Inelastic behaviour of collagen networks in cell-matrix interactions and mechanosensation

Journal of the Royal Society Interface

Volumn 12, Issue 102, 2015, Pages

  Mohammadi, Hamid ^a   Arora, Pamma D ^a   Simmons, Craig A ^b   Janmey, Paul A ^c   McCulloch, Christopher A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cell surface area; Collagen gels; Plasticity; Remodelling

Indexed keywords

BIOMECHANICS; CELL CULTURE; CELL MEMBRANES; DEFORMATION; GELS; MECHANICAL PROPERTIES; PLASTICITY; TISSUE;

CELL MATRIX INTERACTIONS; CELL SURFACES; COLLAGEN CONCENTRATION; COLLAGEN GELS; DEFORMATION RATES; EXTRACELLULAR MATRIX PROTEIN; INELASTIC RESPONSE; REMODELLING;

COLLAGEN;

COLLAGEN; COLLAGEN GEL; SCLEROPROTEIN; CROSS LINKING REAGENT; GEL;

3T3 CELL LINE; ADHERENT CELL; ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL ADHESION; CELL FUNCTION; CELL INTERACTION; CELL STRUCTURE; CELL SURFACE; COLLAGEN FIBER; CONTROLLED STUDY; ELASTICITY; ENVIRONMENTAL FACTOR; EXTRACELLULAR MATRIX; FIBROBLAST; FOCAL ADHESION; GEL; MECHANOSENSATION; MECHANOTRANSDUCTION; MOLECULAR MODEL; MOUSE; NONHUMAN; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN INTERACTION; ANIMAL; BOVINE; CELL COMMUNICATION; CELL CULTURE; CHEMISTRY; CONFOCAL MICROSCOPY; FLUORESCENCE MICROSCOPY; FOURIER ANALYSIS; MECHANICAL STRESS; METABOLISM;

3T3 CELLS; ANIMALS; CATTLE; CELL ADHESION; CELL COMMUNICATION; CELLS, CULTURED; COLLAGEN; CROSS-LINKING REAGENTS; ELASTICITY; EXTRACELLULAR MATRIX; FIBROBLASTS; FOURIER ANALYSIS; GELS; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; STRESS, MECHANICAL;

EID: 84915757715     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2014.1074     Document Type: Article

References (55)

