Mapping local matrix remodeling induced by a migrating tumor cell using three-dimensional multiple-particle tracking

Biophysical Journal

Volumn 95, Issue 8, 2008, Pages 4077-4088

  Bloom, Ryan J ^a   George, Jerry P ^a   Celedon, Alfredo ^a   Sun, Sean X ^a   Wirtz, Denis ^a  

^a Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; MYOSIN II; PROTEINASE INHIBITOR; RAC1 PROTEIN; RHO KINASE;

ANIMAL; ARTICLE; CELL MOTION; CELL SURFACE; DRUG EFFECT; ENZYMOLOGY; EXTRACELLULAR MATRIX; HUMAN; METABOLISM; METHODOLOGY; NEOPLASM; PATHOLOGY; RAT; THREE DIMENSIONAL IMAGING; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURFACE EXTENSIONS; COLLAGEN; EXTRACELLULAR MATRIX; HUMANS; IMAGING, THREE-DIMENSIONAL; MYOSIN TYPE II; NEOPLASMS; PROTEASE INHIBITORS; RAC1 GTP-BINDING PROTEIN; RATS; RHO-ASSOCIATED KINASES;

EID: 56049099030     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.132738     Document Type: Article

References (56)

1. Dembo, M., and Y. L. Wang. 1999. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys. J. 76:2307-2316.
2. Munevar, M., Y. L. Wang, and M. Dembo. 2001. Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts. Biophys. J. 80:1744-1757.
3. Beningo, K. A., M. Dembo, I. Kaverina, J. V. Small, and Y. L. Wang. 2001. Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J. Cell Biol. 153:881-888.
4. Wang, H. B., M. Dembo, S. K. Hanks, and Y. Wang. 2001. Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc. Natl. Acad. Sci. USA. 98:11295-11300.
5. Harris, A. K. 1986. Cell traction in relationship to morphogenesis and malignancy. Dev. Biol. 3:339-357.
6. Bellows, C. G., A. H. Melcher, and J. E. Aubin. 1981. Contraction and organization of collagen gels by cells cultured from periodontal ligament, gingiva and bone suggest functional differences between cell types. J. Cell Sci. 50:299-314.
7. Grinnell, F., and C. R. Lamke. 1984. Reorganization of hydrated collagen lattices by human skin fibroblasts. J. Cell Sci. 66:51-63.
8. Elsdale, T., and J. Bard. 1972. Collagen substrata for studies on cell behavior. J. Cell Biol. 54:626-637.
9. Roy, P., W. M. Petroll, H. D. Cavanagh, C. J. Chuong, and J. V. Jester. 1997. An in vitro force measurement assay to study the early mechanical interaction between corneal fibroblasts and collagen matrix. Exp. Cell Res. 232:106-117.
10. Roy, P., W. M. Petroll, H. D. Cavanagh, and J. V. Jester. 1999. Exertion of tractional force requires the coordinated up-regulation of cell contractility and adhesion. Cell Motil. Cytoskeleton. 43:23-34.
11. Tamariz, E., and F. Grinnell. 2002. Modulation of fibroblast morphology and adhesion during collagen matrix remodeling. Mol. Biol. Cell. 13:3915-3929.
12. Harley, B. A., T. M. Freyman, M. Q. Wong, and L. J. Gibson. 2007. A new technique for calculating individual dermal fibroblast contractile forces generated within collagen-GAG scaffolds. Biophys. J. 93:2911-2922.
13. Petroll, W. M., L. Ma, and J. V. Jester. 2003. Direct correlation of collagen matrix deformation with focal adhesion dynamics in living corneal fibroblasts. J. Cell Sci. 116:1481-1491.
14. Vanni, S. B., C. Lagerholm, O. Otey, D. L. Taylor, and F. Lanni. 2003. Internet-based image analysis quantifies contractile behavior of individual fbroblasts inside model tissue. Biophys. J. 84:2715-2727.
15. Krahn, K. N., C. V. C. Bouten, S. van Tuij, A. M. J. van Zandvoort, and M. Merkx. 2006. Fluorescently labeled collagen binding proteins allow specific visualization of collagen in tissues and live cell culture. Anal. Biochem. 350:177-185.
16. Toprak, E., H. Balci, B. H. Blehm, and P. R. Selvin. 2007. Three-dimensional particle tracking via bifocal imaging. Nano Lett. 7:2043-2045.
