Conformational Changes and Signaling in Cell and Matrix Physics

Current Biology

Volumn 19, Issue 17, 2009, Pages

  Brown, André E X ^a   Discher, Dennis E ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SCLEROPROTEIN;

ANIMAL; BIOLOGICAL MODEL; BIOMECHANICS; CELL ADHESION; CELL MOTION; CELL SHAPE; CYTOSKELETON; EXTRACELLULAR MATRIX; METABOLISM; PHYSIOLOGY; PROTEIN FOLDING; REVIEW; SIGNAL TRANSDUCTION; ULTRASTRUCTURE;

ANIMALS; BIOMECHANICS; CELL ADHESION; CELL MOVEMENT; CELL SHAPE; CYTOSKELETON; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; MODELS, BIOLOGICAL; PROTEIN FOLDING; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 69949143112     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2009.06.054     Document Type: Review

References (94)

1. Pelling A.E., and Horton M.A. An historical perspective on cell mechanics. Pflügers Arch. 456 (2008) 3-12
2. Wirtz D. Particle tracking microrheology of living cells: principles and applications. Annu. Rev. Biophys. 38 (2009)
3. Riveline D., Zamir E., Balaban N.Q., Schwarz U.S., Ishizaki T., Narumiya S., Kam Z., Geiger B., and Bershadsky A.D. 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 (2001) 1175-1186
4. Discher D., Janmey P., and Wang Y. Tissue cells feel and respond to the stiffness of their substrate. Science 310 (2005) 1139-1143
5. Engler A.J., Sen S., Sweeney H.L., and Discher D. Matrix elasticity directs stem cell lineage specification. Cell 126 (2006) 677-689
6. Paszek M.J., Zahir N., Johnson K.R., Lakins J.N., Rozenberg G.I., Gefen A., Reinhart-King C.A., Margulies S.S., Dembo M., Boettiger D., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8 (2005) 241-254
7. Orr A.W., Helmke B.P., Blackman B.R., and Schwartz M.A. Mechanisms of mechanotransduction. Dev. Cell 10 (2006) 11-20
8. Chen C.S. Mechanotransduction - a field pulling together?. J. Cell Sci. 121 (2008) 3285-3292
9. Johnson C.P., Tang H.Y., Carag C., Speicher D.W., and Discher D. Forced unfolding of proteins within cells. Science 317 (2007) 663-666
10. Ingber D.E. Cellular mechanotransduction: putting all the pieces together again. FASEB J. 20 (2006) 811
11. Bershadsky A., Kozlov M., and Geiger B. Adhesion-mediated mechanosensitivity: a time to experiment, and a time to theorize. Curr. Opin. Cell Biol. 18 (2006) 472-481
12. Smock R.G., and Gierasch L.M. Sending signals dynamically. Science 324 (2009) 198-203
13. Rief M., Gautel M., Oesterhelt F., Fernandez J.M., and Gaub H.E. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276 (1997) 1109-1112
14. Kellermayer M.S.Z., Smith S.B., Granzier H.L., and Bustamante C. Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science 276 (1997) 1112-1116
15. Neuman K.C., and Nagy A. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods 5 (2008) 491-505
16. Bell G.I. Models for specific adhesion of cells to cells. Science 200 (1978) 618-627
17. Evans E.A., and Calderwood D.A. Forces and bond dynamics in cell adhesion. Science 316 (2007) 1148-1153
18. Zhong C., Chrzanowska-Wodnicka M., Brown J., Shaub A., Belkin A.M., and Burridge K. Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly. J. Cell Biol. 141 (1998) 539-551
19. Ejim O.S., Blunn G.W., and Brown R.A. Production of artificial-oriented mats and strands from plasma fibronectin - a morphological study. Biomaterials 14 (1993) 743-748
20. Baneyx G., and Vogel V. Self-assembly of fibronectin into fibrillar networks underneath dipalmitoyl phosphatidylcholine monolayers: Role of lipid matrix and tensile forces. Proc. Natl. Acad. Sci. USA 96 (1999) 12518-12523
