Modeling the mechanics of cancer: Effect of changes in cellular and extra-cellular mechanical properties

Frontiers in Oncology

Volumn 3 JUN, Issue , 2013, Pages

  Katira, Parag ^a   Bonnecaze, Roger T ^a   Zaman, Muhammad H ^b  

^a The University of Texas at Austin   (United States)

^b Boston University   (United States)

Author keywords

Cancer modeling; Cell cell interaction; Cell material interactions; Mechanical forces; Review

Indexed keywords

P CADHERIN;

CANCER CELL; CANCER GROWTH; CANCER MODEL; CARCINOGENESIS; CELL ADHESION; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; EXTRACELLULAR MATRIX; HUMAN; MATHEMATICAL MODEL; MECHANICS; METASTASIS; NEOPLASM; SHORT SURVEY; TUMOR GROWTH;

EID: 84891117850     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00145     Document Type: Short Survey

References (105)

1. Alexander, N. R., Branch, K. M., Parekh, A., Clark, E. S., Lwueke, L. C., Guelcher, S. A., et al. (2008). Extracellular matrix rigidity promotes invadopodia activity. Curr. Biol. 18, 1295-1299. doi:10.1016/j.cub.2008.07.090.
2. Alini, M., and Losa, G. A. (1991). Partial characterization of proteoglycans isolated from neoplastic and nonneoplastic human breast tissues. Cancer Res. 51, 1443-1447.
3. Ambrosi, D., and Mollica, F. (2004). The role of stress in the growth of a multicell spheroid. J. Math. Biol. 48, 477-499. doi:10.1007/s00285-003-0238-2.
4. Anderson, A. R. A., Rejniak, K. A., Gerlee, P., and Quaranta, V. (2009). Microenvironment driven invasion: a multiscale multimodel investigation. J. Math. Biol. 58, 579-624. doi:10.1007/s00285-008-0210-2.
5. Anderson, A. R. A., Weaver, A. M., Cummings, P. T., and Quaranta, V. (2006). Tumor morphology and phenotypic evolution driven by selective pressure from the microenvironment. Cell 127, 905-915. doi:10.1016/j.cell.2006.09.042.
6. Armstrong, N. J., Painter, K. J., and Sherratt, J. A. (2006). A continuum approach to modelling cell-cell adhesion. J. Theor. Biol. 243, 98-113. doi:10.1016/j.jtbi.2006.05.030.
7. Assoian, R. K., and Klein, E. A. (2008). Growth control by intracellular tension and extracellular stiffness. Trends Cell Biol. 18, 347-352. doi:10.1016/j.tcb.2008.05.002.
8. Basan, M., Risler, T., Joanny, J. F., Sastre-Garau, X., and Prost, J. (2009). Homeostatic competition drives tumor growth and metastasis nucleation. HFSP J. 3, 265-272. doi:10.2976/1.3086732.
9. Bearer, E. L., Lowengrub, J. S., Frieboes, H. B., Chuang, Y. L., Jin, F., Wise, S. M., et al. (2009). Multiparameter computational modeling of tumor invasion. Cancer Res. 69, 4493-4501. doi:10.1158/0008-5472.CAN-08-3834.
10. Behrens, J., Mareel, M. M., Vanroy, F. M., and Birchmeier, W. (1989). Dissecting tumor-cell invasion-epithelial-cells acquire invasive properties after the loss of uvomorulin-mediated cell cell-adhesion. J. Cell Biol. 108, 2435-2447. doi:10.1083/jcb.108.6.2435.
11. Brodland, G. W., and Veldhuis, J. H. (2012). The mechanics of metastasis: insights from a computational model. PLoS ONE 7:e44281. doi:10.1371/journal.pone.0044281.
12. Brown, L. F., Guidi, A. J., Schnitt, S. J., Van De Water, L., Iruela-Arispe, M. L., Yeo, T. K., et al. (1999). Vascular stroma formation in carcinoma in situ, invasive carcinoma, and metastatic carcinoma of the breast. Clin. Cancer Res. 5, 1041-1056.
