Biphasic response of cell invasion to matrix stiffness in three-dimensional biopolymer networks

Acta Biomaterialia

Volumn 13, Issue , 2015, Pages 61-67

  Lang, Nadine R ^a   Skodzek, Kai ^a   Hurst, Sebastian ^a   Mainka, Astrid ^a   Steinwachs, Julian ^a   Schneider, Julia ^a   Aifantis, Katerina E ^b   Fabry, Ben ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b University of Arizona   (United States)

Author keywords

Cell migration; Crosslinking; Matrix mechanics; Matrix metalloproteinase; Pore size

Indexed keywords

BIOMOLECULES; CELLS; COLLAGEN; CYTOLOGY; ENZYME ACTIVITY; GELS; STIFFNESS; STIFFNESS MATRIX;

CELL INVASION; CELL MIGRATION; COLLAGEN GELS; GEL STIFFNESS; MATRIX; MATRIX MECHANIC; MATRIX METALLOPROTEINASE; METALLOPROTEINASES; STERIC HINDRANCES;

PORE SIZE;

BIOPOLYMER; COLLAGEN GEL; FIBRILLAR COLLAGEN; GLUTARALDEHYDE; COLLAGEN;

ARTICLE; BREAST CARCINOMA; CANCER RESEARCH; CELL FUNCTION; CELL INVASION; CELL MIGRATION; CELL SHAPE; COLLAGEN FIBRIL; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FOCAL ADHESION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CROSS LINKING; SOFT TISSUE; STEREOSPECIFICITY; STRESS STRAIN RELATIONSHIP; SURFACE PROPERTY; BREAST TUMOR; CHEMISTRY; FEMALE; METABOLISM; PATHOLOGY; STATISTICAL MODEL; TUMOR CELL LINE; TUMOR INVASION;

BREAST NEOPLASMS; CELL LINE, TUMOR; COLLAGEN; EXTRACELLULAR MATRIX; FEMALE; HUMANS; MODELS, STATISTICAL; NEOPLASM INVASIVENESS;

EID: 84920642744     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.11.003     Document Type: Article

References (46)

