Slipping or gripping? Fluorescent speckle microscopy in fish keratocytes reveals two different mechanisms for generating a retrograde flow of actin

Molecular Biology of the Cell

Volumn 16, Issue 2, 2005, Pages 507-518

  Jurado, Carlos ^a   Haserick, John R ^a   Lee, Juliet ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (5 IODO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; ACTIN; MYOSIN II; MYOSIN LIGHT CHAIN KINASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MOTILITY; CONTROLLED STUDY; CORNEA CELL; CYTOSKELETON; FISH; FLUORESCENCE MICROSCOPY; LAMELLIPODIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; VELOCITY;

ACTINS; ANIMALS; AZEPINES; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; CORNEA; ENZYME INHIBITORS; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; FLUORESCENT ANTIBODY TECHNIQUE; FLUORESCENT DYES; GELATIN; GREEN FLUORESCENT PROTEINS; IMAGE PROCESSING, COMPUTER-ASSISTED; KINETICS; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MYOSIN TYPE II; MYOSIN-LIGHT-CHAIN KINASE; NAPHTHALENES; PHALLOIDINE; POECILIA; PSEUDOPODIA; TRANSFECTION;

ANIMALIA;

EID: 12844281654     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-10-0860     Document Type: Article

References (62)

1. Anderson, K. I., and Cross, R. (2000). Contact dynamics during keratocyte motility. Curr. Biol. 10, 253-260.
2. Balaban, N. Q. et al. (2001). Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3, 466-472.
3. Beningo, K. A., Dembo, M., Kaverina, I., Small, V., and Wang, Y.-L. (2001). Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J. Cell Biol. 153, 881-887.
4. Choquet, D., Felsenfeld, D. P., and Sheetz, M. P. (1997). Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88, 39-48.
5. 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.
6. Cramer, L. P. (1997). Molecular mechanism of actin-dependent retrograde flow in lamellipodia of motile cells. Front. Biosci. 2, d260-d270.
7. Davies, P. F., Robotewskyj, A., and Griem, M. L. (1993). Endothelial cell adhesion in real time. J. Clin. Invest. 91, 2640-2652.
8. Davies, P. F., Robotewskyj, A., and Griem, M. L. (1994). Quantitative studies of endothelial cell adhesion. J. Clin. Invest. 93, 2031-2038.
9. Delanoe-Ayari, H., Kurdi, R. A., Vallade, M., Gulino-Debrac, D., and Riveline, D. (2004). Membrane and acto-myosin tension promote clustering of adhesion proteins. Proc. Natl. Acad. Sci. USA 101, 2229-2234.
10. Dembo, M., and Wang, Y.-L. (1999). Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys. J. 76, 2307-2316.
11. DiMilla, P. A., Barbee, K., and Lauffenburger, D. A. (1991). Mathematical model for the effects of adhesion and mechanics on cell migration speed. Biophys. J. 60, 15-37.
12. DiMilla, P. A., Stone, J. A., Quinn, J. A., Albelda, S. M., and Lauffenburger, D. A. (1993). Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J. Cell Biol. 122, 729-737.
13. 2+-dependent regulation of cell adhesiveness. J. Cell Sci. (in press).
14. Doyle, A., Marganski, W., and Lee, J. (2004). Calcium transients induce spatially coordinated increases in traction force during the movement of fish keratocytes. J. Cell Sci. 117, 2203-2214.
15. Doyle, A. D., and Lee, J. (2002). Simultaneous, real-time imaging of intracellular calcium and traction force production. Biotechniques 33, 358-364.
16. Euteneuer, U., and Schliwa, M. (1984). Persistent, directional motility of cells and cytoplasmic fragments in the absence of microtubules. Nature 310, 58-61.
17. Forscher, P., and Smith, S. J. (1988). Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 107, 1505-1516.
