Ena drives invasive macrophage migration in Drosophila embryos

DMM Disease Models and Mechanisms

Volumn 4, Issue 1, 2011, Pages 126-134

  Tucker, Philippa K ^a   Evans, Iwan R ^a   Wood, Will ^a  

^a University of Bath   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; PROTEIN ENABLED; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ANIMAL CELL; ARTICLE; BLOOD CELL; BREAST CANCER; CANCER CELL; CELL MIGRATION; CELL MOTILITY; DISEASE COURSE; DROSOPHILA; DYNAMICS; EMBRYO; FIBROBLAST; GENE OVEREXPRESSION; IN VITRO STUDY; MACROPHAGE MIGRATION; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN LOCALIZATION; UPREGULATION;

ACTINS; ANIMALS; BEHAVIOR, ANIMAL; CELL MOVEMENT; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; EMBRYO, NONMAMMALIAN; HEMOCYTES; MACROPHAGES; PROTEIN TRANSPORT; PSEUDOPODIA;

ENA;

EID: 78650874285     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.005694     Document Type: Article

References (58)

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. Ahern-Djamali, S. M., Comer, A. R., Bachmann, C., Kastenmeier, A. S., Reddy, S. K., Beckerle, M. C., Walter, U. and Hoffmann, F. M. (1998). Mutations in Drosophila enabled and rescue by human vasodilator-stimulated phosphoprotein (VASP) indicate important functional roles for Ena/VASP homology domain 1 (EVH1) and EVH2 domains. Mol. Biol. Cell 9, 2157-2171.
3. Applewhite, D. A., Barzik, M., Kojima, S., 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.
4. 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.
5. Bashaw, G. J., Kidd, T., Murray, D., Pawson, T. and Goodman, C. S. (2000). Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101, 703-715.
6. 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.
7. Bear, J. E., Svitkina, T. M., Krause, M., Schafer, D. A., Loureiro, J. J., Strasser, G. A., Maly, I. V., Chaga, O. Y., Cooper, J. A., Borisy, G. G. et al. (2002). Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109, 509-521.
8. 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.
9. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
10. Brantley-Sieders, D. M., Zhuang, G., Hicks, D., Fang, W. B., Hwang, Y., Cates, J. M., Coffman, K., Jackson, D., Bruckheimer, E., Muraoka-Cook, R. S. et al. (2008). The receptor tyrosine kinase EphA2 promotes mammary adenocarcinoma tumorigenesis and metastatic progression in mice by amplifying ErbB2 signaling. J. Clin. Invest. 118, 64-78.
11. 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. (Pubitemid 39172689)
12. Castrillon, D. H. and Wasserman, S. A. (1994). Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 120, 3367-3377.
13. Delon, I. and Brown, N. H. (2009). The integrin adhesion complex changes its composition and function during morphogenesis of an epithelium. J. Cell Sci. 122, 4363-4374.
14. Di Modugno, F., Bronzi, G., Scanlan, M. J., Del Bello, D., Cascioli, S., Venturo, I., Botti, C., Nicotra, M. R., Mottolese, M., Natali, P. G. et al. (2004). Human Mena protein, a serex-defined antigen overexpressed in breast cancer eliciting both humoral and CD8+ T-cell immune response. Int. J. Cancer 109, 909-918.
15. Evans, I. R., Renne, T., Gertler, F. B. and Nobes, C. D. (2007). Ena/VASP proteins mediate repulsion from ephrin ligands. J. Cell Sci. 120, 289-298.
16. Evans, I. R., Hu, N., Skaer, H. and Wood, W. (2010). Interdependence of macrophage migration and ventral nerve cord development in Drosophila embryos. Development 137, 1625-1633.
17. Franz, C. M., Jones, G. E. and Ridley, A. J. (2002). Cell migration in development and disease. Dev. Cell 2, 153-158.
