Regulating tension in three-dimensional culture environments

Experimental Cell Research

Volumn 319, Issue 16, 2013, Pages 2447-2459

  Kural, Mehmet Hamdi ^a   Billiar, Kristen Lawrence ^a,b  

^a Worcester Polytechnic Institute   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

BioMEMS; Collagen gel; Extracellular matrix; Fibrin gel; Mechanobiology; Stiffness; Tension

Indexed keywords

COLLAGEN;

CELL CULTURE; CELL FATE; CELL FUNCTION; HUMAN; HUMAN CELL; IN VIVO STUDY; MECHANOTRANSDUCTION; MODULATION; PRIORITY JOURNAL; REVIEW; TENSION;

EID: 84883551663     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.06.019     Document Type: Review

References (126)

1. Wang J.H., Li B. Mechanics rules cell biology. Sports Med. Arthroscopy Rehabil. Ther. Technol.: SMARTT 2010, 2:16.
2. Huang S., Ingber D.E. The structural and mechanical complexity of cell-growth control. Nat. Cell Biol. 1999, 1:E131-E138.
3. Altman G.H., Horan R.L., Martin I., Farhadi J., Stark P.R.H., Volloch V., Richmond J.C., Vunjak-Novakovic G., Kaplan D.L. Cell differentiation by mechanical stress. FASEB J. 2002, 16:270-272.
4. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
5. Ingber D.E. Mechanobiology and diseases of mechanotransduction. Ann. Med. 2003, 35:564-577.
6. Chen C.S., Tan J., Tien J. Mechanotransduction at cell-matrix and cell-cell contacts. Annu. Rev. Biomed. Eng. 2004, 6:275-302.
7. Schwarz U.S. United we stand: Integrating the actin cytoskeleton and cell-matrix adhesions in cellular mechanotransduction. J. Cell Sci. 2012, 125:3051-3060.
8. Ingber D.E. Cellular mechanotransduction: putting all the pieces together again. FASEB J. 2006, 20:811-827.
9. Grinnell F. Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol. 2003, 13:264-269.
10. Brown R.A., Prajapati R., McGrouther D.A., Yannas I.V., Eastwood M. Tensional homeostasis in dermal fibroblasts: mechanical responses to mechanical loading in three-dimensional substrates. J. Cell Physiol. 1998, 175:323-332.
11. Grinnell F., Petroll W.M. Cell motility and mechanics in three-dimensional collagen matrices. Annu. Rev. Cell Dev. Biol. 2010, 26:335-361.
12. Harris A.K., Wild P., Stopak D. Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 1980, 208:177-179.
13. Pelham R.J., Wang Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. PNAS 1997, 94:13661-13665.
14. Leung D.Y., Glagov S., Mathews M.B. Cyclic stretching stimulates synthesis of matrix components by arterial smooth muscle cells in vitro. Science 1976, 191:475-477.
15. Discher D.E., Janmey P., Wang Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
16. Weiss P. Cellular dynamics. Rev. Mod. Phys. 1959, 31:11-20.
17. Elsdale T., Bard J. Collagen substrata for studies on cell behavior. J. Cell Biol. 1972, 54:626-637.
18. Bell E., Ivarsson B., Merril C. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. PNAS 1979, 76(3):1274-1278.
19. Stopak D., Harris A.K. Connective tissue morphogenesis by fibroblast traction. I. Tissue culture observations. Dev. Biol. 1982, 90:383-398.
20. Billiar K.L. The mechanical environment of cells in collagen gel models. Cellular and Biomolecular Mechanics and Mechanobiology 2011, 201-245. Springer, Berlin Heidelberg. A. Gefen (Ed.).
21. Walpita D., Hay E. Studying actin-dependent processes in tissue culture. Nat. Rev. Mol. Cell Biol. 2002, 3:137-141.
22. Grinnell F. Fibroblast-collagen-matrix contraction: growth-factor signalling and mechanical loading. Trends Cell Biol. 2000, 10:362-365.
23. Roy P., Petroll W.M., Chuong C.J., Cavanagh H.D. J.V. Jester Effect of cell migration on the maintenance of tension on a collagen matrix. Ann. Biomed. Eng. 1999, 27:721-730.
24. Hay E.D. Extracellular matrix alters epithelial differentiation. Curr. Opin. Cell Biol. 1993, 5:1029-1035.