21. Erickson H.P. Reversible unfolding of fibronectin type III and immunoglobulin domains provides the structural basis for stretch and elasticity of titin and fibronectin. Proc. Natl. Acad. Sci. USA 91 (1994) 10114-10118
22. Krammer A., Lu H., Isralewitz B., Schulten K., and Vogel V. Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch. Proc. Nat. Acad. Sci. USA 96 (1999) 1351-1356
23. Gao M., Craig D., Vogel V., and Schulten K. Identifying unfolding intermediates of FN-III10 by steered molecular Dynamics. J. Mol. Biol. 323 (2002) 939-950
24. Oberhauser A.F., Marszalek P.E., Erickson H.P., and Fernandez J.M. The molecular elasticity of the extracellular matrix protein tenascin. Nature 393 (1998) 181-185
25. Baneyx G., Baugh L., and Vogel V. Fibronectin extension and unfolding within cell matrix fibrils controlled by cytoskeletal tension. Proc. Natl. Acad. Sci. USA 99 (2002) 5139-5143
26. Smith M., Gourdon D., Little W., Kubow K., Eguiluz R.A., Luna-Morris S., and Vogel V. Force-induced unfolding of fibronectin in the extracellular matrix of living cells. PLoS Biol. 5 (2007) e268
27. Hynes R.O., and Yamada K.M. Fibronectins: multifunctional modular glycoproteins. J. Cell Biol. 95 (1982) 369-377
28. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 110 (2002) 673-687
29. Vogel V. Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annu. Rev. Biophys. Biomol. Struct. 35 (2006) 459-488
30. Oberhauser A.F., Badilla-Fernandez C., Carrion-Vazquez M., and Fernandez J.M. The mechanical hierarchies of fibronectin observed with single-molecule AFM. J. Mol. Biol. 319 (2002) 433-447
31. Berry M.F., Engler A.J., Woo Y.J., Pirolli T.J., Bish L.T., Jayasankar V., Morine K.J., Gardner T.J., Discher D., and Sweeney H.L. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am. J. Phys. Heart Circ. Phys. 290 (2006) H2196-H2203
32. Singer A.J., and Clark R.A. Cutaneous wound healing. N. Engl. J. Med. 341 (1999) 738-746
33. Brown A.E.X., Litvinov R.I., Discher D.E., and Weisel J.W. Forced unfolding of coiled-coils in fibrinogen by single-molecule AFM. Biophys. J. 92 (2007) L39-L41
34. Lim B.B.C., Lee E.H., Sotomayor M., and Schulten K. Molecular basis of fibrin clot elasticity. Structure 16 (2008) 449-459
35. Brown A.E.X., Litvinov R.I., Discher D.E., Purohit P., and Weisel J.W. Multiscale mechanics of fibrin polymer: Gel stretching with protein unfolding and loss of water. Science 325 (2009) 741-744
36. Joel S.B. Platelet-fibrinogen interactions. Ann. NY Acad. Sci. 936 (2001) 340-354
37. Springer T.A., Zhu J., and Xiao T. Structural basis for distinctive recognition of fibrinogen gammaC peptide by the platelet integrin alphaIIbbeta3. J. Cell Biol. 182 (2008) 791-800
38. Xu J., Rodriguez D., Petitclerc E., Kim J.J., Hangai M., Yuen S.M., Davis G.E., and Brooks P.C. Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo. J. Cell Biol. 154 (2001) 1069
39. Buehler M.J. Nature designs tough collagen: explaining the nanostructure of collagen fibrils. Proc. Nat. Acad. Sci. USA 103 (2006) 12285-12290
40. Wipff P.-J., Rifkin D.B., Meister J.-J., and Hinz B. Myofibroblast contraction activates latent TGF-β1 from the extracellular matrix. J. Cell Biol. 179 (2007) 1311-1323
41. Benoit M., Gabriel D., Gerisch G., and Gaub H.E. Discrete interactions in cell adhesion measured by single-molecule force spectroscopy. Nat. Cell. Biol. 2 (2000) 313-317
42. Helenius J., Heisenberg C.-P., Gaub H.E., and Muller D.J. Single-cell force spectroscopy. J. Cell Sci. 121 (2008) 1785-1791
43. Schmitz J., and Gottschalk K.E. Mechanical regulation of cell adhesion. Soft Matter 4 (2008) 1373-1387
