Calcium transients induce spatially coordinated increases in traction force during the movement of fish keratocytes

Journal of Cell Science

Volumn 117, Issue 11, 2004, Pages 2203-2214

  Doyle, Andrew ^a   Marganski, William ^b   Lee, Juliet ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b Boston University   (United States)

Author keywords

Calcium transients; Keratocyte; Movement; Traction force

Indexed keywords

CALCIUM; CALCIUM CHANNEL; GELATIN;

ANIMAL CELL; ARTICLE; ASSAY; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MOTION; CONTROLLED STUDY; CORNEA CELL; CYTOSKELETON; FISH; FORCE; IMAGING; MECHANICAL STRESS; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CELL MOVEMENT; CELLS, CULTURED; ELASTICITY; EPITHELIAL CELLS; FRICTION; GELATIN; POECILIA; STRESS, MECHANICAL;

ANIMALIA;

EID: 3042551040     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01087     Document Type: Article

References (57)

1. Balaban, N. Q., Schwarz, U. S., Riveline, D., Goichberg, P., Tzur, G., Sabanay, I., Mahalu, D., Safran, S., Bershadsky, A and Addadi, L. (2001). Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3, 466-472.
2. Berridge, M. J. (1997). The AM and FM of calcium signalling. Nature 386, 759-760.
3. Brundage, R. A., Fogarty, K. E., Tuft, R. A. and Fay, F. S. (1991). Calcium gradients underlying polarization and chemotaxis of eosinophils. Science 254, 703-706.
4. Burridge, K. and Chrzanowska-Wodnicka, M. (1996). Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12, 463-518.
5. Burton, K., Park, J. H. and Taylor, D. L. (1999). Keratocytes generate traction forces in two phases. Mol. Biol. Cell 10, 3745-3769.
6. Cheek, T. (1989). Spatial aspects of calcium signalling. J. Cell Sci. 93, 211-216.
7. Chew, T. L., Wolf, W. A., Gallagher, P. J., Matsumura, F. and Chisholm, R. L. (2002). A fluorescent resonant energy transfer-based biosensor reveals transient and regional myosin light chain kinase activation in lamella and cleavage furrows. J. Cell Biol. 156, 543-553.
8. Choquet, D., Felsenfeld, D. P. and Sheetz, M. P. (1997). Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88, 39-48.
9. Chrzanowska-Wodnicka, M. and Burridge, K. (1996). Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133, 1403-1415.
10. Citi, S. and Kendrick-Jones, J. (1987). Regulation of non-muscle myosin structure and function. BioEssays 7, 155-159.
11. Crowley, E. and Horwitz, A. F. (1995). Tyrosine phosphorylation and cytoskeletal tension regulate the release of fibroblast adhesions. J. Cell Biol. 131, 525-537.
12. De Koninck, P. and Schulman, H. (1998). Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 279, 227-230.
13. Dembo, M. and Wang, Y.-L. (1999). Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophysical J. 76, 2307-2316.
14. Dolmetsch, R. E., Lewis, R. S., Goodnow, C. C. and Healy, J. I. (1997). Differential activation of transcription factors induced by Ca2+ response. Nature 386, 855-760.
15. Doyle, A. D. and Lee, J. (2002). Simultaneous, real-time imaging of intracellular calcium and cellular traction force production. Biotechniques 33, 358-364.
16. Eddy, R., Pierini, L. M., Matsumura, F. and Maxfield, F. R. (2000). Ca2+-dependent myosin II activation is required for uropod retraction during neutrophil migration. J. Cell Sci. 113, 1287-1298.
17. Galbraith, C. G. and Sheetz, M. P. (1997a). A micromachined device provides a new bend on fibroblast traction forces. Proc. Natl. Acad. Sci. USA 94, 9114-9118.
18. Galbraith, C. G. and Sheetz, M. P. (1997b). Relationship between cell shape, traction force and speed. Mol. Biol. Cell Suppl. 8, 385.
