Boundary stiffness regulates fibroblast behavior in collagen gels

Annals of Biomedical Engineering

Volumn 38, Issue 3, 2010, Pages 658-673

  John, Jeffrey ^a   Throm Quinlan, Angela ^a,b   Silvestri, Chiara ^a   Billiar, Kristen ^a,b  

^a Worcester Polytechnic Institute   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Collagen gel; Contraction; Fibroblast; Mechanobiology; Myofibroblast; Remodeling; Stiffness

Indexed keywords

CELL BEHAVIORS; CELLULAR BEHAVIORS; COLLAGEN GEL; COLLAGEN GELS; COLLAGEN MATRICES; CULTURE SUBSTRATE; EXPERIMENTAL STUDIES; EXTRACELLULAR MATRICES; FINITE ELEMENT ANALYSIS; IN-BETWEEN; MECHANICAL ENVIRONMENT; MECHANO-BIOLOGY; MYOFIBROBLASTS; PHYSIO-CHEMICAL PROPERTIES; REPRESENTATIVE VOLUME ELEMENTS;

CELL CULTURE; COLLAGEN; FIBROBLASTS; GELS; STIFFNESS; THREE DIMENSIONAL; TISSUE;

STIFFNESS MATRIX;

COLLAGEN;

ARTICLE; BIOLOGICAL MODEL; CELL CULTURE; CHEMISTRY; COMPUTER SIMULATION; CULTURE TECHNIQUE; FIBROBLAST; GEL; HUMAN; MECHANICAL STRESS; MECHANOTRANSDUCTION; METHODOLOGY; PHYSIOLOGY; YOUNG MODULUS;

CELL CULTURE TECHNIQUES; CELLS, CULTURED; COLLAGEN; COMPUTER SIMULATION; ELASTIC MODULUS; FIBROBLASTS; GELS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; STRESS, MECHANICAL;

EID: 77952010712     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-009-9856-1     Document Type: Conference Paper

References (58)