13. Bryan, R. T., Atherfold, P. A., Yeo, Y., Jones, L. J., Harrison, R. F., Wallace, D. M. A., et al. (2008). Cadherin switching dictates the biology of transitional cell carcinoma of the bladder: ex vivo and in vitro studies. J. Pathol. 215, 184-194. doi:10.1002/path.2346.
14. Byrne, H., and Drasdo, D. (2009). Individual-based and continuum models of growing cell populations: a comparison. J. Math. Biol. 58, 657-687. doi:10.1007/s00285-008-0212-0.
15. Byrne, H. M., and Chaplain, M. A. J. (1996). Modelling the role of cell-cell adhesion in the growth and development of carcinoma. Math. Comput. Model 24, 1-17. doi:10.1016/S0895-7177(96)00174-4.
16. Chaplain, M. A. J., Graziano, L., and Preziosi, L. (2006). Mathematical modelling of the loss of tissue compression responsiveness and its role in solid tumour development. Math. Med. Biol. 23, 197-229. doi:10.1093/imammb/dql009.
17. Chen, C. S. (2008). Mechanotransduction-a field pulling together? J. Cell. Sci. 121, 3285-3292. doi:10.1242/jcs.023507.
18. Chen, C. Y., Byrne, H. M., and King, J. R. (2001). The influence of growth-induced stress from the surrounding medium on the development of multicell spheroids. J. Math. Biol. 43, 191-220. doi:10.1007/s002850100091.
19. Cheng, G., Tse, J., Jain, R. K., and Munn, L. L. (2009). Micro-environmental mechanical stress controls tumor spheroid size and morphology by suppressing proliferation and inducing apoptosis in cancer cells. PLoS ONE 4:e4632. doi:10.1371/journal.pone.0004632.
20. Christensen, L. (1992). The distribution of fibronectin, laminin and tetranectin in human breast-cancer with special attention to the extracellular-matrix. APMIS 100, 1-39.
21. Ciarletta, P., Ambrosi, D., Maugin, G. A., and Preziosi, L. (2013). Mechano-transduction in tumour growth modelling. Eur. Phys. J. E Soft Matter 36, 1-9. doi:10.1140/epje/i2013-13023-2.
22. Clark, E. S., Whigham, A. S., Yarbrough, W. G., and Weaver, A. M. (2007). Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res. 67, 4227-4235. doi:10.1158/0008-5472.CAN-06-3928.
23. Cross, S. E., Jin, Y. S., Lu, Q. Y., Rao, J. Y., and Gimzewski, J. K. (2011). Green tea extract selectively targets nanomechanics of live metastatic cancer cells. Nanotechnology 22 doi:10.1088/0957-4484/22/21/215101.
24. Cross, S. E., Jin, Y. S., Rao, J., and Gimzewski, J. K. (2007). Nanomechanical analysis of cells from cancer patients. Nat. Nanotechnol. 2, 780-783. doi:10.1038/nnano.2007.388.
25. D'Antonio, G., Macklin, P., and Preziosi, L. (2013). An agent-based model for elasto-plastic mechanical interactions between cells, basement membrane and extracellular matrix. Math. Biosci. Eng. 10, 75-101. doi:10.3934/mbe.2013.10.75.
26. Deisboeck, T. S., Wang, Z. H., Macklin, P., and Cristini, V. (2011). Multiscale cancer modeling. Annu. Rev. Biomed. Eng. 13, 127-155. doi:10.1146/annurev-bioeng-071910-124729.
27. Drasdo, D., and Hoehme, S. (2012). Modeling the impact of granular embedding media, and pulling versus pushing cells on growing cell clones. New J. Phys. 14. doi:10.1088/1367-2630/14/5/055025.