25. Petersen O.W., Rønnov-Jessen L., Howlett A.R., Bissell M.J. Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. PNAS 1992, 89:9064-9068.
26. John J., Quinlan A.T., Silvestri C., Billiar K. Boundary stiffness regulates fibroblast behavior in collagen gels. Ann. Biomed. Eng. 2010, 38:658-673.
27. Schwartz M.A., Chen C.S. Cell biology. Deconstructing dimensionality. Science 2013, 339:402-404.
28. Pedersen J.A., Swartz M.A. Mechanobiology in the third dimension. Ann Biomed Eng 2005, 33:1469-1490.
29. Baker B.M., Chen C.S. Deconstructing the third dimension: how 3D culture microenvironments alter cellular cues. J. Cell Sci. 2012, 125:3015-3024.
30. Cukierman E., Pankov R., Stevens D.R., Yamada K.M. Taking cell-matrix adhesions to the third dimension. Science 2001, 294:1708-1712.
31. Gieni R.S., Hendzel M.J. Mechanotransduction from the ECM to the genome: are the pieces now in place?. J. Cell. Biochem. 2008, 104:1964-1987.
32. Wipff P.-J., Rifkin D.B., Meister J.-J., Hinz B. Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J. Cell Biol. 2007, 179:1311-1323.
33. Cummings C.L., Gawlitta D., Nerem R.M., Stegemann J.P. Properties of engineered vascular constructs made from collagen, fibrin, and collagen-fibrin mixtures. Biomaterials 2004, 25:3699-3706.
34. Ulrich T.A., Jain A., Tanner K., MacKay J.L., Kumar S. Probing cellular mechanobiology in three-dimensional culture with collagen-agarose matrices. Biomaterials 2010, 31:1875-1884.
35. Janmey P.A., Winer J.P., Weisel J.W. Fibrin gels and their clinical and bioengineering applications. J. R. Soc. Interface 2009, 6:1-10.
36. Tuan T.L., Song A., Chang S., Younai S., Nimni M.E. In vitro fibroplasia: matrix contraction, cell growth, and collagen production of fibroblasts cultured in fibrin gels. Exp Cell Res 1996, 223:127-134.
37. Willerth S.M., Arendas K.J., Gottlieb D.I., Sakiyama-Elbert S.E. Optimization of fibrin scaffolds for differentiation of murine embryonic stem cells into neural lineage cells. Biomaterials 2006, 27:5990-6003.
38. Ye Q., Zünd G., Jockenhoevel S., Hoerstrup S.P., Schoeberlein a., Grunenfelder J., Turina M. Tissue engineering in cardiovascular surgery: new approach to develop completely human autologous tissue. Eur. J. Cardiothorac. Surg. 2000, 17:449-454.
39. Grassl E.D., Oegema T.R., Tranquillo R.T. Fibrin as an alternative biopolymer to type-I collagen for the fabrication of a media equivalent. J. Biomed. Mater. Res. 2002, 60:607-612.
40. Roeder B.A., Kokini K., Sturgis J.E., Robinson J.P., Voytik-Harbin S.L. Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure. J. Biomech. Eng. 2002, 124:214.
41. Yang Y.L., Kaufman L.J. Rheology and confocal reflectance microscopy as probes of mechanical properties and structure during collagen and collagen/hyaluronan self-assembly. Biophys. J. 2009, 96:1566-1585.
42. Achilli M., Mantovani D. Tailoring mechanical properties of collagen-based scaffolds for vascular tissue engineering: the effects of pH, temperature and ionic strength on gelation. Polymers 2010, 2:664-680.
43. Hadjipanayi E., Mudera V., Brown R.A. Guiding cell migration in 3D: a collagen matrix with graded directional stiffness. Cell Motil Cytoskeleton 2009, 66:121-128.
44. Helary C., Bataille I., Abed A., Illoul C., Anglo A., Louedec L., Letourneur D., Meddahi-Pelle A., Giraud-Guille M.M. Concentrated collagen hydrogels as dermal substitutes. Biomaterials 2010, 31:481-490.
45. Kniazeva E., Putnam A. Endothelial cell traction and ECM density influence both capillary morphogenesis and maintenance in 3-D. Am. J. Physiol. Cell Physiol. 2009, 297:C179-C187.
46. Sieminski A.L., Hebbel R.P., Gooch K.J. The relative magnitudes of endothelial force generation and matrix stiffness modulate capillary morphogenesis in vitro. Exp. Cell Res. 2004, 297:574-584.
