Quantitative mapping of averaged focal adhesion dynamics in migrating cells by shape normalization

Journal of Cell Science

Volumn 125, Issue 1, 2012, Pages 155-165

  Möhl, Christoph ^b   Kirchgessner, Norbert ^c   Schäfer, Claudia ^d   Hoffmann, Bernd ^a   Merkel, Rudolf ^a  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^c ETH ZURICH   (Switzerland)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin flow; Cell migration; Focal adhesion dynamics; Traction force

Indexed keywords

VINCULIN;

ARTICLE; CELL ADHESION; CELL MIGRATION; FOCAL ADHESION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ACTIN CYTOSKELETON; ACTINS; CELL MOVEMENT; CELL POLARITY; CELL SHAPE; FOCAL ADHESIONS; HUMANS; KERATINOCYTES; PHOSPHORYLATION; VINCULIN;

EID: 84858122802     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.090746     Document Type: Article

References (56)

1. Alexandrova, A. Y., Arnold, K., Schaub, S., Vasiliev, J. M., Meister, J.-J., Bershadsky, A. D. and Verkhovsky, A. B. (2008). Comparative dynamics of retrograde actin flow and focal adhesions: formation of nascent adhesions triggers transition from fast to slow flow. PLoS ONE 3, e3234.
2. Anderson, K. I. and Cross, R. (2000). Contact dynamics during keratocyte motility. Curr. Biol. 10, 253-260.
3. Balaban, N. Q., Schwarz, U. S., Riveline, D., Goichberg, P., Tzur, G., Sabanay, I., Mahalu, D., Safran, S., Bershadsky, A., Addadi, L. et al. (2001). Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3, 466-472.
4. Ballestrem, C., Hinz, B., Imhof, B. A. and Wehrle-Haller, B. (2001). Marching at the front and dragging behind: differential alphaVbeta3-integrin turnover regulates focal adhesion behavior. J. Cell Biol. 155, 1319-1332.
5. Bellis, S. L., Miller, J. T. and Turner, C. E. (1995). Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase. J. Biol. Chem. 270, 17437-17441.
6. Beningo, K. A., Dembo, M., Kaverina, I., Small, J. V. and Wang, Y. (2001). Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J. Cell Biol. 153, 881-887.
7. Broussard, J. A., Webb, D. J. and Kaverina, I. (2008). Asymmetric focal adhesion disassembly in motile cells. Curr. Opin. Cell Biol. 20, 85-90.
8. Cesa, C. M., Kirchgessner, N., Mayer, D., Schwarz, U. S., Hoffmann, B. and Merkel, R. (2007). Micropatterned silicone elastomer substrates for high resolution analysis of cellular force patterns. Rev. Sci. Instrum. 78, 034301.
9. Chen, C. S., Mrksich, M., Huang, S., Whitesides, G. M. and Ingber, D. E. (1997). Geometric control of cell life and death. Science 276, 1425-1428.
10. Colombelli, J., Besser, A., Kress, H., Reynaud, E. G., Girard, P., Caussinus, E., Haselmann, U., Small, J. V., Schwarz, U. S. and Stelzer, E. H. K. (2009). Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization. J. Cell Sci. 122, 1665.
11. Dubash, A. D., Menold, M. M., Samson, T., Boulter, E., García-Mata, R., Doughman, R. and Burridge, K. (2009). Chapter 1. Focal adhesions: new angles on an old structure. Int. Rev. Cell Mol. Biol. 277, 1-65.
12. Ezratty, E. J., Partridge, M. A. and Gundersen, G. G. (2005). Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat. Cell Biol. 7, 581-590.
13. Fletcher, D. A. and Mullins, R. D. (2010). Cell mechanics and the cytoskeleton. Nature 463, 485-492.
14. Fournier, M. F., Sauser, R., Ambrosi, D., Meister, J.-J. and Verkhovsky, A. B. (2010). Force transmission in migrating cells. J. Cell Biol. 188, 287-297.
15. Galbraith, C. G., Yamada, K. M. and Sheetz, M. P. (2002). The relationship between force and focal complex development. J. Cell Biol. 159, 695-705.