28. Drasdo, D., and Hohme, S. (2005). A single-cell-based model of tumor growth in vitro: monolayers and spheroids. Phys. Biol. 2, 133-147. doi:10.1088/1478-3975/2/3/001.
29. Dunn, G. A., and Heath, J. P. (1976). New hypothesis of contact guidance in tissue-cells. Exp. Cell Res. 101, 1-14. doi:10.1016/0014-4827(76)90405-5.
30. Enderling, H., Alexander, N. R., Clark, E. S., Branch, K. M., Estrada, L., Crooke, C., et al. (2008). Dependence of invadopodia function on collagen fiber spacing and cross-linking: computational modeling and experimental evidence. Biophys. J. 95, 2203-2218. doi:10.1529/biophysj.108.133199.
31. Erler, J. T., Bennewith, K. L., and Giaccia, A. J. (2006). The role of lysyl oxidase in premetastatic niche formation. Breast Cancer Res. Treat. 100, S7-S7.
32. Erler, J. T., and Weaver, V. M. (2009). Three-dimensional context regulation of metastasis. Clin. Exp. Metastasis 26, 35-49. doi:10.1007/s10585-008-9209-8.
33. Finger, E. C., and Giaccia, A. J. (2010). Hypoxia, inflammation, and the tumor microenvironment in metastatic disease. Cancer Metastasis Rev. 29, 285-293. doi:10.1007/s10555-010-9224-5.
34. Franks, S. J., Byrne, H. M., Underwood, J. C. E., and Lewis, C. E. (2005). Biological inferences from a mathematical model of comedo ductal carcinoma in situ of the breast. J. Theor. Biol. 232, 523-543. doi:10.1016/j.jtbi.2004.08.032.
35. Frieboes, H. B., Chaplain, M. A. J., Thompson, A. M., Bearer, E. L., Lowengrub, J. S., and Cristini, V. (2011). Physical oncology: a bench-to-bedside quantitative and predictive approach. Cancer Res. 71, 298-302. doi:10.1158/0008-5472.CAN-10-2676.
36. Frieboes, H. B., Jin, F., Chuang, Y. L., Wise, S. M., Lowengrub, J. S., and Cristini, V. (2010). Three-dimensional multispecies nonlinear tumor growth-II: tumor invasion and angiogenesis. J. Theor. Biol. 264, 1254-1278. doi:10.1016/j.jtbi.2010.02.036.
37. Frieboes, H. B., Lowengrub, J. S., Wise, S., Zheng, X., Macklin, P., Elaine, L. B. D., et al. (2007). Computer simulation of glioma growth and morphology. Neuroimage 37, S59-S70. doi:10.1016/j.neuroimage.2007.03.008.
38. Friedl, P., and Wolf, K. (2008). Tube travel: the role of proteases in individual and collective a cancer cell invasion. Cancer Res. 68, 7247-7249. doi:10.1158/0008-5472.CAN-08-0784.
39. Fritsch, A., Hockel, M., Kiessling, T., Nnetu, K. D., Wetzel, F., Zink, M., et al. (2010). Are biomechanical changes necessary for tumour progression? Nat. Phys. 6, 730-732. doi:10.1038/nphys1800.
40. Fuhrmann, A., Staunton, J. R., Nandakumar, V., Banyai, N., Davies, P. C. W., and Ros, R. (2011). AFM stiffness nanotomography of normal, metaplastic and dysplastic human esophageal cells. Phys. Biol. 8. doi:10.1088/1478-3975/8/1/015007.
41. Galle, J., Aust, G., Schaller, G., Beyer, T., and Drasdo, D. (2006). Individual cell-based models of the spatial-temporal organization of multicellular systems-achievements and limitations. Cytometry A 69A, 704-710. doi:10.1002/cyto.a.20287.
42. Gerlee, P., and Anderson, A. R. A. (2008). A hybrid cellular automaton model of clonal evolution in cancer: the emergence of the glycolytic phenotype. J. Theor. Biol. 250, 705-722. doi:10.1016/j.jtbi.2007.10.038.
