Polarized actin bundles formed by human fascin-1: Their sliding and disassembly on myosin II and myosin V in vitro

Journal of Neurochemistry

Volumn 87, Issue 3, 2003, Pages 676-685

  Ishikawa, Ryoki ^a   Sakamoto, Takeshi ^b   Ando, Toshio ^b   Higashi Fujime, Sugic ^c   Kohama, Kazuhiro ^a  

^a GUNMA UNIVERSITY   (Japan)

^b KANAZAWA UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

Author keywords

Filopodium; Growth cone; Retrograde flow

Indexed keywords

CELL PROTEIN; F ACTIN; FASCIN 1; MEROMYOSIN; MYOSIN II; MYOSIN V; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; DISSOCIATION; ELECTRON MICROSCOPY; FILOPODIUM; GROWTH CONE; HUMAN; IN VITRO STUDY; NERVE CELL GROWTH; NERVE FIBER GROWTH; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; STRUCTURE ANALYSIS;

ACTINS; CARRIER PROTEINS; GROWTH CONES; HUMANS; MACROMOLECULAR SUBSTANCES; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; MUSCLE CONTRACTION; MUSCLE, SKELETAL; MYOSIN SUBFRAGMENTS; MYOSIN TYPE II; MYOSIN TYPE V; PSEUDOPODIA;

EID: 0142148230     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.02058.x     Document Type: Article

References (52)

