Substrate Stiffness Mediated Metastasis Like Phenotype of Colon Cancer Cells is Independent of Cell to Gel Adhesion

Cellular and Molecular Bioengineering

Volumn 7, Issue 4, 2014, Pages 532-543

  Ali, M Yakut ^a   Saif, M Taher A ^a  

^a University of Illinois at Urbana Champaign   (United States)

Author keywords

Cell mechanics; Cells on polyacrylamide gel; Cytoskeleton; Metastasis like phenotype of colon cancer cells; Substrate stiffness

Indexed keywords

ACTIN; ALPHA CATENIN; COLLAGEN; FIBRONECTIN; MYOSIN; MYOSIN II; POLYSTYRENE; UVOMORULIN; VINCULIN;

ACTIN FILAMENT; ARTICLE; CANCER CELL LINE; CELL ADHESION; CELL CULTURE; CELL SPREADING; CELL STRUCTURE; CELL VIABILITY; COLON CANCER; COLON CARCINOMA; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYDROGEL; IMAGE ANALYSIS; IMMUNOFLUORESCENCE MICROSCOPY; MECHANOTRANSDUCTION; METASTASIS; MITOSIS; PHENOTYPE; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RIGIDITY;

EID: 84919822622     PISSN: 18655025     EISSN: 18655033     Source Type: Journal    
DOI: 10.1007/s12195-014-0345-8     Document Type: Article

References (60)

