Force-induced fibronectin assembly and matrix remodeling in a 3D microtissue model of tissue morphogenesis

Integrative Biology (United Kingdom)

Volumn 4, Issue 10, 2012, Pages 1164-1174

  Legant, Wesley R ^a   Chen, Christopher S ^a   Vogel, Viola ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN GEL; COLLAGEN TYPE 1; FIBRONECTIN; COLLAGEN; SILICON;

ANIMAL CELL; ARTICLE; BIOSENSOR; CULTURE MEDIUM; ENCAPSULATION; FIBROBLAST; FLUORESCENCE RESONANCE ENERGY TRANSFER; FORCE; GEOMETRY; MICROTECHNOLOGY; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN LOCALIZATION; WOUND HEALING; ALGORITHM; ANIMAL; CELL STRAIN 3T3; CHEMISTRY; CONFOCAL MICROSCOPY; DRUG DELIVERY SYSTEM; EXTRACELLULAR MATRIX; FLUORESCENCE MICROSCOPY; GENETIC PROCEDURES; MECHANICAL STRESS; METABOLISM; METHODOLOGY; MOUSE; STATISTICAL MODEL; TIME;

ALGORITHMS; ANIMALS; BIOSENSING TECHNIQUES; COLLAGEN; DRUG DELIVERY SYSTEMS; EXTRACELLULAR MATRIX; FIBRONECTINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MODELS, STATISTICAL; MORPHOGENESIS; NIH 3T3 CELLS; PROTEIN CONFORMATION; SILICON; STRESS, MECHANICAL; TIME FACTORS; WOUND HEALING;

EID: 84874439260     PISSN: 17579694     EISSN: 17579708     Source Type: Journal    
DOI: 10.1039/c2ib20059g     Document Type: Article

References (42)

