Filopodia are dispensable for endothelial tip cell guidance

Development (Cambridge)

Volumn 140, Issue 19, 2013, Pages 4031-4040

  Phng, Li Kun ^a,b   Stanchi, Fabio ^a,b   Gerhardt, Holger ^a,b,c  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Actin; Angiogenesis; Endothelial cell; Filopodia; Zebrafish

Indexed keywords

F ACTIN; LATRUNCULIN B;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; BLOOD VESSEL SHUNT; BRANCHIAL ARCH; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOPLASM; ENDOTHELIUM CELL; FILOPODIUM; IMAGE PROCESSING; INHIBITION KINETICS; MACROPHAGE; MICROENVIRONMENT; MOLECULAR DYNAMICS; NERVE CELL; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; VELOCITY; ZEBRA FISH;

ACTIN; ANGIOGENESIS; ENDOTHELIAL CELL; FILOPODIA; ZEBRAFISH;

ACTINS; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; ENDOTHELIAL CELLS; NEOVASCULARIZATION, PHYSIOLOGIC; PSEUDOPODIA; THIAZOLIDINES; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84884258983     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.097352     Document Type: Article

References (53)

1. Adams, R. H. and Eichmann, A. (2010). Axon guidance molecules in vascular patterning. Cold Spring Harb. Perspect. Biol. 2, a001875.
2. Arjonen, A., Kaukonen, R. and Ivaska, J. (2011). Filopodia and adhesion in cancer cell motility. Cell Adh. Migr. 5, 421-430.
3. Bayless, K. J. and Johnson, G. A. (2011). Role of the cytoskeleton in formation and maintenance of angiogenic sprouts. J. Vasc. Res. 48, 369-385.
4. Bentley, D. and Toroian-Raymond, A. (1986). Dioriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment. Nature 323, 712-715.
5. Biyasheva, A., Svitkina, T., Kunda, P., Baum, B. and Borisy, G. (2004). Cascade pathway of filopodia formation downstream of SCAR. J. Cell Sci. 117, 837-848.
6. Blum, Y., Belting, H.-G., Ellertsdottir, E., Herwig, L., Lüders, F. and Affolter, M. (2008). Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Dev. Biol. 316, 312-322.
7. Chhabra, E. S. and Higgs, H. N. (2007). The many faces of actin: matching assembly factors with cellular structures. Nat. Cell Biol. 9, 1110-1121.
8. Chien, C. B., Rosenthal, D. E., Harris, W. A. and Holt, C. E. (1993). Navigational errors made by growth cones without filopodia in the embryonic Xenopus brain. Neuron 11, 237-251.
9. Childs, S., Chen, J.-N., Garrity, D. M. and Fishman, M. C. (2002). Patterning of angiogenesis in the zebrafish embryo. Development 129, 973-982.
10. Covassin, L. D., Villefranc, J. A., Kacergis, M. C., Weinstein, B. M. and Lawson, N. D. (2006). Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish. Proc. Natl. Acad. Sci. USA 103, 6554-6559.
11. De Smet, F., Segura, I., De Bock, K., Hohensinner, P. J. and Carmeliet, P. (2009). Mechanisms of vessel branching: filopodia on endothelial tip cells lead the way. Arterioscler. Thromb. Vasc. Biol. 29, 639-649.
12. Faix, J. and Rottner, K. (2006). The making of filopodia. Curr. Opin. Cell Biol. 18, 18-25.
13. Fraccaroli, A., Franco, C. A., Rognoni, E., Neto, F., Rehberg, M., Aszodi, A., Wedlich-Söldner, R., Pohl, U., Gerhardt, H. and Montanez, E. (2012). Visualization of endothelial actin cytoskeleton in the mouse retina. PLoS ONE 7, e47488.
14. Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D. et al. (2003). VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177.
