1932

Abstract

Molecular force spectroscopy has become a powerful tool to study how mechanics regulates biology, especially the mechanical regulation of molecular interactions and its impact on cellular functions. This force-driven methodology has uncovered a wealth of new information of the physical chemistry of molecular bonds for various biological systems. The new concepts, qualitative and quantitative measures describing bond behavior under force, and structural bases underlying these phenomena have substantially advanced our fundamental understanding of the inner workings of biological systems from the nanoscale (molecule) to the microscale (cell), elucidated basic molecular mechanisms of a wide range of important biological processes, and provided opportunities for engineering applications. Here, we review major force spectroscopic assays, conceptual developments of mechanically regulated kinetics of molecular interactions, and their biological relevance. We also present current challenges and highlight future directions.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-physchem-040214-121742
2015-04-01
2024-10-10
Loading full text...

Full text loading...

/deliver/fulltext/physchem/66/1/annurev-physchem-040214-121742.html?itemId=/content/journals/10.1146/annurev-physchem-040214-121742&mimeType=html&fmt=ahah

Literature Cited

  1. Malmqvist M. 1.  1993. Surface plasmon resonance for detection and measurement of antibody-antigen affinity and kinetics. Curr. Opin. Immunol. 5:282–86 [Google Scholar]
  2. Li P, Jiang N, Nagarajan S, Wohlhueter R, Selvaraj P, Zhu C. 2.  2007. Affinity and kinetic analysis of Fcγ receptor IIIa (CD16a) binding to IgG ligands. J. Biol. Chem. 282:6210–21 [Google Scholar]
  3. O'Shannessy DJ. 3.  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 [Google Scholar]
  4. Marshall BT, Long M, Piper JW, Yago T, McEver RP, Zhu C. 4.  2003. Direct observation of catch bonds involving cell-adhesion molecules. Nature 423:190–93 [Google Scholar]
  5. Kong F, Li Z, Parks WM, Dumbauld DW, García AJ. 5.  et al. 2013. Cyclic mechanical reinforcement of integrin-ligand interactions. Mol. Cell 49:1060–68 [Google Scholar]
  6. Alon R, Hammer DA, Springer TA. 6.  1995. Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature 374:539–42 [Google Scholar]
  7. Bell G. 7.  1978. Models for the specific adhesion of cells to cells. Science 200:618–27 [Google Scholar]
  8. Dembo M, Torney DC, Saxman K, Hammer D. 8.  1988. The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc. R. Soc. Lond. B 234:55–83 [Google Scholar]
  9. Rakshit S, Zhang Y, Manibog K, Shafraz O, Sivasankar S. 9.  2012. Ideal, catch, and slip bonds in cadherin adhesion. Proc. Natl. Acad. Sci. USA 109:18815–20 [Google Scholar]
  10. Marshall BT, Sarangapani KK, Lou JH, McEver RP, Zhu C. 10.  2005. Force history dependence of receptor-ligand dissociation. Biophys. J. 88:1458–66 [Google Scholar]
  11. Guo B, Guilford WH. 11.  2006. Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. Proc. Natl. Acad. Sci. USA 103:9844–49 [Google Scholar]
  12. Sarangapani KK, Qian J, Chen W, Zarnitsyna VI, Mehta P. 12.  et al. 2011. Regulation of catch bonds by rate of force application. J. Biol. Chem. 286:32749–61 [Google Scholar]
  13. Fiore VF, Ju L, Zhu C, Barker TH. 13.  2014. Dynamic catch of a Thy-1-α5β1 + syndecan-4 trimolecular complex. Nat. Commun. 5:4886 [Google Scholar]
  14. Kim J, Zhang CZ, Zhang X, Springer TA. 14.  2010. A mechanically stabilized receptor-ligand flex-bond important in the vasculature. Nature 466:992–95 [Google Scholar]