43. Gevertz, J. L., Gillies, G. T., and Torquato, S. (2008). Simulating tumor growth in confined heterogeneous environments. Phys. Biol. 5, 036010. doi:10.1088/1478-3975/5/3/036010.
44. Giverso, C., Scianna, M., Preziosi, L., Lo Buono, N., and Funaro, A. (2010). Individual cell-based model for in-vitro mesothelial invasion of ovarian cancer. Math. Model. Nat. Phenom. 5, 203-223. doi:10.1051/mmnp/20105109.
45. Guck, J., Schinkinger, S., Lincoln, B., Wottawah, F., Ebert, S., Romeyke, M., et al. (2005). Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys. J. 88, 3689-3698. doi:10.1529/biophysj.104.045476.
46. Guido, S., and Tranquillo, R. T. (1993). A methodology for the systematic and quantitative study of cell contact guidance in oriented collagen gels-correlation of fibroblast orientation and gel birefringence. J. Cell. Sci. 105, 317-331.
47. Harjanto, D., and Zaman, M. H. (2010). Computational study of proteolysis-driven single cell migration in a three-dimensional matrix. Ann. Biomed. Eng. 38, 1815-1825. doi:10.1007/s10439-010-9970-0.
48. Helmlinger, G., Netti, P. A., Lichtenbeld, H. C., Melder, R. J., and Jain, R. K. (1997). Solid stress inhibits the growth of multicellular tumor spheroids. Nat. Biotechnol. 15, 778-783. doi:10.1038/nbt0897-778.
49. Hogg, N. A. S., Harrison, C. J., and Tickle, C. (1983). Lumen formation in the developing mouse mammary-gland. J. Embryol. Exp. Morphol. 73, 39-57.
50. Huang, S., and Ingber, D. E. (2005). Cell tension, matrix mechanics, and cancer development. Cancer Cell 8, 175-176. doi:10.1016/j.ccr.2005.08.009.
51. Jonas, O., Mierke, C. T., and Kas, J. A. (2011). Invasive cancer cell lines exhibit biomechanical properties that are distinct from their noninvasive counterparts. Soft Matter 7, 11488-11495. doi:10.1039/c1sm05532a.
52. Kam, Y., Rejniak, K. A., and Anderson, A. R. A. (2012). Cellular modeling of cancer invasion: integration of in silico and in vitro approaches. J. Cell. Physiol. 227, 431-438. doi:10.1002/jcp.22766.
53. Katira, P., Zaman, M. H., and Bonnecaze, R. T. (2012). How changes in cell mechanical properties induce cancerous behaviour. Phys. Rev. Lett. 108. doi:10.1103/PhysRevLett.108.028103.
54. Kauppila, S., Stenback, F., Risteli, J., Jukkola, A., and Risteli, L. (1998). Aberrant type I and type III collagen gene expression in human breast cancer in vivo. J. Pathol. 186, 262-268. doi:10.1002/(SICI)1096-9896(1998110)186:3<262::AIDPATH191>3.0.CO;2-3.
55. Kim, Y., and Othmer, H. G. (2013). A hybrid model of tumor-stromal interactions in breast cancer. Bull. Math. Biol. doi:10.1007/s11538-012-9787-0. [Epub ahead of print].
56. Klein, E. A., Yin, L. Q., Kothapalli, D., Castagnino, P., Byfield, F. J., Xu, T. N., et al. (2009). Cell-cycle control by physiological matrix elasticity and in vivo tissue stiffening. Curr. Biol. 19, 1511-1518. doi:10.1016/j.cub.2009.07.069.
57. Kraning-Rush, C. M., Califano, J. P., and Reinhart-King, C. A. (2012). Cellular traction stresses increase with increasing metastatic potential. PLoS ONE 7:e32572. doi:10.1371/journal.pone.0032572.
58. Kumar, S., and Weaver, V. (2009). Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev. 28, 113-127. doi:10.1007/s10555-008-9173-4.
