3D Traction Stresses Activate Protease-Dependent Invasion of Cancer Cells

Biophysical Journal

Volumn 107, Issue 11, 2014, Pages 2528-2537

  Aung, Aereas ^a   Seo, Young N ^a   Lu, Shaoying ^a   Wang, Yingxiao ^a   Jamora, Colin ^a,d   del Álamo, Juan C ^b,c   Varghese, Shyni ^a,c,d  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d IFOM inStem Joint Research Laboratory   (India)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; DRUG COMBINATION; LAMININ; MATRIGEL; PEPTIDE HYDROLASE; PROTEOGLYCAN;

BIOMECHANICS; DRUG COMBINATION; DRUG EFFECTS; ENZYME ACTIVATION; HUMAN; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGICAL STRESS; SINGLE CELL ANALYSIS; TUMOR CELL LINE; TUMOR INVASION;

BIOMECHANICAL PHENOMENA; CELL LINE, TUMOR; COLLAGEN; DRUG COMBINATIONS; ENZYME ACTIVATION; HUMANS; LAMININ; NEOPLASM INVASIVENESS; NEOPLASMS; PEPTIDE HYDROLASES; PROTEOGLYCANS; SINGLE-CELL ANALYSIS; STRESS, PHYSIOLOGICAL;

EID: 84914127661     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.07.078     Document Type: Article

References (48)

