretative issues. Ann. Biomed. Eng. 30:305-14
24. Piper JW, Swerlick RA, Zhu C. 1998. Determining force dependence of two-dimensional receptor-ligand binding affinity by centrifugation. Biophys. J. 74:492-513
25. Chesla SE, Selvaraj P, Zhu C. 1998. Measuring two-dimensional receptor-ligand binding kinetics by micropipette. Biophys. J. 75:1553-72
26. Chen W, Lou J, Zhu C. 2010. Forcing switch from short-to intermediate-and long-lived states of the A domain generates LFA-1/ICAM-1 catch bonds. J. Biol. Chem. 285:35967-78
27. Liang J, Fernandez JM. 2009. Mechanochemistry: one bond at a time. ACS Nano 3:1628-45
28. Popa I, Kosuri P, Alegre-Cebollada J, Garcia-Manyes S, Fernandez JM. 2013. Force dependency of biochemical reactions measured by single-molecule force-clamp spectroscopy. Nat. Protoc. 8:1261-76
29. Rognoni L, Stigler J, Pelz B, Ylanne J, Rief M. 2012. Dynamic force sensing of filamin revealed in single-molecule experiments. Proc. Natl. Acad. Sci. USA 109:19679-84
30. Zhu C. 2014. Mechanochemistry: a molecular biomechanics view of mechanosensing. Ann. Biomed. Eng. 42:388-404
31. Vogel V, Sheetz M. 2006. Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell Biol. 7:265-75
32. Wang N, Tytell JD, Ingber DE. 2009. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10:75-82
33. Mammoto T, Mammoto A, Ingber DE. 2013. Mechanobiology and developmental control. Annu. Rev. Cell Dev. Biol. 29:27-61
34. Schoen I, Pruitt BL, Vogel V. 2013. The yin-yang of rigidity sensing: how forces and mechanical properties regulate the cellular response to materials. Annu. Rev. Mater. Res. 43:589-618
35. Hoffman BD, Grashoff C, Schwartz MA. 2011. Dynamic molecular processes mediate cellular mechanotransduction. Nature 475:316-23
36. Lou J, Zhu C. 2007. A structure-based sliding-rebinding mechanism for catch bonds. Biophys. J. 92:1471-85
37. Lou J, Yago T, Klopocki AG, Mehta P, Chen W, et al. 2006. Flow-enhanced adhesion regulated by a selectin interdomain hinge. J. Cell Biol. 174:1107-17
38. Klopocki AG, Yago T, Mehta P, Yang J, Wu T, et al. 2008. Replacing a lectin domain residue in Lselectin enhances binding to P-selectin glycoprotein ligand-1 but not to 6-sulfo-sialyl Lewis X. J. Biol. Chem. 283:11493-500
39. Kang YY, Lu SQ, Ren P, Huo B, Long M. 2012. Molecular dynamics simulation of shear-and stretchinduced dissociation of P-selectin/PSGL-1 complex. Biophys. J. 102:112-20
40. Le Trong I, Aprikian P, Kidd BA, Forero-Shelton M, Tchesnokova V, et al. 2010. Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like sheet twisting. Cell 141:645-55
41. Manibog K, Li H, Rakshit S, Sivasankar S. 2014. Resolving the molecular mechanism of cadherin catch bond formation. Nat. Commun. 5:3941
42. Lee CY, Lou JZ, Wen KK, McKane M, Eskin SG, et al. 2013. Actin depolymerization under force is governed by lysine 113:glutamic acid 195-mediated catch-slip bonds. Proc. Natl. Acad. Sci. USA110:5022-27
43. Lu SQ, Zhang Y, Long MA. 2010. Visualization of allostery in P-selectin lectin domain using MD simulations. PLoS ONE 5:e15417
44. Yago T, Lou J, Wu T, Yang J, Miner JJ, et al. 2008. Platelet glycoprotein Ibforms catch bonds with human WT vWF but not with type 2B von Willebrand disease vWF. J. Clin. Invest. 118:3195-207
45. Lee SE, Chunsrivirot S, Kamm RD, Mofrad MRK. 2008. Molecular dynamics study of talin-vinculin binding. Biophys. J. 95:2027-36
46. Hytonen VP, Vogel V. 2008. How force might activate talin's vinculin binding sites: SMD reveals a structural mechanism. PLoS Comput. Biol. 4:e24
