Physical limits of cell migration: Control by ECM space and nuclear deformation and tuning by proteolysis and traction force

Journal of Cell Biology

Volumn 201, Issue 7, 2013, Pages 1069-1084

  Wolf, Katarina ^a   te Lindert, Mariska ^a   Krause, Marina ^a   Alexander, Stephanie ^b   te Riet, Joost ^a   Willis, Amanda L ^c   Hoffman, Robert M ^d,e   Figdor, Carl G ^a   Weiss, Stephen J ^c   Friedl, Peter ^a,b,f  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d ANTICANCER INC   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f Cancer Genomics Center   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; INTEGRIN; MATRIX METALLOPROTEINASE; MYOSIN ADENOSINE TRIPHOSPHATASE;

ARTICLE; CELL CYCLE ARREST; CELL MIGRATION; CELL NUCLEUS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FORCE; HUMAN; HUMAN CELL; IN VITRO STUDY; NEUTROPHIL; PHYSICAL CHEMISTRY; POROSITY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; SPOROGENESIS; T LYMPHOCYTE; TUMOR CELL; TUNING CURVE;

ANIMALS; CATTLE; CELL LINE; CELL MOVEMENT; COLLAGEN; EXTRACELLULAR MATRIX; HUMANS; HYDROGELS; INTEGRINS; KINETICS; MATRIX METALLOPROTEINASES; PROTEOLYSIS; RATS; SURFACE PROPERTIES;

EID: 84880028245     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201210152     Document Type: Article

References (73)

1. Alexander, S., G.E. Koehl, M. Hirschberg, E.K. Geissler, and P. Friedl. 2008. Dynamic imaging of cancer growth and invasion: a modified skin-fold chamber model. Histochem. Cell Biol. 130:1147-1154. http://dx.doi.org/10.1007/s00418-008-0529-1
2. Balzer, E.M., Z. Tong, C.D. Paul, W.C. Hung, K.M. Stroka, A.E. Boggs, S.S. Martin, and K. Konstantopoulos. 2012. Physical confinement alters tumor cell adhesion and migration phenotypes. FASEB J. 26:4045-4056. http://dx.doi.org/10.1096/fj.12-211441
3. Beadle, C., M.C. Assanah, P. Monzo, R. Vallee, S.S. Rosenfeld, and P. Canoll. 2008. The role of myosin II in glioma invasion of the brain. Mol. Biol. Cell. 19:3357-3368. http://dx.doi.org/10.1091/mbc.E08-03-0319
4. Berton, S., B. Belletti, K. Wolf, V. Canzonieri, F. Lovat, A. Vecchione, A. Colombatti, P. Friedl, and G. Baldassarre. 2009. The tumor suppressor functions of p27(kip1) include control of the mesenchymal/amoeboid transition. Mol. Cell. Biol. 29:5031-5045. http://dx.doi.org/10.1128/MCB.00144-09
5. Brunner, C.A., A. Ehrlicher, B. Kohlstrunk, D. Knebel, J.A. Käs, and M. Goegler. 2006. Cell migration through small gaps. Eur. Biophys. J. 35:713-719. http://dx.doi.org/10.1007/s00249-006-0079-1
6. Butcher, D.T., T. Alliston, and V.M. Weaver. 2009. A tense situation: forcing tumour progression. Nat. Rev. Cancer. 9:108-122. http://dx.doi.org/10.1038/nrc2544
7. Buxboim, A., I.L. Ivanovska, and D.E. Discher. 2010. Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells 'feel' outside and in? J. Cell Sci. 123:297-308. http://dx.doi.org/10.1242/jcs.041186
8. Chow, K.H., R.E. Factor, and K.S. Ullman. 2012. The nuclear envelope environment and its cancer connections. Nat. Rev. Cancer. 12:196-209.
9. Dahl, K.N., S.M. Kahn, K.L. Wilson, and D.E. Discher. 2004. The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. J. Cell Sci. 117:4779-4786. http://dx.doi.org/10.1242/jcs.01357
10. Deryugina, E.I., G.X. Luo, R.A. Reisfeld, M.A. Bourdon, and A. Strongin. 1997. Tumor cell invasion through matrigel is regulated by activated matrix metalloproteinase-2. Anticancer Res. 17(5A):3201-3210.