1. P. Friedl, and K. Wolf Proteolytic interstitial cell migration: a five-step process Cancer Metastasis Rev 2009
2. P. Friedl, and D. Gilmour Collective cell migration in morphogenesis, regeneration and cancer Nat Rev Mol Cell Biol 10 2009 445 457
3. P. Martin, and S.M. Parkhurst Parallels between tissue repair and embryo morphogenesis Development 131 2004 3021 3034
4. V. Lecaudey, and D. Gilmour Organizing moving groups during morphogenesis Curr Opin Cell Biol 18 2006 102 107
5. R.J. Pelham Jr., and Y. Wang Cell locomotion and focal adhesions are regulated by substrate flexibility Proc Natl Acad Sci USA 94 1997 13661 13665
6. L.A. Lautscham, C.Y. Lin, V. Auernheimer, C.A. Naumann, W.H. Goldmann, and B. Fabry Biomembrane-mimicking lipid bilayer system as a mechanically tunable cell substrate Biomaterials 35 2014 3198 3207
7. C.M. Lo, H.B. Wang, M. Dembo, and Y.L. Wang Cell movement is guided by the rigidity of the substrate Biophys J 79 2000 144 152
8. H.B. Wang, M. Dembo, S.K. Hanks, and Y. Wang Focal adhesion kinase is involved in mechanosensing during fibroblast migration Proc Natl Acad Sci USA 98 2001 11295 11300
9. M.H. Zaman, L.M. Trapani, A. Siemeski, D. Mackellar, H. Gong, and R.D. Kamm 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 2006 10889 10894
10. A.D. Doyle, F.W. Wang, K. Matsumoto, and K.M. Yamada One-dimensional topography underlies three-dimensional fibrillar cell migration J Cell Biol 184 2009 481 490
11. P. Friedl, and E.B. Brocker The biology of cell locomotion within three-dimensional extracellular matrix Cell Mol Life Sci 57 2000 41 64
12. M. Ehrbar, A. Sala, P. Lienemann, A. Ranga, K. Mosiewicz, and A. Bittermann Elucidating the role of matrix stiffness in 3D cell migration and remodeling Biophys J 100 2011 284 293
13. Y.L. Yang, and L.J. Kaufman Rheology and confocal reflectance microscopy as probes of mechanical properties and structure during collagen and collagen/hyaluronan self-assembly Biophys J 96 2009 1566 1585
14. Y.L. Yang, S. Motte, and L.J. Kaufman Pore size variable type I collagen gels and their interaction with glioma cells Biomaterials 31 2010 5678 5688
15. C.B. Raub, A.J. Putnam, B.J. Tromberg, and S.C. George Predicting bulk mechanical properties of cellularized collagen gels using multiphoton microscopy Acta Biomater 6 2010 4657 4665
16. I.K. Piechocka, R.G. Bacabac, M. Potters, F.C. Mackintosh, and G.H. Koenderink Structural hierarchy governs fibrin gel mechanics Biophys J 98 2010 2281 2289
17. G.C. Wood, and M.K. Keech The formation of fibrils from collagen solutions. 1. The effect of experimental conditions: kinetic and electron-microscope studies Biochem J 75 1960 588 598
18. K. Wolf, M. Te Lindert, M. Krause, S. Alexander, J. Te Riet, and A.L. Willis Physical limits of cell migration: control by ECM space and nuclear deformation and tuning by proteolysis and traction force J Cell Biol 201 2013 1069 1084
19. N.R. Lang, S. Muenster, C. Metzner, K. Krauss, S. Schuermann, and J. Lange Estimating the 3D pore size distribution of biopolymer networks from directionally biased data Biophys J 105 2013 1967 1975
20. P.A. DiMilla, J.A. Stone, J.A. Quinn, S.M. Albelda, and D.A. Lauffenburger Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength J Cell Biol 122 1993 729 737
21. A. Engler, L. Bacakova, C. Newman, A. Hategan, M. Griffin, and D. Discher Substrate compliance versus ligand density in cell on gel responses Biophys J 86 2004 617 628
22. J.H. Bowes, and C.W. Cater The interaction of aldehydes with collagen Biochim Biophys Acta 168 1968 341 352
23. I. Migneault, C. Dartiguenave, M.J. Bertrand, and K.C. Waldron Glutaraldehyde: behavior in aqueous solution, reaction with proteins, and application to enzyme crosslinking Biotechniques 37 790-796 2004 8 802
24. D. Vader, A. Kabla, D. Weitz, and L. Mahadevan Strain-induced alignment in collagen gels PLoS One 4 2009 e5902
25. P. Kollmannsberger, and B. Fabry High-force magnetic tweezers with force feedback for biological applications Rev Sci Instrum 78 2007 114301-1-6
26. P. Kollmannsberger, and B. Fabry Linear and nonlinear rheology of living cells Annu Rev Mater Res 41 2011 75 97
27. L.M. Jawerth, S. Münster, D.A. Vader, B. Fabry, and D.A. Weitz A blind spot in confocal reflection microscopy: the dependence of fiber brightness on fiber orientation in imaging biopolymer networks Biophys J 98 2009 L01 L03
28. W. Mickel, S. Muenster, L.M. Jawerth, D.A. Vader, D.A. Weitz, and A.P. Sheppard Robust pore size analysis of filamentous networks from 3D confocal microscopy Biophys J 95 2008 6072 6080
29. S. Munster, and B. Fabry A simplified implementation of the bubble analysis of biopolymer network pores Biophys J 104 2013 2774 2775
30. Y.L. Yang, L.M. Leone, and L.J. Kaufman Elastic moduli of collagen gels can be predicted from two-dimensional confocal microscopy Biophys J 97 2009 2051 2060
31. M. Miron-Mendoza, J. Seemann, and F. Grinnell The differential regulation of cell motile activity through matrix stiffness and porosity in three dimensional collagen matrices Biomaterials 31 2010 6425 6435
32. D.E. Discher, P. Janmey, and Y.L. Wang Tissue cells feel and respond to the stiffness of their substrate Science 310 2005 1139 1143
33. T.M. Koch, S. Muenster, N. Bonakdar, J.P. Buttler, and B. Fabry 3D traction forces in cancer cell invasion PloS One 7 2012 e33476
34. F. Sabeh, I. Ota, K. Holmbeck, H. Birkedal-Hansen, P. Soloway, and M. Balbin Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP J Cell Biol 167 2004 769 781
35. R.G. Rowe, and S.J. Weiss Navigating ECM barriers at the invasive front: the cancer cell-stroma interface Annu Rev Cell Dev Biol 25 2009 567 595
36. K. Wolf, and P. Friedl Extracellular matrix determinants of proteolytic and non-proteolytic cell migration Trends Cell Biol 21 2011 736 744
37. B.N. Mason, A. Starchenko, R.M. Williams, L.J. Bonassar, and C.A. Reinhart-King Tuning three-dimensional collagen matrix stiffness independently of collagen concentration modulates endothelial cell behavior Acta Biomater 9 2013 4635 4644
38. S.B. Lindstrom, A. Kulachenko, L. Jawerth, and D.A. Vader Finite strain, finite-size mechanics of rigidly cross-linked biopolymer networks Soft Matter 9 2013 7302 7313
39. A.M. Stein, D.A. Vader, D.A. Weitz, and L.M. Sander The micromechanics of three-dimensional collagen-I gels Complexity 16 2011 22 28
40. S. Munster, L.M. Jawerth, B.A. Leslie, J.I. Weitz, B. Fabry, and D.A. Weitz Strain history dependence of the nonlinear stress response of fibrin and collagen networks Proc Natl Acad Sci USA 110 2013 12197 12202
41. N.Q. Balaban, U.S. Schwarz, D. Riveline, P. Goichberg, G. Tzur, and I. Sabanay Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates Nat Cell Biol 3 2001 466 472
42. A. Pathak, and S. Kumar Independent regulation of tumor cell migration by matrix stiffness and confinement Proc Natl Acad Sci USA 109 2012 10334 10339
43. R.J. Pelham Jr., and Y.L. Wang Cell locomotion and focal adhesions are regulated by the mechanical properties of the substrate Biol Bull 194 1998 348 349 discussion 9-50
44. S.R. Peyton, and A.J. Putnam Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion J Cell Physiol 204 2005 198 209
45. R.J. Hawkins, M. Piel, G. Faure-Andre, A.M. Lennon-Dumenil, J.F. Joanny, and J. Prost Pushing off the walls: a mechanism of cell motility in confinement Phys Rev Lett 102 2009 058103
46. C.T. Mierke, B. Frey, M. Fellner, M. Herrmann, and B. Fabry Integrin {alpha}5{beta}1 facilitates cancer cell invasion through enhanced contractile forces J Cell Sci 124 2010 369 383