Biochemical and mechanical extracellular matrix properties dictate mammary epithelial cell motility and assembly

Biotechnology Journal

Volumn 7, Issue 3, 2012, Pages 397-408

  Shebanova, Olga ^a   Hammer, Daniel A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Breast epithelial metastasis; Polyacrylamide gel; Substrate rigidity; Three dimensional aggregates; Traction force

Indexed keywords

BIPHASIC; BREAST CANCER MODELS; BREAST EPITHELIAL METASTASIS; BREAST TISSUES; CELL MATRIX; CELL MIGRATION; CELL MOTILITY; CELL PAIRS; CELL-CELL ADHESION; CELL-CELL INTERACTION; CELL-MATRIX ADHESION; EXTRACELLULAR MATRICES; FORCE GENERATION; IN-VITRO; LIGAND CONCENTRATION; LIGAND DENSITY; MAMMARY EPITHELIAL CELLS; MATRIX RIGIDITY; MECHANICAL CUES; MIGRATION VELOCITY; POLYACRYLAMIDE GEL; POLYACRYLAMIDE GELS; SINGLE CELLS; SPHERICAL AGGREGATES; TRACTION FORCE; TRACTION FORCES;

ADHESION; AGGREGATES; CELL ADHESION; ELASTICITY; GELS; LIGANDS; RIGIDITY; STIFFNESS; THREE DIMENSIONAL; TISSUE; TRACTION (FRICTION); TWO DIMENSIONAL; VELOCITY;

CELLS;

FIBRONECTIN; POLYACRYLAMIDE GEL;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL; CELL ADHESION; CELL INTERACTION; CELL MIGRATION; CELL MOTILITY; CELL SURFACE; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IN VITRO STUDY; PRECANCER; PRIORITY JOURNAL; RIGIDITY;

CELL ADHESION; CELL COMMUNICATION; CELL MOVEMENT; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; FEMALE; FIBRONECTINS; HUMANS; MAMMARY GLANDS, HUMAN; STRESS, MECHANICAL;

EID: 84857751129     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201100188     Document Type: Article

References (45)