1. Aberle, H., S. Butz, J. Stappert, H. Weissig, R. Kemler, and H. Hoschuetzky. Assembly of the cadherin–catenin complex in vitro with recombinant proteins. J. Cell Sci. 107:655–663, 1994.
2. Abramoff, M. D., P. J. Magalhaes, and S. J. Ram. Image processing with ImageJ. Biophoton. Int. 11(7):36–41, 2004.
3. Alberts, B., A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter. Molecular Biology of the Cell, Chaps. 16 and 19. New York: Garland Science, 2007.
4. Bajaj, P., X. Tang, T. Saif, and R. Bashir. Stiffness of the substrate influences the phenotype of embryonic chicken cardiac myocytes. J. Biomed. Mater. Res. A 95(4):1261–1269, 2010.
5. Baker, E. L., R. T. Bonnecaze, and M. H. Zaman. Extracellular matrix stiffness and architecture govern intracellular rheology in cancer. Biophys. J. 97:1013–1021, 2009.
6. Baker, E. L., J. Lu, D. Yu, R. T. Bonnecaze, and M. H. Zaman. Cancer cell stiffness: integrated roles of three-dimensional matrix stiffness and transforming potential. Biophys. J. 99:2048–2057, 2010.
7. Barkan, D., H. Kleinman, J. L. Simmons, H. Asmussen, A. K. Kamaraju, M. J. Hoenorhoff, Z. Y. Liu, S. V. Costes, E. H. Cho, S. Lockett, C. Khanna, A. F. Chambers, and J. E. Green. Inhibition of metastatic outgrowth from single dormant tumor cells by targeting the cytoskeleton. Cancer Res. 68:6241–6250, 2008.
8. Burdick, M. M., J. M. McCaffery, Y. S. Kim, B. S. Bochner, and K. Konstantopoulos. Colon carcinoma cell glycolipids, integrins, and other glycoproteins mediate adhesion to HUVECs under flow. Am. J. Physiol. Cell Physiol. 284(4):977–987, 2003.
9. Byfield, F. J., Q. Wen, I. Levental, K. Nordstrom, P. E. Arratia, et al. Absence of filamin a prevents cells from responding to stiffness gradients on gels coated with collagen but not fibronectin. Biophys. J. 96:5095–5102, 2009.
10. Chaffer, C. L., and R. A. Weinberg. A perspective on cancer cell metastasis. Science 331:1559–1564, 2011.
11. Choi, J. S., and B. A. Harley. The combined influence of substrate elasticity and ligand density on the viability and biophysical properties of hematopoietic stem and progenitor cells. Biomaterials 33:4460–4468, 2012.
12. Chopra, A., E. Tabdanov, H. Patel, P. A. Janmey, and J. Y. Kresh. Cardiac myocyte remodeling mediated by N-cadherin-dependent mechanosensing. Am. J. Physiol. Heart Circ. Physiol. 300:1252–1266, 2011.
13. Damljanovic, V., B. C. Lagerholm, and K. Jacobson. Bulk and micropatterned conjugation of extracellular matrix proteins to characterized polyacrylamide substrates for cell mechanotransduction assays. Biotechniques 39:847–851, 2005.
14. Discher, D., P. Janmey, and Y. L. Wang. Tissue cells feel and respond to the stiffness of their substrate. Science 310:1139–1143, 2005.
15. Engler, A. J., C. Carag-Krieger, C. P. Johnson, M. Raab, H. Y. Tang, D. W. Speicher, et al. Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J. Cell Sci. 121:3794–3802, 2008.
16. Engler, A. J., F. Rehfeldt, S. Sena, and D. E. Discher. Microtissue elasticity: measurements by atomic force microscopy and its influence on cell differentiation. Methods Cell Biol. 83:521–545, 2007.
17. Engler, A. J., S. Sen, H. L. Sweeney, and D. E. Discher. Matrix elasticity directs stem cell lineage specification. Cell 126:677–689, 2006.
18. Farman, G. P., K. Tachampa, R. Mateja, O. Cazorla, A. Lacampagne, and P. P. de Tombe. Blebbistatin: use as inhibitor of muscle contraction. Eur. J. Physiol. 455:995–1005, 2008.
19. Georges, P. C., and P. A. Janmey. Cell type-specific response to growth on soft materials. J. Appl. Physiol. 98:1547–1553, 2005.
20. Guo, W. H., M. T. Frey, N. A. Burnham, and Y. L. Wang. Substrate rigidity regulates the formation and maintenance of tissues. Biophys. J. 90:2213–2220, 2006.
21. Hayes, A. W. Principles and Methods of Toxicology. New York: Raven Press, pp. 1231–1258, 1994.
22. Ingber, D. E. Can cancer be reversed by engineering the tumor microenvironment? Semin. Cancer Biol. 18:356–364, 2008.
23. Jay, P. Y., P. A. Pham, S. A. Wong, and E. L. Elson. A mechanical function of myosin II in cell motility. J. Cell Sci. 108:387–393, 1995.
24. Jou, T. S., D. B. Stewart, J. Stappert, W. J. Nelson, and J. A. Marrs. Genetic and biochemical dissection of protein linkages in the cadherin–catenin complex. Proc. Natl. Acad. Sci. USA 92:5067–5071, 1995.
25. Kovacs, M., J. Toth, C. Hetenyi, A. Malnasi-Csizmadia, and J. R. Sellers. Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 279:35557–35563, 2004.
26. Kumar, S., and V. M. Weaver. Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev. 28:113–127, 2009.
27. le Duc, Q., Q. Shi, I. Blonk, A. Sonnenberg, N. Wang, D. Leckband, and J. de Rooij. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J. Cell Biol. 189(7):107–115, 2010.
28. Leckband, D. E., Q. le Duc, N. Wang, and J. de Rooij. Mechanotransduction at cadherin-mediated adhesions. Curr. Opin. Cell Biol. 23:523–530, 2011.
29. Levental, I., P. C. Georges, and P. A. Janmey. Soft biological materials and their impact on cell function. Soft Matter 3:299–306, 2007.
30. Levental, K. R., H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. Fong, K. Csiszar, A. Giaccia, W. Weninger, et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139:891–906, 2009.
31. Li, D., J. Zhou, L. Wang, M. E. Shin, P. Su, et al. Integrated biochemical and mechanical signals regulate multifaceted human embryonic stem cell functions. J. Cell Biol. 191:631–644, 2010.