18. Fukui, Y., Kitanishi-Yumura, T., and Yumaura, S. (1999). Myosin-II independent F-actin flow contributes to cell locomotion in Dictyostelium. J. Cell Sci. 112, 877-886.
19. Galbraith, C., and Sheetz, M. (1999). Keratocytes pull with similar forces on their dorsal and ventral surfaces. J. Cell Biol. 147, 1313-1323.
20. Giannone, G., Jiang, G., Sutton, D. H., Critchley, D. R., and Sheetz, M. P. (2003). Talin1 is critical for force-dependent reinforcement of initial integrin-cytoskeleton bonds but not tyrosine kinase activation. J. Cell Biol. 163, 409-419.
21. Grebecki, A. (1994). Membrane and cytoskeletal flow in motile cells with emphasis on the contribution of free-living amoeba. Int. Rev. Cytol. 248, 37-79.
22. Harris, A. K. (1994). Locomotion of tissue culture cells considered in relation to ameboid locomotion. Int. Rev. Cytol. 250, 35-68.
23. Harris, A. K., Wild, P., and Stopak, D. (1980). Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208, 177-179.
24. Heideman, S., and Buxbaum, R. (1998). Cell crawling: first the motor, now the transmission. J. Cell Biol. 142 ,1-4.
25. Henson, J. H., Svitkina, T. M., Burns, A., Hughes, H. E., MacPartland, K. J., Nazarian, R., and Borisy, G. G. (1999). Two components of actin-based retrograde flow in sea urchin coelomocytes. Mol. Biol. Cell 20, 4075-4090.
26. Horwitz, A. F., Duggan, K., Buck, C., Beckerle, M. C., and Burridge, K. (1986). Interactions of plasma membrane fibronectin receptor with talin - a transmembrane linkage. Nature 320, 5312-5313.
27. Jay, D. G. (2000). The clutch hypothesis revisited: ascribing the roles of actin-associated proteins in filopodial protrusion in the nerve growth cone. Review. J. Neurobiol. 44, 114-125.
28. Kaneko, K., Satoh, K., Masamune, A., Satoh, A., and Shomosegawa, T. (2002). Myosin light chain kinase inhibitors can block invasion and adhesion of human pancreatic cancer cell lines. Pancreas 24, 34-41.
29. Leader, W. M., Stopak, D., and Harris, A. K. (1983). Increased contractile strength and tightened adhesions to the substratum result from reverse transformation of Chinese hamster ovary cells by dibutyryl cyclic adenosine monophosphate. J. Cell Sci. 64, 1-11.
30. 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.
31. Lee, J., Ishihara, A., Theriot, J., and Jacobson, K. (1993). Principles of locomotion for simple-shaped cells. Nature 362, 167-171.
32. Lee, J., and Jacobson, K. (1997). The composition and dynamics of cell-substratum adhesions in locomoting fish keratocytes. J. Cell Sci. 110, 2833-2844.
33. Lee, J., Leonard, M., Oliver, T., Ishihara, A., and Jacobson, K. (1994). Traction forces generated by locomoting keratocytes. J. Cell Biol. 127, 1957-1964.
34. Lin, C. H., Espreafico, E. M., and Mooseker, M. S. (1996). Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron 16, 769-782.
35. Lin, C.-H., and Forscher, P. (1995). Growth cone advance is inversely proportional to retrograde F-actin flow. Neuron 14, 763-771.
36. Lin, C.-H., Thompson, C. A., and Forscher, P. (1994). Cytoskeletal reorganization underlying growth cone motility. Curr. Opin. Neurobiol. 4, 640-647.
37. Mallavarapu, A., and Mitchison, T. (1999). Regulating actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J. Cell Biol. 146, 1097-1106.
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. Mitchison, T., and Kirschner, M. (1988). Cytoskeletal dynamics and nerve growth. Neuron 2, 761-772.
40. Moazzam, F., DeLano, F. A., Zweifach, B. W., and Schmid-Schonbein, G. W. (1997). The leukocyte response to fluid shear stress. Proc. Natl. Acad. Sci. USA 94, 5338-5343.