47. 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
48. Ebner A, Nevo R, Rankl C, Preiner J, Gruber H, et al. 2009. Probing the energy landscape of proteinbinding reactions by dynamic force spectroscopy. In Handbook of Single-Molecule Biophysics, ed. P Hinterdorfer, A van Oijen, pp. 407-47. New York: Springer
49. Woodside MT, Block SM. 2014. Reconstructing folding energy landscapes by single-molecule force spectroscopy. Annu. Rev. Biophys. 43:19-39
50. Zoldak G, Rief M. 2013. Force as a single molecule probe of multidimensional protein energy landscapes. Curr. Opin. Struct. Biol. 23:48-57
51. Galera-Prat A, Gomez-Sicilia A, Oberhauser AF, Cieplak M, Carrion-Vazquez M. 2010. Understanding biology by stretching proteins: recent progress. Curr. Opin. Struct. Biol. 20:63-69
52. Ritzefeld M, Walhorn V, Anselmetti D, Sewald N. 2013. Analysis of DNA interactions using singlemolecule force spectroscopy. Amino Acids 44:1457-75
53. Dangkulwanich M, Ishibashi T, Bintu L, Bustamante C. 2014. Molecular mechanisms of transcription through single-molecule experiments. Chem. Rev. 114:3203-23
54. Kaiser CM, Tinoco I. 2014. Probing the mechanisms of translation with force. Chem. Rev. 114:3266-80
55. Chaurasiya KR, Paramanathan T, McCauley MJ, Williams MC. 2010. Biophysical characterization of DNA binding from single molecule force measurements. Phys. Life Rev. 7:299-341
56. Puchner EM, Gaub HE. 2012. Single-molecule mechanoenzymatics. Annu. Rev. Biophys. 41:497-518
57. Alegre-Cebollada J, Perez-Jimenez R, Kosuri P, Fernandez JM. 2010. Single-molecule force spectroscopy approach to enzyme catalysis. J. Biol. Chem. 285:18961-66
58. Guo J, Sachs F, Meng F. 2014. Fluorescence-based force/tension sensors: a novel tool to visualize mechanical forces in structural proteins in live cells. Antioxid. Redox Signal. 20:986-99
59. Wang X, Ha T. 2013. Defining single molecular forces required to activate integrin and notch signaling. Science 340:991-94
60. Moy VT, Florin EL, Gaub HE. 1994. Intermolecular forces and energies between ligands and receptors. Science 266:257-59
61. Florin EL, Moy VT, Gaub HE. 1994. Adhesion forces between individual ligand-receptor pairs. Science 264:415-17
62. Evans E, Ritchie K. 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541-55
63. Merkel R, Nassoy P, Leung A, Ritchie K, Evans E. 1999. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 397:50-53
64. Gergely C, Voegel JC, Schaaf P, Senger B, Maaloum M, et al. 2000. Unbinding process of adsorbed proteins under external stress studied by atomic force microscopy spectroscopy. Proc. Natl. Acad. Sci. USA 97:10802-7
65. Zhu C. 2000. Kinetics and mechanics of cell adhesion. J. Biomech. 33:23-33
66. Zhang XH, Bogorin DF, Moy VT. 2004. Molecular basis of the dynamic strength of the sialyl Lewis X-selectin interaction. ChemPhysChem 5:175-82
67. Hanley W, McCarty O, Jadhav S, Tseng Y, Wirtz D, Konstantopoulos K. 2003. Single molecule characterization of P-selectin/ligand binding. J. Biol. Chem. 278:10556-61
68. Evans E, Kinoshita K, Simon S, Leung A. 2010. Long-lived, high-strength states of ICAM-1 bonds to 2 integrin, I: lifetimes of bonds to recombinant L2 under force. Biophys. J. 98:1458-66
69. Zhang XH, Wojcikiewicz E, Moy VT. 2002. Force spectroscopy of the leukocyte function-associated antigen-1/intercellular adhesion molecule-1 interaction. Biophys. J. 83:2270-79
70. Zhang X, Craig SE, Kirby H, Humphries MJ, Moy VT. 2004. Molecular basis for the dynamic strength of the integrin 41/VCAM-1 interaction. Biophys. J. 87:3470-78