11. Ehrbar, M., A. Sala, P. Lienemann, A. Ranga, K. Mosiewicz, A. Bittermann, S.C. Rizzi, F.E. Weber, and M.P. Lutolf. 2011. Elucidating the role of matrix stiffness in 3D cell migration and remodeling. Biophys. J. 100:284-293. http://dx.doi.org/10.1016/j.bpj.2010.11.082
12. Elbjeirami, W.M., E.O. Yonter, B.C. Starcher, and J.L. West. 2003. Enhancing mechanical properties of tissue-engineered constructs via lysyl oxidase crosslinking activity. J. Biomed. Mater. Res. A. 66:513-521. http://dx.doi.org/10.1002/jbm.a.10021
13. Feng, D., J.A. Nagy, K. Pyne, H.F. Dvorak, and A.M. Dvorak. 1998. Neutrophils emigrate from venules by a transendothelial cell pathway in response to FMLP. J. Exp. Med. 187:903-915. http://dx.doi.org/10.1084/jem.187.6.903
14. Fisher, K.E., A. Sacharidou, A.N. Stratman, A.M. Mayo, S.B. Fisher, R.D. Mahan, M.J. Davis, and G.E. Davis. 2009. MT1-MMP- and Cdc42- dependent signaling co-regulate cell invasion and tunnel formation in 3D collagen matrices. J. Cell Sci. 122:4558-4569. http://dx.doi.org/10.1242/jcs.050724
15. Friedl, P., and S. Alexander. 2011. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell. 147:992-1009. http://dx.doi.org/10.1016/j.cell.2011.11.016
16. Friedl, P., and E.B. Bröcker. 2004. Reconstructing leukocyte migration in 3D extracellular matrix by time-lapse videomicroscopy and computer-assisted tracking. Methods Mol. Biol. 239:77-90.
17. Friedl, P., and K. Wolf. 2009. Proteolytic interstitial cell migration: a fivestep process. Cancer Metastasis Rev. 28:129-135. http://dx.doi.org/10.1007/s10555-008-9174-3
18. Friedl, P., and K. Wolf. 2010. Plasticity of cell migration: a multiscale tuning model. J. Cell Biol. 188:11-19. http://dx.doi.org/10.1083/jcb.200909003
19. Friedl, P., K. Maaser, C.E. Klein, B. Niggemann, G. Krohne, and K.S. Zänker. 1997. Migration of highly aggressive MV3 melanoma cells in 3-dimensional collagen lattices results in local matrix reorganization and shedding of alpha2 and beta1 integrins and CD44. Cancer Res. 57:2061-2070.
20. Friedl, P., K. Wolf, and J. Lammerding. 2011. Nuclear mechanics during cell migration. Curr. Opin. Cell Biol. 23:55-64. http://dx.doi.org/10.1016/j.ceb.2010.10.015
21. Gerlitz, G., and M. Bustin. 2011. The role of chromatin structure in cell migration. Trends Cell Biol. 21:6-11. http://dx.doi.org/10.1016/j.tcb.2010.09.002
22. Goldberg, M.W., I. Huttenlauch, C.J. Hutchison, and R. Stick. 2008. Filaments made from A- and B-type lamins differ in structure and organization. J. Cell Sci. 121:215-225. http://dx.doi.org/10.1242/jcs.022020
23. Grinnell, F., and W.M. Petroll. 2010. Cell motility and mechanics in threedimensional collagen matrices. Annu. Rev. Cell Dev. Biol. 26:335-361. http://dx.doi.org/10.1146/annurev.cellbio.042308.113318
24. Helseth, D.L. Jr., and A. Veis. 1981. Collagen self-assembly in vitro. Differentiating specific telopeptide-dependent interactions using selective enzyme modification and the addition of free amino telopeptide. J. Biol. Chem. 256:7118-7128.
