Mapping of mechanical strains and stresses around quiescent engineered three-dimensional epithelial tissues

Biophysical Journal

Volumn 103, Issue 1, 2012, Pages 152-162

  Gjorevski, Nikolce ^a   Nelson, Celeste M ^a,b  

^a Princeton University   (United States)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1;

ANIMAL; ARTICLE; ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CHEMISTRY; EPITHELIUM; EXTRACELLULAR MATRIX; MECHANICAL STRESS; MOUSE; PHYSIOLOGY; TISSUE ENGINEERING;

ANIMALS; BIOMECHANICS; COLLAGEN TYPE I; EPITHELIUM; EXTRACELLULAR MATRIX; MICE; MICROSCOPY, ATOMIC FORCE; STRESS, MECHANICAL; TISSUE ENGINEERING;

EID: 84863489002     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.05.048     Document Type: Article

References (61)

1. E.W. Gomez, and Q.K. Chen C.M. Nelson Tissue geometry patterns epithelial-mesenchymal transition via intercellular mechanotransduction J. Cell. Biochem. 110 2010 44 51
2. R. McBeath, and D.M. Pirone C.S. Chen Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment Dev. Cell 6 2004 483 495
3. C.M. Nelson, and R.P. Jean C.S. Chen Emergent patterns of growth controlled by multicellular form and mechanics Proc. Natl. Acad. Sci. USA 102 2005 11594 11599
4. A.J. Engler, and S. Sen D.E. Discher Matrix elasticity directs stem cell lineage specification Cell 126 2006 677 689
5. A.C. Martin, M. Kaschube, and E.F. Wieschaus Pulsed contractions of an actin-myosin network drive apical constriction Nature 457 2009 495 499
6. M. Rauzi, and P. Verant P.F. Lenne Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis Nat. Cell Biol. 10 2008 1401 1410
7. E. Farge Mechanical induction of Twist in the Drosophila foregut/stomodeal primordium Curr. Biol. 13 2003 1365 1377
8. K.R. Levental, and H. Yu V.M. Weaver Matrix crosslinking forces tumor progression by enhancing integrin signaling Cell 139 2009 891 906
9. M.J. Paszek, and N. Zahir V.M. Weaver Tensional homeostasis and the malignant phenotype Cancer Cell 8 2005 241 254
10. M. Dembo, and Y.L. Wang Stresses at the cell-to-substrate interface during locomotion of fibroblasts Biophys. J. 76 1999 2307 2316
11. T.E. Angelini, and E. Hannezo D.A. Weitz Cell migration driven by cooperative substrate deformation patterns Phys. Rev. Lett. 104 2010 168104
12. D.T. Tambe, and C.C. Hardin X. Trepat Collective cell guidance by cooperative intercellular forces Nat. Mater. 10 2011 469 475
13. X. Trepat, and M.R. Wasserman J.J. Fredberg Physical forces during collective cell migration Nat. Phys. 5 2009 426 430
14. J.L. Tan, and J. Tien 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
15. O. du Roure, and A. Saez B. Ladoux Force mapping in epithelial cell migration Proc. Natl. Acad. Sci. USA 102 2005 2390 2395
16. (Erratum in Proc. Natl. Acad. Sci. USA. 2005 102:14122)
17. S. Ghassemi, and G. Meacci J. Hone Cells test substrate rigidity by local contractions on submicrometer pillars Proc. Natl. Acad. Sci. USA 109 2012 5328 5333
18. S.S. Hur, and Y. Zhao S. Chien Live cells exert 3-dimensional traction forces on their substrata Cell Mol. Bioeng. 2 2009 425 436
19. S.A. Maskarinec, and C. Franck G. Ravichandran Quantifying cellular traction forces in three dimensions Proc. Natl. Acad. Sci. USA 106 2009 22108 22113
20. C.S. Chen, and M. Mrksich D.E. Ingber Geometric control of cell life and death Science 276 1997 1425 1428
21. M.A. Schwartz Integrins and extracellular matrix in mechanotransduction Cold Spring Harb. Perspect. Biol. 2 2010 a005066
22. W.R. Legant, and J.S. Miller C.S. Chen Measurement of mechanical tractions exerted by cells in three-dimensional matrices Nat. Methods 7 2010 969 971
23. P. Friedl, and D. Gilmour Collective cell migration in morphogenesis, regeneration and cancer Nat. Rev. Mol. Cell Biol. 10 2009 445 457
24. A.A. Khalil, and P. Friedl Determinants of leader cells in collective cell migration Integr. Biol. (Camb.) 2 2010 568 574
25. C.M. Nelson, J.L. Inman, and M.J. Bissell Three-dimensional lithographically defined organotypic tissue arrays for quantitative analysis of morphogenesis and neoplastic progression Nat. Protoc. 3 2008 674 678
26. C.M. Nelson, and M.M. Vanduijn M.J. Bissell Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures Science 314 2006 298 300
27. V.H. Barocas, A.G. Moon, and R.T. Tranquillo The fibroblast-populated collagen microsphere assay of cell traction force - Part 2: Measurement of the cell traction parameter J. Biomech. Eng. 117 1995 161 170
28. C. Franck, and S.A. Maskarinec G. Ravichandran Three-dimensional traction force microscopy: a new tool for quantifying cell-matrix interactions PLoS ONE 6 2011 e17833
29. J.P. Butler, and I.M. Tolić-Nurrelykke J.J. Fredberg Traction fields, moments, and strain energy that cells exert on their surroundings Am. J. Physiol. Cell Physiol. 282 2002 C595 C605
30. B. Sabass, and M.L. Gardel U.S. Schwarz High resolution traction force microscopy based on experimental and computational advances Biophys. J. 94 2008 207 220
