Effects of migrating cell-induced matrix reorganization on 3D cancer cell migration

Cellular and Molecular Bioengineering

Volumn 7, Issue 2, 2014, Pages 205-217

  Sun, Wei ^a   Kurniawan, Nicholas Agung ^a,e   Kumar, Alan Prem ^b   Rajagopalan, Raj ^a,c,f   Lim, Chwee Teck ^a,c,d  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e FOM INSTITUTE AMOLF   (Netherlands)

^f SKOLKOVO INSTITUTE OF SCIENCE AND TECHNOLOGY   (Russian Federation)

Author keywords

3D extracellular matrix; Cancer invasion; Cell contraction; Collective cell migration; Matrix remodeling

Indexed keywords

COLLAGEN;

ARTICLE; BREAST CANCER CELL LINE; CANCER CELL; CELL DENSITY; CELL MIGRATION; CELL MOTILITY; CELL MOTION; CELL POPULATION; CELL SPEED; CELLULAR PARAMETERS; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYDROGEL; MDA MB 231 CELL LINE; PRIORITY JOURNAL; THREE DIMENSIONAL IMAGING; TIME LAPSE IMAGING; TUMOR INVASION;

EID: 84903768997     PISSN: 18655025     EISSN: 18655033     Source Type: Journal    
DOI: 10.1007/s12195-014-0324-0     Document Type: Article

References (53)

