Exploring the roles of diaphanous and enabled activity in shaping the balance between filopodia and lamellipodia

Molecular Biology of the Cell

Volumn 20, Issue 24, 2009, Pages 5138-5155

  Homem, Catarina C F ^a   Peifer, Mark ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; MEMBRANE PROTEIN DIA; MEMBRANE PROTEIN ENA; RHO FACTOR; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ANIMAL CELL; ARTICLE; CELL TYPE; CONTROLLED STUDY; CYTOPLASM; DROSOPHILA; FILOPODIUM; IMMUNOPRECIPITATION; LAMELLIPODIUM; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ACTINS; ANIMALS; CARRIER PROTEINS; CELL ADHESION MOLECULES; CYTOPLASM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENZYME ACTIVATION; GENES, DOMINANT; IMMUNOPRECIPITATION; MICROFILAMENT PROTEINS; MORPHOGENESIS; PHENOTYPE; PHOSPHOPROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PSEUDOPODIA; RHO GTP-BINDING PROTEINS; SEQUENCE DELETION;

ENA;

EID: 73849120348     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-02-0144     Document Type: Article

References (60)

1. Afshar, K., Stuart, B., and Wasserman, S. A. (2000). Functional analysis of the Drosophila diaphanous FH protein in early embryonic development. Development 127, 1887-1897.
2. Akin, O., and Mullins, R. D. (2008). Capping protein increases the rate of actin-based motility by promoting filament nucleation by the Arp2/3 complex. Cell 133, 841-851.
3. Alberts, A. S. (2001). Identification of a carboxyl-terminal diaphanous-related formin homology protein autoregulatory domain. J. Biol. Chem. 276, 2824-2830.
4. Applewhite, D. A., Barzik, M., Kojima, S. I., Svitkina, T. M., Gertler, F. B., and Borisy, G. G. (2007). Ena/VASP proteins have an anti-capping independent function in filopodia formation. Mol. Biol. Cell 18, 2579-2591.
5. Bachmann, C., Fischer, L., Walter, U., and Reinhard, M. (1999). The EVH2 domain of the vasodilator-stimulated phosphoprotein mediates tetramerization, F-actin binding, and actin bundle formation. J. Biol. Chem. 274, 23549-23557.
6. Barzik, M., Kotova, T. I., Higgs, H. N., Hazelwood, L., Hanein, D., Gertler, F. B., and Schafer, D. A. (2005). Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J. Biol. Chem. 280, 28653-28662.
7. Bear, J. E., Loureiro, J. J., Libova, I., Fassler, R., Wehland, J., and Gertler, F. B. (2000). Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 101, 717-728.
8. Bear, J. E., et al. (2002). Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109, 509-521.
9. Beli, P., Mascheroni, D., Xu, D., and Innocenti, M. (2008). WAVE and Arp2/3 jointly inhibit filopodium formation by entering into a complex with mDia2. Nat. Cell Biol. 10, 849-857.
10. Block, J., Stradal, T. E., Hanisch, J., Geffers, R., Kostler, S. A., Urban, E., Small, J. V., Rottner, K., and Faix, J. (2008). Filopodia formation induced by active mDia2/Drf3. J. Microsc. 231, 506-517.
11. Bloor, J. W., and Kiehart, D. P. (2002). Drosophila RhoA regulates the cytoskeleton and cell-cell adhesion in the developing epidermis. Development 129, 3173-3183.
12. Brandt, D. T., Marion, S., Griffiths, G., Watanabe, T., Kaibuchi, K., and Grosse, R. (2007). Dia1 and IQGAP1 interact in cell migration and phagocytic cup formation. J. Cell Biol. 178, 193-200.
13. Breitsprecher, D., Kiesewetter, A. K., Linkner, J., Urbanke, C., Resch, G. P., Small, J. V., and Faix, J. (2008). Clustering of VASP actively drives processive, WH2 domain-mediated actin filament elongation. EMBO J. 27, 2943-2954.
14. Carramusa, L., Ballestrem, C., Zilberman, Y., and Bershadsky, A. D. (2007). Mammalian diaphanous-related formin Dia1 controls the organization of E-cadherin-mediated cell-cell junctions. J. Cell Sci. 120, 3870-3882.
15. Dent, E. W., et al. (2007). Filopodia are required for cortical neurite initiation. Nat. Cell Biol. 9, 1347-1359.
16. Faix, J., and Grosse, R. (2006). Staying in shape with formins. Dev. Cell 10, 693-706.