47. Shamloo A., Heilshorn S.C. Matrix density mediates polarization and lumen formation of endothelial sprouts in VEGF gradients. Lab Chip 2010, 10:3061-3068.
48. Evans M.C., Barocas V.H. The modulus of fibroblast-populated collagen gels is not determined by final collagen and cell concentration: Experiments and an inclusion-based model. J. Biomech. Eng. 2009, 131:7.
49. Nishiyama T., Tominaga N., Nakajima K., Hayashi T. Quantitative evaluation of the factors affecting the process of fibroblast-mediated collagen gel contraction by separating the process into three phases. Coll Relat. Res. 1988, 8:259-273.
50. Zhu Y.K., Umino T., Liu X.D., Wang H.J., Romberger D.J., Spurzem J.R., Rennard S.I. Contraction of fibroblast-containing collagen gels: Initial collagen concentration regulates the degree of contraction and cell survival. In Vitro Cell Dev. Biol. Anim. 2001, 37:10-16.
51. Miron-Mendoza M., Seemann J., Grinnell F. The differential regulation of cell motile activity through matrix stiffness and porosity in three dimensional collagen matrices. Biomaterials 2010, 31:6425-6435.
52. Raub C.B., Suresh V., Krasieva T., Lyubovitsky J., Mih J.D., Putnam A.J., Tromberg B.J., George S.C. Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy. Biophys. J. 2007, 92:2212-2222.
53. Carey S.P., Kraning-Rush C.M., Williams R.M., Reinhart-King C.A. Biophysical control of invasive tumor cell behavior by extracellular matrix microarchitecture. Biomaterials 2012, 33:4157-4165.
54. Takahashi A., Kita R., Shinozaki T., Kubota K., Kaibara M. Real space observation of three-dimensional network structure of hydrated fibrin gel. Colloid Polym. Sci. 2003, 281:832-838.
55. Ryan E.A., Mockros L.F., Weisel J.W., Lorand L. Structural origins of fibrin clot rheology. Biophys. J. 1999, 77:2813-2826.
56. Duong H., Wu B., Tawil B. Modulation of 3D fibrin matrix stiffness by intrinsic fibrinogen-thrombin compositions and by extrinsic cellular activity. Tissue Eng. A 2009, 15:1865-1876.
57. Brown R.A., Wiseman M., Chuo C.B., Cheema U., Nazhat S.N. Ultrarapid engineering of biomimetic materials and tissues: fabrication of nano- and microstructures by plastic compression. Adv. Funct. Mater. 2005, 15:1762-1770.
58. Mason B.N., Starchenko A., Williams R.M., Bonassar L.J., Reinhart-King C.A. Tuning three-dimensional collagen matrix stiffness independently of collagen concentration modulates endothelial cell behavior. Acta Biomater. 2013, 9:4635-4644.
59. Girton T.S., Oegema T.R., Grassl E.D., Isenberg B.C., Tranquillo R.T. Mechanisms of stiffening and strengthening in media-equivalents fabricated using glycation. J. Biomech. Eng. 2000, 122:216-223.
60. McCarthy A.D., Uemura T., Etcheverry S.B., Cortizo A.M. Advanced glycation endproducts interefere with integrin-mediated osteoblastic attachment to a type-I collagen matrix. Int. J. Biochem. Cell Biol. 2004, 36:840-848.
61. Motte S., Kaufman L.J. Strain stiffening in collagen I networks. Biopolymers 2013, 99:35-46.
62. Sundararaghavan H.G., Monteiro G.A., Lapin N.A., Chabal Y.J., Miksan J.R., Shreiber D.I. Genipin-induced changes in collagen gels: correlation of mechanical properties to fluorescence. J. Biomed. Mater. Res. A 2008, 87:308-320.
63. Brinkman W.T., Nagapudi K., Thomas B.S., Chaikof E.L. Photo-cross-linking of type I collagen gels in the presence of smooth muscle cells: mechanical properties, cell viability, and function. Biomacromolecules 2003, 4:890-895.
64. Paik D.C., Saito L.Y., Sugirtharaj D.D., Holmes J.W. Nitrite-induced cross-linking alters remodeling and mechanical properties of collagenous engineered tissues. Connect. Tissue Res. 2006, 47:163-176.
65. Francis-Sedlak M.E., Uriel S., Larson J.C., Greisler H.P., Venerus D.C., Brey E.M. Characterization of type I collagen gels modified by glycation. Biomaterials 2009, 30:1851-1856.