17. Speidel, M., A. Jonáš, and E. L. Florin. 2003. Three-dimensional tracking of fluorescent nanoparticles with subnanometer precision by use of offfocus imaging. Opt. Lett. 69:69-71.
18. Levi, V., Q. Ruan, and E. Gratton. 2005. 3-D particle tracking in a two-photon microscope: Application to the study of molecular dynamics in cells. Biophys. J. 88:2919-2928.
19. Gosse, C., and V. Croquette. 2002. Magnetic tweezers: micromanipulation and force measurement at the molecular level. Biophys. J. 82:3314-3329.
20. Wolf, K., I. Mazo, H. Leung, K. Engelke, U. H. von Andrian, E. I. Deryugina, A. Y. Strongin, E. B. Brocker, and P. Friedl. 2003. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160:267-277.
21. Chang, M. I., P. Panorchan, T. M. Dobrowsky, Y. Tseng, and D. Wirtz. 2005. Single-molecule analysis of human immunodeficiency virus type 1 gp120-receptor interactions in living cells. J. Virol. 79:14748-14755.
22. Grinnell, F. 2000. Fibroblast-collagen-matrix contraction: growth-factor signalling and mechanical loading. Trends Cell Biol. 10:362-365.
23. Ridley, A. J. 2001. Rho GTPases and cell migration. J. Cell Sci. 114:2713-2722.
24. Delanoe-Ayari, H., R. Al Kurdi, M. Vallade, D. Gulino-Debrac, and D. Riveline. 2004. Membrane and acto-myosin tension promote clustering of adhesion proteins. Proc. Natl. Acad. Sci. USA. 101:2229-2234.
25. Pankov, R., Y. Endo, S. Even-Ram, M. Araki, K. Clark, E. Cukierman, K. Matsumoto, and K. M. Yamada. 2005. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170:793-802.
26. Sahai, E., and C. J. Marshall. 2003. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 5:711-719.
27. Ramamurthy, B., C. M. Yengo, A. F. Straight, T. J. Mitchison, and H. L. Sweeney. 2004. Kinetic mechanism of blebbistatin inhibition of nonmuscle myosin IIB. Biochemistry. 43:14832-14839.
28. Shu, S., X. Liu, and E. D. Korn. 2005. Blebbistatin and blebbistatin-inactivated myosin II inhibit myosin II-independent processes in Dictyostelium. Proc. Natl. Acad. Sci. USA. 102:1472-1477.
29. Uehata, M., T. Ishizaki, H. Satoh, T. Ono, T. Kawahara, T. Morishita, H. Tamakawa, K. Yamagami, J. Inui, M. Maekawa, and S. Narumiya. 1999. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature. 389:990-994.
30. Kole, T. P., Y. Tseng, L. Huang, J. L. Katz, and D. Wirtz. 2004. Rho kinase regulates the intracellular micromechanical response of adherent cells to rho activation. Mol. Biol. Cell. 15:3475-3484.
31. Carragher, N. O., S. M. Walker, L. A. Scott Carragher, F. Harris, T. K. Sawyer, V. G. Brunton, B. W. Ozanne, and M. C. Frame. 2006. Calpain 2 and Src dependence distinguishes mesenchymal and amoeboid modes of tumour cell invasion: a link to integrin function. Oncogene. 25:5726-5740.
32. Gao, Y., J. B. Dickerson, F. Guo, J. Zheng, and Y. Zheng. 2004. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc. Natl. Acad. Sci. USA. 101:7618-7623.
33. Tseng, Y., K. M. An, and D. Wirtz. 2002. Microheterogeneity controls the rate of gelation of actin filament networks. J. Biol. Chem. 277:18143-18150.
34. Tseng, Y., K. M. An, O. Esue, and D. Wirtz. 2004. The bimodal role of filamin in controlling the architecture and mechanics of F-actin networks. J. Biol. Chem. 279:1819-1826.
35. Tseng, Y., E. Fedorov, J. M. McCaffery, S. C. Almo, and D. Wirtz. 2001. Micromechanics and microstructure of actin filament networks in the presence of the actin-bundling protein human fascin: a comparison with a-actinin. J. Mol. Biol. 310:351-366.