  15. Binnig G, Quate CF, Gerber C. 15.  1986. Atomic force microscope. Phys. Rev. Lett. 56:930–33 [Google Scholar]
  16. Evans E, Ritchie K, Merkel R. 16.  1995. Sensitive force technique to probe molecular adhesion and structural linkages at biological interfaces. Biophys. J. 68:2580–87 [Google Scholar]
  17. Ashkin A, Dziedzic JM, Bjorkholm JE, Chu S. 17.  1986. Observation of a single-beam gradient force optical trap for dielectric particles. Opt. Lett. 11:288–90 [Google Scholar]
  18. Neuman KC, Nagy A. 18.  2008. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods 5:491–505 [Google Scholar]
  19. Evans E. 19.  2001. Probing the relation between force—lifetime—and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 30:105–28 [Google Scholar]
  20. Chen W, Zarnitsyna VI, Sarangapani KK, Huang J, Zhu C. 20.  2008. Measuring receptor-ligand binding kinetics on cell surfaces: from adhesion frequency to thermal fluctuation methods. Cell. Mol. Bioeng. 1:276–88 [Google Scholar]
  21. Evans E, Leung A, Hammer D, Simon S. 21.  2001. Chemically distinct transition states govern rapid dissociation of single L-selectin bonds under force. Proc. Natl. Acad. Sci. USA 98:3784–89 [Google Scholar]
  22. Liu B, Chen W, Evavold BD, Zhu C. 22.  2014. Accumulation of dynamic catch bonds between TCR and agonist peptide-MHC triggers T cell signaling. Cell 157:357–68 [Google Scholar]
  23. Zhu C, Long M, Chesla SE, Bongrand P. 23.  2002. Measuring receptor/ligand interaction at the single-bond level: experimental and interpretative issues. Ann. Biomed. Eng. 30:305–14 [Google Scholar]
  24. Piper JW, Swerlick RA, Zhu C. 24.  1998. Determining force dependence of two-dimensional receptor-ligand binding affinity by centrifugation. Biophys. J. 74:492–513 [Google Scholar]
  25. Chesla SE, Selvaraj P, Zhu C. 25.  1998. Measuring two-dimensional receptor-ligand binding kinetics by micropipette. Biophys. J. 75:1553–72 [Google Scholar]
  26. Chen W, Lou J, Zhu C. 26.  2010. Forcing switch from short- to intermediate- and long-lived states of the αA domain generates LFA-1/ICAM-1 catch bonds. J. Biol. Chem. 285:35967–78 [Google Scholar]
  27. Liang J, Fernandez JM. 27.  2009. Mechanochemistry: one bond at a time. ACS Nano 3:1628–45 [Google Scholar]
  28. Popa I, Kosuri P, Alegre-Cebollada J, Garcia-Manyes S, Fernandez JM. 28.  2013. Force dependency of biochemical reactions measured by single-molecule force-clamp spectroscopy. Nat. Protoc. 8:1261–76 [Google Scholar]
  29. Rognoni L, Stigler J, Pelz B, Ylanne J, Rief M. 29.  2012. Dynamic force sensing of filamin revealed in single-molecule experiments. Proc. Natl. Acad. Sci. USA 109:19679–84 [Google Scholar]
  30. Zhu C. 30.  2014. Mechanochemistry: a molecular biomechanics view of mechanosensing. Ann. Biomed. Eng. 42:388–404 [Google Scholar]
  31. Vogel V, Sheetz M. 31.  2006. Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell Biol. 7:265–75 [Google Scholar]
  32. Wang N, Tytell JD, Ingber DE. 32.  2009. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10:75–82 [Google Scholar]
  33. Mammoto T, Mammoto A, Ingber DE. 33.  2013. Mechanobiology and developmental control. Annu. Rev. Cell Dev. Biol. 29:27–61 [Google Scholar]
  34. Schoen I, Pruitt BL, Vogel V. 34.  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 [Google Scholar]
  35. Hoffman BD, Grashoff C, Schwartz MA. 35.  2011. Dynamic molecular processes mediate cellular mechanotransduction. Nature 475:316–23 [Google Scholar]