19. Giannone, G., Ronde, P., Gaire, M., Haich, J. and Takeda, K. (2002). Calcium oscillations trigger focal adhesion disassembly in human U87 astrocytoma cells. J. Biol. Chem. 277, 26364-26371.
20. Gilbert, S. H., Perry, K. and Fay, F. S. (1994). Mediation of chemoattractant-induced changes in [Ca2+]i and cell shape, polarity and locomotion by InsP3, DAG, and protein kinase C in newt eosinophils. J. Cell Biol. 127, 489-503.
21. Glogauer, M., Arora, P., Yao, G., Sokholov, I., Ferrier, J. and McCulloch, C. A. G. (1997). Calcium ions and tyrosine phosphorylation interact coordinately with actin to regulate cytoprotective responses to stretching. J. Cell Sci. 110, 11-21.
22. Goekeler, Z. M. and Wysolmerski, R. B. (1995). Myosin light chain kinase regulated endothelial cell contraction:the relationship between isometric tension, actin polymerization and myosin phosphorylation. J. Cell Biol. 130, 613-627.
23. Hartwig, J. H. and Yin, H. (1988). The organization and regulation of the macrophage cytoskeleton. Cell Motil. Cytoskeleton 10, 117-125.
24. Hendey, B., Klee, C. B. and Maxfield, F. R. (1992). Inhibition of neutrophil chemokinesis on vitronectin by inhibitors of calcineurin. Science 258, 296-299.
25. Huttenlocher, A., Palecek, S. P., Lu, Q., Zhang, W., Mellgren, R. L., Lauffenburger, D. A., Ginsberg, M. H. and Horwitz, A. F. (1997). Regulation of cell migration by the calcium-dependent protease calpain. J. Biol. Chem. 272, 32719-32722.
26. Ishihara, A., Gee, K., Schwartz, S., Jacobson, K. and Lee, J. (1997). Photoactivation of caged compounds in single, living cells: An application to the study of cell locomotion. Biotechniques 23, 268-274.
27. Kamm, K. E. and Stull, J. T. (2000). Dedicated myosin light chain kinases with diverse cellular functions. J. Biol. Chem. 276, 4527-4530.
28. Katoh, K., Kaibuchi, Y. and Fujiwara, K. (2001). Rho-kinase-mediated contraction of isolated stress fibers. J. Cell Biol. 153, 569-583.
29. Katsumi, A., Milanini, J., Kiosses, W. B., del Pozo, M. A., Kaunas, R., Chien, S., Hahn, K. M. and Scwartz, M. A. (2002). Effects of cell tension on the small GTPase Rac. J. Cell Biol. 158, 153-164.
30. Kolega, J. (1986). Effects of mechanical tension on protrusive activity and microfilament and intermediate filament organization in an epidermal epithelium moving in culture. J. Cell Biol. 102, 1400-1411.
31. Lauffenburger, D. A. and Horwitz, A. F. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
32. Lee, J., Ishihara, A., Oxford, G., Johnson, B. and Jacobson, K. (1999). Regulation of cell movement is mediated by stretch-activated calcium channels. Nature 400, 382-386.
33. Lee, J., Ishihara, A., Theriot, J. and Jacobson, K. (1993). Principles of locomotion for simple-shaped cells. Nature 362, 167-171.
34. Lee, J. and Jacobson, K. (1997). The composition and dynamics of cell-substratum adhesions in locomoting fish keratocytes. J. Cell Sci. 110, 2833-2844.
35. Lee, J., Leonard, M., Oliver, T., Ishihara, A. and Jacobson, K. (1994). Traction forces generated by locomoting keratocytes. J. Cell Biol. 127, 1957-1964.
36. Lo, C.-M., Wang, H.-B., Dembo, M. and Wang, Y.-L. (2000). Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144-152.
37. Mandeville, J. T., Ghosh, R. N. and Maxfield, E. R. (1995). Intracellular calcium levels correlate with speed and persistent forward motion in migrating neutrophils. Biophys. J. 68, 1207-1217.
38. Marganski, W. A., Dembo, M. and Wang, Y.-L. (2003). Measurements of cell-generated deformations on flexible substrata using correlation-based optical flow. Methods Enzymol. 161, 197-211.