1. F. Grinnell W. M. Petroll Cell motility and mechanics in three-dimensional collagen matrices Annu. Rev. Cell Dev. Biol. 2010 26 335 361
2. S. Nakagawa P. Pawelek F. Grinnell Extracellular matrix organization modulates fibroblast growth and growth factor responsiveness Exp. Cell Res. 1989 182 572 582
3. D. Stopak A. K. Harris Connective tissue morphogenesis by fibroblast traction. I. Tissue culture observations Dev. Biol. (Amsterdam, Neth.) 1982 90 383 398
4. D. Stopak N. K. Wessells A. K. Harris Morphogenetic rearrangement of injected collagen in developing chicken limb buds Proc. Natl. Acad. Sci. U. S. A. 1985 82 2804 2808
5. T. Eschenhagen C. Fink U. Remmers H. Scholz J. Wattchow J. Weil W. Zimmermann H. H. Dohmen H. Schafer N. Bishopric T. Wakatsuki E. L. Elson Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system FASEB J. 1997 11 683 694
6. D. G. Wallace J. Rosenblatt Collagen gel systems for sustained delivery and tissue engineering Adv. Drug Delivery Rev. 2003 55 1631 1649
7. W. H. Zimmermann I. Melnychenko G. Wasmeier M. Didie H. Naito U. Nixdorff A. Hess L. Budinsky K. Brune B. Michaelis S. Dhein A. Schwoerer H. Ehmke T. Eschenhagen Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts Nat. Med. 2006 12 452 458
8. Y. Adachi T. Mio K. Takigawa I. Striz D. J. Romberger J. R. Spurzem S. I. Rennard Fibronectin production by cultured human lung fibroblasts in three-dimensional collagen gel culture In Vitro Cell. Dev. Biol.: Anim. 1998 34 203 210
9. R. Chiquet-Ehrismann M. Tannheimer M. Koch A. Brunner J. Spring D. Martin S. Baumgartner M. Chiquet Tenascin-C expression by fibroblasts is elevated in stressed collagen gels J. Cell Biol. 1994 127 2093 2101
10. E. A. Davenport P. Nettesheim Type I collagen gel modulates extracellular matrix synthesis and deposition by tracheal epithelial cells Exp. Cell Res. 1996 223 155 162
11. K. E. Kadler A. Hill E. G. Canty-Laird Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators Curr. Opin. Cell Biol. 2008 20 495 501
12. K. S. Midwood L. V. Williams J. E. Schwarzbauer Tissue repair and the dynamics of the extracellular matrix Int. J. Biochem. Cell Biol. 2004 36 1031 1037
13. J. Sottile D. C. Hocking Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions Mol. Biol. Cell 2002 13 3546 3559
14. J. Sottile F. Shi I. Rublyevska H. Y. Chiang J. Lust J. Chandler Fibronectin-dependent collagen I deposition modulates the cell response to fibronectin Am. J. Physiol. Cell Physiol. 2007 293 C1934 C1946
15. B. J. Dzamba K. R. Jakab M. Marsden M. A. Schwartz D. W. DeSimone Cadherin adhesion, tissue tension, and noncanonical Wnt signaling regulate fibronectin matrix organization Dev. Cell 2009 16 421 432
16. C. A. Lemmon C. S. Chen L. H. Romer Cell traction forces direct fibronectin matrix assembly Biophys. J. 2009 96 729 738
17. 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 e268
18. 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 141 539 551
19. K. E. Kubow E. Klotzsch M. L. Smith D. Gourdon W. C. Little V. Vogel Crosslinking of cell-derived 3D scaffolds up-regulates the stretching and unfolding of new extracellular matrix assembled by reseeded cells Integr. Biol. 2009 1 635 648
20. M. Chabria S. Hertig M. L. Smith V. Vogel Stretching fibronectin fibres disrupts binding of bacterial adhesins by physically destroying an epitope Nat. Commun. 2010 1 135
21. W. C. Little R. Schwartlander M. L. Smith D. Gourdon V. Vogel Stretched extracellular matrix proteins turn fouling and are functionally rescued by the chaperones albumin and casein Nano Lett. 2009 9 4158 4167
22. 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 5139 5143
23. T. Boudou W. R. Legant A. Mu M. A. Borochin N. Thavandiran M. Radisic P. W. Zandstra J. A. Epstein K. B. Margulies C. S. Chen A microfabricated platform to measure and manipulate the mechanics of engineered cardiac microtissues Tissue Eng., Part A 2012 18 910 919
24. W. R. Legant A. Pathak M. T. Yang V. S. Deshpande R. M. McMeeking C. S. Chen Microfabricated tissue gauges to measure and manipulate forces from 3D microtissues Proc. Natl. Acad. Sci. U. S. A. 2009 106 10097 10102
25. M. Antia G. Baneyx K. E. Kubow V. Vogel Fibronectin in aging extracellular matrix fibrils is progressively unfolded by cells and elicits an enhanced rigidity response Faraday Discuss. 2008 139 229 249
26. L. Baugh V. Vogel Structural changes of fibronectin adsorbed to model surfaces probed by fluorescence resonance energy transfer J. Biomed. Mater. Res., Part A 2004 69 525 534
27. V. Vogel Mechanotransduction involving multimodular proteins: converting force into biochemical signals Annu. Rev. Biophys. Biomol. Struct. 2006 35 459 488
28. D. C. Hocking J. Sottile K. J. Langenbach Stimulation of integrin-mediated cell contractility by fibronectin polymerization J. Biol. Chem. 2000 275 10673 10682
29. Y. Liu R. Yanai Y. Lu K. Kimura T. Nishida Promotion by fibronectin of collagen gel contraction mediated by human corneal fibroblasts Exp. Eye Res. 2006 83 1196 1204
30. 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 2153 2158
31. F. Baaijens C. Bouten N. Driessen Modeling collagen remodeling J. Biomech. 2010 43 166 175
32. V. H. Barocas R. T. Tranquillo An anisotropic biphasic theory of tissue-equivalent mechanics: the interplay among cell traction, fibrillar network deformation, fibril alignment, and cell contact guidance J. Biomech. Eng. 1997 119 137 145
33. E. A. Sander T. Stylianopoulos R. T. Tranquillo V. H. Barocas Image-based multiscale modeling predicts tissue-level and network-level fiber reorganization in stretched cell-compacted collagen gels Proc. Natl. Acad. Sci. U. S. A. 2009 106 17675 17680
34. A. D. Freed T. C. Doehring Elastic model for crimped collagen fibrils J. Biomech. Eng. 2005 127 587 593
35. M. A. Lan C. A. Gersbach K. E. Michael B. G. Keselowsky A. J. Garcia Myoblast proliferation and differentiation on fibronectin-coated self-assembled monolayers presenting different surface chemistries Biomaterials 2005 26 4523 4531
36. M. Salmeron-Sanchez P. Rico D. Moratal T. T. Lee J. E. Schwarzbauer A. J. Garcia Role of material-driven fibronectin fibrillogenesis in cell differentiation Biomaterials 2011 32 2099 2105
37. T. Rozario B. Dzamba G. F. Weber L. A. Davidson D. W. DeSimone The physical state of fibronectin matrix differentially regulates morphogenetic movements in vivo Dev. Biol. 2009 327 386 398
38. B. Geiger J. P. Spatz A. D. Bershadsky Environmental sensing through focal adhesions Nat. Rev. Mol. Cell Biol. 2009 10 21 33
39. E. Klotzsch M. L. Smith K. E. Kubow S. Muntwyler W. C. Little F. Beyeler D. Gourdon B. J. Nelson V. Vogel Fibronectin forms the most extensible biological fibers displaying switchable force-exposed cryptic binding sites Proc. Natl. Acad. Sci. U. S. A. 2009 106 18267 18272
40. A. Villa E. Trachsel M. Kaspar C. Schliemann R. Sommavilla J. N. Rybak C. Rosli L. Borsi D. Neri A high-affinity human monoclonal antibody specific to the alternatively spliced EDA domain of fibronectin efficiently targets tumor neo-vasculature in vivo Int. J. Cancer 2008 122 2405 2413
41. A. M. Bazen S. H. Gerez Systematic Methods for the Computation of the Directional Fields and Singular Points of Fingerprints IEEE Trans. Pattern. Anal. Mach. Intell. 2002 24 905 919
42. Y. Gao M. L. Kilfoil Accurate detection and complete tracking of large populations of features in three dimensions Opt. Express 2009 17 4685 4704