44. Sims P.J., Ginsberg M.H., Plow E.F., and Shattil S.J. Effect of platelet activation on the conformation of the plasma membrane glycoprotein IIb-IIIa complex. J. Biol. Chem. 266 (1991) 7345-7352
45. Hato T., Pampori N., and Shattil S.J. Complementary roles for receptor clustering and conformational change in the adhesive and signaling functions of Integrin alpha IIbbeta 3. J. Cell Biol. 141 (1998) 1685-1695
46. Friedland J.C., Lee M.H., and Boettiger D. Mechanically activated integrin switch controls alpha5beta1 function. Science 323 (2009) 642-644
47. Marshall B.T., Long M., Piper J.W., Yago T., McEver R.P., and Zhu C. Direct observation of catch bonds involving cell-adhesion molecules. Nature 423 (2003) 190-193
48. Yakovenko O., Sharma S., Forero M., Tchesnokova V., Aprikian P., Kidd B., Mach A., Vogel V., Sokurenko E., and Thomas W.E. FimH forms catch bonds that are enhanced by mechanical force due to allosteric regulation. J. Biol. Chem. 283 (2008) 11596-11605
49. Evans E., Leung A., Heinrich V., and Zhu C. Mechanical switching and coupling between two dissociation pathways in a P-selectin adhesion bond. Proc. Nat. Acad. Sci. USA 101 (2004) 11281-11286
50. Zaidel-Bar R., Itzkovitz S., Ma'ayan A., Iyengar R., and Geiger B. Functional atlas of the integrin adhesome. Nat. Cell Bio. 9 (2007) 858-867
51. Sawada Y., and Sheetz M.P. Force transduction by Triton cytoskeletons. J. Cell Bio. 156 (2002) 609-615
52. Galbraith C.G., Yamada K.M., and Sheetz M.P. The relationship between force and focal complex development. J. Cell Bio. 159 (2002) 695-705
53. Gingras A.R., Ziegler W.H., Frank R., Roberts G.C.K., Critchley D.R., and Emsley J. Mapping and consensus sequence identification for multiple vinculin binding sites within the talin rod. J. Biol. Chem. 280 (2005) 37217-37224
54. Lee S.E., Kamm R.D., and Mofrad M.R. Force-induced activation of talin and its possible role in focal adhesion mechanotransduction. J. Biomech. 40 (2007) 2096-2106
55. del Rio A., Perez-Jimenez R., Liu R., Roca-Cusachs P., Fernandez J.M., and Sheetz M.P. Stretching single talin rod molecules activates vinculin binding. Science 323 (2009) 638-641
56. Lee S.E., Chunsrivirot S., Kamm R.D., and Mofrad M.R. Molecular dynamics study of talin-vinculin binding. Biophys. J. 95 (2008) 2027-2036
57. Papagrigoriou E., Gingras A.R., Barsukov I.L., Bate N., Fillingham I.J., Patel B., Frank R., Ziegler W.H., Roberts G.C., Critchley D.R., et al. Activation of a vinculin-binding site in the talin rod involves rearrangement of a five-helix bundle. EMBO J. 23 (2004) 2942-2951
58. Sawada Y., Tamada M., Dubin-Thaler B.J., Cherniavskaya O., Sakai R., Tanaka S., and Sheetz M.P. Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127 (2006) 1015-1026
59. Pellegrin S., and Mellor H. Actin stress fibres. J. Cell Sci. 120 (2007) 3491-3499
60. Wang J.H., and Lin J.S. Cell traction force and measurement methods. Biomech. Model Mechanobiol. 6 (2007) 361-371
61. Gardel M.L., Nakamura F., Hartwig J.H., Crocker J.C., Stossel T.P., and Weitz D.A. Prestressed F-actin networks cross-linked by hinged filamins replicate mechanical properties of cells. Proc. Natl. Acad. Sci. USA 103 (2006) 1762-1767
62. Rafelski S.M., and Theriot J.A. Crawling toward a unified model of cell mobility: spatial and temporal regulation of actin dynamics. Annu. Rev. Biochem. 73 (2004) 209-239
63. Revenu C., Athman R., Robine S., and Louvard D. The co-workers of actin filaments: from cell structures to signals. Nat. Rev. Mol. Cell Biol. 5 (2004) 635-646