1. P Arora N Narani C McCulloch 1999 The compliance of collagen gels regulates transforming growth factor-beta induction of alpha-smooth muscle actin in fibroblasts Am. J. Pathol. 154 3 871 882 10079265
2. JL Balestrini KL Billiar 2006 Equibiaxial cyclic stretch stimulates fibroblasts to rapidly remodel fibrin J. Biomech. 39 16 2983 2990 10.1016/j.jbiomech.2005.10.025 16386746
3. E Bell B Ivarsson C Merrill 1979 Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro Proc. Natl. Acad. Sci. USA 76 3 1274 1278 10.1073/pnas.76.3.1274 286310
4. KL Billiar AM Throm MT Frey 2005 Biaxial failure properties of planar living tissue equivalents J. Biomed. Mater. Res. A 73 2 182 191 15761827
5. RA Brown KK Sethi I Gwanmesia D Raemdonck M Eastwood V Mudera 2002 Enhanced fibroblast contraction of 3D collagen lattices and integrin expression by TGF-beta1 and -beta3: mechanoregulatory growth factors? Exp. Cell Res. 274 2 310 322 10.1006/excr.2002.5471 11900491
6. B Campbell W Clark J Wang 2003 A multi-station culture force monitor system to study cellular contractility J. Biomech. 36 1 137 140 10.1016/S0021-9290(02)00325-1 12485649
7. M Carlson M Longaker J Thompson 2003 Wound splinting regulates granulation tissue survival J. Surg. Res. 110 1 304 309 10.1016/S0022-4804(02) 00098-7 12697415
8. J Chen H Li N Sundarraj JH Wang 2007 Alpha-smooth muscle actin expression enhances cell traction force Cell Motil. Cytoskeleton 64 4 248 257 10.1002/cm.20178 17183543
9. B Chevallay D Herbage 2000 Collagen-based biomaterials as 3D scaffold for cell cultures: applications for tissue engineering and gene therapy Med. Biol. Eng. Comput. 38 2 211 218 10.1007/BF02344779 10829416
10. E Cukierman R Pankov DR Stevens KM Yamada 2001 Taking cell-matrix adhesions to the third dimension Science 294 5547 1708 1712 10.1126/science. 1064829 11721053
11. P Delvoye P Wiliquet JL Leveque BV Nusgens CM Lapiere 1991 Measurement of mechanical forces generated by skin fibroblasts embedded in a three-dimensional collagen gel J. Invest. Dermatol. 97 5 898 902 10.1111/1523-1747.ep12491651 1919053
12. A Desmouliere C Badid ML Bochaton-Piallat G Gabbiani 1997 Apoptosis during wound healing, fibrocontractive diseases and vascular wall injury Int. J. Biochem. Cell Biol. 29 1 19 30 10.1016/S1357-2725(96)00117-3 9076938
13. A Desmouliere A Geinoz F Gabbiani G Gabbiani 1993 Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts J. Cell Biol. 122 1 103 111 10.1083/jcb.122.1.103 8314838
14. D Discher P Janmey Y Wang 2005 Tissue cells feel and respond to the stiffness of their substrate Science 310 5751 1139 1143 10.1126/science.1116995 16293750
15. M Eastwood DA McGrouther RA Brown 1994 A culture force monitor for measurement of contraction forces generated in human dermal fibroblast cultures: evidence for cell-matrix mechanical signalling Biochim. Biophys. Acta 1201 2 186 192 7947931
16. M Eastwood R Porter U Khan G McGrouther R Brown 1996 Quantitative analysis of collagen gel contractile forces generated by dermal fibroblasts and the relationship to cell morphology J. Cell. Physiol. 166 1 33 42 10.1002/(SICI)1097-4652(199601)166:1<33::AID-JCP4>3.0.CO;2-H 8557773
17. T Elsdale J Bard 1972 Collagen substrata for studies on cell behavior J. Cell Biol. 54 3 626 637 10.1083/jcb.54.3.626 4339818
18. AJ Engler S Sen HL Sweeney DE Discher 2006 Matrix elasticity directs stem cell lineage specification Cell 126 4 677 689 10.1016/j.cell.2006.06.044 16923388
19. J Fluck C Querfeld A Cremer S Niland T Krieg S Sollberg 1998 Normal human primary fibroblasts undergo apoptosis in three-dimensional contractile collagen gels J. Invest. Dermatol. 110 2 153 157 10.1046/j.1523-1747.1998.00095.x 9457911
20. T Freyman I Yannas R Yokoo L Gibson 2002 Fibroblast contractile force is independent of the stiffness which resists the contraction Exp. Cell Res. 272 2 153 162 10.1006/excr.2001.5408 11777340