1. Mierke CT. 2014 The fundamental role of mechanical properties in the progression of cancer disease and inflammation. Rep. Prog. Phys. 77, 076602. (doi:10.1088/0034-4885/77/7/076602)
2. Wang N, Butler JP, Ingber DE. 1993 Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124-1127. (doi:10.1126/science.7684161)
3. Choquet D, Felsenfeld DP, Sheetz MP. 1997 Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88, 39-48. (doi:10.1016/S0092-8674(00)81856-5)
4. Janmey PA, Schliwa M. 2008 Rheology. Curr. Biol. 18, R639-R641. (doi:10.1016/j.cub.2008.05.001)
5. Storm C, Pastore JJ, MacKintosh FC, Lubensky TC, Janmey PA. 2005 Nonlinear elasticity in biological gels. Nature 435, 191-194. (doi:10.1038/nature03521)
6. Timoshenko SP, Gere JM. 2012 Theory of elastic stability. New York, NY: Courier Dover Publications.
7. Landau LD, Lifshitz EM. 1987 Theory of elasticity, 2nd edn, vol. 7. New York, NY: Pergamon.
8. Pelham Jr RJ, Wang Y. 1997 Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl Acad. Sci. USA 94, 13 661-13 665. (doi:10.1073/pnas.94.25.13661)
9. Rape AD, Guo WH, Wang YL. 2011 The regulation of traction force in relation to cell shape and focal adhesions. Biomaterials 32, 2043-2051. (doi:10.1016/j.biomaterials.2010.11.044)
10. Wen Q, Basu A, Janmey PA, Yodh AG. 2012 Non-affine deformations in polymer hydrogels. Soft Matter 8, 8039-8049. (doi:10.1039/c2sm25364j)
11. Gross J, Highberger JH, Schmitt FO. 1952 Some factors involved in the fibrogenesis of collagen in vitro. Proc. Soc. Exp. Biol. Med. 80, 462-465. (doi:10.3181/00379727-80-19657)
12. Grinnell F, Petroll WM. 2010 Cell motility and mechanics in three-dimensional collagen matrices. Annu. Rev. Cell Dev. Biol. 26, 335-361. (doi:10.1146/annurev.cellbio.042308.113318)
13. Mohammadi H, McCulloch CA. 2013 Impact of elastic and inelastic substrate behaviors on mechanosensation. Soft Matter 10, 408-420. (doi:10.1039/c3sm52729h)
14. Billiar KL. 2011 The mechanical environment of cells in collagen gel models. In Cellular and biomolecular mechanics and mechanobiology (ed. A Gefen), pp. 201-245. Berlin, Germany: Springer. (doi:10.1007/8415-2010-30)
15. Munster S, Jawerth LM, Leslie BA, Weitz JI, Fabry B, Weitz DA. 2013 Strain history dependence of the nonlinear stress response of fibrin and collagen networks. Proc. Natl Acad. Sci. USA 110, 12 197- 12 202. (doi:10.1073/pnas.1222787110)
16. Lopez-Garcia MD, Beebe DJ, Crone WC. 2010 Young's modulus of collagen at slow displacement rates. Biomed. Mater. Eng. 20, 361-369. (doi:10.3233/BME-2010-0649)
17. Yang YL, Kaufman LJ. 2009 Rheology and confocal reflectance microscopy as probes of mechanical properties and structure during collagen and collagen/hyaluronan self-assembly. Biophys. J. 96, 1566-1585. (doi:10.1016/j.bpj.2008.10.063)
18. Motte S, Kaufman LJ. 2013 Strain stiffening in collagen I networks. Biopolymers 99, 35-46. (doi:10.1002/bip.22133)
19. Grinnell F. 2003 Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol. 13, 264-269. (doi:10.1016/S0962-8924(03)00057-6)
20. Mohammadi H, Janmey PA, McCulloch CA. 2014 Lateral boundary mechanosensing by adherent cells in a collagen gel system. Biomaterials 35, 1138-1149. (doi:10.1016/j.biomaterials.2013.10.059)
21. Ballard DH. 1981 Generalizing the Hough transform to detect arbitrary shapes. Pattern Recognit. 13, 111-122. (doi:10.1016/0031-3203(81)90009-1)
22. Levental I, Levental KR, Klein EA, Assoian R, Miller RT, Wells RG, Janmey PA. 2010 A simple indentation device for measuring micrometer-scale tissue stiffness. J. Phys. Condens. Matter 22, 194120. (doi:10.1088/0953-8984/22/19/194120)
23. Pizzo AM, Kokini K, Vaughn LC, Waisner BZ, Voytik-Harbin SL. 2005 Extracellular matrix (ECM) microstructural composition regulates local cell-ECM biomechanics and fundamental fibroblast behavior: a multidimensional perspective. J. Appl. Physiol. 98, 1909-1921. (doi:10.1152/japplphysiol.01137.2004)
24. Fung YC. 1993 Biomechanics: mechanical properties of living tissues, 2nd edn. New York, NY: Springer.
25. Arora PD, Narani N, McCulloch CA. 1999 The compliance of collagen gels regulates transforming growth factor-beta induction of alpha-smooth muscle actin in fibroblasts. Am. J. Pathol. 154, 871-882. (doi:10.1016/S0002-9440(10)65334-5)
26. Nakagawa S, Pawelek P, Grinnell F. 1989 Long-term culture of fibroblasts in contracted collagen gels: effects on cell growth and biosynthetic activity. J. Invest. Dermatol. 93, 792-798. (doi:10.1111/1523-1747.ep12284425)
27. Chandran PL, Paik DC, Holmes JW. 2012 Structural mechanism for alteration of collagen gel mechanics by glutaraldehyde crosslinking. Connect. Tissue Res. 53, 285-297. (doi:10.3109/03008207.2011.640760)
28. Miron-Mendoza M, Seemann J, Grinnell F. 2010 The differential regulation of cell motile activity through matrix stiffness and porosity in three dimensional collagen matrices. Biomaterials 31, 6425-6435. (doi:10.1016/j.biomaterials.2010.04.064)
29. Ito Y. 1999 Surface micropatterning to regulate cell functions. Biomaterials 20, 2333-2342. (doi:10.1016/S0142-9612(99)00162-3)