71. Li F, Redick SD, Erickson HP, Moy VT. 2003. Force measurements of the 51 integrin-fibronectin interaction. Biophys. J. 84:1252-62
72. DobrowskyTM, Rabi SA, NedellecR, Daniels BR, Mullins JI, et al. 2013. Adhesion and fusion efficiencies of human immunodeficiency virus type 1 (HIV-1) surface proteins. Sci. Rep. 3:3014
73. Chang MI, Panorchan P, Dobrowsky TM, Tseng Y, Wirtz D. 2005. Single-molecule analysis of human immunodeficiency virus type 1 gp120-receptor interactions in living cells. J. Virol. 79:14748-55
74. Yu JP, Wang Q, Shi XL, Ma XY, Yang HY, et al. 2007. Single-molecule force spectroscopy study of interaction between transforming growth factor 1 and its receptor in living cells. J. Phys. Chem. B 111:13619-25
75. Sasuga S, Abe R, Nikaido O, Kiyosaki S, Sekiguchi H, et al. 2012. Interaction between pheromone and its receptor of the fission yeast Schizosaccharomyces pombe examined by a force spectroscopy study. J. Biomed. Biotechnol. 2012:804793
76. Zhang J, Wu GM, Song CL, Li YJ, Qiao HY, et al. 2012. Single molecular recognition force spectroscopy study of a luteinizing hormone-releasing hormone analogue as a carcinoma target drug. J. Phys. Chem. B 116:13331-37
77. Whited AM, Park PSH. 2014. Atomic force microscopy: a multifaceted tool to study membrane proteins and their interactions with ligands. Biochim. Biophys. Acta 1838:56-68
78. Pierres A, Benoliel AM, Bongrand P, van der Merwe PA. 1996. Determination of the lifetime and force dependence of interactions of single bonds between surface-attached CD2 and CD48 adhesion molecules. Proc. Natl. Acad. Sci. USA 93:15114-18
79. Kong F, Garca AJ, Mould AP, Humphries MJ, Zhu C. 2009. Demonstration of catch bonds between an integrin and its ligand. J. Cell Biol. 185:1275-84
80. Sarangapani KK, Yago T, Klopocki AG, Lawrence MB, Fieger CB, et al. 2004. Low force decelerates L-selectin dissociation from P-selectin glycoprotein ligand-1 and endoglycan. J. Biol. Chem. 279:2291-98
81. Evans E. 1998. Energy landscapes of biomolecular adhesion and receptor anchoring at interfaces explored with dynamic force spectroscopy. Faraday Discuss. 111:1-16
82. Evans E. 1999. Looking inside molecular bonds at biological interfaces with dynamic force spectroscopy. Biophys. Chem. 82:83-97
83. Evans E, Heinrich V, Ludwig F, Rawicz W. 2003. Dynamic tension spectroscopy and strength of biomembranes. Biophys. J. 85:2342-50
84. Finger EB, Puri KD, Alon R, Lawrence MB, von Andrian UH, Springer TA. 1996. Adhesion through L-selectin requires a threshold hydrodynamic shear. Nature 379:266-69
85. Lawrence MB, Kansas GS, Kunkel EJ, Ley K. 1997. Threshold levels of fluid shear promote leukocyte adhesion through selectins (CD62L, P, E). J. Cell Biol. 136:717-27
86. Savage B, Saldivar E, Ruggeri ZM. 1996. Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor. Cell 84:289-97
87. Thomas WE, Trintchina E, Forero M, Vogel V, Sokurenko EV. 2002. Bacterial adhesion to target cells enhanced by shear force. Cell 109:913-23
88. Yago T, Wu JH, Wey CD, Klopocki AG, Zhu C, McEver RP. 2004. Catch bonds govern adhesion through L-selectin at threshold shear. J. Cell Biol. 166:913-23
89. Wayman AM, Chen W, McEver RP, Zhu C. 2010. Triphasic force dependence of E-selectin/ligand dissociation governs cell rolling under flow. Biophys. J. 99:1166-74
90. Ju L, Dong JF, Cruz MA, Zhu C. 2013. The N-terminal flanking region of the A1 domain regulates the force-dependent binding of von Willebrand factor to platelet glycoprotein Ib. J. Biol. Chem. 288:32289-301
