Fibronectin in aging extracellular matrix fibrils is progressively unfolded by cells and elicits an enhanced rigidity response

Faraday Discussions

Volumn 139, Issue , 2008, Pages 229-249

  Antia, Meher ^a,b   Baneyx, Gretchen ^a,b   Kubow, Kristopher E ^a   Vogel, Viola ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACRYLIC ACID RESIN; ACTIN; BETA1 INTEGRIN; FIBRONECTIN; POLYACRYLAMIDE;

ANIMAL; ARTICLE; CELL STRAIN 3T3; CHEMISTRY; EXTRACELLULAR MATRIX; FLUORESCENCE RESONANCE ENERGY TRANSFER; MOUSE; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; STRESS FIBER;

ACRYLIC RESINS; ACTINS; ANIMALS; ANTIGENS, CD29; EXTRACELLULAR MATRIX; FIBRONECTINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; MICE; NIH 3T3 CELLS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; STRESS FIBERS;

EID: 50849090315     PISSN: 13596640     EISSN: 13645498     Source Type: Journal    
DOI: 10.1039/b718714a     Document Type: Article

References (88)

1. R. J. Pelham Jr. Y. Wang Cell locomotion and focal adhesions are regulated by substrate flexibility Proc. Natl. Acad. Sci. U. S. A. 1997 94 25 13661 13665
2. S. R. Peyton A. J. Putnam Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion J. Cell. Physiol. 2005 204 1 198 209
3. C. M. Lo H. B. Wang M. Dembo Y. L. Wang Cell movement is guided by the rigidity of the substrate Biophys. J. 2000 79 1 144 152
4. J. H. Wang B. P. Thampatty J. S. Lin H. J. Im Mechanoregulation of gene expression in fibroblasts Gene 2007 391 1-2 1 15
5. D. MacKenna S. R. Summerour F. J. Villarreal Role of mechanical factors in modulating cardiac fibroblast function and extracellular matrix synthesis Cardiovasc. Res. 2000 46 2 257 263
6. M. J. Paszek N. Zahir K. R. Johnson J. N. Lakins G. I. Rozenberg A. Gefen C. A. Reinhart-King S. S. Margulies M. Dembo D. Boettiger D. A. Hammer V. M. Weaver Tensional homeostasis and the malignant phenotype Cancer Cell 2005 8 3 241 254
7. H. B. Wang M. Dembo Y. L. Wang Substrate flexibility regulates growth and apoptosis of normal but not transformed cells Am. J. Physiol.: Cell Physiol. 2000 279 5 C1345 1350
8. M. Tamada M. P. Sheetz Y. Sawada Activation of a signaling cascade by cytoskeleton stretch Dev. Cell 2004 7 5 709 718
9. A. J. Engler S. Sen H. L. Sweeney D. E. Discher Matrix elasticity directs stem cell lineage specification Cell 2006 126 4 677 89
10. P. A. Janmey D. A. Weitz Dealing with mechanics: mechanisms of force transduction in cells Trends Biochem. Sci. 2004 29 7 364 70
11. T. Yeung P. C. Georges L. A. Flanagan B. Marg M. Ortiz M. Funaki N. Zahir W. Ming V. Weaver P. A. Janmey Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion Cell Motil. Cytoskeleton 2005 60 1 24 34
12. P. C. Georges P. A. Janmey Cell type-specific response to growth on soft materials J. Appl. Physiol. 2005 98 4 1547 53
13. D. E. Discher P. Janmey Y. L. Wang Tissue cells feel and respond to the stiffness of their substrate Science 2005 310 5751 1139 43
14. E. J. Semler P. A. Lancin A. Dasgupta P. V. Moghe Engineering hepatocellular morphogenesis and function via ligand-presenting hydrogels with graded mechanical compliance Biotechnol. Bioeng. 2005 89 3 296 307
15. E. Cukierman R. Pankov D. R. Stevens K. M. Yamada Taking cell-matrix adhesions to the third dimension Science 2001 294 5547 1708 1712
16. M. A. Wozniak R. Desai P. A. Solski C. J. Der P. J. Keely ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix J. Cell Biol. 2003 163 3 583 95
17. K. Wolf Y. I. Wu Y. Liu J. Geiger E. Tam C. Overall M. S. Stack P. Friedl Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion Nat. Cell Biol. 2007 9 8 893 904
18. K. E. Gregory R. N. Ono N. L. Charbonneau C. L. Kuo D. R. Keene H. P. Bachinger L. Y. Sakai The prodomain of BMP-7 targets the BMP-7 complex to the extracellular matrix J. Biol. Chem. 2005 280 30 27970 80
19. S. L. Dallas K. Miyazono T. M. Skerry G. R. Mundy L. F. Bonewald Dual role for the latent transforming growth factor-beta binding protein in storage of latent TGF-beta in the extracellular matrix and as a structural matrix protein J. Cell Biol. 1995 131 2 539 49