66. Bjork J.W., Johnson S.L., Tranquillo R.T. Ruthenium-catalyzed photo cross-linking of fibrin-based engineered tissue. Biomaterials 2011, 32:2479-2488.
67. Dare E.V., Griffith M., Poitras P., Kaupp J.A., Waldman S.D., Carlsson D.J., Dervin G., Mayoux C., Hincke M.T. Genipin cross-linked fibrin hydrogels for in vitro human articular cartilage tissue-engineered regeneration. Cells Tissues Organs 2009, 190:313-325.
68. Bensai{dotless}r̈d W., Triffitt J.T., Blanchat C., Oudina K., Sedel L., Petite H.A. Biodegradable fibrin scaffold for mesenchymal stem cell transplantation. Biomaterials 2003, 24:2497-2502.
69. Redden R.A., Doolin E.J. Collagen crosslinking and cell density have distinct effects on fibroblast-mediated contraction of collagen gels. Skin Res. Technol. 2003, 9:290-293.
70. Stevenson M.D., Sieminski A.L., McLeod C.M., Byfield F.J., Barocas V.H., Gooch K.J. Pericellular conditions regulate extent of cell-mediated compaction of collagen gels. Biophys. J. 2010, 99:19-28.
71. Helary C., Bataille I., Abed A., Illoul C., Anglo A., Louedec L., Letourneur D., Meddahi-Pellé A., Giraud-Guille M.M. Concentrated collagen hydrogels as dermal substitutes. Biomaterials 2010, 31:481-490.
72. Nakagawa S., Pawelek P., Grinnell F. Extracellular matrix organization modulates fibroblast growth and growth factor responsiveness. Exp. Cell Res. 1989, 182:572-582.
73. Legant W.R., Pathak A., Yang M.T., Deshpande V.S., McMeeking R.M., Chen C.S. Microfabricated tissue gauges to measure and manipulate forces from 3D microtissues. PNAS 2009, 106:10097-10102.
74. Boudou T., Legant W.R., Mu A., Borochin M.A., Thavandiran N., Radisic M., Zandstra P.W., Epstein J.A., Margulies K.B., Chen C.S. A microfabricated platform to measure and manipulate the mechanics of engineered cardiac microtissues. Tissue Eng. A 2012, 18:910-919.
75. Ahlfors J.E., Billiar K.L. Biomechanical and biochemical characteristics of a human fibroblast-produced and remodeled matrix. Biomaterials 2007, 28:2183-2191.
76. Arora P.D., Narani N., McCulloch C.A. The compliance of collagen gels regulates transforming growth factor-beta induction of alpha-smooth muscle actin in fibroblasts. Am. J. Pathol. 1999, 154:871-882.
77. Germain L., Jean A., Auger F.A., Garrel D.R. Human wound healing fibroblasts have greater contractile properties than dermal fibroblasts. J. Surg. Res. 1994, 57:268-273.
78. Yamato M., Adachi E., Yamamoto K., Hayashi T. Condensation of collagen fibrils to the direct vicinity of fibroblasts as a cause of gel contraction. J. Biochem. 1995, 117:940-946.
79. Knapp D.M., Tower T.T., Tranquillo R.T., Barocas V.H. Estimation of cell traction and migration in an isometric cell traction assay. AIChE J. 1999, 45:2628-2640.
80. Galie Pa Westfall M.V., Stegemann J.P. Reduced serum content and increased matrix stiffness promote the cardiac myofibroblast transition in 3D collagen matrices. Cardiovasc. Pathol. 2011.
81. Park J.S.H.N., Kurpinski K.T., Patel S., Hsu S., Li S. Mechanobiology of mesenchymal stem cells and their use in cardiovascular repair. Front. Biosci. 2007, 12:5098-5116.
82. Dallon J.C., Ehrlich H.P.A. Review of fibroblast populated collagen lattices. Wound Repair Regener. 2008, 16:472-479.
83. Tamariz E., Grinnell F. Modulation of fibroblast morphology and adhesion during collagen matrix remodeling. Mol. Biol. Cell 2002, 13:3915-3929.
84. Dean D.M., Rago A.P., Morgan J.R. Fibroblast elongation and dendritic extensions in constrained versus unconstrained microtissues. Cell Motil Cytoskeleton 2009, 66:129-141.
85. Tomasek J.J., Gabbiani G., Hinz B., Chaponnier C., Brown R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 2002, 3:349-363.
86. Grinnell F., Ho C.H., Tamariz E., Lee D.J., Skuta G. Dendritic fibroblasts in three-dimensional collagen matrices. Mol. Biol. Cell 2003, 14:384-395.