1. Bloom, R. J., J. P. George, A. Celedon, S. X. Sun, and D. Wirtz. Mapping local matrix remodeling induced by a migrating tumor cell using three-dimensional multiple-particle tracking. Biophys. J. 95:4077-4088, 2008.
2. Borau, C., R. D. Kamm, and J. M. Garcia-Aznar. Mechano-sensing and cell migration: a 3D model approach. Phys. Biol. 8:066008, 2011.
3. Brightman, A. O., B. P. Rajwa, J. E. Sturgis, M. E. McCallister, J. P. Robinson, and S. L. Voytik-Harbin. Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro. Biopolymers 54:222-234, 2000. (Pubitemid 30482322)
4. Broedersz, C. P., K. E. Kasza, L. M. Jawerth, S. Munster, D. A. Weitz, and F. C. MacKintosh. Measurement of nonlinear rheology of cross-linked biopolymer gels. Soft Matter 6:4120-4127, 2010.
5. Broedersz, C. P., M. Sheinman, and F. C. MacKintosh. Filament-length- controlled elasticity in 3D fiber networks. Phys. Rev. Lett. 108:078102, 2012.
6. Castello-Cros, R., D. R. Khan, J. Simons, M. Valianou, and E. Cukierman. Staged stromal extracellular 3D matrices differentially regulate breast cancer cell responses through PI3K and beta1-integrins. BMC Cancer 9:94, 2009.
7. Condeelis, J., and J. E. Segall. Intravital imaging of cell movement in tumours. Nat. Rev. Cancer 3:921-930, 2003. (Pubitemid 37500177)
8. Decaestecker, C., O. Debeir, P. Van Ham, and R. Kiss. Can anti-migratory drugs be screened in vitro? A review of 2D and 3D assays for the quantitative analysis of cell migration. Med. Res. Rev. 27:149-176, 2007. (Pubitemid 46281145)
9. Dickinson, R. B., S. Guido, and R. T. Tranquillo. Biased cell migration of fibroblasts exhibiting contact guidance in oriented collagen gels. Ann. Biomed. Eng. 22:342-356, 1994. (Pubitemid 24264082)
10. Entschladen, F., T. L. Drell, K. Lang, K. Masur, D. Palm, P. Bastian, B. Niggemann, and K. S. Zaenker. Analysis methods of human cell migration. Exp. Cell Res. 307:418-426, 2005. (Pubitemid 40799366)
11. Even-Ram, S., and K. M. Yamada. Cell migration in 3D matrix. Curr. Opin. Cell Biol. 17:524-532, 2005. (Pubitemid 41267167)
12. Friedl, P. Dynamic imaging of cellular interactions with extracellular matrix. Histochem. Cell Biol. 122:183-190, 2004. (Pubitemid 39371487)
13. Friedl, P., and K. Wolf. Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Res. 68:7247-7249, 2008.
14. Fukata, Y., M. Amano, and K. Kaibuchi. Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells. Trends Pharmacol. Sci. 22:32-39, 2001. (Pubitemid 32126284)
15. Gaggioli, C., 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. 9:1392-1400, 2007. (Pubitemid 350201752)
16. Goetz, J. G., S. Minguet, I. Navarro-Lérida, J. J. Lazcano, R. Samaniego, E. Calvo, M. Tello, T. Osteso-Ibáñez, T. Pellinen, A. Echarri, A. Cerezo, A. J. P. Klein-Szanto, R. Garcia, P. J. Keely, P. Sánchez-Mateos, E. Cukierman, and M. A. Del Pozo. Biomechanical remodeling of the microenvironment by stromal Caveolin-1 favors tumor invasion and metastasis. Cell 146:148-163, 2011.
17. Grinnell, F., L. B. Rocha, C. Iucu, S. Rhee, and H. Jiang. Nested collagen matrices: a new model to study migration of human fibroblast populations in three dimensions. Exp. Cell Res. 312:86-94, 2006. (Pubitemid 41668594)
18. Han, J., H. Chang, O. Giricz, G. Y. Lee, F. L. Baehner, J. W. Gray, M. J. Bissell, P. A. Kenny, and B. Parvin. Molecular predictors of 3D morphogenesis by breast cancer cell lines in 3D culture. PLoS Comput. Biol. 6:e1000684, 2010.
19. Hanahan, D., and R. A. Weinberg. The hallmarks of cancer. Cell 100:57-70, 2000. (Pubitemid 30046295)
20. Harjanto, D., and M. H. Zaman. Modeling extracellular matrix reorganization in 3D environments. PLoS ONE 8:e52509, 2013.
21. Jones, P. A., and Y. A. De Clerck. Extracellular matrix destruction by invasive tumor cells. Cancer Metastasis Rev. 1:289-317, 1982.
22. Junkin, M., and P. K. Wong. Probing cell migration in confined environments by plasma lithography. Biomaterials 32:1848-1855, 2011.
23. Kenny, P. A., G. Y. Lee, C. A. Myers, R. M. Neve, J. R. Semeiks, P. T. Spellman, K. Lorenz, E. H. Lee, M. H. Barcellos-Hoff, O. W. Petersen, J. W. Gray, and M. J. Bissell. The morphologies of breast cancer cell lines in three-dimensional assays correlate with their profiles of gene expression. Mol. Oncol. 1:84-96, 2007. (Pubitemid 46776616)
24. Kim, A., N. Lakshman, and W. M. Petroll. Quantitative assessment of local collagenmatrix remodeling in 3-D culture: the role of Rho kinase. Exp. Cell Res. 312:3683-3692, 2006. (Pubitemid 44470785)
25. Koch, T. M., S. Münster, N. Bonakdar, J. P. Butler, and B. Fabry. 3D traction forces in cancer cell invasion. PLoS ONE 7:e33476, 2012.
26. Kolodney, M. S., and E. L. Elson. Correlation of myosin light chain phosphorylation with isometric contraction of fibroblasts. J. Biol. Chem. 268:23850-23855, 1993. (Pubitemid 23335357)