30. Vader D, Kabla A, Weitz D, Mahadevan L. 2009 Strain-induced alignment in collagen gels. PLoS ONE 4, e5902. (doi:10.1371/journal.pone.0005902)
31. Boyde A, Wolfe LA, Maly M, Jones SJ. 1995 Vital confocal microscopy in bone. Scanning 17, 72-85. (doi:10.1002/sca.4950170203)
32. Friedl P. 2004 Dynamic imaging of cellular interactions with extracellular matrix. Histochem. Cell Biol. 122, 183-190. (doi:10.1007/s00418-004-0682-0)
33. Ingber DE. 2003 Mechanosensation through integrins: cells act locally but think globally. Proc. Natl Acad. Sci. USA 100, 1472-1474. (doi:10.1073/pnas.0530201100)
34. Leong WS, Tay CY, Yu H, Li A, Wu SC, Duc DH, Lim CT, Tan LP. 2010 Thickness sensing of hMSCs on collagen gel directs stem cell fate. Biochem. Biophys. Res. Commun. 401, 287-292. (doi:10.1016/j.bbrc.2010.09.052)
35. Rudnicki MS, Cirka HA, Aghvami M, Sander EA, Wen Q, Billiar KL. 2013 Nonlinear strain stiffening is not sufficient to explain how far cells can feel on fibrous protein gels. Biophys. J. 105, 11-20. (doi:10.1016/j.bpj.2013.05.032)
36. Hoffman BD, Grashoff C, Schwartz MA. 2011 Dynamic molecular processes mediate cellular mechanotransduction. Nature 475, 316-323. (doi:10.1038/nature10316)
37. Prager-Khoutorsky M, Lichtenstein A, Krishnan R, Rajendran K, Mayo A, Kam Z, Geiger B, Bershadsky AD. 2011 Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing. Nat. Cell Biol. 13, 1457-1465. (doi:10.1038/ncb2370)
38. Rajshankar D, Downey GP, McCulloch CA. 2012 IL-1beta enhances cell adhesion to degraded fibronectin. FASEB J. 26, 4429-4444. (doi:10.1096/fj.12-207381)
39. Wang Q, Downey GP, McCulloch CA. 2011 Focal adhesions and Ras are functionally and spatially integrated to mediate IL-1 activation of ERK. FASEB J. 25, 3448-3464. (doi:10.1096/fj.11-183459)
40. Carey SP, Kraning-Rush CM, Williams RM, Reinhart-King CA. 2012 Biophysical control of invasive tumor cell behavior by extracellular matrix microarchitecture. Biomaterials 33, 4157-4165. (doi:10.1016/j.biomaterials.2012.02.029)
41. Ma X, Schickel ME, Stevenson MD, Sarang-Sieminski AL, Gooch KJ, Ghadiali SN, Hart RT. 2013 Fibers in the extracellular matrix enable long-range stress transmission between cells. Biophys. J. 104, 1410-1418. (doi:10.1016/j.bpj.2013.02.017)
42. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. 2002 Myofibroblasts and mechanoregulation of connective tissue remodelling. Nat. Rev. 3, 349-363. (doi:10.1038/nrm809)
43. Daley GQ. 2008 Common themes of dedifferentiation in somatic cell reprogramming and cancer. Cold Spring Harb. Symp. Quant. Biol. 73, 171-174. (doi:10.1101/sqb.2008.73.041)
44. Friedl P, Sahai E, Weiss S, Yamada KM. 2012 New dimensions in cell migration. Nat. Rev. Mol. Cell Biol. 13, 743-747. (doi:10.1038/nrm3459)
45. Helary C, Bataille I, Abed A, Illoul C, Anglo A, Louedec L, Letourneur D, Meddahi-Pelle A, Giraud- Guille MM. 2010 Concentrated collagen hydrogels as dermal substitutes. Biomaterials 31, 481-490. (doi:10.1016/j.biomaterials.2009.09.073)
46. Kwok CB, Ho FC, Li CW, Ngan AH, Chan D, Chan BP. 2013 Compression-induced alignment and elongation of human mesenchymal stem cell (hMSC) in 3D collagen constructs is collagen concentration dependent. J. Biomed. Mater. Res. A 101, 1716-1725. (doi:10.1002/jbm.a.34475)
47. Nishiyama T, Tominaga N, Nakajima K, Hayashi T. 1988 Quantitative evaluation of the factors affecting the process of fibroblast-mediated collagen gel contraction by separating the process into three phases. Collagen Relat. Res. 8, 259-273. (doi:10.1016/S0174-173X(88)80045-1)
48. Roeder BA, Kokini K, Voytik-Harbin SL. 2009 Fibril microstructure affects strain transmission within collagen extracellular matrices. J. Biomech. Eng. 131, 031004. (doi:10.1115/1.3005331)
49. Reilly GC, Engler AJ. 2010 Intrinsic extracellular matrix properties regulate stem cell differentiation. J. Biomech. 43, 55-62. (doi:10.1016/j.jbiomech.2009.09.009)
50. Cox MA, Driessen NJ, Boerboom RA, Bouten CV, Baaijens FP. 2008 Mechanical characterization of anisotropic planar biological soft tissues using finite indentation: experimental feasibility. J. Biomech. 41, 422-429. (doi:10.1016/j.jbiomech.2007.08.006)
51. Achilli M, Meghezi S, Mantovani D. 2012 On the viscoelastic properties of collagen-gel-based lattices under cyclic loading: applications for vascular tissue engineering. Macromol. Mater. Eng. 297, 724-734. (doi:10.1002/mame.201100363)
52. Silver FH. 2006 Mechanosensing and mechanochemical transduction in extracellular matrix. Berlin, Germany: Springer.
53. Chandran PL, Barocas VH. 2004 Microstructural mechanics of collagen gels in confined compression: poroelasticity, viscoelasticity, and collapse. J. Biomech. Eng.126, 152-166. (doi:10.1115/1.1688774)
54. Discher DE, Janmey P, Wang YL. 2005 Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143. (doi:10.1126/science.1116995)
55. Engler A, Bacakova L, Newman C, Hategan A, Griffin M, Discher D. 2004 Substrate compliance versus ligand density in cell on gel responses. Biophys. J. 86, 617-628. (doi:10.1016/S0006-3495(04) 74140-5)