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., 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. Gertler, F. B., Doctor, J. S. and Hoffmann, F. M. (1990). Genetic suppression of mutations in the Drosophila abl proto-oncogene homolog. Science 248, 857-860.
21. Gertler, F. B., Comer, A. R., Juang, J. L., Ahern, S. M., Clark, M. J., Liebl, E. C. and Hoffmann, F. M. (1995). enabled, a dosage-sensitive suppressor of mutations in the Drosophila Abl tyrosine kinase, encodes an Abl substrate with SH3 domain-binding properties. Genes Dev. 9, 521-533.
22. Gertler, F. B., Niebuhr, K., Reinhard, M., Wehland, J. and Soriano, P. (1996). Mena, a relative of VASP and Drosophila Enabled, is implicated in the control of microfilament dynamics. Cell 87, 227-239.
23. Hanahan, D. and Weinberg, R. A. (2000). The hallmarks of cancer. Cell 100, 57-70.
24. Hinz, B., Alt, W., Johnen, C., Herzog, V. and Kaiser, H. W. (1999). Quantifying lamella dynamics of cultured cells by SACED, a new computer-assisted motion analysis. Exp. Cell Res. 251, 234-243.
25. Homem, C. C. and Peifer, M. (2009). Exploring the roles of diaphanous and enabled activity in shaping the balance between filopodia and lamellipodia. Mol. Biol. Cell 20, 5138-5155.
26. Huelsmann, S., Hepper, C., Marchese, D., Knoll, C. and Reuter, R. (2006). The PDZGEF dizzy regulates cell shape of migrating macrophages via Rap1 and integrins in the Drosophila embryo. Development 133, 2915-2924.
27. Kaufmann, S., Kuphal, S., Schubert, T. and Bosserhoff, A. K. (2009). Functional implication of Netrin expression in malignant melanoma. Cell Oncol. 31, 415-422.
28. Lammermann, T., Bader, B. L., Monkley, S. J., Worbs, T., Wedlich-Soldner, R., Hirsch, K., Keller, M., Forster, R., Critchley, D. R., Fassler, R. et al. (2008). Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453, 51-55.
29. Lanier, L. M., Gates, M. A., Witke, W., Menzies, A. S., Wehman, A. M., Macklis, J. D., Kwiatkowski, D., Soriano, P. and Gertler, F. B. (1999). Mena is required for neurulation and commissure formation. Neuron 22, 313-325.
30. 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.
31. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461. (Pubitemid 29159845)
32. Legg, J. A., Herbert, J. M., Clissold, P. and Bicknell, R. (2008). Slits and Roundabouts in cancer, tumour angiogenesis and endothelial cell migration. Angiogenesis 11, 13-21.
33. Luo, L., Liao, Y. J., Jan, L. Y. and Jan, Y. N. (1994). Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8, 1787-1802.
34. Mauro, L. V., Grossoni, V. C., Urtreger, A. J., Yang, C., Colombo, L. L., Morandi, A., Pallotta, M. G., Kazanietz, M. G., Bal de Kier Joffe, E. D. and Puricelli, L. L. (2010). PKC Delta (PKCdelta) promotes tumoral progression of human ductal pancreatic cancer. Pancreas 39, e31-e41.
35. Millard, T. H. and Martin, P. (2008). Dynamic analysis of filopodial interactions during the zippering phase of Drosophila dorsal closure. Development 135, 621-626.
36. Moreira, S., Stramer, B., Evans, I., Wood, W. and Martin, P. (2010). Prioritization of competing damage and developmental signals by migrating macrophages in the Drosophila embryo. Curr. Biol. 20, 464-470.
37. Philippar, U., Roussos, E. T., Oser, M., Yamaguchi, H., Kim, H. D., Giampieri, S., Wang, Y., Goswami, S., Wyckoff, J. B., Lauffenburger, D. A. et al. (2008). A Mena invasion isoform potentiates EGF-induced carcinoma cell invasion and metastasis. Dev. Cell 15, 813-828.
38. Pollard, T. D. and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