1. Adelstein R. S. and Klee C. B. (1981) Purification and characterization of smooth muscle myosin light chain kinase. J. Biol. Chem. 256, 7501-7509.
2. Ando T., Kodera N., Takai E., Maruyama D., Saito K. and Toda A. (2001) A high-speed atomic force microscope for studying biological macromolecules. Proc. Natl Acad. Sci. USA 98, 12468-12472.
3. Banzai Y., Miki H., Yamaguchi H. and Takenawa T. (2000) Essential role of neural Wiskott-Aldrich syndrome protein in neurite extension in PC12 cells and rat hippocampal primary culture cells. J. Biol. Chem. 275, 11987-11992.
4. Bentley D. and Toroian-Raymond A. (1986) Disoriented pathfinding by pioneer neuron growth cones deprived of filopodia by cytochalasin treatment. Nature 323, 712-715.
5. Bridgman P. C. and Dailey M. E. (1989) The organization of myosin and actin in rapid frozen nerve growth cones. J. Cell Biol. 108, 95-109.
6. Bridgman P. C., Dave S., Asnes C. F., Tullio A. N. and Adelstein R. S. (2001) Myosin IIB is required for growth cone motility. J. Neurosci. 21, 6159-6169.
7. Bryan J. and Kane R. E. (1978) Separation and interaction of the major components of sea urchin actin gel. J. Mol. Biol. 125, 207-224.
8. Bryan J., Edwards R., Matsudaira P., Otto J. and Wulfkuhle J. (1993) Fascin, an echinoid actin-bundling protein, is a homolog of the Drosophila singed gene product. Proc. Natl Acad. Sci. USA 90, 9115-9119.
9. Cant K., Knowles B. A., Mooseker M. S. and Cooley L. (1994) Drosophila singed, a fascin homolog, is required for actin bundle formation during oogenesis and bristle extension. J. Cell Biol. 125, 369-380.
10. Cheney R. E. (1998) Purification and assay of myosin V. Meth. Enzymol. 298, 3-18.
11. Chien C.-B., Rosenthal D. E., Harris W. A. and Holt C. E. (1993) Navigational errors made by growth cone without filopodia in the embryonic Xenopus brain. Neuron 11, 237-251.
12. Cohan C. S., Welnhofer E. A., Zhao L., Matsumura E and Yamashiro S. (2001) Role of the actin bundling protein fascin in growth cone morphogenesis: localization in filopodia and lamellipodia. Cell Motil. Cytoskeleton 48, 109-120.
13. DeRosier D. J. and Censullo R. (1981) Structure of F-actin needles from extract of sea urchin oocytes. J. Mol. Biol. 146, 77-99.
14. Edwards R. A. and Bryan J. (1995) Fascin, a family of actin bundling proteins. Cell Motil. Cytoskeleton 32, 1-9.
15. Edwards R. A., Herrera-Sosa H., Otto J. and Bryan J. (1995) Cloning and expression of murine fascin homolog from mouse brain. J. Biol. Chem. 270, 10764-10770.
16. Forscher P. and Smith S. J. (1988) Action of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 107, 1505-1516.
17. Hong K., Nishiyama M., Henley J., Tessier-Lavigne M. and Poo M.-M. (2000) Calcium signaling in the guidance of nerve growth by netrin-1. Nature 403, 93-98.
18. Ishikawa R., Yamashiro S., Kohama K. and Matsumura F. (1998) Regulation of actin binding and actin bundling activities of fascin by caldesmon coupled with tropomyosin. J. Biol. Chem. 273, 26991-26997.
19. Kane R. E. (1975) Preparation and purification of polymerized actin from sea urchin egg extracts. J. Cell Biol. 66, 305-315.
20. Katoh K., Hammer K., Smith P. J. S. and Oldenbourg R. (1999) Birefringence imaging directly reveals architectural dynamics of filamentous actin in living growth cones. Mol. Biol. Cell 10, 197-210.
21. Kodama T., Fukui K. and Kometani K. (1986) The initial phosphate burst in ATP hydrolysis by myosin and subfragment-1 as studied by a modified malachite green method for determination of inorganic phosphate. J. Biochem. (Tokyo) 99, 1465-1472.
22. Kureishy N., Sapountzi V., Prag S., Anilkumar N. and Adams J. C. (2002) Fascins, and their roles in cell structure and function. Bioessays 24, 350-361.
23. Lau P.-M., Zucker R. S. and Bentley D. (1999) Induction of filopodia by direct local elevation of intracellular calcium ion concentration. J. Cell Biol. 145, 1265-1275.
24. Lewis A. K. and Bridgman P. C. (1992) Nerve growth cone lamellipodia contain two populations of actin filaments that differ in organization and polarity. J. Cell Biol. 119, 1219-1243.
25. Lin C. H., Espreafico E. M., Mooseker M. S. and Forscher P. (1996) Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron 16, 769-782.
26. Mallavarapu A. and Mitchison T. (1999) Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J. Cell Biol. 146, 1097-1106.
27. Marsh L. and Letourneau P. C. (1984) Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B. J. Cell Biol. 99, 2041-2047.
28. Matsumura F., Yamashiro-Matsumura S. and Lin J. J.-C. (1982) Isolation and characterization of tropomyosin-containing microfilaments from cultured cells. J. Biol. Chem. 258, 6636-6644.
29. Neely M. D. and Gesemann M. (1994) Disruption of microfilaments in growth cones following depolarization and calcium influx. J. Neurosci. 14, 7511-7520.
30. Okabe S. and Hirokawa N. (1991) Actin dynamics in growth cone. J. Neurosci. 11, 1918-1929.
31. Ono S., Yamakita Y., Yamashiro S., Matsudaira P. T., Gnara J. R., Obinata T. and Matsumura F. (1997) Identification of an actin binding region and a protein kinase C phosphorylation site on human fascin. J. Biol. Chem. 272, 2527-2533.
32. Otto J. J. (1994) Actin-bundling proteins. Curr. Opin. Cell Biol. 6, 105-109.
33. Otto J. J., Kane R. E. and Bryan J. (1979) Formation of filopodia in coelomocytes: localization of fascin, a 58,000 dalton actin crosslinking protein. Cell 17, 285-293.
34. Pato M. D., Sellers J. R., Preston Y. A., Harvey E. V. and Adelstein R. S. (1996) Baculovirus expression of chicken nonmuscle heavy meromyosin II-B. J. Biol. Chem. 271, 2689-2695.
35. Perry S. V. (1955) Myosin adenosintriphosphatase. Meth. Enzymol. 2, 582-588.
36. Rohatgi R., Ho H. Y. and Kirschner M. W. (2000) Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4,5-biphosphate. J. Cell Biol. 150, 117-120.
37. Sakamoto T., Amitani I., Yokota E. and Ando T. (2000) Direct observation of processive movement by individual myosin V molecules. Biochem. Biophys. Res. Commun. 272, 586-590.
38. Sasaki Y., Hayashi K., Shirao T., Ishikawa R. and Kohama K. (1996) Inhibition by drebrin of the actin-bundling activity of brain fascin, a protein localized in filopodia of growth cones. J. Neurochem. 66, 980-988.
39. Steketee M. B. and Tosney K. W. (2002) Three functionally distinct adhesions in filopodia: shaft adhesions control lamellar extension. J. Neurosci. 22, 8071-8083.
40. Steketee M., Balazovich K. and Tosney K. W. (2001) Filopodial initiation and a novel filament-organizing center, the focal ring. Mol. Biol. Cell 12, 2378-2395.
41. Svitkina T. M. and Borisy G. G. (1999) Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J. Cell Biol. 145, 1009-1026.
42. Svitkina T. M., Bulanova E. A., Chaga O. Y., Vignjevic D. M., Kojima S., Vasiliev J. M. and Borisy G. G. (2003) Mechanism of filopodia initiation by reorganization of a dendritic network. J. Cell Biol. 160, 409-421.
43. Tilney L. G., Tilney M. S. and Guild G. M. (1995) F actin bundles in Drosophila bristles. I. Two filament cross-links are involved in bundling. J. Cell Biol. 130, 629-638.
44. Toyoshima Y., Kron S. J., McNally E. M., Niebling K. R., Toyoshima C. and Spudich J. A. (1987) Myosin subfragment-1 is sufficient to move actin filaments in vitro. Nature 328, 536-539.
45. Tseng Y., Fedorov E., McCaffery J. M., Almo S. C. and Wirtz D. (2001) Micromechnics and ultrastructure of actin filament networks crosslinked by human fascin: a comparison with α-actinin. J. Mol. Biol. 310, 351-366.
46. Wang F.-S., Wolenski J. S., Cheney R. E., Mooseker M. S. and Jay D. G. (1996) Function of myosin-V in filopodial extension of neuronal growth cones. Science 273, 660-663.
47. Wylie S. R. and Chantler P. D. (2001) Separate but linked functions of conventional myosins modulate adhesion and neurite outgrowth. Nat. Cell Biol. 3, 88-92.
48. Wylie S. R., Wu F.-J., Patel H. and Chantler P. D. (1998) A conventional myosin motor drives neurite outgrowth. Proc. Natl Acad. Sci. USA 95, 12967-12972.
49. Yamashiro-Matsumura S. and Matsumura F. (1985) Purification and characterization of an F-actin-bundling 55-kilodalton protein from HeLa cells. J. Biol. Chem. 260, 5087-5097.
50. Zheng J. Q. (2000) Turning of nerve growth cones induced by localized increases in intracellular calcium ions. Nature 403, 89-93.
51. Zheng J. Q., Felder M., Connor J. A. and Poo M.-M. (1994) Turning of nerve growth cones induced by neurotransmitters. Nature 368, 140-144.
52. Zhou F. Q. and Cohan C. S. (2001) Growth cone collapse through coincident loss of actin bundles and leading edge actin without actin depolymerization. J. Cell Biol. 153, 1071-1084.