59. Lautenschlager, F., Paschke, S., Schinkinger, S., Bruel, A., Beil, M., and Guck, J. (2009). The regulatory role of cell mechanics for migration of differentiating myeloid cells. Proc. Natl. Acad. Sci. U.S.A. 106, 15696-15701. doi:10.1073/pnas.0811261106.
60. Lekka, M., Laidler, P., Ignacak, J., Labedz, M., Lekki, J., Struszczyk, H., et al. (2001). The effect of chitosan on stiffness and glycolytic activity of human bladder cells. Biochim. Biophys. Acta 1540, 127-136. doi:10.1016/S0167-4889(01)00125-2.
61. Levental, K. R., Yu, H. M., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., et al. (2009). Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906. doi:10.1016/j.cell.2009.10.027.
62. Lopez, J. I., Mouw, J. K., and Weaver, V. M. (2008). Biomechanical regulation of cell orientation and fate. Oncogene 27, 6981-6993. doi:10.1038/onc.2008.348.
63. Macklin, P., and Lowengrub, J. (2007). Nonlinear simulation of the effect of microenvironment on tumor growth. J. Theor. Biol. 245, 677-704. doi:10.1016/j.jtbi.2006.12.004.
64. Macklin, P., and Lowengrub, J. S. (2008). A new ghost cell/level set method for moving boundary problems: application to tumor growth. J. Sci. Comput. 35, 266-299. doi:10.1007/s10915-008-9190-z.
65. Macklin, P., McDougall, S., Anderson, A. R. A., Chaplain, M. A. J., Cristini, V., and Lowengrub, J. (2009). Multiscale modelling and nonlinear simulation of vascular tumour growth. J. Math. Biol. 58, 765-798. doi:10.1007/s00285-008-0216-9.
66. Mammoto, A., and Ingber, D. E. (2009). Cytoskeletal control of growth and cell fate switching. Curr. Opin. Cell Biol. 21, 864-870. doi:10.1016/j.ceb.2009.08.001.
67. Montel, F., Delarue, M., Elgeti, J., Vignjevic, D., Cappello, G., and Prost, J. (2012). Isotropic stress reduces cell proliferation in tumor spheroids. New J. Phys. 14. doi:10.1088/1367-2630/14/5/055008.
68. Moreo, P., Garcia-Aznar, J. M., and Doblare, M. (2008). Modeling mechanosensing and its effect on the migration and proliferation of adherent cells. Acta Biomater. 4, 613-621. doi:10.1016/j.actbio.2007.10.014.
69. Nelson, C. M., and Gleghorn, J. P. (2012). Sculpting organs: mechanical regulation of tissue development. Annu. Rev. Biomed. Eng. 14, 129-154. doi:10.1146/annurev-bioeng-071811-150043.
70. Painter, K. J. (2009). Modelling cell migration strategies in the extracellular matrix. J. Math. Biol. 58, 511-543. doi:10.1007/s00285-008-0217-8.
71. Paredes, J., Albergaria, A., Oliveira, J. T., Jeronimo, C., Milanezi, F., and Schmitt, F. C. (2005). P-cadherin overexpression is an indicator of clinical outcome in invasive breast carcinomas and is associated with CDH3 promoter hypomethylation. Clin. Cancer Res. 11, 5869-5877. doi:10.1158/1078-0432.CCR-05-0059.
72. Park, S., Koch, D., Cardenas, R., Kas, J., and Shih, C. K. (2005). Cell motility and local viscoelasticity of fibroblasts. Biophys. J. 89, 4330-4342. doi:10.1529/biophysj.104.053462.
73. Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254. doi:10.1016/j.ccr.2005.08.010.
74. Peyton, S. R., Ghajar, C. M., Khatiwala, C. B., and Putnam, A. J. (2007). The emergence of ECM mechanics and cytoskeletal tension as important regulators of cell function. Cell Biochem. Biophys. 47, 300-320. doi:10.1007/s12013-007-0004-y.