  36. Lou J, Zhu C. 36.  2007. A structure-based sliding-rebinding mechanism for catch bonds. Biophys. J. 92:1471–85 [Google Scholar]
  37. Lou J, Yago T, Klopocki AG, Mehta P, Chen W. 37.  et al. 2006. Flow-enhanced adhesion regulated by a selectin interdomain hinge. J. Cell Biol. 174:1107–17 [Google Scholar]
  38. Klopocki AG, Yago T, Mehta P, Yang J, Wu T. 38.  et al. 2008. Replacing a lectin domain residue in L-selectin enhances binding to P-selectin glycoprotein ligand-1 but not to 6-sulfo-sialyl Lewis X. J. Biol. Chem. 283:11493–500 [Google Scholar]
  39. Kang YY, Lu SQ, Ren P, Huo B, Long M. 39.  2012. Molecular dynamics simulation of shear- and stretch-induced dissociation of P-selectin/PSGL-1 complex. Biophys. J. 102:112–20 [Google Scholar]
  40. Trong I, Aprikian P, Kidd BA, Forero-Shelton M, Tchesnokova V. 40.  Le et al. 2010. Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like β sheet twisting. Cell 141:645–55 [Google Scholar]
  41. Manibog K, Li H, Rakshit S, Sivasankar S. 41.  2014. Resolving the molecular mechanism of cadherin catch bond formation. Nat. Commun. 5:3941 [Google Scholar]
  42. Lee CY, Lou JZ, Wen KK, McKane M, Eskin SG. 42.  et al. 2013. Actin depolymerization under force is governed by lysine 113:glutamic acid 195-mediated catch-slip bonds. Proc. Natl. Acad. Sci. USA 110:5022–27 [Google Scholar]
  43. Lu SQ, Zhang Y, Long MA. 43.  2010. Visualization of allostery in P-selectin lectin domain using MD simulations. PLoS ONE 5:e15417 [Google Scholar]
  44. Yago T, Lou J, Wu T, Yang J, Miner JJ. 44.  et al. 2008. Platelet glycoprotein Ibα forms catch bonds with human WT vWF but not with type 2B von Willebrand disease vWF. J. Clin. Invest. 118:3195–207 [Google Scholar]
  45. Lee SE, Chunsrivirot S, Kamm RD, Mofrad MRK. 45.  2008. Molecular dynamics study of talin-vinculin binding. Biophys. J. 95:2027–36 [Google Scholar]
  46. Hytonen VP, Vogel V. 46.  2008. How force might activate talin's vinculin binding sites: SMD reveals a structural mechanism. PLoS Comput. Biol. 4:e24 [Google Scholar]
  47. del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP. 47.  2009. Stretching single talin rod molecules activates vinculin binding. Science 323:638–41 [Google Scholar]
  48. Ebner A, Nevo R, Rankl C, Preiner J, Gruber H. 48.  et al. 2009. Probing the energy landscape of protein-binding reactions by dynamic force spectroscopy. Handbook of Single-Molecule Biophysics P Hinterdorfer, A van Oijen 407–47 New York: Springer [Google Scholar]
  49. Woodside MT, Block SM. 49.  2014. Reconstructing folding energy landscapes by single-molecule force spectroscopy. Annu. Rev. Biophys. 43:19–39 [Google Scholar]
  50. Zoldak G, Rief M. 50.  2013. Force as a single molecule probe of multidimensional protein energy landscapes. Curr. Opin. Struct. Biol. 23:48–57 [Google Scholar]
  51. Galera-Prat A, Gomez-Sicilia A, Oberhauser AF, Cieplak M, Carrion-Vazquez M. 51.  2010. Understanding biology by stretching proteins: recent progress. Curr. Opin. Struct. Biol. 20:63–69 [Google Scholar]
  52. Ritzefeld M, Walhorn V, Anselmetti D, Sewald N. 52.  2013. Analysis of DNA interactions using single-molecule force spectroscopy. Amino Acids 44:1457–75 [Google Scholar]
  53. Dangkulwanich M, Ishibashi T, Bintu L, Bustamante C. 53.  2014. Molecular mechanisms of transcription through single-molecule experiments. Chem. Rev. 114:3203–23 [Google Scholar]
  54. Kaiser CM, Tinoco I. 54.  2014. Probing the mechanisms of translation with force. Chem. Rev. 114:3266–80 [Google Scholar]