17. Faix, J., and Rottner, K. (2006). The making of filopodia. Curr. Opin. Cell Biol. 18, 18-25.
18. Gates, J., Mahaffey, J. P., Rogers, S. L., Emerson, M., Rogers, E. M., Sottile, S. L., Van Vactor, D., Gertler, F. B., and Peifer, M. (2007). Enabled plays key roles in embryonic epithelial morphogenesis in Drosophila. Development 134, 2027-2039.
19. Gates, J., Nowotarski, S. H., Yin, H., Mahaffey, J. P., Bridges, T., Herrera, C., Homem, C.C.F., Janody, F., Montell, D. J., and Peifer, M. (2009). Enabled and Capping protein play important roles in shaping cell behavior during Drosophila oogenesis. Dev. Biol. 333, 90-107.
20. Goode, B. L., and Eck, M. J. (2007). Mechanism and function of formins in the control of actin assembly. Annu. Rev. Biochem. 76, 593-627.
21. Gorfinkiel, N., and Martinez-Arias, A. (2007). Requirements for adherens junction components in the interaction between epithelial tissues during dorsal closure in Drosophila. J. Cell Sci. 120, 3289-3298.
22. Grosse, R., Copeland, J. W., Newsome, T. P., Way, M., and Treisman, R. (2003). A role for VASP in RhoA-Diaphanous signalling to actin dynamics and SRF activity. EMBO J. 22, 3050-3061.
23. Homem, C. C., and Peifer, M. (2008). Diaphanous regulates myosin and adherens junctions to control cell contractility and protrusive behavior during morphogenesis. Development 135, 1005-1018.
24. Huttelmaier, S., Harbeck, B., Steffens, O., Messerschmidt, T., Illenberger, S., and Jockusch, B. M. (1999). Characterization of the actin binding properties of the vasodilator-stimulated phosphoprotein VASP. FEBS Lett. 451, 68-74.
25. Jacinto, A., Wood, W., Balayo, T., Turmaine, M., Martinez-Arias, A., and Martin, P. (2000). Dynamic actin-based epithelial adhesion and cell matching during Drosophila dorsal closure. Curr. Biol. 10, 1420-1426.
26. Korobova, F., and Svitkina, T. (2008). Arp2/3 complex is important for filopodia formation, growth cone motility, and neuritogenesis in neuronal cells. Mol. Biol. Cell 19, 1561-1574.
27. Krause, M., et al. (2004). Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev. Cell 7, 571-583.
28. Lacayo, C. I., Pincus, Z., VanDuijn, M. M., Wilson, C. A., Fletcher, D. A., Gertler, F. B., Mogilner, A., and Theriot, J. A. (2007). Emergence of large-scale cell morphology and movement from local actin filament growth dynamics. PLoS Biol. 5, e233.
29. Laurent, V., Loisel, T. P., Harbeck, B., Wehman, A., Grobe, L., Jockusch, B. M., Wehland, J., Gertler, F. B., and Carlier, M. F. (1999). Role of proteins of the Ena/VASP family in actin-based motility of Listeria monocytogenes. J. Cell Biol. 144, 1245-1258.
30. Le Clainche, C., and Carlier, M. F. (2008). Regulation of actin assembly associated with protrusion and adhesion in cell migration. Physiol. Rev. 88, 489-513.
31. Lebrand, C., Dent, E. W., Strasser, G. A., Lanier, L. M., Krause, M., Svitkina, T. M., Borisy, G. G., and Gertler, F. B. (2004). Critical role of Ena/VASP proteins for filopodia formation in neurons and in function downstream of netrin-1. Neuron 42, 37-49.
32. Magie, C. R., Pinto-Santini, D., and Parkhurst, S. M. (2002). Rho1 interacts with p120(ctn) and alpha-catenin, and regulates cadherin- based adherens junction components in Drosophila. Development 129, 3771-3782.
33. Martin, P., and Parkhurst, S. M. (2004). Parallels between tissue repair and embryo morphogenesis. Development 131, 3021-3034.
34. Mattila, P. K., and Lappalainen, P. (2008). Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9, 446-454.
35. Mejillano, M. R., Kojima, S., Applewhite, D. A., Gertler, F. B., Svitkina, T. M., and Borisy, G. G. (2004). Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118, 363-373.
36. Nelson, W. J. (2008). Regulation of cell-cell adhesion by the cadherin-catenin complex. Biochem. Soc. Trans. 36, 149-155.
37. Pellegrin, S., and Mellor, H. (2005). The Rho family GTPase Rif induces filopodia through mDia2. Curr. Biol. 15, 129-133.