64. Shizuta Y., Shizuta H., Gallo M., Davies P., and Pastan I. Purification and properties of filamin, and actin binding protein from chicken gizzard. J. Biol. Chem. 251 (1976) 6562-6567
65. Tseng Y., An K.M., Esue O., and Wirtz D. The bimodal role of filamin in controlling the architecture and mechanics of F-actin networks. J. Biol. Chem. 279 (2004) 1819-1826
66. Janmey P.A., Hvidt S., Lamb J., and Stossel T.P. Resemblance of actin-binding protein/actin gels to covalently crosslinked networks. Nature 345 (1990) 89-92
67. Cunningham C.C., Gorlin J.B., Kwiatkowski D.J., Hartwig J.H., Janmey P.A., Byers H.R., and Stossel T.P. Actin-binding protein requirement for cortical stability and efficient locomotion. Science 255 (1992) 325-327
68. Tandon R., Levental I., Huang C., Byfield F.J., Ziembicki J., Schelling J.R., Bruggeman L.A., Sedor J.R., Janmey P.A., and Miller R.T. HIV infection changes glomerular podocyte cytoskeletal composition and results in distinct cellular mechanical properties. Am. J. Physiol. Renal Physiol. 292 (2007) F701-F710
69. Coughlin M.F., Puig-de-Morales M., Bursac P., Mellema M., Millet E., and Fredberg J.J. Filamin-A and rheological properties of cultured melanoma cells. Biophys. J. 90 (2006) 2199-2205
70. Kasza K.E., Nakamura F., Hu S., Kollmannsberger P., Bonakdar N., Fabry B., Stossel T.P., Wang N., and Weitz D.A. Filamin A is essential for active cell stiffening but not passive stiffening under external force. Biophys. J. 96 (2009) 4326-4335
71. Knuth M., Khaire N., Kuspa A., Lu S.J., Schleicher M., and Noegel A.A. A novel partner for Dictyostelium filamin is an alpha-helical developmentally regulated protein. J. Cell Sci. 117 (2004) 5013-5022
72. Popowicz G.M., Schleicher M., Noegel A., and Holak T.A. Filamins: promiscuous organizers of the cytoskeleton. Trends Biochem. Sci. 31 (2006) 411-419
73. Stossel T.P., Condeelis J., Cooley L., Hartwig J.H., Noegel A., Schleicher M., and Shapiro S.S. Filamins as integrators of cell mechanics and signalling. Nat. Rev. Mol. Cell Biol. 2 (2001) 138-145
74. Kiema T., Lad Y., Jiang P., Oxley C.L., Baldassarre M., Wegener K.L., Campbell I.D., Ylänne J., and Calderwood D.A. The molecular basis of filamin binding to integrins and competition with talin. Mol. Cell 21 (2006) 337-347
75. Furuike S., Ito T., and Yamazaki M. Mechanical unfolding of single filamin A (ABP-280) molecules detected by atomic force microscopy. FEBS Lett. 498 (2001) 72-75
76. Kolahi K.S., and Mofrad M.R. Molecular mechanics of filamin's rod domain. Biophys. J. 94 (2008) 1075-1083
77. Schwaiger I., Kardinal A., Schleicher M., Noegel A.A., and Rief M. A mechanical unfolding intermediate in an actin-crosslinking protein. Nat. Struct. Mol. Biol. 11 (2004) 81-85
78. Ferrer J.M., Lee H., Chen J., Pelz B., Nakamura F., Kamm R.D., and Lang M.J. Measuring molecular rupture forces between single actin filaments and actin-binding proteins. Proc. Natl. Acad. Sci. USA 105 (2008) 9221-9226
79. Yoshida N., Ogata T., Tanabe K., Li S., Nakazato M., Kohu K., Takafuta T., Shapiro S., Ohta Y., Satake M., et al. Filamin A-bound PEBP2 beta/CBF beta is retained in the cytoplasm and prevented from functioning as a partner of the Runx1 transcription factor. Mol. Cell. Biol. 25 (2005) 1003-1012
80. Lange S., Xiang F., Yakovenko A., Vihola A., Hackman P., Rostkova E., Kristensen J., Brandmeier B., Franzen G., Hedberg B., et al. The kinase domain of Titin controls muscle gene expression and protein turnover. Science 308 (2005) 1599-1603
81. Gräter, F., Shen, J., Jiang, H., Gautel, M., and Grubmüller, H. (2005). Mechanically induced titin kinase activation studied by force-probe molecular dynamics simulations. 88, 790-804.
