Fascin is required for blood cell migration during Drosophila embryogenesis

Development

Volumn 136, Issue 15, 2009, Pages 2557-2565

  Zanet, Jennifer ^a,c   Stramer, Brain ^b,d   Millard, Thomas ^b,e   Martin, Paul ^b   Payre, François ^a,c   Plaza, Serge ^a,c  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c CNRS UMR5547   (France)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Actin; Drosophila; Fascin (Singed); Hemocytes; Migration; Wound healing

Indexed keywords

ACTIN; FASCIN; SERINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD CELL; CELL MIGRATION; CELL MOTILITY; CELL SHAPE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; UPREGULATION; WOUND HEALING;

AMINO ACID SEQUENCE; ANIMAL STRUCTURES; ANIMALS; BLOOD CELLS; CARRIER PROTEINS; CELL MOVEMENT; CELL POLARITY; CELL SURVIVAL; CYTOSKELETON; DROSOPHILA MELANOGASTER; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INFLAMMATION; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; MUTATION; OOGENESIS; ORGAN SPECIFICITY; PHOSPHORYLATION; PSEUDOPODIA; SERINE;

EID: 69049098975     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.036517     Document Type: Article

References (41)

1. Adams, J. C. (2004). Roles of fascin in cell adhesion and motility. Curr. Opin. Cell Biol. 16, 590-596.
2. Anilkumar, N., Parsons, M., Monk, R., Ng, T. and Adams, J. C. (2003). Interaction of fascin and protein kinase Calpha: a novel intersection in cell adhesion and motility. EMBO J. 22, 5390-5402.
3. Aratyn, Y. S., Schaus, T. E., Taylor, E. W. and Borisy, G. G. (2007). Intrinsic dynamic behavior of fascin in filopodia. Mol. Biol. Cell 18, 3928-3940.
4. Babcock, D. T., Brock, A. R., Fish, G. S., Wang, Y., Perrin, L., Krasnow, M. A. and Galko, M. J. (2008). Circulating blood cells function as a surveillance system for damaged tissue in Drosophila larvae. Proc. Natl. Acad. Sci. USA 105, 10017-10022.
5. Borghese, L., Fletcher, G., Mathieu, J., Atzberger, A., Eades, W. C., Cagan, R. L. and Rorth, P. (2006). Systematic analysis of the transcriptional switch inducing migration of border cells. Dev. Cell 10, 497-508.
6. Brock, A. R., Babcock, D. T. and Galko, M. J. (2008). Active cop, passive cop: developmental stage-specific modes of wound-induced blood cell recruitment in Drosophila. Fly (Austin) 2, 303-305.
7. Bruckner, K., Kockel, L., Duchek, P., Luque, C. M., Rorth, P. and Perrimon, N. (2004). The PDGF/VEGF receptor controls blood cell survival in Drosophila. Dev. Cell 7, 73-84.
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. and Cooley, L. (1996). Single amino acid mutations in Drosophila fascin disrupt actin bundling function in vivo. Genetics 143, 249-258.
10. 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.
11. Chanut-Delalande, H., Fernandes, I., Roch, F., Payre, F. and Plaza, S. (2006). Shavenbaby couples patterning to epidermal cell shape control. PLoS Biol. 4, e290.
12. Cohan, C. S., Welnhofer, E. A., Zhao, L., Matsumura, F. 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. De Arcangelis, A., Georges-Labouesse, E. and Adams, J. C. (2004). Expression of fascin-1, the gene encoding the actin-bundling protein fascin-1, during mouse embryogenesis. Gene Expr. Patterns 4, 637-643.
14. Delon, I., Chanut-Delalande, H. and Payre, F. (2003). The Ovo/ Shavenbaby transcription factor specifies actin remodelling during epidermal differentiation in Drosophila. Mech. Dev. 120, 747-758.
15. DeRosier, D. J. and Edds, K. T. (1980). Evidence for fascin cross-links between the actin filaments in coelomocyte filopodia. Exp. Cell Res. 126, 490-494.
16. Dickinson, W. J. and Thatcher, J. W. (1997). Morphogenesis of denticles and hairs in Drosophila embryos: involvement of actin-associated proteins that also affect adult structure. Cell Motil. Cytoskeleton 38, 9-21.
17. Dutta, D., Bloor, J. W., Ruiz-Gomez, M., VijayRaghavan, K. and Kiehart, D. P. (2002). Real-time imaging of morphogenetic movements in Drosophila using Gal4-UAS-driven expression of GFP fused to the actin-binding domain of moesin. Genesis 34, 146-151.