20. J. Taipale J. Keski-Oja Growth factors in the extracellular matrix FASEB J. 1997 11 1 51 9
21. A. Sarikaya R. Record C. C. Wu B. Tullius S. Badylak M. Ladisch Antimicrobial activity associated with extracellular matrices Tissue Eng. 2002 8 1 63 71
22. M. L. Barilla S. E. Carsons Fibronectin fragments and their role in inflammatory arthritis Semin. Arthritis Rheum. 2000 29 4 252 65
23. M. Bailly Connecting cell adhesion to the actin polymerization machinery: vinculin as the missing link? Trends Cell Biol. 2003 13 4 163 5
24. C. Brakebusch R. Fassler The integrin-actin connection, an eternal love affair EMBO J. 2003 22 10 2324 2333
25. C. S. Chen J. Tan J. Tien Mechanotransduction at cell-matrix and cell-cell contacts Annu. Rev. Biomed. Eng. 2004 6 275 302
26. D. Choquet D. P. Felsenfeld M. P. Sheetz Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages Cell 1997 88 1 39 48
27. B. Geiger A. Bershadsky R. Pankov K. M. Yamada Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk Nat. Rev. Mol. Cell Biol. 2001 2 11 793 805
28. R. O. Hynes, Fibronectins, Springer, New York, 1990
29. E. Zamir M. Katz Y. Posen N. Erez K. M. Yamada B. Z. Katz S. Lin D. C. Lin A. Bershadsky Z. Kam B. Geiger Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts Nat. Cell Biol. 2000 2 4 191 196
30. D. C. Hocking J. Sottile P. J. McKeown-Longo Fibronectin's III-1 module contains a conformation-dependent binding site for the amino-terminal region of fibronectin J. Biol. Chem. 1994 269 29 19183 19187
31. C. Zhong M. Chrzanowska-Wodnicka J. Brown A. Shaub A. M. Belkin K. Burridge Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly J. Cell Biol. 1998 141 2 539 551
32. G. Baneyx L. Baugh V. Vogel Coexisting conformations of fibronectin in cell culture imaged using fluorescence resonance energy transfer Proc. Natl. Acad. Sci. U. S. A. 2001 98 25 14464 14468
33. M. L. Smith D. Gourdon W. C. Little K. E. Kubow R. A. Eguiluz S. Luna-Morris V. Vogel Force-induced unfolding of fibronectin in the extracellular matrix of living cells PLoS Biol. 2007 5 10 e268
34. Y. Mao J. E. Schwarzbauer Fibronectin fibrillogenesis, a cell-mediated matrix assembly process Matrix Biol. 2005 24 6 389 99
35. M. Gao D. Craig O. Lequin I. D. Campbell V. Vogel K. Schulten Structure and functional significance of mechanically unfolded fibronectin type III1 intermediates Proc. Natl. Acad. Sci. U. S. A. 2003 100 25 14784 14789
36. K. C. Ingham S. A. Brew S. Huff S. V. Litvinovich Cryptic self-association sites in type III modules of fibronectin J. Biol. Chem. 1997 272 3 1718 1724
37. A. Krammer H. Lu B. Isralewitz K. Schulten V. Vogel Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch Proc. Natl. Acad. Sci. U. S. A. 1999 96 4 1351 1356
38. G. Baneyx L. Baugh V. Vogel Fibronectin extension and unfolding within cell matrix fibrils controlled by cytoskeletal tension Proc. Natl. Acad. Sci. U. S. A. 2002 99 8 5139 5143
39. M. Antia L. D. Islas D. A. Boness G. Baneyx V. Vogel Single molecule fluorescence studies of surface-adsorbed fibronectin Biomaterials 2006 27 5 679 90
40. M. Halter M. Antia V. Vogel Fibronectin conformational changes induced by adsorption to liposomes J. Controlled Release 2005 101 1-3 209 22
41. L. Baugh V. Vogel Structural changes of fibronectin adsorbed to model surfaces probed by fluorescence resonance energy transfer J. Biomed. Mater. Res. 2004 69A 3 525 534
42. K. A. Beningo M. Dembo I. Kaverina J. V. Small Y. L. Wang Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts J. Cell Biol. 2001 153 4 881 888
43. A. Engler L. Richert J. Wong C. Picart D. Discher Surface probe measurements of the elasticity of sectioned tissue, thin gels and polyelectrolyte multilayer films: Correlations between substrate stiffness and cell adhesion Surf. Sci. 2004 570 142 154