  55. Chaurasiya KR, Paramanathan T, McCauley MJ, Williams MC. 55.  2010. Biophysical characterization of DNA binding from single molecule force measurements. Phys. Life Rev. 7:299–341 [Google Scholar]
  56. Puchner EM, Gaub HE. 56.  2012. Single-molecule mechanoenzymatics. Annu. Rev. Biophys. 41:497–518 [Google Scholar]
  57. Alegre-Cebollada J, Perez-Jimenez R, Kosuri P, Fernandez JM. 57.  2010. Single-molecule force spectroscopy approach to enzyme catalysis. J. Biol. Chem. 285:18961–66 [Google Scholar]
  58. Guo J, Sachs F, Meng F. 58.  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 [Google Scholar]
  59. Wang X, Ha T. 59.  2013. Defining single molecular forces required to activate integrin and notch signaling. Science 340:991–94 [Google Scholar]
  60. Moy VT, Florin EL, Gaub HE. 60.  1994. Intermolecular forces and energies between ligands and receptors. Science 266:257–59 [Google Scholar]
  61. Florin EL, Moy VT, Gaub HE. 61.  1994. Adhesion forces between individual ligand-receptor pairs. Science 264:415–17 [Google Scholar]
  62. Evans E, Ritchie K. 62.  1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541–55 [Google Scholar]
  63. Merkel R, Nassoy P, Leung A, Ritchie K, Evans E. 63.  1999. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 397:50–53 [Google Scholar]
  64. Gergely C, Voegel JC, Schaaf P, Senger B, Maaloum M. 64.  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 [Google Scholar]
  65. Zhu C. 65.  2000. Kinetics and mechanics of cell adhesion. J. Biomech. 33:23–33 [Google Scholar]
  66. Zhang XH, Bogorin DF, Moy VT. 66.  2004. Molecular basis of the dynamic strength of the sialyl Lewis X–selectin interaction. ChemPhysChem 5:175–82 [Google Scholar]
  67. Hanley W, McCarty O, Jadhav S, Tseng Y, Wirtz D, Konstantopoulos K. 67.  2003. Single molecule characterization of P-selectin/ligand binding. J. Biol. Chem. 278:10556–61 [Google Scholar]
  68. Evans E, Kinoshita K, Simon S, Leung A. 68.  2010. Long-lived, high-strength states of ICAM-1 bonds to β2 integrin, I: lifetimes of bonds to recombinant αLβ2 under force. Biophys. J. 98:1458–66 [Google Scholar]
  69. Zhang XH, Wojcikiewicz E, Moy VT. 69.  2002. Force spectroscopy of the leukocyte function-associated antigen-1/intercellular adhesion molecule-1 interaction. Biophys. J. 83:2270–79 [Google Scholar]
  70. Zhang X, Craig SE, Kirby H, Humphries MJ, Moy VT. 70.  2004. Molecular basis for the dynamic strength of the integrin α4β1/VCAM-1 interaction. Biophys. J. 87:3470–78 [Google Scholar]
  71. Li F, Redick SD, Erickson HP, Moy VT. 71.  2003. Force measurements of the α5β1 integrin-fibronectin interaction. Biophys. J. 84:1252–62 [Google Scholar]
  72. Dobrowsky TM, Rabi SA, Nedellec R, Daniels BR, Mullins JI. 72.  et al. 2013. Adhesion and fusion efficiencies of human immunodeficiency virus type 1 (HIV-1) surface proteins. Sci. Rep. 3:3014 [Google Scholar]
  73. Chang MI, Panorchan P, Dobrowsky TM, Tseng Y, Wirtz D. 73.  2005. Single-molecule analysis of human immunodeficiency virus type 1 gp120-receptor interactions in living cells. J. Virol. 79:14748–55 [Google Scholar]
  74. Yu JP, Wang Q, Shi XL, Ma XY, Yang HY. 74.  et al. 2007. Single-molecule force spectroscopy study of interaction between transforming growth factor β1 and its receptor in living cells. J. Phys. Chem. B 111:13619–25 [Google Scholar]
  75. Sasuga S, Abe R, Nikaido O, Kiyosaki S, Sekiguchi H. 75.  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 [Google Scholar]
  76. Zhang J, Wu GM, Song CL, Li YJ, Qiao HY. 76.  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 [Google Scholar]