31. U.S. Schwarz, and N.Q. Balaban S.A. Safran Calculation of forces at focal adhesions from elastic substrate data: the effect of localized force and the need for regularization Biophys. J. 83 2002 1380 1394
32. T.M. Koch, and S. Münster B. Fabry 3D Traction forces in cancer cell invasion PLoS ONE 7 2012 e33476
33. N. Gjorevski, and C.M. Nelson Bidirectional extracellular matrix signaling during tissue morphogenesis Cytokine Growth Factor Rev. 20 2009 459 465
34. C.W. Daniel, S. Robinson, and G.B. Silberstein The role of TGF-beta in patterning and growth of the mammary ductal tree J. Mammary Gland Biol. Neoplasia 1 1996 331 341
35. H. Mori, and N. Gjorevski C.M. Nelson Self-organization of engineered epithelial tubules by differential cellular motility Proc. Natl. Acad. Sci. USA 106 2009 14890 14895
36. M.D. Sternlicht, and S.W. Sunnarborg Z. Werb Mammary ductal morphogenesis requires paracrine activation of stromal EGFR via ADAM17-dependent shedding of epithelial amphiregulin Development 132 2005 3923 3933
37. B.S. Wiseman, and M.D. Sternlicht Z. Werb Site-specific inductive and inhibitory activities of MMP-2 and MMP-3 orchestrate mammary gland branching morphogenesis J. Cell Biol. 162 2003 1123 1133
38. C.M. Kraning-Rush, and S.P. Carey C.A. Reinhart-King The role of the cytoskeleton in cellular force generation in 2D and 3D environments Phys. Biol. 8 2011 015009
39. Y. Pang, and A.A. Ucuzian H.P. Greisler The temporal and spatial dynamics of microscale collagen scaffold remodeling by smooth muscle cells Biomaterials 30 2009 2023 2031
40. Y. Pang, and X. Wang H.P. Greisler Dynamic quantitative visualization of single cell alignment and migration and matrix remodeling in 3-D collagen hydrogels under mechanical force Biomaterials 32 2011 3776 3783
41. P.P. Provenzano, and D.R. Inman P.J. Keely Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization Biophys. J. 95 2008 5374 5384
42. P. Fernandez, and A.R. Bausch The compaction of gels by cells: a case of collective mechanical activity Integr. Biol. (Camb.) 1 2009 252 259
43. R.J. Bloom, and J.P. George D. Wirtz Mapping local matrix remodeling induced by a migrating tumor cell using three-dimensional multiple-particle tracking Biophys. J. 95 2008 4077 4088
44. M.D. Stevenson, and A.L. Sieminski K.J. Gooch Pericellular conditions regulate extent of cell-mediated compaction of collagen gels Biophys. J. 99 2010 19 28
45. T.A. Ulrich, and A. Jain S. Kumar Probing cellular mechanobiology in three-dimensional culture with collagen-agarose matrices Biomaterials 31 2010 1875 1884
46. J.P. Winer, S. Oake, and P.A. Janmey Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation PLoS ONE 4 2009 e6382
47. A.O. Brightman, and B.P. Rajwa S.L. Voytik-Harbin Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro Biopolymers 54 2000 222 234
48. P. Friedl, and K. Maaser K.S. Zänker Migration of highly aggressive MV3 melanoma cells in 3-dimensional collagen lattices results in local matrix reorganization and shedding of alpha2 and beta1 integrins and CD44 Cancer Res. 57 1997 2061 2070
49. Y. Pang, and X. Wang H.P. Greisler Local delivery of a collagen-binding FGF-1 chimera to smooth muscle cells in collagen scaffolds for vascular tissue engineering Biomaterials 31 2010 878 885
50. V.D. Gordon, and M.T. Valentine T.S. Deisboeck Measuring the mechanical stress induced by an expanding multicellular tumor system: a case study Exp. Cell Res. 289 2003 58 66
51. N. Gjorevski, and C.M. Nelson Integrated morphodynamic signalling of the mammary gland Nat. Rev. Mol. Cell Biol. 12 2011 581 593
52. C.M. Nelson Geometric control of tissue morphogenesis Biochim. Biophys. Acta 1793 2009 903 910
53. I.B. Bischofs, and U.S. Schwarz Cell organization in soft media due to active mechanosensing Proc. Natl. Acad. Sci. USA 100 2003 9274 9279
54. C.A. Reinhart-King, M. Dembo, and D.A. Hammer Cell-cell mechanical communication through compliant substrates Biophys. J. 95 2008 6044 6051
55. X. Trepat, B. Fabry, and J.J. Fredberg Pulling it together in three dimensions Nat. Methods 7 2010 963 965
56. E. Caussinus, J. Colombelli, and M. Affolter Tip-cell migration controls stalk-cell intercalation during Drosophila tracheal tube elongation Curr. Biol. 18 2008 1727 1734
57. M. Rauzi, P.F. Lenne, and T. Lecuit Planar polarized actomyosin contractile flows control epithelial junction remodelling Nature 468 2010 1110 1114
58. E. Cukierman, and R. Pankov K.M. Yamada Taking cell-matrix adhesions to the third dimension Science 294 2001 1708 1712
59. J. Muschler, and C.H. Streuli Cell-matrix interactions in mammary gland development and breast cancer Cold Spring Harb. Perspect. Biol. 2 2010 a003202
60. P. Schedin, and T. Mitrenga M. Kaeck Mammary ECM composition and function are altered by reproductive state Mol. Carcinog. 41 2004 207 220
61. L. Hinck, and G.B. Silberstein Key stages in mammary gland development: the mammary end bud as a motile organ Breast Cancer Res. 7 2005 245 251