25. Hotary, K., E. Allen, A. Punturieri, I. Yana, and S.J. Weiss. 2000. Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J. Cell Biol. 149:1309-1323. http://dx.doi.org/10.1083/jcb.149.6.1309
26. 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. 114:33-45. http://dx.doi.org/10.1016/S0092-8674(03)00513-0
27. Huttenlocher, A., R.R. Sandborg, and A.F. Horwitz. 1995. Adhesion in cell migration. Curr. Opin. Cell Biol. 7:697-706. http://dx.doi.org/10.1016/0955-0674(95)80112-X
28. Ilina, O., G.J. Bakker, A. Vasaturo, R.M. Hofmann, and P. Friedl. 2011. Two-photon laser-generated microtracks in 3D collagen lattices: principles of MMPdependent and -independent collective cancer cell invasion. Phys. Biol. 8:015010. http://dx.doi.org/10.1088/1478-3975/8/1/015010
29. Jacobelli, J., R.S. Friedman, M.A. Conti, A.M. Lennon-Dumenil, M. Piel, C.M. Sorensen, R.S. Adelstein, and M.F. Krummel. 2010. Confinementoptimized three-dimensional T cell amoeboid motility is modulated via myosin IIA-regulated adhesions. Nat. Immunol. 11:953-961. http://dx.doi.org/10.1038/ni.1936
30. Jawerth, L.M., S. Münster, D.A. Vader, B. Fabry, and D.A. Weitz. 2010. A blind spot in confocal reflection microscopy: the dependence of fiber brightness on fiber orientation in imaging biopolymer networks. Biophys. J. 98:L1-L3. http://dx.doi.org/10.1016/j.bpj.2009.09.065
31. Lämmermann, T., B.L. Bader, S.J. Monkley, T. Worbs, R. Wedlich-Söldner, K. Hirsch, M. Keller, R. Förster, D.R. Critchley, R. Fässler, and M. Sixt. 2008. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature. 453:51-55. http://dx.doi.org/10.1038/nature06887
32. Lautenschläger, F., S. Paschke, S. Schinkinger, A. Bruel, M. Beil, and J. Guck. 2009. The regulatory role of cell mechanics for migration of differentiating myeloid cells. Proc. Natl. Acad. Sci. USA. 106:15696-15701. http://dx.doi.org/10.1073/pnas.0811261106
33. 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. 2009. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell. 139:891- 906. http://dx.doi.org/10.1016/j.cell.2009.10.027
34. Lin, D.C., E.K. Dimitriadis, and F. Horkay. 2007. Robust strategies for automated AFM force curve analysis-I. Non-adhesive indentation of soft, inhomogeneous materials. J. Biomech. Eng. 129:430-440. http://dx.doi.org/10.1115/1.2720924
35. Miron-Mendoza, M., J. Seemann, and F. Grinnell. 2010. The differential regulation of cell motile activity through matrix stiffness and porosity in three dimensional collagen matrices. Biomaterials. 31:6425-6435. http://dx.doi.org/10.1016/j.biomaterials.2010.04.064
36. Moss, N.M., Y.I. Wu, Y. Liu, H.G. Munshi, and M.S. Stack. 2009. Modulation of the membrane type 1 matrix metalloproteinase cytoplasmic tail enhances tumor cell invasion and proliferation in three-dimensional collagen matrices. J. Biol. Chem. 284:19791-19799. http://dx.doi.org/10.1074/jbc.M109.020362
37. Packard, B.Z., V.V. Artym, A. Komoriya, and K.M. Yamada. 2009. Direct visualization of protease activity on cells migrating in three-dimensions. Matrix Biol. 28:3-10. http://dx.doi.org/10.1016/j.matbio.2008.10.001
38. Provenzano, P.P., K.W. Eliceiri, J.M. Campbell, D.R. Inman, J.G. White, and P.J. Keely. 2006. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med. 4:38. http://dx.doi.org/10.1186/1741-7015-4-38
39. Puklin-Faucher, E., and M.P. Sheetz. 2009. The mechanical integrin cycle. J. Cell Sci. 122:179-186. http://dx.doi.org/10.1242/jcs.042127
40. Raub, C.B., V. Suresh, T. Krasieva, J. Lyubovitsky, J.D. Mih, A.J. Putnam, B.J. Tromberg, and S.C. George. 2007. Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy. Biophys. J. 92:2212-2222. http://dx.doi.org/10.1529/biophysj.106.097998
41. Ren, X.D., R. Wang, Q. Li, L.A. Kahek, K. Kaibuchi, and R.A. Clark. 2004. Disruption of Rho signal transduction upon cell detachment. J. Cell Sci. 117:3511-3518. http://dx.doi.org/10.1242/jcs.01205
