Matrix microarchitecture and myosin II determine adhesion in 3D matrices

Current Biology

Volumn 23, Issue 17, 2013, Pages 1607-1619

  Kubow, Kristopher E ^a   Conrad, Sarah K ^a   Horwitz, A Rick ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN II;

ARTICLE; CELL ADHESION; CELL LINE; EXTRACELLULAR MATRIX; HUMAN; PHYSIOLOGY;

CELL ADHESION; CELL LINE; EXTRACELLULAR MATRIX; HUMANS; MYOSIN TYPE II;

EID: 84883756003     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2013.06.053     Document Type: Article

References (53)

1. B.M. Baker, and C.S. Chen Deconstructing the third dimension: how 3D culture microenvironments alter cellular cues J. Cell Sci. 125 2012 3015 3024
2. A. Pathak, and S. Kumar Biophysical regulation of tumor cell invasion: moving beyond matrix stiffness Integr. Biol. (Camb.) 3 2011 267 278
3. F. Grinnell, and W.M. Petroll Cell motility and mechanics in three-dimensional collagen matrices Annu. Rev. Cell Dev. Biol. 26 2010 335 361
4. B. Knight, C. Laukaitis, N. Akhtar, N.A. Hotchin, M. Edlund, and A.R. Horwitz Visualizing muscle cell migration in situ Curr. Biol. 10 2000 576 585
5. J.S. Harunaga, and K.M. Yamada Cell-matrix adhesions in 3D Matrix Biol. 30 2011 363 368
6. K.M. Yamada, and E. Cukierman Modeling tissue morphogenesis and cancer in 3D Cell 130 2007 601 610
7. P. Friedl, and K. Wolf Plasticity of cell migration: a multiscale tuning model J. Cell Biol. 188 2010 11 19
8. M.A. Wozniak, K. Modzelewska, L. Kwong, and P.J. Keely Focal adhesion regulation of cell behavior Biochim. Biophys. Acta 1692 2004 103 119
9. B. Geiger, J.P. Spatz, and A.D. Bershadsky Environmental sensing through focal adhesions Nat. Rev. Mol. Cell Biol. 10 2009 21 33
10. K.M. Hakkinen, J.S. Harunaga, A.D. Doyle, and K.M. Yamada Direct comparisons of the morphology, migration, cell adhesions, and actin cytoskeleton of fibroblasts in four different three-dimensional extracellular matrices Tissue Eng. Part A 17 2011 713 724
11. W.M. Petroll, and L. Ma Direct, dynamic assessment of cell-matrix interactions inside fibrillar collagen lattices Cell Motil. Cytoskeleton 55 2003 254 264
12. S. Geraldo, A. Simon, N. Elkhatib, D. Louvard, L. Fetler, and D.M. Vignjevic Do cancer cells have distinct adhesions in 3D collagen matrices and in vivo? Eur. J. Cell Biol. 91 2012 930 937
13. S.I. Fraley, Y. Feng, R. Krishnamurthy, D.H. Kim, A. Celedon, G.D. Longmore, and D. Wirtz A distinctive role for focal adhesion proteins in three-dimensional cell motility Nat. Cell Biol. 12 2010 598 604
14. D.E. Discher, P.A. Janmey, and Y.-L. Wang Tissue cells feel and respond to the stiffness of their substrate Science 310 2005 1139 1143
15. E. Tamariz, and F. Grinnell Modulation of fibroblast morphology and adhesion during collagen matrix remodeling Mol. Biol. Cell 13 2002 3915 3929
16. K.E. Kubow, and A.R. Horwitz Reducing background fluorescence reveals adhesions in 3D matrices Nat. Cell Biol. 13 2011 3 5 author reply 5-7
17. S. Rhee, H. Jiang, C.H. Ho, and F. Grinnell Microtubule function in fibroblast spreading is modulated according to the tension state of cell-matrix interactions Proc. Natl. Acad. Sci. USA 104 2007 5425 5430
18. P.P. Provenzano, D.R. Inman, K.W. Eliceiri, and P.J. Keely Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage Oncogene 28 2009 4326 4343
19. M.A. Wozniak, R. Desai, P.A. Solski, C.J. Der, and P.J. Keely ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix J. Cell Biol. 163 2003 583 595
20. E. Cukierman, R. Pankov, D.R. Stevens, and K.M. Yamada Taking cell-matrix adhesions to the third dimension Science 294 2001 1708 1712
21. K.R. Levental, H. Yu, L. Kass, J.N. Lakins, M. Egeblad, J.T. Erler, S.F. Fong, K. Csiszar, A. Giaccia, and W. Weninger Matrix crosslinking forces tumor progression by enhancing integrin signaling Cell 139 2009 891 906
22. A.D. Doyle, M.L. Kutys, M.A. Conti, K. Matsumoto, R.S. Adelstein, and K.M. Yamada Micro-environmental control of cell migration - myosin IIA is required for efficient migration in fibrillar environments through control of cell adhesion dynamics J. Cell Sci. 125 2012 2244 2256
23. 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
24. J.A. Pedersen, and M.A. Swartz Mechanobiology in the third dimension Ann. Biomed. Eng. 33 2005 1469 1490
25. T. Wakatsuki, and E.L. Elson Reciprocal interactions between cells and extracellular matrix during remodeling of tissue constructs Biophys. Chem. 100 2003 593 605
26. A.J. Ridley, M.A. Schwartz, K. Burridge, R.A. Firtel, M.H. Ginsberg, G. Borisy, J.T. Parsons, and A.R. Horwitz Cell migration: integrating signals from front to back Science 302 2003 1704 1709
27. B.A. Roeder, K. Kokini, J.E. Sturgis, J.P. Robinson, and S.L. Voytik-Harbin Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure J. Biomech. Eng. 124 2002 214 222