21. G Gabbiani 2003 The myofibroblast in wound healing and fibrocontractive diseases J. Pathol. 200 4 500 503 10.1002/path.1427 12845617
22. TS Girton TR Oegema ED Grassl BC Isenberg RT Tranquillo 2000 Mechanisms of stiffening and strengthening in media-equivalents fabricated using glycation J. Biomech. Eng. 122 3 216 223 10.1115/1.429652 10923288
23. F Grinnell 1994 Fibroblasts, myofibroblasts, and wound contraction J. Cell Biol. 124 4 401 404 10.1083/jcb.124.4.401 8106541
24. F Grinnell 2003 Fibroblast biology in three-dimensional collagen matrices Trends Cell Biol. 13 5 264 269 10.1016/S0962-8924(03)00057-6 12742170
25. B Harley T Freyman M Wong L Gibson 2007 A new technique for calculating individual dermal fibroblast contractile forces generated within collagen-GAG scaffolds Biophys. J. 93 8 2911 2922 10.1529/biophysj.106.095471 17586570
26. B Hinz D Mastrangelo C Iselin C Chaponnier G Gabbiani 2001 Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation Am. J. Pathol. 159 3 1009 1020 11549593
27. B Hinz S Phan V Thannickal A Galli M Bochaton-Piallat G Gabbiani 2007 The myofibroblast: one function, multiple origins Am. J. Pathol. 170 6 1807 1816 10.2353/ajpath.2007.070112 17525249
28. S Huang D Ingber 2005 Cell tension, matrix mechanics, and cancer development Cancer Cell 8 3 175 176 10.1016/j.ccr.2005.08.009 16169461
29. S Ibusuki GJ Halbesma MA Randolph RW Redmond IE Kochevar TJ Gill 2007 Photochemically cross-linked collagen gels as three-dimensional scaffolds for tissue engineering Tissue Eng. 13 8 1995 2001 10.1089/ten.2006.0153 17518705
30. DE Ingber D Prusty Z Sun H Betensky N Wang 1995 Cell shape, cytoskeletal mechanics, and cell cycle control in angiogenesis J. Biomech. 28 12 1471 1484 10.1016/0021-9290(95)00095-X 8666587
31. H Jiang S Rhee CH Ho F Grinnell 2008 Distinguishing fibroblast promigratory and procontractile growth factor environments in 3-D collagen matrices FASEB J. 22 7 2151 2160 10.1096/fj.07-097014 18272655
32. BF Ju K-K Liu S-F Ling W Hong Ng 2002 A novel technique for characterizing elastic properties of thin biological membrane Mech. Mater. 34 11 749 754 10.1016/S0167-6636(02)00182-5
33. JP Junker C Kratz A Tollback G Kratz 2008 Mechanical tension stimulates the transdifferentiation of fibroblasts into myofibroblasts in human burn scars Burns 34 7 942 946 10.1016/j.burns.2008.01.010 18472340
34. D Karamichos RA Brown V Mudera 2006 Complex dependence of substrate stiffness and serum concentration on cell-force generation J. Biomed. Mater. Res. A 78 2 407 415 16715519
35. D Karamichos RA Brown V Mudera 2007 Collagen stiffness regulates cellular contraction and matrix remodeling gene expression J. Biomed. Mater. Res. A 83 3 887 894 17567861
36. D Karamichos J Skinner R Brown V Mudera 2008 Matrix stiffness and serum concentration effects matrix remodelling and ECM regulatory genes of human bone marrow stem cells J. Tissue Eng. Regen. Med. 2 2-3 97 105 10.1002/term.69 18338818
37. JD Kershaw M Misfeld HH Sievers MH Yacoub AH Chester 2004 Specific regional and directional contractile responses of aortic cusp tissue J. Heart Valve Dis. 13 5 798 803 15473483
38. D Knapp T Tower R Tranquillo VH Barocas 1999 Estimation of cell traction and migration in an isometric cell traction assay AIChE J. 45 12 2628 2640 10.1002/aic.690451219
39. V Knezevic AJ Sim TK Borg JW Holmes 2002 Isotonic biaxial loading of fibroblast-populated collagen gels: a versatile, low-cost system for the study of mechanobiology Biomech. Model. Mechanobiol. 1 1 59 67 10.1007/s10237-002- 0005-0 14586707
40. MS Kolodney RB Wysolmerski 1992 Isometric contraction by fibroblasts and endothelial cells in tissue culture: a quantitative study J. Cell Biol. 117 1 73 82 10.1083/jcb.117.1.73 1556157