42. Ridley, A.J., M.A. Schwartz, K. Burridge, R.A. Firtel, M.H. Ginsberg, G. Borisy, J.T. Parsons, and A.R. Horwitz. 2003. Cell migration: integrating signals from front to back. Science. 302:1704-1709. http://dx.doi.org/10.1126/science.1092053
43. Rolli, C.G., T. Seufferlein, R. Kemkemer, and J.P. Spatz. 2010. Impact of tumor cell cytoskeleton organization on invasiveness and migration: a microchannel- based approach. PLoS ONE. 5:e8726. http://dx.doi.org/10.1371/journal.pone.0008726
44. Rowe, R.G., and S.J. Weiss. 2009. Navigating ECM barriers at the invasive front: the cancer cell-stroma interface. Annu. Rev. Cell Dev. Biol. 25:567-595. http://dx.doi.org/10.1146/annurev.cellbio.24.110707.175315
45. Sabeh, F., I. Ota, K. Holmbeck, H. Birkedal-Hansen, P. Soloway, M. Balbin, C. Lopez-Otin, S. Shapiro, M. Inada, S. Krane, et al. 2004. Tumor cell traffic through the extracellular matrix is controlled by the membraneanchored collagenase MT1-MMP. J. Cell Biol. 167:769-781. http://dx.doi.org/10.1083/jcb.200408028
46. Sabeh, F., R. Shimizu-Hirota, and S.J. Weiss. 2009. Protease-dependent versus - independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J. Cell Biol. 185:11-19. http://dx.doi.org/10.1083/jcb.200807195
47. Salmon, H., K. Franciszkiewicz, D. Damotte, M.C. Dieu-Nosjean, P. Validire, A. Trautmann, F. Mami-Chouaib, and E. Donnadieu. 2012. Matrix architecture defines the preferential localization and migration of T cells into the stroma of human lung tumors. J. Clin. Invest. 122:899-910. http://dx.doi.org/10.1172/JCI45817
48. Sanz-Moreno, V., G. Gadea, J. Ahn, H. Paterson, P. Marra, S. Pinner, E. Sahai, and C.J. Marshall. 2008. Rac activation and inactivation control plasticity of tumor cell movement. Cell. 135:510-523. http://dx.doi.org/10.1016/j.cell.2008.09.043
49. Schoumacher, M., R.D. Goldman, D. Louvard, and D.M. Vignjevic. 2010. Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J. Cell Biol. 189:541-556. http://dx.doi.org/10.1083/jcb.200909113
50. Shankar, J., A. Messenberg, J. Chan, T.M. Underhill, L.J. Foster, and I.R. Nabi. 2010. Pseudopodial actin dynamics control epithelial-mesenchymal transition in metastatic cancer cells. Cancer Res. 70:3780-3790. http://dx.doi.org/10.1158/0008-5472.CAN-09-4439
51. Sodek, K.L., M.J. Ringuette, and T.J. Brown. 2007. MT1-MMP is the critical determinant of matrix degradation and invasion by ovarian cancer cells. Br. J. Cancer. 97:358-367. http://dx.doi.org/10.1038/sj.bjc.6603863
52. Sodek, K.L., T.J. Brown, and M.J. Ringuette. 2008. Collagen I but not Matrigel matrices provide an MMP-dependent barrier to ovarian cancer cell penetration. BMC Cancer. 8:223. http://dx.doi.org/10.1186/1471-2407-8-223
53. Starborg, T., Y. Lu, K.E. Kadler, and D.F. Holmes. 2008. Electron microscopy of collagen fibril structure in vitro and in vivo including three-dimensional reconstruction. Methods Cell Biol. 88:319-345. http://dx.doi.org/10.1016/S0091-679X(08)00417-2
54. Stein, A.M., D.A. Vader, L.M. Jawerth, D.A. Weitz, and L.M. Sander. 2008. An algorithm for extracting the network geometry of three-dimensional collagen gels. J. Microsc. 232:463-475. http://dx.doi.org/10.1111/j.1365-2818.2008.02141.x
55. Stoitzner, P., K. Pfaller, H. Stössel, and N. Romani. 2002. A close-up view of migrating Langerhans cells in the skin. J. Invest. Dermatol. 118:117-125. http://dx.doi.org/10.1046/j.0022-202x.2001.01631.x
56. Tanaka, Y., K. Matsuo, and S. Yuzuriha. 2010. Long-term histological comparison between near-infrared irradiated skin and scar tissues. Clin Cosmet Investig Dermatol. 3:143-149. http://dx.doi.org/10.2147/CCID.S15729
57. te Riet, J., A.J. Katan, C. Rankl, S.W. Stahl, A.M. van Buul, I.Y. Phang, A. Gomez-Casado, P. Schön, J.W. Gerritsen, A. Cambi, et al. 2011. Interlaboratory round robin on cantilever calibration for AFM force spectroscopy. Ultramicroscopy. 111:1659-1669. http://dx.doi.org/10.1016/j.ultramic.2011.09.012