91. Yakovenko O, Sharma S, Forero M, Tchesnokova V, Aprikian P, et al. 2008. FimH forms catch bonds that are enhanced by mechanical force due to allosteric regulation. J. Biol. Chem. 283:11596-605
92. Zhu C, Yago T, Lou J, Zarnitsyna V, McEver R. 2008. Mechanisms for flow-enhanced cell adhesion. Ann. Biomed. Eng. 36:604-21
93. McEver RP, Zhu C. 2010. Rolling cell adhesion. Annu. Rev. Cell Dev. Biol. 26:363-96
94. Chen W, Lou J, Evans EA, Zhu C. 2012. Observing force-regulated conformational changes and ligand dissociation from a single integrin on cells. J. Cell Biol. 199:497-512
95. Choi YI, Duke-Cohan JS, Chen W, Liu B, Rossy J, et al. 2014. Dynamic control of 1 integrin adhesion by the plexinD1-sema3E axis. Proc. Natl. Acad. Sci. USA 111:379-84
96. Laakso JM, Lewis JH, Shuman H, Ostap EM. 2008. Myosin I can act as a molecular force sensor. Science 321:133-36
97. Akiyoshi B, Sarangapani KK, Powers AF, Nelson CR, Reichow SL, et al. 2010. Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468:576-79
98. Arya M, Kolomeisky AB, Romo GM, Cruz MA, Lopez JA, Anvari B. 2005. Dynamic force spectroscopy of glycoprotein Ib-IX and von Willebrand factor. Biophys. J. 88:4391-401
99. Evans E, Leung A, Heinrich V, Zhu C. 2004. Mechanical switching and coupling between two dissociation pathways in a P-selectin adhesion bond. Proc. Natl. Acad. Sci. USA 101:11281-86
100. Dudko OK, Hummer G, Szabo A. 2008. Theory, analysis, and interpretation of single-molecule force spectroscopy experiments. Proc. Natl. Acad. Sci. USA 105:15755-60
101. Isralewitz B, Baudry J, Gullingsrud J, Kosztin D, Schulten K. 2001. Steered molecular dynamics investigations of protein function. J. Mol. Graph. Model. 19:13-25
102. Liu GJ, Fang Y, Wu JH. 2013. A mechanism for localized dynamics-driven affinity regulation of the binding of von Willebrand factor to platelet glycoprotein Ib. J. Biol. Chem. 288:26658-67
103. Thomas WE, Vogel V, Sokurenko E. 2008. Biophysics of catch bonds. Annu. Rev. Biophys. 37:399-416
104. Aprikian P, Tchesnokova V, Kidd B, Yakovenko O, Yarov-Yarovoy V, et al. 2007. Interdomain interaction in the FimH adhesin of Escherichia coli regulates the affinity to mannose. J. Biol. Chem. 282:23437-46
105. Bouckaert J, Berglund J, Schembri M, De Genst E, Cools L, et al. 2005. Receptor binding studies disclose a novel class of high-affinity inhibitors of the Escherichia coli FimH adhesin. Mol. Microbiol. 55:441-55
106. Xiang X, Lee CY, Li T, Chen W, Lou J, Zhu C. 2011. Structural basis and kinetics of force-induced conformational changes of an A domain-containing integrin. PLoS ONE 6:e27946
107. Kim MC, Neal DM, Kamm RD, Asada HH. 2013. Dynamic modeling of cell migration and spreading behaviors on fibronectin coated planar substrates and micropatterned geometries. PLoS Comput. Biol. 9:e1002926
108. Qian J, Wang J, GaoH. 2008. Lifetime and strength of adhesive molecular bond clusters between elastic media. Langmuir 24:1262-70
109. Hammer DA, Lauffenburger DA. 1987. A dynamical model for receptor-mediated cell adhesion to surfaces. Biophys. J. 52:475-87
110. Wang WW, Mody NA, King MR. 2013. Multiscale model of platelet translocation and collision. J. Comput. Phys. 244:223-35
111. Prezhdo OV, Pereverzev YV. 2009. Theoretical aspects of the biological catch bond. Acc. Chem. Res. 42:693-703