75. Plodinec, M., Loparic, M., Monnier, C. A., Obermann, E. C., Zanetti-Dallenbach, R., Oertle, P., et al. (2012). The nanomechanical signature of breast cancer. Nat. Nanotechnol. 7, 757-765. doi:10.1038/nnano.2012.167.
76. Ramis-Conde, I., Chaplain, M. A. J., and Anderson, A. R. A. (2008a). Mathematical modelling of cancer cell invasion of tissue. Math. Comput. Model 47, 533-545. doi:10.1016/j.mcm.2007.02.034.
77. Ramis-Conde, I., Drasdo, D., Anderson, A. R. A., and Chaplain, M. A. J. (2008b). Modeling the influence of the E-cadherin-beta-catenin pathway in cancer cell invasion: a multiscale approach. Biophys. J. 95, 155-165. doi:10.1529/biophysj.107.114678.
78. Rejniak, K. A., and McCawley, L. J. (2010). Current trends in mathematical modeling of tumor-microenvironment interactions: a survey of tools and applications. Exp. Biol. Med. 235, 411-423. doi:10.1258/ebm.2009.009230.
79. Rejniak, K. A., Wang, S. Z. E., Bryce, N. S., Chang, H., Parvin, B., Jourquin, J., et al. (2010). Linking changes in epithelial morphogenesis to cancer mutations using computational modeling. PLoS Comput. Biol. 6:e1000900. doi:10.1371/journal.pcbi.1000900.
80. Remmerbach, T. W., Wottawah, F., Dietrich, J., Lincoln, B., Wittekind, C., and Guck, J. (2009). Oral cancer diagnosis by mechanical phenotyping. Cancer Res. 69, 1728-1732. doi:10.1158/0008-5472.CAN-08-4073.
81. Ribeiro, A. S., Albergaria, A., Sousa, B., Correia, A. L., Bracke, M., Seruca, R., et al. (2010a). Extracellular cleavage and shedding of P-cadherin: a mechanism underlying the invasive behaviour of breast cancer cells. Oncogene 29, 392-402. doi:10.1038/onc.2009.338.
82. Ribeiro, A. S., Carreto, L. C., Albergaria, A., Sousa, B., Ricardo, S., Milanezi, F., et al. (2010b). Co-expression of E- and P-cadherin in breast cancer: role as an invasion suppressor or as an invasion promoter? EJC Suppl. 8, 131-132.
83. Rizki, A., Weaver, V. M., Lee, S. Y., Rozenberg, G. I., Chin, K., Myers, C. A., et al. (2008). A human breast cell model of preinvasive to invasive transition. Cancer Res. 68, 1378-1387. doi:10.1158/0008-5472.CAN-07-2225.
84. Rubenstein, B. M., and Kaufman, L. J. (2008). The role of extracellular matrix in glioma invasion: a cellular Potts model approach. Biophys. J. 95, 5661-5680. doi:10.1529/biophysj.108.140624.
85. Sanga, S., Frieboes, H. B., Zheng, X. M., Gatenby, R., Bearer, E. L., and Cristini, V. (2007). Predictive oncology: a review of multidisciplinary, multiscale in silico modeling linking phenotype, morphology and growth. Neuroimage 37, S120-S134. doi:10.1016/j.neuroimage.2007.05.043.
86. Scianna, M., and Preziosi, L. (2013). Modeling the influence of nucleus elasticity on cell invasion in fiber networks and microchannels. J. Theor. Biol. 317, 394-406. doi:10.1016/j.jtbi.2012.11.003.
87. Stein, A. M., Vader, D. A., Weitz, D. A., and Sander, L. M. (2011). The micromechanics of three-dimensional collagen-I gels. Complexity 16, 22-28. doi:10.1002/cplx.20332.
88. Stolarska, M. A., Kim, Y., and Othmer, H. G. (2009). Multi-scale models of cell and tissue dynamics. Philos. Trans. A Math. Phys. Eng. Sci. 367, 3525-3553. doi:10.1098/rsta.2009.0095.