  77. Whited AM, Park PSH. 77.  2014. Atomic force microscopy: a multifaceted tool to study membrane proteins and their interactions with ligands. Biochim. Biophys. Acta 1838:56–68 [Google Scholar]
  78. Pierres A, Benoliel AM, Bongrand P, van der Merwe PA. 78.  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 [Google Scholar]
  79. Kong F, García AJ, Mould AP, Humphries MJ, Zhu C. 79.  2009. Demonstration of catch bonds between an integrin and its ligand. J. Cell Biol. 185:1275–84 [Google Scholar]
  80. Sarangapani KK, Yago T, Klopocki AG, Lawrence MB, Fieger CB. 80.  et al. 2004. Low force decelerates L-selectin dissociation from P-selectin glycoprotein ligand-1 and endoglycan. J. Biol. Chem. 279:2291–98 [Google Scholar]
  81. Evans E. 81.  1998. Energy landscapes of biomolecular adhesion and receptor anchoring at interfaces explored with dynamic force spectroscopy. Faraday Discuss. 111:1–16 [Google Scholar]
  82. Evans E. 82.  1999. Looking inside molecular bonds at biological interfaces with dynamic force spectroscopy. Biophys. Chem. 82:83–97 [Google Scholar]
  83. Evans E, Heinrich V, Ludwig F, Rawicz W. 83.  2003. Dynamic tension spectroscopy and strength of biomembranes. Biophys. J. 85:2342–50 [Google Scholar]
  84. Finger EB, Puri KD, Alon R, Lawrence MB, von Andrian UH, Springer TA. 84.  1996. Adhesion through L-selectin requires a threshold hydrodynamic shear. Nature 379:266–69 [Google Scholar]
  85. Lawrence MB, Kansas GS, Kunkel EJ, Ley K. 85.  1997. Threshold levels of fluid shear promote leukocyte adhesion through selectins (CD62L,P,E). J. Cell Biol. 136:717–27 [Google Scholar]
  86. Savage B, Saldivar E, Ruggeri ZM. 86.  1996. Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor. Cell 84:289–97 [Google Scholar]
  87. Thomas WE, Trintchina E, Forero M, Vogel V, Sokurenko EV. 87.  2002. Bacterial adhesion to target cells enhanced by shear force. Cell 109:913–23 [Google Scholar]
  88. Yago T, Wu JH, Wey CD, Klopocki AG, Zhu C, McEver RP. 88.  2004. Catch bonds govern adhesion through L-selectin at threshold shear. J. Cell Biol. 166:913–23 [Google Scholar]
  89. Wayman AM, Chen W, McEver RP, Zhu C. 89.  2010. Triphasic force dependence of E-selectin/ligand dissociation governs cell rolling under flow. Biophys. J. 99:1166–74 [Google Scholar]
  90. Ju L, Dong JF, Cruz MA, Zhu C. 90.  2013. The N-terminal flanking region of the A1 domain regulates the force-dependent binding of von Willebrand factor to platelet glycoprotein Ibα. J. Biol. Chem. 288:32289–301 [Google Scholar]
  91. Yakovenko O, Sharma S, Forero M, Tchesnokova V, Aprikian P. 91.  et al. 2008. FimH forms catch bonds that are enhanced by mechanical force due to allosteric regulation. J. Biol. Chem. 283:11596–605 [Google Scholar]
  92. Zhu C, Yago T, Lou J, Zarnitsyna V, McEver R. 92.  2008. Mechanisms for flow-enhanced cell adhesion. Ann. Biomed. Eng. 36:604–21 [Google Scholar]
  93. McEver RP, Zhu C. 93.  2010. Rolling cell adhesion. Annu. Rev. Cell Dev. Biol. 26:363–96 [Google Scholar]
  94. Chen W, Lou J, Evans EA, Zhu C. 94.  2012. Observing force-regulated conformational changes and ligand dissociation from a single integrin on cells. J. Cell Biol. 199:497–512 [Google Scholar]
  95. Choi YI, Duke-Cohan JS, Chen W, Liu B, Rossy J. 95.  et al. 2014. Dynamic control of β1 integrin adhesion by the plexinD1-sema3E axis. Proc. Natl. Acad. Sci. USA 111:379–84 [Google Scholar]
  96. Laakso JM, Lewis JH, Shuman H, Ostap EM. 96.  2008. Myosin I can act as a molecular force sensor. Science 321:133–36 [Google Scholar]