1. Kass, L., Erler, J. T., Dembo, M., Weaver, V. M., Mammary epithelial cell: Influence of extracellular matrix composition and organization during development and tumorigenesis. Int. J. Biochem. Cell Biol. 2007, 39, 1987-1994.
2. Tognon, C., Knezevich, S. R., Huntsman, D., Roskelley, C. D. et al., Expression of the ETV6-NTRK3 gene fusion as a primary event in human secretory breast carcinoma. Cancer Cell 2002, 2, 367-376.
3. Weaver, V. M., Petersen, O. W., Wang, F., Larabell, C. A. et al., Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J. Cell Biol. 1997, 137, 231-245.
4. Wolfe, J. N., Risk for breast-cancer development determined by mammographic parenchymal pattern. Cancer 1976, 37, 2486-2492.
5. Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N. et al., Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8, 241-254.
6. Debnath, J., Brugge, J. S., Modelling glandular epithelial cancers in three-dimensional cultures. Nat. Rev. Cancer 2005, 5, 675-688.
7. Debnath, J., Muthuswamy, S. K., Brugge, J. S., Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003, 30, 256-268.
8. Li, T., Sun, L. M., Miller, N., Nicklee, T. et al., The association of measured breast tissue characteristics with mammographic density and other risk factors for breast cancer. Cancer Epidemiol. Biomarkers Prevention 2005, 14, 343-349.
9. Brown, L. F., Guidi, A. J., Schnitt, S. J., Van De Water, L. et al., Vascular stroma formation in carcinoma in situ, invasive carcinoma, and metastatic carcinoma of the breast. Clin. Cancer Res. 1999, 5, 1041-1056.
10. Hao, X. S., Sun, B. C., Hu, L. M., Lahdesmaki, H. et al., Differential gene and protein expression in primary breast malignancies and their lymph node metastases as revealed by combined cDNA microarray and tissue microarray analysis. Cancer 2004, 100, 1110-1122.
11. Tawil, N. J., Gowri, V., Djoneidi, M., Nip, J. et al., Integrin alpha(3)beta(1) can promote adhesion and spreading of metastatic breast carcinoma cells on the lymph node stroma. Int. J. Cancer 1996, 66, 703-710.
12. Duguay, D., Foty, R. A., Steinberg, M. S., Cadherin-mediated cell adhesion and tissue segregation: Qualitative and quantitative determinants. Dev. Biol. 2003, 253, 309-323.
13. Foty, R. A., Steinberg, M. S., Cadherin-mediated cell-cell adhesion and tissue segregation in relation to malignancy. Int. J. Dev. Biol. 2004, 48, 397-409.
14. Califano, J. P., Reinhart-King, C. A., A balance of substrate mechanics and matrix chemistry regulates endothelial cell network assembly. Cell. Mol. Bioeng. 2008, 1, 122-132.
15. Lauffenburger, D. A., Griffith, L. G., Who's got pull around here? Cell organization in development and tissue engineering. Proc. Natl. Acad. Sci. USA 2001, 98, 4282-4284.
16. Saunders, R. L., Hammer, D. A., Assembly of human umbilical vein endothelial cells on compliant hydrogels. Cell. Mol. Bioeng. 2010, 3, 60-67.
17. Lo, C. M., Wang, H. B., Dembo, M., Wang, Y. L., Cell movement is guided by the rigidity of the substrate. Biophys. J. 2000, 79, 144-152.
18. Peyton, S. R., Putnam, A. J., Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J. Cell. Physiol. 2005, 204, 198-209.
19. Wong, J. Y., Velasco, A., Rajagopalan, P., Pham, Q., Directed movement of vascular smooth muscle cells on gradient-compliant hydrogels. Langmuir 2003, 19, 1908-1913.
20. Yeung, T., Georges, P. C., Flanagan, L. A., Marg, B. et al., Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskeleton 2005, 60, 24-34.
21. Reinhart-King, C. A., Dembo, M., Hammer, D. A., Cell-cell mechanical communication through compliant substrates. Biophys. J. 2008, 95, 6044-6051.
22. Butcher, D. T., Alliston, T., Weaver, V. M., A tense situation: Forcing tumour progression. Nat. Rev. Cancer 2009, 9, 108-122.
23. Chen, C. S., Mechanotransduction - a field pulling together? J. Cell Sci. 2008, 121, 3285-3292.
24. Vial, E., Sahai, E., Marshall, C. J., ERK-MAPK signaling coordinately regulates activity of Rac1 and RhoA for tumor cell motility. Cancer Cell 2003, 4, 67-79.
25. Gaudet, C., Marganski, W. A., Kim, S., Brown, C. T. et al., Influence of type I collagen surface density on fibroblast spreading, motility, and contractility. Biophys. J. 2003, 85, 3329-3335.
26. Dimilla, P. A., Stone, J. A., Quinn, J. A., Albelda, S. M., Lauffenburger, D. A., Maximal migration of human smooth-muscle cells on fibronectin and type-Iv collagen occurs at an intermediate attachment strength. J. Cell Biol. 1993, 122, 729-737.
27. Dimilla, P. A., Barbee, K., Lauffenburger, D. A., Mathematical-model for the effects of adhesion and mechanics on cell-migration speed. Biophys. J. 1991, 60, 15-37.
28. Zaman, M. H., Kamm, R. D., Matsudaira, P., Lauffenburger, D. A., Computational model for cell migration in three-dimensional matrices. Biophys. J. 2005, 88, 516A-517A.
29. Zaman, M. H., Trapani, L. M., Siemeski, A., MacKellar, D. et al., Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc. Natl. Acad. Sci. USA 2006, 103, 10889-10894.
30. Chen, X., Gumbiner, B. M., Crosstalk between different adhesion molecules. Curr. Opin. Cell Biol. 2006, 18, 572-578.
31. Miyoshi, J., Takai, Y., Structural and functional associations of apical junctions with cytoskeleton. Biochim. Biophys. Acta 2008, 1778, 670-691.
32. Yamada, S., Nelson, W. J., Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J. Cell Biol. 2007, 178, 517-527.
33. Tsai, J., Kam, L., Rigidity-dependent cross talk between integrin and cadherin signaling. Biophys. J. 2009, 96, L39-L41.
34. Wang, Y. L., Pelham, R. J., Preparation of a flexible, porous polyacrylamide substrate for mechanical studies of cultured cells. Mol. Motors Cytoskeleton, Pt B 1998, 298, 489-496.
35. Wong, J. Y., Leach, J. B., Brown, X. Q., Balance of chemistry, topography, and mechanics at the cell-biomaterial interface: Issues and challenges for assessing the role of substrate mechanics on cell response. Surf. Sci. 2004, 570, 119-133.
36. Pless, D. D., Lee, Y. C., Roseman, S., Schnaar, R. L., Specific cell-adhesion to immobilized glycoproteins demonstrated using new reagents for protein and glycoprotein immobilization. J. Biol. Chem. 1983, 258, 2340-2349.
37. Dembo, M., Oliver, T., Ishihara, A., Jacobson, K. Imaging the traction stresses exerted by locomoting cells with the elastic substratum method. Biophys. J. 1996, 70, 2008-2022.
38. Marganski, W. A., Dembo, M., Wang, Y. L., Measurements of cell-generated deformations on flexible substrata using correlation-based optical flow. Methods Enzymol. 2003, 361, 197-211.
39. Dembo, M., Wang, Y. L., Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys. J. 1999, 76, 2307-2316.
40. Reinhart-King, C. A., Dembo, M., Hammer, D. A., Endothelial cell traction forces on RGD-derivatized polyacrylamide substrata. Langmuir 2003, 19, 1573-1579.
41. Reinhart-King, C. A., Dembo, M., Hammer, D. A., The dynamics and mechanics of endothelial cell spreading. Biophys. J. 2005, 89, 676-689.
42. Engler, A., Bacakova, L., Newman, C., Hategan, A. et al., Substrate compliance versus ligand density in cell on gel responses. Biophys. J. 2004, 86, 617-628.
43. Guo, W. H., Frey, M. T., Burnham, N. A., Wang, Y. L., Substrate rigidity regulates the formation and maintenance of tissues. Biophys. J. 2006, 90, 2213-2220.
44. Palecek, S. P., Loftus, J. C., Ginsberg, M. H., Lauffenburger, D. A., Horwitz, A. F., Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 1997, 385, 537-540.
45. Fournier, A. K., Campbell, L. E., Castagnino, P., Liu, W. F. et al., Rac-dependent cyclin D1 gene expression regulated by cadherin- and integrin-mediated adhesion. J. Cell Sci. 2008, 121, 226-233.