32. Lo, C. M., H. B. Wang, M. Dembo, and Y. L. Wang. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79:144–152, 2000.
33. Mason, B. N., A. Starchenko, R. M. Williams, L. J. Bonassar, and C. A. Reinhart-King. Tuning 3D collagen matrix stiffness independently of collagen concentration modulates endothelial cell behavior. Acta Biomater. 9:4635–4644, 2013.
34. Ochsner, M., M. Textor, V. Vogel, and M. L. Smith. Dimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape. PLoS ONE 5(3):e9445, 2010. doi:10.1371/journal.pone.0009445.
35. Paszek, M. J., N. Zahir, K. R. Johnson, J. N. Lakins, G. I. Rozenberg, et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8:241–254, 2005.
36. Pathak, A., and S. Kumar. Biophysical regulation of tumor cell invasion: moving beyond matrix stiffness. Integr. Biol. 3(4):267–278, 2011.
37. Pathak, A., and S. Kumar. Independent regulation of tumor cell migration by matrix stiffness and confinement. Proc. Natl. Acad. Sci. USA 109(26):10334–10339, 2012.
38. Pelham, R. J., and Y. L. Wang. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. USA 94(25):3661–3665, 1997.
39. Pelham, Jr., J. R., and Y. L. Wang. High resolution detection of mechanical forces exerted by locomoting fibroblasts on the substrate. Mol. Biol. Cell 10:935–945, 1999.
40. Radmacher, M. Measuring the elastic properties of living cells by the atomic force microscope. Methods Cell Biol. 68:67–90, 2002.
41. Rosenthal, K. L., W. A. Tompkins, G. L. Frank, P. McCulloch, and W. E. Rawls. Variants of a human colon adenocarcinoma cell line which differ in morphology and carcinoembryonic antigen production. Cancer Res. 37:4024–4030, 1977.
42. Saif, T. On the capillary interaction between solid plates forming menisci on the surface of a liquid. J. Fluid Mech. 473:321–347, 2002.
43. Solon, J., I. Levental, K. Sengupta, P. C. Georges, and P. A. Janmey. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys. J. 93:4453–4461, 2007.
44. Straight, A. F., A. Cheung, J. Limouze, I. Chen, N. J. Westwood, J. R. Sellers, and T. J. Mitchison. Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 229:1743–1747, 2003.
45. Tang, X., M. Y. Ali, and T. Saif. A novel technique for micro-patterning proteins and cells on polyacrylamide gels. Soft Matter 8:3197–3206, 2012.
46. Tang, X., P. Bajaj, R. Bashir, and T. Saif. How far cardiac cells can see each other mechanically. Soft Matter 7:6151–6158, 2011.
47. Tang, X., T. Cappa, T. Kuhlenschmidt, M. Kuhlenschmidt, and T. Saif. Specific and non-specific adhesion in cancer cells with various metastatic potentials. In: Mechanobiology of Cell–Cell and Cell–Matrix Interactions, edited by A. W. Johnson, and B. Harley. New York: Springer Science, 2011, pp. 105–122.
48. Tang, X., T. B. Kuhlenschmidt, J. Zhou, P. Bell, F. Wang, M. S. Kuhlenschmidt, and T. Saif. Mechanical force affects expression of an in vitro metastasis-like phenotype in HCT-8 cells. Biophys. J. 99:2460–2469, 2010.
49. Tilghman, R. W., C. R. Cowan, J. D. Mih, Y. Koryakina, D. Gioeli, et al. Matrix rigidity regulates cancer cell growth and cellular phenotype. PLoS ONE 5(9):e12905, 2010. doi:10.1371/journal.pone.0012905.
50. Twiss, F., Q. le Duc, S. van der Horst, H. Tabdili, G. van der Krogt, N. Wang, H. Rehmann, S. Huveneers, D. E. Leckband, and J. de Rooij. Vinculin-dependent Cadherin mechanosensing regulates efficient epithelial barrier formation. Biol. Open. 1(11):1128–1140, 2012.
51. Ulrich, T. A., E. M. de Juan Pardo, and S. Kumar. The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res. 69:4167–4174, 2009.
52. Vermeulen, S. J., E. A. Bruyneel, M. E. Bracke, G. K. De Bruyne, K. M. Vennekens, K. L. Vleminckx, G. J. Berx, F. M. Van Roy, and M. M. Mareel. Transition from the noninvasive to the invasive phenotype and loss of a-Catenin in human colon cancer cells. Cancer Res. 55:4722–4728, 1995.
53. Vermeulen, S. J., T. R. Chen, F. Speleman, F. Nollet, F. M. Van Roy, and M. M. Mareel. Did the four human cancer cell lines DLD-1, HCT-15, HCT-8, and HRT-18 originate from one and the same patient? Cancer Genet. Cytogenet. 107:76–79, 1998.
54. Vermeulen, S. J., F. Nollet, E. Teugels, K. M. Vennekens, F. Malfait, J. Philippe, F. Speleman, M. E. Bracke, F. M. Van Roy, and M. M. Mareel. The alpha-E-catenin gene (CTNNA1) acts as an invasion-suppressor gene in human colon cancer cells. Oncogene 18:905–915, 1999.
55. Wang, H. B., M. Dembo, and Y. L. Wang. Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. Am. J. Physiol. Cell. Physiol. 279:1345–1350, 2000.
56. Wang, Y. L., and R. Pelham. Preparation of a flexible, porous polyacrylamide substrate for mechanical studies of cultured cells. Methods Enzymol. 298:489–496, 1998.
57. Yamada, Y., F. Katagiri, K. Hozumi, Y. Kikkawa, and M. Nomizu. Cell behavior on protein matrices containing laminin α1 peptide AG73. Biomaterials 32(19):4327–4335, 2011.
58. Yeung, T., P. C. Georges, L. A. Flanagan, B. Marg, M. Ortiz, M. Funaki, N. Zahir, W. Ming, V. Weaver, and P. A. Janmey. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskelet 60:24–34, 2005.
59. Yonemura, S., Y. Wada, T. Watanabe, A. Nagafuchi, and M. Shibata. Alpha-catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 12:533–542, 2010.
60. Yu, W., A. Datta, P. Leroy, L. E. O’Brien, G. Mak, T. S. Jou, et al. β1-integrin orients epithelial polarity via Rac1 and laminin. Mol. Biol. Cell 16(2):433–445, 2005.