15. Helbling, P. M., Saulnier, D. M. and Brändli, A. W. (2000). The receptor tyrosine kinase EphB4 and ephrin-B ligands restrict angiogenic growth of embryonic veins in Xenopus laevis. Development 127, 269-278.
16. Herwig, L., Blum, Y., Krudewig, A., Ellertsdottir, E., Lenard, A., Belting, H.-G. and Affolter, M. (2011). Distinct cellular mechanisms of blood vessel fusion in the zebrafish embryo. Curr. Biol. 21, 1942-1948.
17. Hogan, B. M., Bos, F. L., Bussmann, J., Witte, M., Chi, N. C., Duckers, H. J. and Schulte-Merker, S. (2009a). Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat. Genet. 41, 396-398.
18. Hogan, B. M., Herpers, R., Witte, M., Heloterä, H., Alitalo, K., Duckers, H. J. and Schulte-Merker, S. (2009b). Vegfc/Flt4 signalling is suppressed by Dll4 in developing zebrafish intersegmental arteries. Development 136, 4001-4009.
19. Isogai, S., Horiguchi, M. and Weinstein, B. M. (2001). The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Dev. Biol. 230, 278-301.
20. Isogai, S., Lawson, N. D., Torrealday, S., Horiguchi, M. and Weinstein, B. M. (2003). Angiogenic network formation in the developing vertebrate trunk. Development 130, 5281-5290.
21. 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.
22. Kapustina, M., Elston, T. C. and Jacobson, K. (2013). Compression and dilation of the membrane-cortex layer generates rapid changes in cell shape. J. Cell Biol. 200, 95-108.
23. Kim, J.-D., Kang, H., Larrivée, B., Lee, M. Y., Mettlen, M., Schmid, S. L., Roman, B. L., Qyang, Y., Eichmann, A. and Jin, S.-W. (2012). Contextdependent proangiogenic function of bone morphogenetic protein signaling is mediated by disabled homolog 2. Dev. Cell 23, 441-448.
24. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
25. Kolodkin, A. L. and Tessier-Lavigne, M. (2011). Mechanisms and molecules of neuronal wiring: a primer. Cold Spring Harb. Perspect. Biol. 3, a001727.
26. Krueger, J., Liu, D., Scholz, K., Zimmer, A., Shi, Y., Klein, C., Siekmann, A., Schulte-Merker, S., Cudmore, M., Ahmed, A. et al. (2011). Flt1 acts as a negative regulator of tip cell formation and branching morphogenesis in the zebrafish embryo. Development 138, 2111-2120.
27. Kwan, K. M., Fujimoto, E., Grabher, C., Mangum, B. D., Hardy, M. E., Campbell, D. S., Parant, J. M., Yost, H. J., Kanki, J. P. and Chien, C.-B. (2007). The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236, 3088-3099.
28. Lawson, N. D. and Weinstein, B. M. (2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318.
29. Leslie, J. D., Ariza-McNaughton, L., Bermange, A. L., McAdow, R., Johnson, S. L. and Lewis, J. (2007). Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development 134, 839-844.
30. Lu, X., Le Noble, F., Yuan, L., Jiang, Q., De Lafarge, B., Sugiyama, D., Bréant, C., Claes, F., De Smet, F., Thomas, J.-L. et al. (2004). The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 432, 179-186.
31. Mattila, P. K. and Lappalainen, P. (2008). Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9, 446-454.
32. Mellor, H. (2010). The role of formins in filopodia formation. Biochim. Biophys. Acta 1803, 191-200.
33. Millard, T. H. and Martin, P. (2008). Dynamic analysis of filopodial interactions during the zippering phase of Drosophila dorsal closure. Development 135, 621-626.
34. Morton, W. M., Ayscough, K. R. and McLaughlin, P. J. (2000). Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat. Cell Biol. 2, 376-378.