18. Guild, G. M., Connelly, P. S., Shaw, M. K. and Tilney, L. G. (1997). Actin filament cables in Drosophila nurse cells are composed of modules that slide passively past one another during dumping. J. Cell Biol. 138, 783-797.
19. Hashimoto, Y., Skacel, M. and Adams, J. C. (2005). Roles of fascin in human carcinoma motility and signaling: prospects for a novel biomarker? Int. J. Biochem. Cell Biol. 37, 1787-1804.
20. Hashimoto, Y., Parsons, M. and Adams, J. C. (2007). Dual actin-bundling and protein kinase C-binding activities of fascin regulate carcinoma cell migration downstream of Rac and contribute to metastasis. Mol. Biol. Cell 18, 4591-4602.
21. Hayashi, Y., Toda, K., Saibara, T., Okamoto, S., Osanai, M., Enzan, H. and Lee, G. H. (2008). Expression of fascin-1, an actin-bundling protein, in migrating hepatoblasts during rat liver development. Cell Tissue Res. 334, 219-226.
22. Lin-Jones, J. and Burnside, B. (2007). Retina-specific protein fascin 2 is an actin cross-linker associated with actin bundles in photoreceptor inner segments and calycal processes. Invest. Ophthalmol. Vis. Sci. 48, 1380-1388.
23. Mattila, P. K. and Lappalainen, P. (2008). Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9, 446-454.
24. Nemethova, M., Auinger, S. and Small, J. V. (2008). Building the actin cytoskeleton: filopodia contribute to the construction of contractile bundles in the lamella. J. Cell Biol. 180, 1233-1244.
25. Ono, S., Yamakita, Y., Yamashiro, S., Matsudaira, P. T., Gnarra, 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.
26. Paladi, M. and Tepass, U. (2004). Function of Rho GTPases in embryonic blood cell migration in Drosophila. J. Cell Sci. 117, 6313-6326.
27. Paterson, J. and O'Hare, K. (1991). Structure and transcription of the singed locus of Drosophila melanogaster. Genetics 129, 1073-1084.
28. Pollard, T. D. and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
29. Rottner, K., Behrendt, B., Small, J. V. and Wehland, J. (1999). VASP dynamics during lamellipodia protrusion. Nat. Cell Biol. 1, 321-322.
30. Stramer, B., Wood, W., Galko, M. J., Redd, M. J., Jacinto, A., Parkhurst, S. M. and Martin, P. (2005). Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration. J. Cell Biol. 168, 567-573.
31. Stramer, B., Winfield, M., Shaw, T., Millard, T. H., Woolner, S. and Martin, P. (2008). Gene induction following wounding of wild-type versus macrophage-deficient Drosophila embryos. EMBO Rep. 9, 465-471.
32. 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.
33. Tilney, L. G., Connelly, P. S., Vranich, K. A., Shaw, M. K. and Guild, G. M. (2000). Regulation of actin filament cross-linking and bundle shape in Drosophila bristles. J. Cell Biol. 148, 87-100.
34. Vignjevic, D. and Montagnac, G. (2008). Reorganisation of the dendritic actin network during cancer cell migration and invasion. Semin. Cancer Biol. 18, 12-22.
35. Vignjevic, D., Yarar, D., Welch, M. D., Peloquin, J., Svitkina, T. and Borisy, G. G. (2003). Formation of filopodia-like bundles in vitro from a dendritic network. J. Cell Biol. 160, 951-962.
36. Vignjevic, D., Kojima, S., Aratyn, Y., Danciu, O., Svitkina, T. and Borisy, G. G. (2006). Role of fascin in filopodial protrusion. J. Cell Biol. 174, 863-875.
37. Wada, Y., Abe, T., Takeshita, T., Sato, H., Yanashima, K. and Tamai, M. (2001). Mutation of human retinal fascin gene (FSCN2) causes autosomal dominant retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci. 42, 2395-2400.
38. Wood, W. and Jacinto, A. (2007). Drosophila melanogaster embryonic haemocytes: masters of multitasking. Nat. Rev. Mol. Cell Biol. 8, 542-551.
39. Wood, W., Faria, C. and Jacinto, A. (2006). Distinct mechanisms regulate hemocyte chemotaxis during development and wound healing in Drosophila melanogaster. J. Cell Biol. 173, 405-416.
40. Yamakita, Y., Ono, S., Matsumura, F. and Yamashiro, S. (1996). Phosphorylation of human fascin inhibits its actin binding and bundling activities. J. Biol. Chem. 271, 12632-12638.
41. Yamashiro, S., Yamakita, Y., Ono, S. and Matsumura, F. (1998). Fascin, an actin-bundling protein, induces membrane protrusions and increases cell motility of epithelial cells. Mol. Biol. Cell 9, 993-1006.