  97. Akiyoshi B, Sarangapani KK, Powers AF, Nelson CR, Reichow SL. 97.  et al. 2010. Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468:576–79 [Google Scholar]
  98. Arya M, Kolomeisky AB, Romo GM, Cruz MA, Lopez JA, Anvari B. 98.  2005. Dynamic force spectroscopy of glycoprotein Ib-IX and von Willebrand factor. Biophys. J. 88:4391–401 [Google Scholar]
  99. Evans E, Leung A, Heinrich V, Zhu C. 99.  2004. Mechanical switching and coupling between two dissociation pathways in a P-selectin adhesion bond. Proc. Natl. Acad. Sci. USA 101:11281–86 [Google Scholar]
  100. Dudko OK, Hummer G, Szabo A. 100.  2008. Theory, analysis, and interpretation of single-molecule force spectroscopy experiments. Proc. Natl. Acad. Sci. USA 105:15755–60 [Google Scholar]
  101. Isralewitz B, Baudry J, Gullingsrud J, Kosztin D, Schulten K. 101.  2001. Steered molecular dynamics investigations of protein function. J. Mol. Graph. Model. 19:13–25 [Google Scholar]
  102. Liu GJ, Fang Y, Wu JH. 102.  2013. A mechanism for localized dynamics-driven affinity regulation of the binding of von Willebrand factor to platelet glycoprotein Ibα. J. Biol. Chem. 288:26658–67 [Google Scholar]
  103. Thomas WE, Vogel V, Sokurenko E. 103.  2008. Biophysics of catch bonds. Annu. Rev. Biophys. 37:399–416 [Google Scholar]
  104. Aprikian P, Tchesnokova V, Kidd B, Yakovenko O, Yarov-Yarovoy V. 104.  et al. 2007. Interdomain interaction in the FimH adhesin of Escherichia coli regulates the affinity to mannose. J. Biol. Chem. 282:23437–46 [Google Scholar]
  105. Bouckaert J, Berglund J, Schembri M, De Genst E, Cools L. 105.  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 [Google Scholar]
  106. Xiang X, Lee CY, Li T, Chen W, Lou J, Zhu C. 106.  2011. Structural basis and kinetics of force-induced conformational changes of an αA domain-containing integrin. PLoS ONE 6:e27946 [Google Scholar]
  107. Kim MC, Neal DM, Kamm RD, Asada HH. 107.  2013. Dynamic modeling of cell migration and spreading behaviors on fibronectin coated planar substrates and micropatterned geometries. PLoS Comput. Biol. 9:e1002926 [Google Scholar]
  108. Qian J, Wang J, Gao H. 108.  2008. Lifetime and strength of adhesive molecular bond clusters between elastic media. Langmuir 24:1262–70 [Google Scholar]
  109. Hammer DA, Lauffenburger DA. 109.  1987. A dynamical model for receptor-mediated cell adhesion to surfaces. Biophys. J. 52:475–87 [Google Scholar]
  110. Wang WW, Mody NA, King MR. 110.  2013. Multiscale model of platelet translocation and collision. J. Comput. Phys. 244:223–35 [Google Scholar]
  111. Prezhdo OV, Pereverzev YV. 111.  2009. Theoretical aspects of the biological catch bond. Acc. Chem. Res. 42:693–703 [Google Scholar]
  112. Zhu C, Lou JZ, McEver RP. 112.  2005. Catch bonds: physical models, structural bases, biological function and rheological relevance. Biorheology 42:443–62 [Google Scholar]
  113. Barsegov V, Thirumalai D. 113.  2005. Dynamics of unbinding of cell adhesion molecules: transition from catch to slip bonds. Proc. Natl. Acad. Sci. USA 102:1835–39 [Google Scholar]
  114. Thomas W, Forero M, Yakovenko O, Nilsson L, Vicini P. 114.  et al. 2006. Catch-bond model derived from allostery explains force-activated bacterial adhesion. Biophys. J. 90:753–64 [Google Scholar]
  115. Chakrabarti S, Hinczewski M, Thirumalai D. 115.  2014. Plasticity of hydrogen bond networks regulates mechanochemistry of cell adhesion complexes. Proc. Natl. Acad. Sci. USA 111:9048–53 [Google Scholar]