89. Suresh, S. (2007). Biomechanics and biophysics of cancer cells. Acta Mater. 55, 3989-4014. doi:10.1016/j.actamat.2007.04.022.
90. Swaminathan, V., Mythreye, K., O'Brien, E. T., Berchuck, A., Blobe, G. C., and Superfine, R. (2011). Mechanical stiffness grades metastatic potential in patient tumor cells and in cancer cell lines. Cancer Res. 71, 5075-5080. doi:10.1158/0008-5472.CAN-11-0247.
91. Swanton, C., Burrell, R. A., and Futreal, P. A. (2011). Breast cancer genome heterogeneity: a challenge to personalised medicine? Breast Cancer Res. 13, 104-105. doi:10.1186/bcr2807.
92. Torquato, S. (2011). Toward an Ising model of cancer and beyond. Phys. Biol. 8, 015017. doi:10.1088/1478-3975/8/1/015017.
93. Trucu, D., Lin, P., Chaplain, M. A. J., and Wang, Y. (2013). A multiscale moving boundary model arising in cancer invasion. Multiscale Model. Simul. 11, 309-335. doi:10.1137/110839011.
94. Ulrich, T. A., Pardo, E. M. D., and Kumar, S. (2009). The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res. 69, 4167-4174. doi:10.1158/0008-5472.CAN-08-4859.
95. Vader, D., Kabla, A., Weitz, D., and Mahadevan, L. (2009). Strain-induced alignment in collagen gels. PLoS ONE 4:e5902. doi:10.1371/journal.pone.0005902.
96. Van Marck, V., Stove, C., Van Den Bossche, K., Stove, V., Paredes, J., Haeghen, Y. V., et al. (2005). P-cadherin promotes cell-cell adhesion and counteracts invasion in human melanoma. Cancer Res. 65, 8774-8783. doi:10.1158/0008-5472.CAN-04-4414.
97. Vijayagopal, P., Figueroa, J. E., and Levine, E. A. (1998). Altered composition and increased endothelial cell proliferative activity of proteoglycans isolated from breast carcinoma. J. Surg. Oncol. 68, 250-254. doi:10.1002/(SICI)1096-9098(199808)68:4<250::AIDJSO9>3.3.CO;2-9.
98. Visvader, J. E. (2011). Cells of origin in cancer. Nature 469, 314-322. doi:10.1038/nature09781.
99. West-Foyle, H., and Robinson, D. N. (2012). Cytokinesis mechanics and mechanosensing. Cytoskeleton (Hoboken) 69, 700-709. doi:10.1002/cm.21045.
100. Wolf, K., Wu, Y. I., Liu, Y., Geiger, J., Tam, E., Overall, C., et al. (2007). Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat. Cell Biol. 9, 893-U839. doi:10.1038/ncb1616.
101. Yang, C. M., Chien, C. S., Yao, C. C., Hsiao, L. D., Huang, Y. C., and Wu, C. B. (2004). Mechanical strain induces collagenase-3 (MMP-13) expression in MC3T3-E1 osteoblastic cells. J. Biol. Chem. 279, 22158-22165. doi:10.1074/jbc.M401343200.
102. Zaman, M. H. (2006). Multiscale modeling of tumor cell migration. Phys. Biol. 851, 117-122.
103. Zaman, M. H., Matsudaira, P., and Lauffenburger, D. A. (2007). Understanding effects of matrix protease and matrix organization on directional persistence and translational speed in three-dimensional cell migration. Ann. Biomed. Eng. 35, 91-100. doi:10.1007/s10439-006-9205-6.
104. Zaman, M. H., Trapani, L. M., Siemeski, A., MacKellar, D., Gong, H., Kamm, R. D., et al. (2006). Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc. Natl. Acad. Sci. U.S.A. 103, 13897-13897. doi:10.1073/pnas.0604460103.
105. Zhang, Y. H., Nojima, S., Nakayama, H., Jin, Y. L., and Enza, H. (2003). Characteristics of normal stromal components and their correlation with cancer occurrence in human prostate. Oncol. Rep. 10, 207-211.