27. Kurniawan, N. A., S. Enemark, and R. Rajagopalan. The role of structure in the nonlinear mechanics of cross-linked semiflexible polymer networks. J. Chem. Phys. 136:065101, 2012.
28. Kurniawan, N. A., L. H. Wong, and R. Rajagopalan. Early stiffening and softening of collagen: interplay of deformation mechanisms in biopolymer networks. Biomacromolecules 13:691-698, 2012.
29. 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. (Pubitemid 30436733)
30. Menezes, G. C., M. Miron-Mendoza, C. H. Ho, H. Jiang, and F. Grinnell. Oncogenic Ras-transformed human fibroblasts exhibit differential changes in contraction and migration in 3D collagen matrices. Exp. Cell Res. 314:3081-3091, 2008.
31. Menon, S., and K. A. Beningo. Cancer cell invasion is enhanced by applied mechanical stimulation. PLoS ONE 6:e17277, 2011.
32. Miller, E. D., K. Li, T. Kanade, L. E. Weiss, L. M. Walker, and P. G. Campbell. Spatially directed guidance of stem cell population migration by immobilized patterns of growth factors. Biomaterials 32:2775-2785, 2011.
33. Miron-Mendoza, M., J. Seemann, and F. Grinnell. Collagen fibril flow and tissue translocation coupled to fibroblast migration in 3D collagen matrices. Mol. Biol. Cell 19:2051-2058, 2008.
34. Nelson, C. M., and M. J. Bissell. Modeling dynamic reciprocity: engineering three-dimensional culture models of breast architecture, function, and neoplastic transformation. Semin. Cancer Biol. 15:342-352, 2005. (Pubitemid 41140304)
35. Packard, B. Z., V. V. Artym, A. Komoriya, and K. M. Yamada. Direct visualization of protease activity on cells migrating in three-dimensions. Matrix Biol. 28:3-10, 2009.
36. Petroll, W. M., and L. Ma. Direct, dynamic assessment of cell-matrix interactions inside fibrillar collagen lattices. Cell Motil. Cytoskeleton 55:254-264, 2003. (Pubitemid 36897530)
37. Petroll, W. M., L. Ma, and J. V. Jester. Direct correlation of collagen matrix deformation with focal adhesion dynamics in living corneal fibroblasts. J. Cell Sci. 116:1481-1491, 2003. (Pubitemid 36527495)
38. Provenzano, P. P., D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely. Collagen density promotes mammary tumor initiation and progression. BMC Med. 6:11, 2008.
39. Provenzano, P. P., 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. 95:5374-5384, 2008.
40. Riento, K., and A. J. Ridley. Rocks: multifunctional kinases in cell behaviour. Nat. Rev. Mol. Cell Biol. 4:446-456, 2003. (Pubitemid 36648590)
41. Sahai, E., and C. J. Marshall. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 5:711-719, 2003. (Pubitemid 36986778)
42. Scanlon, E. F., and S. Murthy. The process of metastasis. CA Cancer J. Clin. 41:301-305, 1991.
43. Schedin, P., and P. J. Keely. Mammary gland ECM remodeling, stiffness, and mechanosignaling in normal development and tumor progression. Cold Spring Harb. Perspect. Biol. 3:a003228, 2011.
44. Shieh, A. C., H. A. Rozansky, B. Hinz, and M. A. Swartz. Tumor cell invasion is promoted by interstitial flow-induced matrix priming by stromal fibroblasts. Cancer Res. 71:790-800, 2011.
45. Sporn, M. B. The war on cancer. Lancet 347:1377-1381, 1996. (Pubitemid 26147937)
46. Vishwanath, M., L. Ma, C. A. Otey, J. V. Jester, and W. M. Petroll. Modulation of corneal fibroblast contractility within fibrillar collagen matrices. Invest. Ophthalmol. Vis. Sci. 44:4724-4735, 2003. (Pubitemid 37315284)
47. Wirtz, D., K. Konstantopoulos, and P. C. Searson. The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nat. Rev. Cancer 11:512-522, 2011.
48. Wolf, K., I. Mazo, H. Leung, K. Engelke, U. H. von Andrian, E. I. Deryugina, A. Y. Strongin, E. B. Brocker, and P. Friedl. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160:267-277, 2003. (Pubitemid 36254960)
49. Wolf, K., 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. 9:893-904, 2007. (Pubitemid 47190444)
50. Wolf, K., S. Alexander, V. Schacht, L. M. Coussens, U. H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl. Collagen-based cell migration models in vitro and in vivo. Semin. Cell Dev. Biol. 20:931-941, 2009.
51. Wong, L. H., N. A. Kurniawan, H.-P. Too, and R. Rajagopalan. Spatially resolved microrheology of heterogeneous biopolymer hydrogels using covalently bound microspheres. Biomech. Model. Mechanobiol. 2013. doi:10.1007/s10237-013- 0538-4.
52. Yu, X., and L. M. Machesky. Cells assemble invadopodia-like structures and invade into matrigel in a matrix metalloprotease dependent manner in the circular invasion assay. PLoS ONE 7:e30605, 2012.
53. Zaman, M. H. The role of engineering approaches in analysing cancer invasion and metastasis. Nat. Rev. Cancer 13:596-603, 2013.