  116. Margadant F, Chew LL, Hu X, Yu H, Bate N. 116.  et al. 2011. Mechanotransduction in vivo by repeated talin stretch-relaxation events depends upon vinculin. PLoS Biol. 9:e1001223 [Google Scholar]
  117. Puchner EM, Gaub HE. 117.  2009. Force and function: probing proteins with AFM-based force spectroscopy. Curr. Opin. Struct. Biol. 19:605–14 [Google Scholar]
  118. Hoffmann T, Dougan L. 118.  2012. Single molecule force spectroscopy using polyproteins. Chem. Soc. Rev. 41:4781–96 [Google Scholar]
  119. Marszalek PE, Dufrene YF. 119.  2012. Stretching single polysaccharides and proteins using atomic force microscopy. Chem. Soc. Rev. 41:3523–34 [Google Scholar]
  120. Juliano RL. 120.  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 [Google Scholar]
  121. Manz BN, Groves JT. 121.  2010. Spatial organization and signal transduction at intercellular junctions. Nat. Rev. Mol. Cell Biol. 11:342–52 [Google Scholar]
  122. Eyckmans J, Boudou T, Yu X, Chen CS. 122.  2011. A hitchhiker's guide to mechanobiology. Dev. Cell 21:35–47 [Google Scholar]
  123. Mendolicchio GL, Ruggeri ZM. 123.  2005. New perspectives on von Willebrand factor functions in hemostasis and thrombosis. Semin. Hematol. 42:5–14 [Google Scholar]
  124. Zheng XL. 124.  2013. Structure-function and regulation of ADAMTS-13 protease. J. Thromb. Haemost. 11:11–23 [Google Scholar]
  125. Zhang XH, Halvorsen K, Zhang CZ, Wong WP, Springer TA. 125.  2009. Mechanoenzymatic cleavage of the ultralarge vascular protein von Willebrand factor. Science 324:1330–34 [Google Scholar]
  126. Wu T, Lin JG, Cruz MA, Dong JF, Zhu C. 126.  2010. Force-induced cleavage of single VWF A1A2A3 tridomains by ADAMTS-13. Blood 115:370–78 [Google Scholar]
  127. Vogel V. 127.  2006. Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annu. Rev. Biophys. Biomol. Struct. 35:459–88 [Google Scholar]
  128. Ciobanasu C, Faivre B, Le Clainche C. 128.  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 [Google Scholar]
  129. Hirata H, Tatsumi H, Lim CT, Sokabe M. 129.  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 [Google Scholar]
  130. Grashoff C, Hoffman BD, Brenner MD, Zhou RB, Parsons M. 130.  et al. 2010. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466:263–66 [Google Scholar]
  131. Kim ST, Takeuchi K, Sun Z-YJ, Touma M, Castro CE. 131.  et al. 2009. The αβ T cell receptor is an anisotropic mechanosensor. J. Biol. Chem. 284:31028–37 [Google Scholar]
  132. Xie J, Huppa JB, Newell EW, Huang J, Ebert PJR. 132.  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 [Google Scholar]
  133. Sims TN, Soos TJ, Xenias HS, Dubin-Thaler B, Hofman JM. 133.  et al. 2007. Opposing effects of PKCθ and WASp on symmetry breaking and relocation of the immunological synapse. Cell 129:773–85 [Google Scholar]
  134. Mempel TR, Henrickson SE, von Andrian UH. 134.  2004. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427:154–59 [Google Scholar]
  135. Zhu C, Jiang N, Huang J, Zarnitsyna VI, Evavold BD. 135.  2013. Insights from in situ analysis of TCR-pMHC recognition: response of an interaction network. Immunol. Rev. 251:49–64 [Google Scholar]
  136. Huang J, Zarnitsyna VI, Liu B, Edwards LJ, Jiang N. 136.  et al. 2010. The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 464:932–36 [Google Scholar]
  137. Huppa JB, Axmann M, Mortelmaier MA, Lillemeier BF, Newell EW. 137.  et al. 2010. TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity. Nature 463:963–67 [Google Scholar]
  138. Gascoigne NR, Zal T, Alam SM. 138.  2001. T-cell receptor binding kinetics in T-cell development and activation. Expert Rev. Mol. Med. 2001:1–17 [Google Scholar]