36. Sabeh, F., I. Ota, K. Holmbeck, H. Birkedal-Hansen, P. Soloway, M. Balbin, C. Lopez-Otin, S. Shapiro, M. Inada, S. Krane, E. Allen, D. Chung, and S. J. Weiss. 2004. Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J. Cell Biol. 167:769-781.
37. Chun, T. H., K. B. Hotary, F. Sabeh, A. R. Saltiel, E. D. Allen, and S. J. Weiss. 2006. A pericellular collagenase directs the 3-dimensional development of white adipose tissue. Cell. 125:577-591.
38. Zaman, M. H., L. M. Trapani, A. L. Sieminski, D. Mac, H. Kellar, K. R. D. Gong, A. Wells, D. A. Lauffenburger, and P. Matsudaira. 2006. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc. Natl. Acad. Sci. USA. 103:10889-10894.
39. Hotary, K., X. Y. Li, E. Allen, S. L. Stevens, and S. J. Weiss. 2006. A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev. 20:2673-2686.
40. Demou, Z. N., M. Awad, T. McKee, J. Y. Perentes, X. Wang, L. L. Munn, R. K. Jain, and Y. Boucher. 2005. Lack of telopeptides in fibrillar collagen I promotes the invasion of a metastatic breast tumor cell line. Cancer Res. 65:5674-5682.
41. Woodley, D. T., M. Yamauchi, K. C. Wynn, G. Mechanic, and R. A. Briggaman. 1991. Collagen telopeptides (cross-linking sites) play a role in collagen gel lattice contraction. J. Invest. Dermatol. 97:580-585.
42. Lo, C. M., H. B. Wang, M. Dembo, and Y. L. Wang. 2000. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79:144-152.
43. Walpita, D., and E. Hay. 2002. Studying actin-dependent processes in tissue culture. Nat. Rev. Mol. Cell Biol. 3:137-141.
44. Hotary, K. B., E. D. Allen, P. C. Brooks, N. S. Datta, M. W. Long, and S. J. Weiss. 2003. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell. 11:33-45.
45. Cukierman, E., R. Pankov, and K. M. Yamada. 2002. Cell interactions with three-dimensional matrices. Curr. Opin. Cell Biol. 14:633-639.
46. Panorchan, P., J. S. Lee, T. P. Kole, Y. Tseng, and D. Wirtz. 2006. Microrheology and ROCK signaling of human endothelial cells embedded in a 3D matrix. Biophys. J. 91:3499-3507.
47. Prass, M., K. Jacobson, A. Mogilner, and M. Radmacher. 2006. Direct measurement of the lamellipodial protrusive force in a migrating cell. J. Cell Biol. 174:767-772.
48. Miron-Mendoza, M., J. Seemann, and F. Grinnell. 2008. Collagen fibril flow and tissue translocation coupled to fibroblast migration in 3D collagen matrices. Mol. Biol. Cell. 19:2051-2058.
49. Wolf, K., Y. I. Wu, Y. Liu, J. Geiger, E. Tam, C. Overall, M. S. Stack, and P. Friedl. 2007. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat. Cell Biol. 9:893-904.
50. Barocas, V. H., A. G. Moon, and R. T. Tranquillo. 1995. The fibroblast-populated collagen microsphere assay of cell traction force. Part 2: Measurement of the cell traction parameter. J. Biomech. Eng. 117:161-170.
51. Parekh, A., and D. Velegol. 2007. Collagen gel anisotropy measured by 2-D laser trap microrheometry. Ann. Biomed. Eng. 35:1231-1246.
52. Tseng, Y., T. P. Kole, and D. Wirtz. 2002. Micromechanical mapping of live cells by multiple-particle-tracking microrheology. Biophys. J. 83:3162-3176.
53. Kole, T. P., Y. Tseng, I. Jiang, J. L. Katz, and D. Wirtz. 2005. Intracellular mechanics of migrating fibroblasts. Mol. Biol. Cell. 16:328-338.
54. Tseng, Y., J. S. Lee, T. P. Kole, I. Jiang, and D. Wirtz. 2004. Microorganization and visco-elasticity of the interphase nucleus revealed by particle nanotracking. J. Cell Sci. 117:2159-2167.
55. Dobrowsky, T. M., Y. Zhou, S. X. Sun, R. F. Siliciano, and D. Wirtz. 2008. Monitoring early fusion dynamics of human immunodeficiency virus type 1 at single-molecule resolution. J Virol. 82:7022-7033.
56. Suh, J., D. Wirtz, and J. Hanes. 2003. Efficient active transport of gene nanocarriers to the cell nucleus. Proc. Natl. Acad. Sci. USA. 100:3878-3882.