38. Peng, J., Wallar, B. J., Flanders, A., Swiatek, P. J., and Alberts, A. S. (2003). Disruption of the Diaphanous-related formin Drf1 gene encoding mDia1 reveals a role for Drf3 as an effector for Cdc42. Curr. Biol. 13, 534-545.
39. Pollard, T. D. (2007). Regulation of actin filament assembly by arp2/3 complex and formins. Annu. Rev. Biophys. Biomol. Struct. 36, 451-477.
40. Pollard, T. D., and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
41. Pruyne, D., Evangelista, M., Yang, C., Bi, E., Zigmond, S., Bretscher, A., and Boone, C. (2002). Role of formins in actin assembly: nucleation and barbed-end association. Science 297, 612-615.
42. Ridley, A. J. (2006). Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 16, 522-529.
43. Rorth, P. (1998). Gal4 in the Drosophila female germline. Mech. Dev. 78, 113-118.
44. Rose, R., Weyand, M., Lammers, M., Ishizaki, T., Ahmadian, M. R., and Wittinghofer, A. (2005). Structural and mechanistic insights into the interaction between Rho and mammalian Dia. Nature 435, 513-518.
45. Ryu, J. R., Echarri, A., Li, R., and Pendergast, A. M. (2009). Regulation of cell-cell adhesion by Abi/Diaphanous complexes. Mol. Cell Biol. 29, 1735-1748.
46. Sagot, I., Rodal, A. A., Moseley, J., Goode, B. L., and Pellman, D. (2002). An actin nucleation mechanism mediated by Bni1 and profilin. Nat. Cell Biol. 4, 626-631.
47. Samarin, S., Romero, S., Kocks, C., Didry, D., Pantaloni, D., and Carlier, M. F. (2003). How VASP enhances actin-based motility. J. Cell Biol. 163, 131-142.
48. Schirenbeck, A., Arasada, R., Bretschneider, T., Schleicher, M., and Faix, J. (2005a). Formins and VASPs may co-operate in the formation of filopodia. Biochem. Soc. Trans. 33, 1256-1259.
49. Schirenbeck, A., Arasada, R., Bretschneider, T., Stradal, T. E., Schleicher, M., and Faix, J. (2006). The bundling activity of vasodilator-stimulated phosphoprotein is required for filopodium formation. Proc. Natl. Acad. Sci. USA 103, 7694-7699.
50. Schirenbeck, A., Bretschneider, T., Arasada, R., Schleicher, M., and Faix, J. (2005b). The Diaphanous-related formin dDia2 is required for the formation and maintenance of filopodia. Nat. Cell Biol. 7, 619-625.
51. Scott, J. A., Shewan, A. M., den Elzen, N. R., Loureiro, J. J., Gertler, F. B., and Yap, A. S. (2006). Ena/VASP proteins can regulate distinct modes of actin organization at cadherin-adhesive contacts. Mol. Biol. Cell 17, 1085-1095.
52. Sheffield, M., Loveless, T., Hardin, J., and Pettitt, J. (2007). C. elegans Enabled exhibits novel interactions with N-WASP, Abl, and cell-cell junctions. Curr. Biol. 17, 1791-1796.
53. Somogyi, K., and Rorth, P. (2004). Evidence for tension-based regulation of Drosophila MAL and SRF during invasive cell migration. Dev. Cell 7, 85-93.
54. Steffen, A., Faix, J., Resch, G. P., Linkner, J., Wehland, J., Small, J. V., Rottner, K., and Stradal, T. E. (2006). Filopodia formation in the absence of functional WAVE- and Arp2/3-complexes. Mol. Biol. Cell 17, 2581-2591.
55. 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.
56. Vasioukhin, V., Bauer, C., Yin, M., and Fuchs, E. (2000). Directed actin polymerization is the driving force for epithelial cell- cell adhesion. Cell 100, 209-219.
57. Yang, C., Czech, L., Gerboth, S., Kojima, S., Scita, G., and Svitkina, T. (2007). Novel roles of formin mDia2 in lamellipodia and filopodia formation in motile cells. PLoS Biol. 5, e317.
58. Zigmond, S. H. (2004a). Beginning and ending an actin filament: control at the barbed end. Curr. Top. Dev. Biol. 63, 145-188.
59. Zigmond, S. H. (2004b). Formin-induced nucleation of actin filaments. Curr. Opin. Cell Biol. 16, 99-105.
60. Zigmond, S. H., Evangelista, M., Boone, C., Yang, C., Dar, A. C., Sicheri, F., Forkey, J., and Pring, M. (2003). Formin leaky cap allows elongation in the presence of tight capping proteins. Curr. Biol. 13, 1820-1823.