82. Puchner E.M., Alexandrovich A., Kho A.L., Hensen U., Schäfer L.V., Brandmeier B., Gräter F., Grubmüller H., Gaub H.E., and Gautel M. Mechanoenzymatics of titin kinase. Proc. Natl. Acad. Sci. USA 105 (2008) 13385-13390
83. Rief M., Pascual J., Saraste M., and Gaub H.E. Single molecule force spectroscopy of spectrin repeats: Low unfolding forces in helix bundles. J. Mol. Biol. 286 (1999) 553-561
84. Law R., Carl P., Harper S., Dalhaimer P., Speicher D.W., and Discher D.E. Cooperativity in forced unfolding of tandem spectrin repeats. Biophys. J. 84 (2003) 533-544
85. Randles L.G., Rounsevell R.W.S., and Clarke J. Spectrin domains lose cooperativity in forced unfolding. Biophys. J. 92 (2007) 571-577
86. Law R., Harper S., Speicher D.W., and Discher D.E. Influence of lateral association on forced unfolding of antiparallel spectrin heterodimers. J. Biol. Chem. 279 (2004) 16410-16416
87. Bhasin N., Law R., Liao G., Safer D., Ellmer J., Discher B.M., Sweeney H.L., and Discher D.E. Molecular extensibility of mini-dystrophins and a dystrophin rod construct. J. Mol. Biol. 352 (2005) 795-806
88. Lu H., Isralewitz B., Krammer A., Vogel V., and Schulten K. Unfolding of Titin immunoglobulin domains by steered molecular dynamics simulation. Biophys. J. 75 (1998) 662-671
89. Law R., Liao G., Harper S., Yang G., Speicher D.W., and Discher D.E. Pathway shifts and thermal softening in temperature-coupled forced unfolding of spectrin domains. Biophys. J. 85 (2003) 3286-3293
90. Schlierf M., and Rief M. Temperature softening of a protein in single-molecule experiments. J. Mol. Biol. 354 (2005) 497-503
91. An X., Guo X., Zhang X., Baines A.J., Debnath G., Moyo M., Salomao M., Bhasin N., Johnson C., Discher D., et al. Conformational stabilities of the structural repeats of erythroid spectrin and their functional implications. J. Biol. Chem. 281 (2006) 10527-10532
92. Brown A.E.X., Hategan A., Safer D., Goldman Y., and Discher D.E. Cross-correlated TIRF/AFM reveals asymmetric distributions of force generating heads along self-assembled, 'synthetic' myosin filaments. Biophys. J. 96 (2009) 1952-1960
93. Engler A.J., Carag-Krieger C., Johnson C.P., Raab M., Tang H.-Y., Speicher D.W., Sanger J.W., Sanger J.M., and Discher D.E. Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J. Cell Sci. 121 (2008) 3794-3802
94. Colet J.P., Allali Y., Lesty C., Tanguy M.L., Silvain J., Ankri A., Blanchet B., Dumaine R., Gianetti J., Payot L., et al. Altered fibrin architecture is associated with hypofibrinolysis and premature coronary atherothrombosis. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 2567-2573