16. Gardel, M. L., Sabass, B., Ji, L., Danuser, G., Schwarz, U. S. and Waterman, C. M. (2008). Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed. J. Cell Biol. 183, 999-1005.
17. Geiger, B., Bershadsky, A., Pankov, R. and Yamada, K. M. (2001). Transmembrane crosstalk between the extracellular matrix and the cytoskeleton. Nat. Rev. Mol. Cell Biol. 2, 793-805.
18. Halir, R. and Flusser, J. (1998). Numerically stable direct least squares fitting of ellipses. In Proceedings of the Sixth International Conference in Central Europe on Computer Graphics and Visualization, pp. 125-132. Pilzen, Czech Republic.
19. Hotulainen, P. and Lappalainen, P. (2006). Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J. Cell Biol. 173, 383-394.
20. Hu, K., Ji, L., Applegate, K. T., Danuser, G. and Waterman-Storer, C. M. (2007). Differential transmission of actin motion within focal adhesions. Science 315, 111-115.
21. Ji, L. and Danuser, G. (2005). Tracking quasi-stationary flow of weak fluorescent signals by adaptive multi-frame correlation. J. Microsc. 220, 150-167.
22. Kirchgessner, N., Spies, H., Scharr, H., and Schurr, U. (2001). Root growth and analysis in physiological coordinates. In Proceedings of the 11th international conference on image analysis and processing. 1, 589-594.
23. Kruse, K., Joanny, J. F., Jülicher, F. and Prost, J. (2006). Contractility and retrograde flow in lamellipodium motion. Phys. Biol. 3, 130-137.
24. Kuusela, E. and Alt, W. (2009). Continuum model of cell adhesion and migration. J. Math. Biol. 58, 135-161.
25. Lauffenburger, D. A. and Horwitz, A. F. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
26. Machacek, M., Hodgson, L., Welch, C., Elliott, H., Pertz, O., Nalbant, P., Abell, A., Johnson, G. L., Hahn, K. M. and Danuser, G. (2009). Coordination of Rho GTPase activities during cell protrusion. Nature 461, 99-103.
27. Merkel, R., Kirchgesner, N., Cesa, C. and Hoffmann, B. (2007). Cell force microscopy on elastic layers of finite thickness. Biophys. J. 93, 3314-3323.
28. Mitra, S. K., Hanson, D. A. and Schlaepfer, D. D. (2005). Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6, 56-68.
29. Mogilner, A. and Verzi, D. W. (2003). A simple 1-D physical model for the crawling nematode sperm cell. J. Stat. Phys. 110, 1169-1189.
30. Möhl, C., Kirchgessner, N., Schäfer, C., Küpper, K., Born, S., Diez, G., Goldmann, W. H., Merkel, R. and Hoffmann, B. (2009). Becoming stable and strong: the interplay between vinculin exchange dynamics and adhesion strength during adhesion site maturation. Cell Motil. Cytoskeleton 66, 350-364.
31. Oliver, T., Dembo, M. and Jacobson, K. (1995). Traction forces in locomoting cells. Cell Motil. Cytoskeleton 31, 225-240.
32. Parri, M. and Chiarugi, P. (2010). Rac and Rho GTPases in cancer cell motility control. Cell Commun. Signal. 8, 23.
33. Paul, R., Heil, P., Spatz, J. P. and Schwarz, U. S. (2008). Propagation of mechanical stress through the actin cytoskeleton toward focal adhesions: model and experiment. Biophys. J. 94, 1470-1482.
34. Pollard, T. D. and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
35. Rid, R., Schiefermeier, N., Grigoriev, I., Small, J. V. and Kaverina, I. (2005). The last but not the least: the origin and significance of trailing adhesions in fibroblastic cells. Cell Motil. Cytoskeleton 61, 161-171.
36. Rubinstein, B., Fournier, M. F., Jacobson, K., Verkhovsky, A. B. and Mogilner, A. (2009). Actin-myosin viscoelastic flow in the keratocyte lamellipod. Biophys. J. 97, 1853-1863.
37. Sambeth, R. and Baumgaertner, A. (2001). Autocatalytic polymerization generates persistent random walk of crawling cells. Phys. Rev. Lett. 86, 5196.