87. Hinz B., Gabbiani G. Cell-matrix and cell-cell contacts of myofibroblasts: role in connective tissue remodeling. Thromb. Haemost. 2003, 90:993-1002.
88. Grinnell F. Fibroblasts, myofibroblasts, and wound contraction. J. Cell. Biochem. 1994, 124:401-404.
89. Carlson M.A., Longaker M.T. The fibroblast-populated collagen matrix as a model of wound healing: a review of the evidence. Wound Repair Regener. 2004, 12:134-147.
90. Vanni S., Lagerholm B.C., Otey C., Taylor D.L., Lanni F. Internet-based image analysis quantifies contractile behavior of individual fibroblasts inside model tissue. Biophys. J. 2003, 84:2715-2727.
91. Simon D.D., Humphrey J.D. On a class of admissible constitutive behaviors in free-floating engineered tissues. Int. J. NonLinear Mech. 2012, 47:173-178.
92. Simon D.D., Horgan C.O., Humphrey J.D. Mechanical restrictions on biological responses by adherent cells within collagen gels. J. Mech. Behav. Biomed. Mater. 2012, 14:216-226.
93. Eastwood M., Porter R., Khan U., McGrouther G., Brown R. Quantitative analysis of collagen gel contractile forces generated by dermal fibroblasts and the relationship to cell morphology. J. Cell Physiol. 1996, 166:33-42.
94. Kolodney M.S., Elson E.L. Correlation of myosin light chain phosphorylation with isometric contraction of fibroblasts. J. Biol. Chem. 1993, 268:23850-23855.
95. Hinz B., Mastrangelo D., Iselin C.E., Chaponnier C., Gabbiani G. Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation. Am. J. Pathol. 2001, 159:1009-1020.
96. Hinz B., Phan S.H., Thannickal V.J., Galli A., Bochaton-Piallat M.L., Gabbiani G. The myofibroblast: one function, multiple origins. Am. J. Pathol. 2007, 170:1807-1816.
97. Grinnell F., Ho C.H. Transforming growth factor beta stimulates fibroblast-collagen matrix contraction by different mechanisms in mechanically loaded and unloaded matrices. Exp. Cell Res. 2002, 273:248-255.
98. Tomasek J.J., Haaksma C.J., Eddy R.J., Vaughan M.B. Fibroblast contraction occurs on release of tension in attached collagen lattices: dependency on an organized actin cytoskeleton and serum. Anat. Rec. 1992, 232:359-368.
99. Carlson M.A., Longaker M.T., Thompson J.S. Wound splinting regulates granulation tissue survival. J. Surg. Res. 2003, 110:304-309.
100. Grouf J.L., Throm A.M., Balestrini J.L., Bush K.A., Billiar K.L. Differential effects of EGF and TGF-beta1 on fibroblast activity in fibrin-based tissue equivalents. Tissue Eng. 2007, 13:799-807.
101. Vaughan M.B., Howard E.W., Tomasek J.J. Transforming growth factor-beta1 promotes the morphological and functional differentiation of the myofibroblast. Exp. Cell Res. 2000, 257:180-189.
102. Mochitate K., Pawelek P., Grinnell F. Stress relaxation of contracted collagen gels: disruption of actin filament bundles, release of cell surface fibronectin, and down-regulation of DNA and protein synthesis. Exp. Cell Res. 1991, 193:198-207.
103. Grinnell F., Zhu M., Carlson M.A., Abrams J.M. Release of mechanical tension triggers apoptosis of human fibroblasts in a model of regressing granulation tissue. Exp. Cell Res. 1999, 248:608-619.
104. Chipev C.C., Simon M. Phenotypic differences between dermal fibroblasts from different body sites determine their responses to tension and TGFbeta1. BMC Dermatol. 2002, 2:13.
105. Balestrini J.L., Billiar K.L. Magnitude and duration of stretch modulate fibroblast remodeling. J. Biomech. Eng. 2009, 131:051005.
106. Costa K.D., Lee E.J., Holmes J.W. Creating alignment and anisotropy in engineered heart tissue: role of boundary conditions in a model three-dimensional culture system. Tissue Eng. 2003, 9:567-577.
107. Sander E.A., Barocas V.H., Tranquillo R.T. Initial fiber alignment pattern alters extracellular matrix synthesis in fibroblast-populated fibrin gel cruciforms and correlates with predicted tension. Ann. Biomed. Eng. 2011, 39:714-729.