44. R. E. Mahaffy C. K. Shih F. C. MacKintosh J. Kas Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells Phys. Rev. Lett. 2000 85 4 880 883
45. K. A. Beningo C. M. Lo Y. L. Wang Flexible polyacrylamide substrata for the analysis of mechanical interactions at cell-substratum adhesions Methods Cell Biol. 2002 69 325 339
46. P. J. McKeown-Longo D. F. Mosher Interaction of the 70,000-mol-wt amino-terminal fragment of fibronectin with the matrix-assembly receptor of fibroblasts J. Cell Biol. 1985 100 2 364 74
47. K. J. Johnson H. Sage G. Briscoe H. P. Erickson The compact conformation of fibronectin is determined by intramolecular ionic interactions J. Biol. Chem. 1999 274 22 15473 15479
48. M. Y. Khan M. S. Medow S. A. Newman Unfolding transitions of fibronectin and its domains. Stabilization and structural alteration of the N-terminal domain by heparin Biochem. J. 1990 270 1 33 38
49. W. C. Little M. L. Smith U. Ebneter V. Vogel Assay to mechanically tune and optically probe fibrillar fibronectin conformations from fully relaxed to breakage Matrix Biol. 2008
50. R. Gueta D. Barlam R. Z. Shneck I. Rousso Measurement of the mechanical properties of isolated tectorial membrane using atomic force microscopy Proc. Natl. Acad. Sci. U. S. A. 2006 103 40 14790 5
51. J. L. Sechler H. Rao A. M. Cumiskey I. Vega-Colon M. S. Smith T. Murata J. E. Schwarzbauer A novel fibronectin binding site required for fibronectin fibril growth during matrix assembly J. Cell Biol. 2001 154 5 1081 1088
52. T. H. Barker G. Baneyx M. Cardo-Vila G. A. Workman M. Weaver P. M. Menon S. Dedhar S. A. Rempel W. Arap R. Pasqualini V. Vogel E. H. Sage SPARC regulates extracellular matrix organization through its modulation of integrin-linked kinase activity J. Biol. Chem. 2005 280 43 36483 93
53. Y. Mao J. E. Schwarzbauer Accessibility to the fibronectin synergy site in a 3D matrix regulates engagement of α5β1 versus αvβ3 integrin receptors Cell Commun. Adhes. 2006 13 5-6 267 77
54. M. D. Amatangelo D. E. Bassi A. J. Klein-Szanto E. Cukierman Stroma-derived three-dimensional matrices are necessary and sufficient to promote desmoplastic differentiation of normal fibroblasts Am. J. Pathol. 2005 167 2 475 88
55. J. T. Yang R. O. Hynes Fibronectin receptor functions in embryonic cells deficient in α 5 β 1 integrin can be replaced by α V integrins Mol. Biol. Cell 1996 7 11 1737 1748
56. C. Wu J. S. Bauer R. L. Juliano J. A. McDonald The α 5 β 1 integrin fibronectin receptor, but not the α 5 cytoplasmic domain, functions in an early and essential step in fibronectin matrix assembly J. Biol. Chem. 1993 268 29 21883 21888
57. K. Wennerberg L. Lohikangas D. Gullberg M. Pfaff S. Johansson R. Fassler β 1 integrin-dependent and -independent polymerization of fibronectin J. Cell Biol. 1996 132 1-2 227 238
58. R. Zaidel-Bar C. Ballestrem Z. Kam B. Geiger Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells J. Cell Sci. 2003 116 22 4605 4613
59. Y. Mao J. E. Schwarzbauer Stimulatory effects of a three-dimensional microenvironment on cell-mediated fibronectin fibrillogenesis J. Cell Sci. 2005 118 Pt 19 4427 36
60. N. I. Abu-Lail T. Ohashi R. L. Clark H. P. Erickson S. Zauscher Understanding the elasticity of fibronectin fibrils: Unfolding strengths of FN-III and GFP domains measured by single molecule force spectroscopy Matrix Biol. 2006 25 3 175 184
61. H. P. Erickson 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. U. S. A. 1994 91 21 10114 10118
62. T. Ohashi D. P. Kiehart H. P. Erickson Dynamics and elasticity of the fibronectin matrix in living cell culture visualized by fibronectin-green fluorescent protein Proc. Natl. Acad. Sci. U. S. A. 1999 96 5 2153 2158
63. W. C. Little M. L. Smith U. Ebneter V. Vogel Assay to mechanically tune and optically probe fibrillar fibronectin conformations from fully relaxed to breakage Matrix Biol. 2008
64. V. Vogel Mechanotransduction involving multimodular proteins: converting force into biochemical signals Annu. Rev. Biophys. Biomol. Struct. 2006 35 459 88