38. Schäfer, C., Borm, B., Born, S., Möhl, C., Eibl, E.-M. and Hoffmann, B. (2009). One step ahead: role of filopodia in adhesion formation during cell migration of keratinocytes. Exp. Cell Res. 315, 1212-1224.
39. Schäfer, C., Born, S., Möhl, C., Houben, S., Kirchgeßner, N., Merkel, R. and Hoffmann, B. (2010). The key feature for early migratory processes: dependence of adhesion, actin bundles, force generation and transmission on filopodia. Cell Adh. Migr. 4, 215-225.
40. Schaub, S., Bohnet, S., Laurent, V. M., Meister, J.-J. and Verkhovsky, A. B. (2007). Comparative maps of motion and assembly of filamentous actin and myosin II in migrating cells. Mol. Biol. Cell 18, 3723-3732.
41. Schwarz, U., Balaban, N., Riveline, D., Bershadsky, A., Geiger, B. and Safran, S. (2002). Calculation of forces at focal adhesions from elastic substrate data: the effect of localized force and the need for regularization. Biophys. J. 83, 1380-1394.
42. Sedgewick, R. (1997). Algorithms in C, Parts 1-4: Fundamentals, Data Structures, Sorting, Searching, 3rd edn. London: Addison-Wesley Professional.
43. Svitkina, T. M., Verkhovsky, A. B., McQuade, K. M. and Borisy, G. G. (1997). Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation. J. Cell. Biol. 139, 397-415.
44. Thery, M., Racine, V., Pepin, A., Piel, M., Chen, Y., Sibarita, J.-B. and Bornens, M. (2005). The extracellular matrix guides the orientation of the cell division axis. Nat. Cell Biol. 7, 947-953.
45. Urban, E., Jacob, S., Nemethova, M., Resch, G. P. and Small, J. V. (2010). Electron tomography reveals unbranched networks of actin filaments in lamellipodia. Nat. Cell Biol. 12, 429-435.
46. Vallotton, P., Danuser, G., Bohnet, S., Meister, J.-J. and Verkhovsky, A. B. (2005). Tracking retrograde flow in keratocytes: news from the Front. Mol. Biol. Cell 16, 1223-1231.
47. Verkhovsky, A. B., Svitkina, T. M. and Borisy, G. G. (1999). Self-polarization and directional motility of cytoplasm. Curr. Biol. 9, 11-20.
48. Vicente-Manzanares, M., Webb, D. J. and Horwitz, A. R. (2005). Cell migration at a glance. J. Cell Sci. 118, 4917-4919.
49. Vicente-Manzanares, M., Koach, M. A., Whitmore, L., Lamers, M. L. and Horwitz, A. F. (2008). Segregation and activation of myosin IIB creates a rear in migrating cells. J. Cell Biol. 183, 543-554.
50. Wagner, S., Storbek, C. J., Roovers, K., Chaar, Z. Y., Kolodziej, P., McKay, M. and Sabourin, L. A. (2008). FAK/src-family dependent activation of the ste20-like kinase SLK is required for microtubule-dependent focal adhesion turnover and cell migration. PLoS ONE 3, e1868.
51. Wang, Y.-L (2007). Flux at focal adhesions: slippage clutch, mechanical gauge, or signal depot. Sci. STKE 2007, pe10.
52. Webb, D. J., Parsons, J. T. and Horwitz, A. F. (2002). Adhesion assembly, disassembly and turnover in migrating cells - over and over and over again. Nat. Cell Biol. 4, E97-E100.
53. Yam, P. T., Wilson, C. A., Ji, L., Hebert, B., Barnhart, E. L., Dye, N. A., Wiseman, P. W., Danuser, G. and Theriot, J. A. (2007). Actin myosin network reorganization breaks symmetry at the cell rear to spontaneously initiate polarized cell motility. J. Cell Biol. 178, 1207-1221.
54. Zaidel-Bar, R., Ballestrem, C., Kam, Z. and Geiger, B. (2003). Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J. Cell Sci. 116, 4605-4613.
55. Zamir, E., Katz, B. Z., Aota, S., Yamada, K. M., Geiger, B. and Kam, Z. (1999). Molecular diversity of cell-matrix adhesions. J. Cell. Sci. 112, 1655-1669.
56. Zhang, Z., Izaguirre, G., Lin, S.-Y., Lee, H. Y., Schaefer, E. and Haimovich, B. (2004). The phosphorylation of vinculin on tyrosine residues 100 and 1065, mediated by src kinases, affects cell spreading. Mol. Biol. Cell 15, 4234-4247.