28. M. Vicente-Manzanares, and A.R. Horwitz Myosin light chain mono- and di-phosphorylation differentially regulate adhesion and polarity in migrating cells Biochem. Biophys. Res. Commun. 402 2010 537 542
29. C.K. Choi, M. Vicente-Manzanares, J. Zareno, L.A. Whitmore, A. Mogilner, and A.R. Horwitz Actin and alpha-Actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner Nat. Cell Biol. 10 2008 1039 1050
30. M. Vicente-Manzanares, K. Newell-Litwa, A.I. Bachir, L.A. Whitmore, and A.R. Horwitz Myosin IIA/IIB restrict adhesive and protrusive signaling to generate front-back polarity in migrating cells J. Cell Biol. 193 2011 381 396
31. M. Vicente-Manzanares, X. Ma, R.S. Adelstein, and A.R. Horwitz Non-muscle myosin II takes centre stage in cell adhesion and migration Nat. Rev. Mol. Cell Biol. 10 2009 778 790
32. R.S. Fischer, M. Gardel, X. Ma, R.S. Adelstein, and C.M. Waterman Local cortical tension by myosin II guides 3D endothelial cell branching Curr. Biol. 19 2009 260 265
33. 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
34. D. Velegol, and F. Lanni Cell traction forces on soft biomaterials. I. Microrheology of type I collagen gels Biophys. J. 81 2001 1786 1792
35. E. Kniazeva, J.W. Weidling, R. Singh, E.L. Botvinick, M.A. Digman, E. Gratton, and A.J. Putnam Quantification of local matrix deformations and mechanical properties during capillary morphogenesis in 3D Integr. Biol. (Camb.) 4 2012 431 439
36. J.G. Goetz, S. Minguet, I. Navarro-Lérida, J.J. Lazcano, R. Samaniego, E. Calvo, M. Tello, T. Osteso-Ibáñez, T. Pellinen, and A. Echarri Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis Cell 146 2011 148 163
37. M. Guthold, W. Liu, E.A. Sparks, L.M. Jawerth, L. Peng, M. Falvo, R. Superfine, R.R. Hantgan, and S.T. Lord A comparison of the mechanical and structural properties of fibrin fibers with other protein fibers Cell Biochem. Biophys. 49 2007 165 181
38. M. Vicente-Manzanares, C.K. Choi, and A.R. Horwitz Integrins in cell migration - the actin connection J. Cell Sci. 122 2009 199 206
39. S.R. Coyer, A. Singh, D.W. Dumbauld, D.A. Calderwood, S.W. Craig, E. Delamarche, and A.J. García Nanopatterning reveals an ECM area threshold for focal adhesion assembly and force transmission that is regulated by integrin activation and cytoskeleton tension J. Cell Sci. 125 2012 5110 5123
40. J.L. Tan, J. Tien, D.M. Pirone, D.S. Gray, K. Bhadriraju, and C.S. Chen Cells lying on a bed of microneedles: an approach to isolate mechanical force Proc. Natl. Acad. Sci. USA 100 2003 1484 1489
41. J. Nam, J. Johnson, J.J. Lannutti, and S. Agarwal Modulation of embryonic mesenchymal progenitor cell differentiation via control over pure mechanical modulus in electrospun nanofibers Acta Biomater. 7 2011 1516 1524
42. J. Kirchner, Z. Kam, G. Tzur, A.D. Bershadsky, and B. Geiger Live-cell monitoring of tyrosine phosphorylation in focal adhesions following microtubule disruption J. Cell Sci. 116 2003 975 986
43. R. Zaidel-Bar, C. Ballestrem, Z. Kam, and B. Geiger Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells J. Cell Sci. 116 2003 4605 4613
44. J.T. Parsons, A.R. Horwitz, and M.A. Schwartz Cell adhesion: integrating cytoskeletal dynamics and cellular tension Nat. Rev. Mol. Cell Biol. 11 2010 633 643
45. P.P. Provenzano, D.R. Inman, K.W. Eliceiri, S.M. Trier, and P.J. Keely Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization Biophys. J. 95 2008 5374 5384
46. T.A. Ulrich, A. Jain, K. Tanner, J.L. MacKay, and S. Kumar Probing cellular mechanobiology in three-dimensional culture with collagen-Agarose matrices Biomaterials 31 2010 1875 1884
47. 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
48. W.R. Legant, C.K. Choi, J.S. Miller, L. Shao, L. Gao, E. Betzig, and C.S. Chen Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions Proc. Natl. Acad. Sci. USA 110 2013 881 886
49. P. Schedin, and P.J. Keely Mammary gland ECM remodeling, stiffness, and mechanosignaling in normal development and tumor progression Cold Spring Harb. Perspect. Biol. 3 2011 a003228
50. C. Gaggioli, S. Hooper, C. Hidalgo-Carcedo, R. Grosse, J.F. Marshall, K. Harrington, and E. Sahai Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells Nat. Cell Biol. 9 2007 1392 1400
51. K. Wolf, Y.I. Wu, Y. Liu, J. Geiger, E. Tam, C. Overall, M.S. Stack, and P. Friedl Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion Nat. Cell Biol. 9 2007 893 904
52. M.J. Paszek, N. Zahir, K.R. Johnson, J.N. Lakins, G.I. Rozenberg, A. Gefen, C.A. Reinhart-King, S.S. Margulies, M. Dembo, and D. Boettiger Tensional homeostasis and the malignant phenotype Cancer Cell 8 2005 241 254
53. G.P. Raeber, M.P. Lutolf, and J.A. Hubbell Molecularly engineered PEG hydrogels: a novel model system for proteolytically mediated cell migration Biophys. J. 89 2005 1374 1388