112. Zhu C, Lou JZ, McEver RP. 2005. Catch bonds: physical models, structural bases, biological function and rheological relevance. Biorheology 42:443-62
113. Barsegov V, Thirumalai D. 2005. Dynamics of unbinding of cell adhesion molecules: transition from catch to slip bonds. Proc. Natl. Acad. Sci. USA 102:1835-39
114. Thomas W, Forero M, Yakovenko O, Nilsson L, Vicini P, et al. 2006. Catch-bond model derived from allostery explains force-activated bacterial adhesion. Biophys. J. 90:753-64
115. Chakrabarti S, Hinczewski M, Thirumalai D. 2014. Plasticity of hydrogen bond networks regulates mechanochemistry of cell adhesion complexes. Proc. Natl. Acad. Sci. USA 111:9048-53
116. Margadant F, Chew LL, Hu X, Yu H, Bate N, et al. 2011. Mechanotransduction in vivo by repeated talin stretch-relaxation events depends upon vinculin. PLoS Biol. 9:e1001223
117. Puchner EM, Gaub HE. 2009. Force and function: probing proteins with AFM-based force spectroscopy. Curr. Opin. Struct. Biol. 19:605-14
118. Hoffmann T, Dougan L. 2012. Single molecule force spectroscopy using polyproteins. Chem. Soc. Rev. 41:4781-96
119. Marszalek PE, Dufrene YF. 2012. Stretching single polysaccharides and proteins using atomic force microscopy. Chem. Soc. Rev. 41:3523-34
120. Juliano RL. 2002. Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu. Rev. Pharmacol. Toxicol. 42:283-323
121. Manz BN, Groves JT. 2010. Spatial organization and signal transduction at intercellular junctions. Nat. Rev. Mol. Cell Biol. 11:342-52
122. Eyckmans J, Boudou T, Yu X, Chen CS. 2011. A hitchhiker's guide to mechanobiology. Dev. Cell 21:35-47
123. Mendolicchio GL, Ruggeri ZM. 2005. New perspectives on von Willebrand factor functions in hemostasis and thrombosis. Semin. Hematol. 42:5-14
124. Zheng XL. 2013. Structure-function and regulation of ADAMTS-13 protease. J. Thromb. Haemost. 11:11-23
125. Zhang XH, Halvorsen K, Zhang CZ, Wong WP, Springer TA. 2009. Mechanoenzymatic cleavage of the ultralarge vascular protein von Willebrand factor. Science 324:1330-34
126. Wu T, Lin JG, Cruz MA, Dong JF, Zhu C. 2010. Force-induced cleavage of single VWF A1A2A3 tridomains by ADAMTS-13. Blood 115:370-78
127. Vogel V. 2006. Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annu. Rev. Biophys. Biomol. Struct. 35:459-88
128. Ciobanasu C, Faivre B, Le Clainche C. 2013. Integrating actin dynamics, mechanotransduction and integrin activation: the multiple functions of actin binding proteins in focal adhesions. Eur. J. Cell Biol. 92:339-48
129. Hirata H, Tatsumi H, Lim CT, Sokabe M. 2014. Force-dependent vinculin binding to talin in live cells: a crucial step in anchoring the actin cytoskeleton to focal adhesions. Am. J. Physiol. Cell Physiol. 306:C607-20
130. Grashoff C, Hoffman BD, Brenner MD, Zhou RB, Parsons M, et al. 2010. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466:263-66
131. Kim ST, Takeuchi K, Sun Z-YJ, Touma M, Castro CE, et al. 2009. The T cell receptor is an anisotropic mechanosensor. J. Biol. Chem. 284:31028-37
132. Xie J, Huppa JB, Newell EW, Huang J, Ebert PJR, et al. 2012. Photocrosslinkable pMHC monomers stain T cells specifically and cause ligand-bound TCRs to be 'preferentially' transported to the cSMAC. Nat. Immunol. 13:674-80
133. Sims TN, Soos TJ, Xenias HS, Dubin-Thaler B, Hofman JM, et al. 2007. Opposing effects of PKC and WASp on symmetry breaking and relocation of the immunological synapse. Cell 129:773-85
134. Mempel TR, Henrickson SE, von Andrian UH. 2004. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427:154-59