39. Ridley, A. J., Paterson, H. F., Johnston, C. L., Diekmann, D. and Hall, A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410.
40. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T. and Horwitz, A. R. (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709.
41. Siekhaus, D., Haesemeyer, M., Moffitt, O. and Lehmann, R. (2010). RhoL controls invasion and Rap1 localization during immune cell transmigration in Drosophila. Nat. Cell Biol. 12, 605-610.
42. Small, J. V., Stradal, T., Vignal, E. and Rottner, K. (2002). The lamellipodium: where motility begins. Trends Cell Biol. 12, 112-120.
43. Srinivasan, D., Sims, J. T. and Plattner, R. (2008). Aggressive breast cancer cells are dependent on activated Abl kinases for proliferation, anchorage-independent growth and survival. Oncogene 27, 1095-1105.
44. 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.
45. 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.
46. Tepass, U., Fessler, L. I., Aziz, A. and Hartenstein, V. (1994). Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120, 1829-1837.
47. Toyoda, A., Kawana, H., Azuhata, K., Yu, J., Omata, A., Kishi, H., Higashi, M. and Harigaya, K. (2009). Aberrant expression of human ortholog of mammalian enabled (hMena) in human colorectal carcinomas: implications for its role in tumor progression. Int. J. Oncol. 34, 53-60.
48. Urbano, J. M., Torgler, C. N., Molnar, C., Tepass, U., Lopez-Varea, A., Brown, N. H., de Celis, J. F. and Martin-Bermudo, M. D. (2009). Drosophila laminins act as key regulators of basement membrane assembly and morphogenesis. Development 136, 4165-4176.
49. Vlisidou, I., Dowling, A. J., Evans, I. R., Waterfield, N., ffrench-Constant, R. H. and Wood, W. (2009). Drosophila embryos as model systems for monitoring bacterial infection in real time. PLoS Pathog. 5, e1000518.
50. Wang, W., Goswami, S., Lapidus, K., Wells, A. L., Wyckoff, J. B., Sahai, E., Singer, R. H., Segall, J. E. and Condeelis, J. S. (2004). Identification and testing of a gene expression signature of invasive carcinoma cells within primary mammary tumors. Cancer Res. 64, 8585-8594.
51. Wentworth, J. K., Pula, G. and Poole, A. W. (2006). Vasodilator- stimulated phosphoprotein (VASP) is phosphorylated on Ser157 by protein kinase C-dependent and -independent mechanisms in thrombin-stimulated human platelets. Biochem. J. 393, 555-564.
52. Wills, Z., Bateman, J., Korey, C. A., Comer, A. and Van Vactor, D. (1999). The tyrosine kinase Abl and its substrate enabled collaborate with the receptor phosphatase Dlar to control motor axon guidance. Neuron 22, 301-312.
53. Wolf, K., Wu, Y. I., Liu, Y., Geiger, J., Tam, E., Overall, C., Stack, M. S. and Friedl, P. (2007). Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat. Cell Biol. 9, 893-904.
54. Wood, W. and Jacinto, A. (2005). Imaging cell movement during dorsal closure in Drosophila embryos. Methods Mol. Biol. 294, 203-210.
55. Wood, W., Jacinto, A., Grose, R., Woolner, S., Gale, J., Wilson, C. and Martin, P. (2002). Wound healing recapitulates morphogenesis in Drosophila embryos. Nat. Cell Biol. 4, 907-912. (Pubitemid 35331367)
56. 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.
57. Zanet, J., Stramer, B., Millard, T., Martin, P., Payre, F. and Plaza, S. (2009). Fascin is required for blood cell migration during Drosophila embryogenesis. Development 136, 2557-2565.
58. Zervas, C. G., Gregory, S. L. and Brown, N. H. (2001). Drosophila integrin-linked kinase is required at sites of integrin adhesion to link the cytoskeleton to the plasma membrane. J. Cell Biol. 152, 1007-1018.