108. Jhun C.S., Evans M.C., Barocas V.H., Tranquillo R.T. Planar biaxial mechanical behavior of bioartificial tissues possessing prescribed fiber alignment. J. Biomech. Eng. 2009, 131:081006.
109. Grinnell F., Rocha L.B., Iucu C., Rhee S., Jiang H. Nested collagen matrices: a new model to study migration of human fibroblast populations in three dimensions. Exp. Cell Res. 2006, 312:86-94.
110. Miron-Mendoza M., Seemann J., Grinnell F. Collagen fibril flow and tissue translocation coupled to fibroblast migration in 3D collagen matrices. Mol. Biol. Cell 2008, 19:2051-2058.
111. Feng C.H., Cheng Y.C., Chao P.H. The influence and interactions of substrate thickness, organization and dimensionality on cell morphology and migration. Acta Biomater. 2013, 9:5502-5510.
112. Delvoye P., Wiliquet P., Leveque J.L., Nusgens B.V., Lapiere C.M. Measurement of mechanical forces generated by skin fibroblasts embedded in a three-dimensional collagen gel. J. Invest. Dermatol. 1991, 97:898-902.
113. Kolodney M.S., Wysolmerski R.B. Isometric contraction by fibroblasts and endothelial cells in tissue culture: a quantitative study. J. Cell Biol. 1992, 117:73-82.
114. Eastwood M., McGrouther D.A., Brown R.A. A culture force monitor for measurement of contraction forces generated in human dermal fibroblast cultures: evidence for cell-matrix mechanical signalling. Biochim. Biophys. Acta 1994, 1201:186-192.
115. Marenzana M., Wilson-Jones N., Mudera V., Brown R.A. The origins and regulation of tissue tension: identification of collagen tension-fixation process in vitro. Exp. Cell Res. 2006, 312:423-433.
116. Eastwood M., McGrouther D.A., Brown R.A. Fibroblast responses to mechanical forces. Proc. Inst. Mech. Eng. H 1998, 212:85-92.
117. Knezevic V., Sim A.J., Borg T.K., Holmes J.W. Isotonic biaxial loading of fibroblast-populated collagen gels: a versatile, low-cost system for the study of mechanobiology. Biomech. Model Mechanobiol. 2002, 1:59-67.
118. Lee E.J., Holmes J.W., Costa K.D. Remodeling of engineered tissue anisotropy in response to altered loading conditions. Ann. Biomed. Eng. 2008, 36:1322-1334.
119. Freyman T.M., Yannas I.V., Pek Y.S., Yokoo R., Gibson L.J. Micromechanics of fibroblast contraction of a collagen-GAG matrix. Exp. Cell Res. 2001, 269:140-153.
120. Freyman T.M., Yannas I.V., Yokoo R., Gibson L.J. Fibroblast contraction of a collagen-GAG matrix. Biomaterials 2001, 22:2883-2891.
121. Hansen A., Eder A., Bonstrup M., Flato M., Mewe M., Schaaf S., Aksehirlioglu B., Schwoerer A.P., Uebeler J., Eschenhagen T. Development of a drug screening platform based on engineered heart tissue. Circ. Res. 2010, 107:35-44.
122. Serrao G.W., Turnbull I.C., Ancukiewicz D., Kim do E., Kao E., Cashman T.J., Hadri L., Hajjar R.J., Costa K.D. Myocyte-depleted engineered cardiac tissues support therapeutic potential of mesenchymal stem cells. Tissue Eng. A 2012, 18:1322-1333.
123. West A.R., Zaman N., Cole D.J., Walker M.J., Legant W.R., Boudou T., Chen C.S., Favreau J.T., Gaudette G.R., Ea Cowley., Maksym G.N. Development and characterization of a 3D multicell microtissue culture model of airway smooth muscle. Am. J. Physiol. Lung Cell Mol. Physiol. 2013, 304:L4-L16.
124. Sakar M.S., Neal D., Boudou T., Borochin M.A., Li Y., Weiss R., Kamm R.D., Chen C.S., Asada H.H. Formation and optogenetic control of engineered 3D skeletal muscle bioactuators. Lab Chip 2012, 12:4976-4985.
125. Zhao R., Boudou T., Wang W.G., Chen C.S., Reich D.H. Decoupling cell and matrix mechanics in engineered microtissues using magnetically actuated microcantilevers. Adv. Mater. 2013, 25:1699-1705.
126. Jiang H., Rhee S., Ho C.-H., Grinnell F. Distinguishing fibroblast promigratory and procontractile growth factor environments in 3-D collagen matrices. FASEB J. 2008, 22:2151-2160.