35. Phng, L. K. and Gerhardt, H. (2009). Angiogenesis: a team effort coordinated by notch. Dev. Cell 16, 196-208.
36. Pollard, T. D. and Cooper, J. A. (2009). Actin, a central player in cell shape and movement. Science 326, 1208-1212.
37. Preibisch, S., Saalfeld, S. and Tomancak, P. (2009). Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics 25, 1463-1465.
38. Ridley, A. J. (2011). Life at the leading edge. Cell 145, 1012-1022.
39. Riedl, J., Crevenna, A. H., Kessenbrock, K., Yu, J. H., Neukirchen, D., Bista, M., Bradke, F., Jenne, D., Holak, T. A., Werb, Z. et al. (2008). Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5, 605-607.
40. Riedl, J., Flynn, K. C., Raducanu, A., Gärtner, F., Beck, G., Bösl, M., Bradke, F., Massberg, S., Aszodi, A., Sixt, M. et al. (2010). Lifeact mice for studying Factin dynamics. Nat. Methods 7, 168-169.
41. Roman, B. L., Pham, V. N., Lawson, N. D., Kulik, M., Childs, S., Lekven, A. C., Garrity, D. M., Moon, R. T., Fishman, M. C., Lechleider, R. J. et al. (2002). Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels. Development 129, 3009-3019.
42. Rymo, S. F., Gerhardt, H., Wolfhagen Sand, F., Lang, R., Uv, A. and Betsholtz, C. (2011). A two-way communication between microglial cells and angiogenic sprouts regulates angiogenesis in aortic ring cultures. PLoS ONE 6, e15846.
43. Salbreux, G., Charras, G. and Paluch, E. (2012). Actin cortex mechanics and cellular morphogenesis. Trends Cell Biol. 22, 536-545.
44. Schäfer, C., Faust, U., Kirchgeßner, N., Merkel, R. and Hoffmann, B. (2011). The filopodium: a stable structure with highly regulated repetitive cycles of elongation and persistence depending on the actin cross-linker fascin. Cell Adh. Migr. 5, 431-438.
45. Sedzinski, J., Biro, M., Oswald, A., Tinevez, J.-Y., Salbreux, G. and Paluch, E. (2011). Polar actomyosin contractility destabilizes the position of the cytokinetic furrow. Nature 476, 462-466.
46. Siekmann, A. F. and Lawson, N. D. (2007). Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445, 781-784.
47. Thévenaz, P., Ruttimann, U. E. and Unser, M. (1998). A pyramid approach to subpixel registration based on intensity. IEEE Trans. 7, 27-41.
48. Torres-Vázquez, J., Gitler, A. D., Fraser, S. D., Berk, J. D., Pham, Van N., Fishman, M. C., Childs, S., Epstein, J. A., Weinstein, B. M. (2004). Semaphorin-plexin signaling guides patterning of the developing vasculature. Dev. Cell 7, 117-123.
49. Wiley, D. M., Kim, J.-D., Hao, J., Hong, C. C., Bautch, V. L. and Jin, S.-W. (2011). Distinct signalling pathways regulate sprouting angiogenesis from the dorsal aorta and the axial vein. Nat. Cell Biol. 13, 686-692.
50. Wright, L. P. and Philips, M. R. (2006). Thematic review series: lipid posttranslational modifications. CAAX modification and membrane targeting of Ras. J. Lipid Res. 47, 883-891.
51. Yoo, S. K., Deng, Q., Cavnar, P. J., Wu, Y. I., Hahn, K. M. and Huttenlocher, A. (2010). Differential regulation of protrusion and polarity by PI3K during neutrophil motility in live zebrafish. Dev. Cell 18, 226-236.
52. Zheng, J. Q., Wan, J. J. and Poo, M. M. (1996). Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J. Neurosci. 16, 1140-1149.
53. Zygmunt, T., Gay, C. M., Blondelle, J., Singh, M. K., Flaherty, K. M., Means, P. C., Herwig, L., Krudewig, A., Belting, H.-G., Affolter, M. et al. (2011). Semaphorin-PlexinD1 signaling limits angiogenic potential via the VEGF decoy receptor sFlt1. Dev. Cell 21, 301-314.