41. WR Legant A Pathak MT Yang VS Deshpande RM McMeeking CS Chen 2009 Microfabricated tissue gauges to measure and manipulate forces from 3D microtissues Proc. Natl. Acad. Sci. USA 106 25 10097 10102 10.1073/pnas. 0900174106 19541627
42. L Mazzolai T Pedrazzini F Nicoud G Gabbiani HR Brunner J Nussberger 2000 Increased cardiac angiotensin II levels induce right and left ventricular hypertrophy in normotensive mice Hypertension 35 4 985 991 10775573
43. V Moulin BY Tam G Castilloux FA Auger MD O'Connor-McCourt A Philip L Germain 2001 Fetal and adult human skin fibroblasts display intrinsic differences in contractile capacity J. Cell. Physiol. 188 2 211 222 10.1002/jcp.1110 11424088
44. CM Nelson RP Jean JL Tan WF Liu NJ Sniadecki AA Spector CS Chen 2005 Emergent patterns of growth controlled by multicellular form and mechanics Proc. Natl. Acad. Sci. USA 102 33 11594 11599 10.1073/pnas.0502575102 16049098
45. KT Nguyen JL West 2002 Photopolymerizable hydrogels for tissue engineering applications Biomaterials 23 22 4307 4314 10.1016/S0142-9612(02) 00175-8 12219820
46. T Nishiyama N Tominaga K Nakajima T Hayashi 1988 Quantitative evaluation of the factors affecting the process of fibroblast-mediated collagen gel contraction by separating the process into three phases Coll. Relat. Res. 8 3 259 273 3396309
47. JA Pedersen MA Swartz 2005 Mechanobiology in the third dimension Ann. Biomed. Eng. 33 11 1469 1490 10.1007/s10439-005-8159-4 16341917
48. SR Peyton CM Ghajar CB Khatiwala AJ Putnam 2007 The emergence of ECM mechanics and cytoskeletal tension as important regulators of cell function Cell Biochem. Biophys. 47 2 300 320 10.1007/s12013-007-0004-y 17652777
49. RA Redden EJ Doolin 2003 Collagen crosslinking and cell density have distinct effects on fibroblast-mediated contraction of collagen gels Skin Res. Technol. 9 3 290 293 10.1034/j.1600-0846.2003.00023.x 12877693
50. A Rowlands P George J Cooper-White 2008 Directing osteogenic and myogenic differentiation of MSCs: interplay of stiffness and adhesive ligand presentation Am. J. Physiol. Cell Physiol. 295 4 C1037 C1044 10.1152/ajpcell.67.2008 18753317
51. K Shapira-Schweitzer D Seliktar 2007 Matrix stiffness affects spontaneous contraction of cardiomyocytes cultured within a PEGylated fibrinogen biomaterial Acta Biomater. 3 1 33 41 10.1016/j.actbio.2006.09.003 17098488
52. E Tamariz F Grinnell 2002 Modulation of fibroblast morphology and adhesion during collagen matrix remodeling Mol. Biol. Cell 13 11 3915 3929 10.1091/mbc.E02-05-0291 12429835
53. S Thomopoulos GM Fomovsky JW Holmes 2005 The development of structural and mechanical anisotropy in fibroblast populated collagen gels J. Biomech. Eng. 127 5 742 750 10.1115/1.1992525 16248303
54. J Tomasek G Gabbiani B Hinz C Chaponnier R Brown 2002 Myofibroblasts and mechano-regulation of connective tissue remodelling Nat. Rev. Mol. Cell Biol. 3 5 349 363 10.1038/nrm809 11988769
55. DS Torres TM Freyman IV Yannas M Spector 2000 Tendon cell contraction of collagen-GAG matrices in vitro: effect of cross-linking Biomaterials 21 15 1607 1619 10.1016/S0142-9612(00)00051-X 10885733
56. G Walker K Masters D Shah K Anseth L Leinwand 2004 Valvular myofibroblast activation by transforming growth factor-beta: implications for pathological extracellular matrix remodeling in heart valve disease Circ. Res. 95 3 253 260 10.1161/01.RES.0000136520.07995.aa 15217906
57. M Zaman L Trapani A Sieminski A Siemeski D Mackellar H Gong R Kamm A Wells D Lauffenburger P Matsudaira 2006 Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis Proc. Natl. Acad. Sci. USA 103 29 10889 10894 10.1073/pnas.0604460103 16832052
58. YK Zhu T Umino XD Liu HJ Wang DJ Romberger JR Spurzem SI Rennard 2001 Contraction of fibroblast-containing collagen gels: initial collagen concentration regulates the degree of contraction and cell survival In Vitro Cell Dev. Biol. Anim. 37 1 10 16 10.1290/1071-2690(2001)037<0010:COFCCG>2. 0.CO;2 11249200