  139. Hayakawa K, Tatsumi H, Sokabe M. 139.  2012. Mechano-sensing by actin filaments and focal adhesion proteins. Commun. Integr. Biol. 5:572–77 [Google Scholar]
  140. Campbell ID, Humphries MJ. 140.  2011. Integrin structure, activation, and interactions. Cold Spring Harb. Perspect. Biol. 3:a004994 [Google Scholar]
  141. Askari JA, Buckley PA, Mould AP, Humphries MJ. 141.  2009. Linking integrin conformation to function. J. Cell Sci. 122:165–70 [Google Scholar]
  142. Ross TD, Coon BG, Yun S, Baeyens N, Tanaka K. 142.  et al. 2013. Integrins in mechanotransduction. Curr. Opin. Cell Biol. 25:613–18 [Google Scholar]
  143. Santaguida S, Musacchio A. 143.  2009. The life and miracles of kinetochores. EMBO J. 28:2511–31 [Google Scholar]
  144. Sarangapani KK, Asbury CL. 144.  2014. Catch and release: How do kinetochores hook the right microtubules during mitosis?. Trends Genet. 30:150–59 [Google Scholar]
  145. Biggins S, Severin FF, Bhalla N, Sassoon I, Hyman AA, Murray AW. 145.  1999. The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Gene Dev. 13:532–44 [Google Scholar]
  146. Liu D, Lampson MA. 146.  2009. Regulation of kinetochore-microtubule attachments by Aurora B kinase. Biochem. Soc. Trans. 37:976–80 [Google Scholar]
  147. Liu Y, Yehl K, Narui Y, Salaita K. 147.  2013. Tension sensing nanoparticles for mechano-imaging at the living/nonliving interface. J. Am. Chem. Soc. 135:5320–23 [Google Scholar]
  148. Stabley DR, Jurchenko C, Marshall SS, Salaita KS. 148.  2012. Visualizing mechanical tension across membrane receptors with a fluorescent sensor. Nat. Methods 9:64–67 [Google Scholar]
  149. le Duc Q, Shi Q, Blonk I, Sonnenberg A, Wang N. 149.  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 [Google Scholar]
  150. Tabdili H, Langer M, Shi Q, Poh Y-C, Wang N, Leckband D. 150.  2012. Cadherin-dependent mechanotransduction depends on ligand identity but not affinity. J. Cell Sci. 125:4362–71 [Google Scholar]
  151. Judokusumo E, Tabdanov E, Kumari S, Dustin ML, Kam LC. 151.  2012. Mechanosensing in T lymphocyte activation. Biophys. J. 102:L5–7 [Google Scholar]
  152. Pryshchep S, Zarnitsyna VI, Hong J, Evavold BD, Zhu C. 152.  2014. Accumulation of serial forces on TCR and CD8 frequently applied by agonist antigenic peptides embedded in MHC molecules triggers calcium in T cells. J. Immunol. 193:68–76 [Google Scholar]
  153. O'Connor RS, Hao XL, Shen KY, Bashour K, Akimova T. 153.  et al. 2012. Substrate rigidity regulates human T cell activation and proliferation. J. Immunol. 189:1330–39 [Google Scholar]
  154. Wan ZP, Zhang SS, Fan YL, Liu K, Du F. 154.  et al. 2013. B cell activation is regulated by the stiffness properties of the substrate presenting the antigens. J. Immunol. 190:4661–75 [Google Scholar]
  155. Arkhipov A, Shan YB, Das R, Endres NF, Eastwood MP. 155.  et al. 2013. Architecture and membrane interactions of the EGF receptor. Cell 152:557–69 [Google Scholar]
  156. Dror RO, Green HF, Valant C, Borhani DW, Valcourt JR. 156.  et al. 2013. Structural basis for modulation of a G-protein-coupled receptor by allosteric drugs. Nature 503:295–99 [Google Scholar]
  157. Endres NF, Das R, Smith AW, Arkhipov A, Kovacs E. 157.  et al. 2013. Conformational coupling across the plasma membrane in activation of the EGF receptor. Cell 152:543–56 [Google Scholar]
/content/journals/10.1146/annurev-physchem-040214-121742
Loading
/content/journals/10.1146/annurev-physchem-040214-121742
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error