39. Marks, P. W. and Maxfield, F. R. (1990). Transient increases in cytosolic free calcium appear to be required for the migration of adherent human neutrophils. J. Cell Biol. 110, 43-52.
40. Mitchison, T. J. and Cramer, L. P. (1996). Actin-based cell motility and cell locomotion. Cell 84, 371-379.
41. Munevar, S., Wang, Y.-L. and Dembo, M. (2001). Traction force microscopy of normal and H-ras transformed 3T3 fibroblasts. Biophys. J. 80, 1744-1757.
42. Nebl, T. and Fisher, P. R. (1997). Intracellular Ca2+ signals in Dictyostelium chemotaxis are mediated exclusively by Ca2+ influx. J. Cell Sci. 110, 2845-2853.
43. Oliver, T., Dembo, M. and Jacobson, K. (1999). Separation of propulsive and adhesive traction stresses in locomoting keratocytes. J. Cell Biol. 145, 589-604.
44. Palecek, S. P., Huttenlocher, A., Horwitz, A. F. and Lauffenburger, D. A. (1998). Physical and biochemical regulation of integrin release during rear detachment of migrating cells. J. Cell Sci. 111, 929-940.
45. Pelletier, A. J., Bodary, S. C. and Levinson, A. D. (1992). Signal transduction by the platelet integrin alpha IIb beta 3: induction of calcium oscillations required for protein-tyrosine phosphorylation and ligand-induced spreading of stably transfected cells. Mol. Biol. Cell 3, 989-998.
46. Pollard, T. D. and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
47. Rees, D. A., Charlton, J., Ataliotis, P., Woods, A., Stones, A. J. and Bayley, S. A. (1989). Myosin regulation and calcium transients in fibroblast shape change, attachment and patching. Cell Motil. Cytoskeleton 13, 112-122.
48. Riveline, D., Zamir, E., Balaban, N. Q., Schwarz, U. S., Ishizaki, T., Narumiya, S., Kam, Z., Geiger, B. and Bershadsky, A. (2001). Focal contacts as mechanosensors: Externally applied local mechanical force induces growth of focal contacts by an mDia-dependent and ROCK-independent mechanism. J. Cell Biol. 153, 1175-1185.
49. Roy, P., Petroll, W. M., Cavanagh, H. D. and Jester, J. V. (1999). Exertion of tractional force requires the coordinated up-regulation of cell contractility and adhesion. Cell Motil. Cytoskeleton 43, 23-43.
50. Sieck, G. C., Han, Y.-S., Pabelick, C. M. and Prakask, Y. S. (2001). Temporal aspects of excitation-contraction coupling in airway smooth muscle. J. Appl. Physiol. 91, 2266-2274.
51. Sjaastad, M., Angres, B., Lewis, R. S. and Nelson, J. (1994). Feedback regulation of cell-substratum adhesion by integrin-mediated intracellular Ca2+ signaling. Proc. Natl. Acad. Sci. USA 91, 8214-8218.
52. Sjaastad, M. D. and Nelson, J. (1996). Integrin-mediated calcium signaling and regulation of cell adhesion by intracellular calcium. Bioassays 19, 47-55.
53. Svitkina, T. M., Verkhovsky, A. B., Quade, K. M. M. and Borisy, G. C. (1997). Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation. J. Cell Biol. 139, 397-415.
54. Tan, J. L., Tien, J., Pirone, D. M., Gray, D. S., Bhadriraju, K. and Chen, C. S. (2003). Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc. Natl. Acad. Sci. USA 100, 1484-1489.
55. Walker, J. W., Gilbert, S. H., Drummond, R. M., Yamada, M., Sreekumar, R., Carraway, R. E., Ikeebe, M. and Fay, F. (1998). Signaling pathways underlying eosinophil cell motility revealed by using caged peptides. Proc. Natl. Acad. Sci. USA 95, 1568-1573.
56. Wang, Y.-L. and Pelham, R. J. (1998). Preparation of a flexible porous polyacrylamide substrate for mechanical studies of cultured cells. Methods Enzymol. 298, 489-496.
57. Zeng, Q., Lagunoff, D., Masaracchia, R., Goeckeler, Z. and Cote, G. (2000). Endothelial cell retraction is induced by PAK2 monophosphorylation of myosin II. J. Cell Sci. 113, 471-482.