65. W. Liu L. M. Jawerth E. A. Sparks M. R. Falvo R. R. Hantgan R. Superfine S. T. Lord M. Guthold Fibrin fibers have extraordinary extensibility and elasticity Science 2006 313 5787 634
66. L. Y. Leung D. Tian C. P. Brangwynne D. A. Weitz D. J. Tschumperlin A new microrheometric approach reveals individual and cooperative roles for TGF-β1 and IL-1β in fibroblast-mediated stiffening of collagen gels FASEB J. 2007
67. P. Sivakumar A. Czirok B. J. Rongish V. P. Divakara Y. P. Wang S. L. Dallas New insights into extracellular matrix assembly and reorganization from dynamic imaging of extracellular matrix proteins in living osteoblasts J. Cell Sci. 2006 119 Pt 7 1350 60
68. X. Wu Y. A. Dzenis Size effect in polymer nanofibers under tension J. Appl. Phys. 2007 102 4 044306 044312
69. C. Storm J. J. Pastore F. C. MacKintosh T. C. Lubensky P. A. Janmey Nonlinear elasticity in biological gels Nature 2005 435 7039 191 4
70. N. Wang J. P. Butler D. E. Ingber Mechanotransduction across the cell surface and through the cytoskeleton Science 1993 260 5111 1124 7
71. J. Diez Mechanisms of cardiac fibrosis in hypertension J. Clin. Hypertens. 2007 9 7 546 50
72. A. S. Meshel Q. Wei R. S. Adelstein M. P. Sheetz Basic mechanism of three-dimensional collagen fibre transport by fibroblasts Nat. Cell Biol. 2005 7 2 157 64
73. P. Fernandez P. A. Pullarkat A. Ott A master relation defines the nonlinear viscoelasticity of single fibroblasts Biophys. J. 2006 90 10 3796 805
74. T. Wakatsuki E. L. Elson Reciprocal interactions between cells and extracellular matrix during remodeling of tissue constructs Biophys. Chem. 2003 100 1-3 593 605
75. C. Streuli Extracellular matrix remodelling and cellular differentiation Curr. Opin. Cell Biol. 1999 11 5 634 40
76. J. Sottile J. Chandler Fibronectin matrix turnover occurs through a caveolin-1-dependent process Mol. Biol. Cell 2005 16 2 757 68
77. M. D. Pierschbacher E. Ruoslahti Variants of the cell recognition site of fibronectin that retain attachment-promoting activity Proc. Natl. Acad. Sci. U. S. A. 1984 81 19 5985 8
78. J. Takagi K. Strokovich T. A. Springer T. Walz Structure of integrin α5β1 in complex with fibronectin EMBO J. 2003 22 18 4607 15
79. S. D. Redick D. L. Settles G. Briscoe H. P. Erickson Defining fibronectin's cell adhesion synergy site by site-directed mutagenesis J. Cell Biol. 2000 149 2 521 7
80. A. Sharma J. A. Askari M. J. Humphries E. Y. Jones D. I. Stuart Crystal structure of a heparin- and integrin-binding segment of human fibronectin EMBO J. 1999 18 6 1468 79
81. A. P. Mould M. J. Humphries Identification of a novel recognition sequence for the integrin α 4 α 1 in the COOH-terminal heparin-binding domain of fibronectin EMBO J. 1991 10 13 4089 95
82. S. Takahashi M. Leiss M. Moser T. Ohashi T. Kitao D. Heckmann A. Pfeifer H. Kessler J. Takagi H. P. Erickson R. Fassler The RGD motif in fibronectin is essential for development but dispensable for fibril assembly J. Cell Biol. 2007 178 1 167 78
83. F. Curnis R. Longhi L. Crippa A. Cattaneo E. Dondossola A. Bachi A. Corti Spontaneous formation of l-isoaspartate and gain of function in fibronectin J. Biol. Chem. 2006 281 47 36466 76
84. D. C. Hocking Fibronectin matrix deposition and cell contractility: implications for airway remodeling in asthma Chest 2002 122 6 Suppl 275S 278S
85. K. C. Ingham S. A. Brew H. P. Erickson Localization of a cryptic binding site for tenascin on fibronectin J. Biol. Chem. 2004 279 27 28132 5
86. J. Schnepel H. Tschesche The proteolytic activity of the recombinant cryptic human fibronectin type IV collagenase from E. coli expression J. Protein Chem. 2000 19 8 685 92
87. J. Schnepel J. Unger H. Tschesche Recombinant cryptic human fibronectinase cleaves actin and myosin: substrate specificity and possible role in muscular dystrophy Biol. Chem. 2001 382 12 1707 14
88. K. J. Langenbach J. Sottile Identification of protein-disulfide isomerase activity in fibronectin J. Biol. Chem. 1999 274 11 7032 8