1. Chaffer, C.L., Weinberg, R.A., A perspective on cancer cell metastasis. Science 331 (2011), 1559–1564.
2. Sabeh, F., Shimizu-Hirota, R., Weiss, S.J., Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J. Cell Biol. 185 (2009), 11–19.
3. Zaman, M.H., Trapani, L.M., et al., Matsudaira, P., Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc. Natl. Acad. Sci. USA 103 (2006), 10889–10894.
4. Wolf, K., Friedl, P., Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. Trends Cell Biol. 21 (2011), 736–744.
5. Wolf, K., Mazo, I., et al., Friedl, P., Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160 (2003), 267–277.
6. Poincloux, R., Collin, O., et al., Chavrier, P., Contractility of the cell rear drives invasion of breast tumor cells in 3D Matrigel. Proc. Natl. Acad. Sci. USA 108 (2011), 1943–1948.
7. Wolf, K., Te Lindert, M., et al., Friedl, P., Physical limits of cell migration: control by ECM space and nuclear deformation and tuning by proteolysis and traction force. J. Cell Biol. 201 (2013), 1069–1084.
8. Kirmse, R., Otto, H., Ludwig, T., Interdependency of cell adhesion, force generation and extracellular proteolysis in matrix remodeling. J. Cell Sci. 124 (2011), 1857–1866.
9. Wirtz, D., Konstantopoulos, K., Searson, P.C., The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nat. Rev. Cancer 11 (2011), 512–522.
10. Pathak, A., Kumar, S., Independent regulation of tumor cell migration by matrix stiffness and confinement. Proc. Natl. Acad. Sci. USA 109 (2012), 10334–10339.
11. Friedl, P., Alexander, S., Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 147 (2011), 992–1009.
12. Jerrell, R.J., Parekh, A., Cellular traction stresses mediate extracellular matrix degradation by invadopodia. Acta Biomater. 10 (2014), 1886–1896.
13. Alexander, N.R., Branch, K.M., et al., Weaver, A.M., Extracellular matrix rigidity promotes invadopodia activity. Curr. Biol. 18 (2008), 1295–1299.
14. Butcher, D.T., Alliston, T., Weaver, V.M., A tense situation: forcing tumour progression. Nat. Rev. Cancer 9 (2009), 108–122.
15. Levental, K.R., Yu, H., et al., Weaver, V.M., Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139 (2009), 891–906.
16. Tse, J.M., Cheng, G., et al., Munn, L.L., Mechanical compression drives cancer cells toward invasive phenotype. Proc. Natl. Acad. Sci. USA 109 (2012), 911–916.
17. Mierke, C.T., Bretz, N., Altevogt, P., Contractile forces contribute to increased glycosylphosphatidylinositol-anchored receptor CD24-facilitated cancer cell invasion. J. Biol. Chem. 286 (2011), 34858–34871.
18. Guck, J., Schinkinger, S., et al., Bilby, C., Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys. J. 88 (2005), 3689–3698.
19. Hur, S.S., Zhao, Y., et al., Chien, S., Live cells exert 3-dimensional traction forces on their substrata. Cell. Mol. Bioeng. 2 (2009), 425–436.
20. Gospodarowicz, D., Gonzalez, R., Fujii, D.K., Are factors originating from serum, plasma, or cultured cells involved in the growth-promoting effect of the extracellular matrix produced by cultured bovine corneal endothelial cells?. J. Cell. Physiol. 114 (1983), 191–202.
21. Ouyang, M., Sun, J., et al., Wang, Y., Determination of hierarchical relationship of Src and Rac at subcellular locations with FRET biosensors. Proc. Natl. Acad. Sci. USA 105 (2008), 14353–14358.
22. Lu, S., Ouyang, M., et al., Wang, Y., The spatiotemporal pattern of Src activation at lipid rafts revealed by diffusion-corrected FRET imaging. PLOS Comput. Biol., 4, 2008, e1000127.
23. Lu, S., Kim, T.J., et al., Wang, Y., Computational analysis of the spatiotemporal coordination of polarized PI3K and Rac1 activities in micro-patterned live cells. PLoS ONE, 6, 2011, e21293.
24. Ilina, O., Bakker, G.J., et al., Friedl, P., Two-photon laser-generated microtracks in 3D collagen lattices: principles of MMP-dependent and -independent collective cancer cell invasion. Phys. Biol., 8, 2011, 015010.
25. Friedl, P., Wolf, K., Plasticity of cell migration: a multiscale tuning model. J. Cell Biol. 188 (2010), 11–19.
26. del Álamo, J.C., Meili, R., et al., Lasheras, J.C., Three-dimensional quantification of cellular traction forces and mechanosensing of thin substrata by Fourier traction force microscopy. PLoS ONE, 8, 2013, e69850.
27. del Álamo, J.C., Meili, R., et al., Lasheras, J.C., Spatio-temporal analysis of eukaryotic cell motility by improved force cytometry. Proc. Natl. Acad. Sci. USA 104 (2007), 13343–13348.
28. Butler, J.P., Tolić-Nørrelykke, I.M., et al., Fredberg, J.J., Traction fields, moments, and strain energy that cells exert on their surroundings. Am. J. Physiol. Cell Physiol. 282 (2002), C595–C605.
29. Legant, W.R., Miller, J.S., et al., Chen, C.S., Measurement of mechanical tractions exerted by cells in three-dimensional matrices. Nat. Methods 7 (2010), 969–971.
30. Koch, T.M., Münster, S., et al., Fabry, B., 3D Traction forces in cancer cell invasion. PLoS ONE, 7, 2012, e33476.
31. Khetan, S., Guvendiren, M., et al., Burdick, J.A., Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels. Nat. Mater. 12 (2013), 458–465.
32. Bloom, R.J., George, J.P., et al., Wirtz, D., Mapping local matrix remodeling induced by a migrating tumor cell using three-dimensional multiple-particle tracking. Biophys. J. 95 (2008), 4077–4088.
33. Khatau, S.B., Bloom, R.J., et al., Wirtz, D., The distinct roles of the nucleus and nucleus-cytoskeleton connections in three-dimensional cell migration. Sci. Rep., 2, 2012, 488.
34. Reed, J., Walczak, W.J., et al., Gimzewski, J.K., In situ mechanical interferometry of matrigel films. Langmuir 25 (2009), 36–39.
35. Poincloux, R., Lizárraga, F., Chavrier, P., Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J. Cell Sci. 122 (2009), 3015–3024.
36. Schoumacher, M., Goldman, R.D., et al., Vignjevic, D.M., Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J. Cell Biol. 189 (2010), 541–556.
37. Buccione, R., Orth, J.D., McNiven, M.A., Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat. Rev. Mol. Cell Biol. 5 (2004), 647–657.
38. Yu, X., Machesky, L.M., Cells assemble invadopodia-like structures and invade into matrigel in a matrix metalloprotease dependent manner in the circular invasion assay. PLoS ONE, 7, 2012, e30605.
39. Artym, V.V., Zhang, Y., et al., Mueller, S.C., Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res. 66 (2006), 3034–3043.
40. Bergert, M., Chandradoss, S.D., et al., Paluch, E., Cell mechanics control rapid transitions between blebs and lamellipodia during migration. Proc. Natl. Acad. Sci. USA 109 (2012), 14434–14439.
41. Giri, A., Bajpai, S., et al., Wirtz, D., The Arp2/3 complex mediates multigeneration dendritic protrusions for efficient 3-dimensional cancer cell migration. FASEB J. 27 (2013), 4089–4099.
42. Lu, S., Wang, Y., et al., Wang, Y., Quantitative FRET imaging to visualize the invasiveness of live breast cancer cells. PLoS ONE, 8, 2013, e58569.
43. Trappmann, B., Gautrot, J.E., et al., Huck, W.T., Extracellular-matrix tethering regulates stem-cell fate. Nat. Mater. 11 (2012), 642–649.
44. Ayala, R., Zhang, C., et al., Varghese, S., Engineering the cell-material interface for controlling stem cell adhesion, migration, and differentiation. Biomaterials 32 (2011), 3700–3711.
45. Adhikari, A.S., Chai, J., Dunn, A.R., Mechanical load induces a 100-fold increase in the rate of collagen proteolysis by MMP-1. J. Am. Chem. Soc. 133 (2011), 1686–1689.
46. Dimitriadis, E.K., Horkay, F., et al., Chadwick, R.S., Determination of elastic moduli of thin layers of soft material using the atomic force microscope. Biophys. J. 82 (2002), 2798–2810.
47. Reference deleted in proof.
48. Troeberg, L., Nagase, H., Measurement of matrix metalloproteinase activities in the medium of cultured synoviocytes using zymography. Methods Mol. Biol. 225 (2003), 77–87.