58. Tong, Z., E.M. Balzer, M.R. Dallas, W.C. Hung, K.J. Stebe, and K. Konstantopoulos. 2012. Chemotaxis of cell populations through confined spaces at single-cell resolution. PLoS ONE. 7:e29211. http://dx.doi.org/10.1371/journal.pone.0029211
59. van Spriel, A.B., J.H. Leusen, M. van Egmond, H.B. Dijkman, K.J. Assmann, T.N. Mayadas, and J.G. van de Winkel. 2001. Mac-1 (CD11b/CD18) is essential for Fc receptor-mediated neutrophil cytotoxicity and immunologic synapse formation. Blood. 97:2478-2486. http://dx.doi.org/10.1182/blood.V97.8.2478
60. Vicente-Manzanares, M., M.A. Koach, L. Whitmore, M.L. Lamers, and A.F. Horwitz. 2008. Segregation and activation of myosin IIB creates a rear in migrating cells. J. Cell Biol. 183:543-554. http://dx.doi.org/10.1083/jcb.200806030
61. Voisin, M.B., A. Woodfin, and S. Nourshargh. 2009. Monocytes and neutrophils exhibit both distinct and common mechanisms in penetrating the vascular basement membrane in vivo. Arterioscler. Thromb. Vasc. Biol. 29:1193- 1199. http://dx.doi.org/10.1161/ATVBAHA.109.187450
62. Weigelin, B., G.J. Bakker, and P. Friedl. 2012. Intravital third harmonic generation microscopy of collective melanoma cell invasion: Principles of interface guidance and microvesicle dynamics. IntraVital. 1:32-43. http://dx.doi.org/10.4161/intv.21223
63. Wolf, K., and P. Friedl. 2011. Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. Trends Cell Biol. 21:736-744. http://dx.doi.org/10.1016/j.tcb.2011.09.006
64. Wolf, K., I. Mazo, H. Leung, K. Engelke, U.H. von Andrian, E.I. Deryugina, A.Y. Strongin, E.B. Bröcker, and P. Friedl. 2003a. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160:267-277. http://dx.doi.org/10.1083/jcb.200209006
65. Wolf, K., R. Müller, S. Borgmann, E.B. Bröcker, and P. Friedl. 2003b. Amoeboid shape change and contact guidance: T-lymphocyte crawling through fibrillar collagen is independent of matrix remodeling by MMPs and other proteases. Blood. 102:3262-3269. http://dx.doi.org/10.1182/blood-2002-12-3791
66. 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. http://dx.doi.org/10.1038/ncb1616
67. Wolf, K., S. Alexander, V. Schacht, L.M. Coussens, U.H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl. 2009. Collagen-based cell migration models in vitro and in vivo. Semin. Cell Dev. Biol. 20:931-941. http://dx.doi.org/10.1016/j.semcdb.2009.08.005
68. Yamamoto, N., P. Jiang, M. Yang, M. Xu, K. Yamauchi, H. Tsuchiya, K. Tomita, G.M. Wahl, A.R. Moossa, and R.M. Hoffman. 2004. Cellular dynamics visualized in live cells in vitro and in vivo by differential dualcolor nuclear-cytoplasmic fluorescent-protein expression. Cancer Res. 64:4251-4256. http://dx.doi.org/10.1158/0008-5472.CAN-04-0643
69. Yamauchi, K., M. Yang, P. Jiang, N. Yamamoto, M. Xu, Y. Amoh, K. Tsuji, M. Bouvet, H. Tsuchiya, K. Tomita, et al. 2005. Real-time in vivo dual-color imaging of intracapillary cancer cell and nucleus deformation and migration. Cancer Res. 65:4246-4252. http://dx.doi.org/10.1158/0008-5472.CAN-05-0069
70. Yamauchi, K., M. Yang, P. Jiang, M. Xu, N. Yamamoto, H. Tsuchiya, K. Tomita, A.R. Moossa, M. Bouvet, and R.M. Hoffman. 2006. Development of real-time subcellular dynamic multicolor imaging of cancer-cell trafficking in live mice with a variable-magnification whole-mouse imaging system. Cancer Res. 66:4208-4214. http://dx.doi.org/10.1158/0008-5472.CAN-05-3927
71. Yang, Y.L., and L.J. Kaufman. 2009. Rheology and confocal reflectance microscopy as probes of mechanical properties and structure during collagen and collagen/hyaluronan self-assembly. Biophys. J. 96:1566-1585. http://dx.doi.org/10.1016/j.bpj.2008.10.063
72. Yang, Y.L., S. Motte, and L.J. Kaufman. 2010. Pore size variable type I collagen gels and their interaction with glioma cells. Biomaterials. 31:5678-5688. http://dx.doi.org/10.1016/j.biomaterials.2010.03.039
73. Zaman, M.H., L.M. Trapani, A.L. Sieminski, D. Mackellar, H. Gong, R.D. Kamm, 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. http://dx.doi.org/10.1073/pnas.0604460103