41. Munevar, S., Wang, Y.-L., and Dembo, M. (2001). Traction force microscopy in normal and H-ras transformed 3T3 fibroblasts. Biophys. J. 80, 1744-1757.
42. Oliver, T., Dembo, M., and Jacobson, K. (1999). Separation of propulsive and adhesive traction stresses in locomoting keratocytes. J. Cell Biol. 145, 589-604.
43. Paddock, S. W. (1989). Tandem scanning reflected light microscopy of cell-substratum adhesions and stress fibers in Swiss 3T3 cells. J. Cell Sci. 93, 242-146.
44. Paku, S., Tovari, J., Lorincz, Z., Timar, F., Dome, B., Kopper, L., Raz, A., and Timar, J. (2003). Adhesion dynamics and cytoskeletal structure of gliding human fibrosarcoma cells: a hypothetical model of cell migration. Exp. Cell Res. 290, 246-253.
45. Palecek, S. P., Loftus, J. C., Ginsberg, M. H., Lauffenberger, D. A., and Horwitz, A. F. (1997). Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385, 537-540.
46. 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.
47. Roy, P., Petroll, W. M., Cavanagh, H. D., and Jester, J. V. (1999). Exertion of fractional force requires the coordinated up-regulation of cell contractility and adhesion. Cell Motil. Cytoskelet. 43, 23-43.
48. Royal, D., Royal, M., Italiano, J., Roberts, T., and Soll, D. R. (1995). In Ascaris sperm pseudopods, MSP fibers move proximally at a constant rate regardless of the forward rate of cellular translocation. Cell Motil. Cytoskelet. 31, 241-253.
49. Saitoh, M., Ishikawa, T., Matsushima, S., Naka, M., and Hidaka, H. (1987). Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase. J. Biol. Chem. 262, 7796-7801.
50. Smilenov, L. B., Mikhailov, A., Pelham, R. J., Marcantonio, E. E., and Gunderson, G. G. (1999). Focal adhesion motility revealed in stationary fibroblasts. Science 286, 1172-1174.
51. Suter, D., and Forscher, P. (2001). Transmission of growth cone traction force through apCAM-cytoskeletal linkages is regulated by Src family tyrosine kinase activity. J. Cell Biol. 155, 427-438.
52. Suter, D. M., Errante, L. D., Belotserkovsky, V., and Forscher, P. (1998). The immunoglobulin superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J. Cell Biol. 141, 227-240.
53. Suter, D. M., and Forscher, P. (1998). An emerging link between cytoskeletal dynamics and cell adhesion molecules in growth cone guidance. Curr. Opin. Neurobiol. 8, 106-116.
54. Suter, D. M., and Forscher, P. (2000). Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J. Neurobiol. 44, 97-113.
55. 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.
56. Sydor, A. M., Su, A. L., Wang, F. S., Xu, A., and Jay, D. G. (1996). Talin and vinculin play dintinct roles in filopodial motility in neuronal growth cones. J. Cell Biol. 134, 1197-1208.
57. Theriot, J. A., and Mitchison, T. J. (1991). Actin microfilament dynamcs in locomoting cells. Nature 352, 126-131.
58. Theriot, J. A., and Mitchison, T. J. (1992). Comparison of actin and cell surface dynamics in motile fibroblasts. J. Cell Biol. 118, 367-377.
59. Verkhovsky, A. B., Svitkina, T. M., and Borisy, G. G. (1999). Self-polarization and directional motility of cytoplasm. Curr. Biol. 9, 11-20.
60. Wang, Y.-L. (1985). Exchange of actin subunits at the leading edge of living fibroblasts: possible role of treadmilling. J. Cell Biol. 101, 597-602.
61. Watanabe, N., and Mitchison, T. J. (2002). Single-molecule speckle analysis of actin filament turnover in lamellipodia. Science 295, 1083-1086.
62. Waterman-Storer, C. M., Desai, A., Bulinski, J. C., and Salmon, E. D. (1998). Fluorescent speckle microscopy, a method to visualize the dynamics of protein assemblies in living cells. Curr. Biol. 8, 1227-1230.