135. Zhu C, Jiang N, Huang J, Zarnitsyna VI, Evavold BD. 2013. Insights from in situ analysis of TCRpMHC recognition: response of an interaction network. Immunol. Rev. 251:49-64
136. Huang J, Zarnitsyna VI, Liu B, Edwards LJ, Jiang N, et al. 2010. The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 464:932-36
137. Huppa JB, Axmann M, Mortelmaier MA, Lillemeier BF, Newell EW, et al. 2010. TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity. Nature 463:963-67
138. Gascoigne NR, Zal T, Alam SM. 2001. T-cell receptor binding kinetics in T-cell development and activation. Expert Rev. Mol. Med. 2001:1-17
139. Hayakawa K, Tatsumi H, Sokabe M. 2012. Mechano-sensing by actin filaments and focal adhesion proteins. Commun. Integr. Biol. 5:572-77
140. Campbell ID, Humphries MJ. 2011. Integrin structure, activation, and interactions. Cold Spring Harb. Perspect. Biol. 3:a004994
141. Askari JA, Buckley PA, Mould AP, Humphries MJ. 2009. Linking integrin conformation to function. J. Cell Sci. 122:165-70
142. Ross TD, Coon BG, Yun S, Baeyens N, Tanaka K, et al. 2013. Integrins in mechanotransduction. Curr. Opin. Cell Biol. 25:613-18
143. Santaguida S, Musacchio A. 2009. The life and miracles of kinetochores. EMBO J. 28:2511-31
144. Sarangapani KK, Asbury CL. 2014. Catch and release: How do kinetochores hook the right microtubules during mitosis Trends Genet. 30:150-59
145. Biggins S, Severin FF, Bhalla N, Sassoon I, Hyman AA, Murray AW. 1999. The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Gene Dev. 13:532-44
146. Liu D, Lampson MA. 2009. Regulation of kinetochore-microtubule attachments by Aurora B kinase. Biochem. Soc. Trans. 37:976-80
147. Liu Y, Yehl K, Narui Y, Salaita K. 2013. Tension sensing nanoparticles for mechano-imaging at the living/nonliving interface. J. Am. Chem. Soc. 135:5320-23
148. Stabley DR, Jurchenko C, Marshall SS, Salaita KS. 2012. Visualizing mechanical tension across membrane receptors with a fluorescent sensor. Nat. Methods 9:64-67
149. le Duc Q, Shi Q, Blonk I, Sonnenberg A, Wang N, et al. 2010. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J. Cell Biol. 189:1107-15
150. Tabdili H, Langer M, Shi Q, Poh Y-C, Wang N, Leckband D. 2012. Cadherin-dependent mechanotransduction depends on ligand identity but not affinity. J. Cell Sci. 125:4362-71
151. Judokusumo E, Tabdanov E, Kumari S, Dustin ML, Kam LC. 2012. Mechanosensing in T lymphocyte activation. Biophys. J. 102:L5-7
152. Pryshchep S, Zarnitsyna VI, Hong J, Evavold BD, Zhu C. 2014. Accumulation of serial forces on TCR and CD8 frequently applied by agonist antigenic peptides embedded inMHCmolecules triggers calcium in T cells. J. Immunol. 193:68-76
153. O'Connor RS, Hao XL, Shen KY, Bashour K, Akimova T, et al. 2012. Substrate rigidity regulates human T cell activation and proliferation. J. Immunol. 189:1330-39
154. Wan ZP, Zhang SS, Fan YL, Liu K, Du F, et al. 2013. B cell activation is regulated by the stiffness properties of the substrate presenting the antigens. J. Immunol. 190:4661-75
155. Arkhipov A, Shan YB, Das R, Endres NF, Eastwood MP, et al. 2013. Architecture and membrane interactions of the EGF receptor. Cell 152:557-69
156. Dror RO, Green HF, Valant C, Borhani DW, Valcourt JR, et al. 2013. Structural basis for modulation of a G-protein-coupled receptor by allosteric drugs. Nature 503:295-99
157. Endres NF, Das R, Smith AW, Arkhipov A, Kovacs E, et al. 2013. Conformational coupling across the plasma membrane in activation of the EGF receptor. Cell 152:543-56