A Rac/Cdc42 exchange factor complex promotes formation of lateral filopodia and blood vessel lumen morphogenesis

Nature Communications

Volumn 6, Issue , 2015, Pages

  Abraham, Sabu ^a,e   Scarcia, Margherita ^b,e   Bagshaw, Richard D ^c,f   McMahon, Kathryn ^b   Grant, Gary ^b   Harvey, Tracey ^b,g   Yeo, Maggie ^a   Esteves, Filomena O G ^b   Thygesen, Helene H ^b,h   Jones, Pamela F ^d   Speirs, Valerie ^b   Hanby, Andrew M ^b   Selby, Peter J ^b   Lorger, Mihaela ^b   Dear, T Neil ^d,i   Pawson, Tony ^c   Marshall, Christopher J ^a   Mavria, Georgia ^b  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF LEEDS   (United Kingdom)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f HOSPITAL FOR SICK CHILDREN   (Canada)

^g UNIVERSITY OF QUEENSLAND   (Australia)

^h NETHERLANDS CANCER INSTITUTE   (Netherlands)

ⁱ SOUTH AUSTRALIAN HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DEDICATOR OF CYTOKINESIS 4; DEDICATOR OF CYTOKINESIS 9; PROTEIN CDC42; RAC PROTEIN; RAC1 PROTEIN; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN; DOCK4 PROTEIN, HUMAN; DOCK9 PROTEIN, HUMAN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOG PROTEIN, HUMAN; VASCULOTROPIN A;

BLOOD; CELLS AND CELL COMPONENTS; CYTOLOGY; MORPHOGENESIS; PHYSIOLOGICAL RESPONSE; PROTEIN; SKELETON;

ANGIOGENESIS; ANGIOGENESIS ASSAY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CONTACT; CELL JUNCTION; COCULTURE; CONTROLLED STUDY; CYTOKINESIS; FIBROBLAST; FILOPODIA; MOUSE; NONHUMAN; PSEUDOPODIUM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR TUMOR; ANIMAL; C57BL MOUSE; CYTOSKELETON; HUMAN; KNOCKOUT MOUSE; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PHYSIOLOGY;

ANIMALS; CDC42 GTP-BINDING PROTEIN; CYTOSKELETON; GTPASE-ACTIVATING PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PSEUDOPODIA; RHO GTP-BINDING PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84935140511     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8286     Document Type: Article

References (54)

1. Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646-674 (2011).
2. Goel, S. et al. Normalization of the vasculature for treatment of cancer and other diseases. Physiol. Rev. 91, 1071-1121 (2011).
3. Eilken, H. M. & Adams, R. H. Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr. Opin. Cell Biol. 22, 617-625 (2010).
4. Abraham, S. et al. VE-Cadherin-mediated cell-cell interaction suppresses sprouting via signaling to MLC2 phosphorylation. Curr. Biol. 19, 668-674 (2009).
5. Gerhardt, H. et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177 (2003).
6. De Smet, F., Segura, I., De Bock, K., Hohensinner, P. J. & Carmeliet, P. Mechanisms of vessel branching: filopodia on endothelial tip cells lead the way. Arterioscler. Thromb. Vasc. Biol. 29, 639-649 (2009).
7. Phng, L. K., Stanchi, F. & Gerhardt, H. Filopodia are dispensable for endothelial tip cell guidance. Development 140, 4031-4040 (2013).
8. Almagro, S. et al. The motor protein myosin-X transports VE-cadherin along filopodia to allow the formation of early endothelial cell-cell contacts. Mol. Cell Biol. 30, 1703-1717 (2010).
9. Wacker, A. & Gerhardt, H. Endothelial development taking shape. Curr. Opin. Cell Biol. 23, 676-685 (2011).
10. Rousseau, S., Houle, F. & Huot, J. Integrating the VEGF signals leading to actin-based motility in vascular endothelial cells. Trends. Cardiovasc. Med. 10, 321-327 (2000).
11. Fan, Y. et al. Stimulus-dependent phosphorylation of profilin-1 in angiogenesis. Nat. Cell Biol. 14, 1046-1056 (2012).
12. Tan, W. et al. An essential role for Rac1 in endothelial cell function and vascular development. FASEB J. 22, 1829-1838 (2008).
13. Kaur, S. et al. RhoJ/TCL regulates endothelial motility and tube formation and modulates actomyosin contractility and focal adhesion numbers. Arterioscler. Thromb. Vasc. Biol. 31, 657-664 (2011).
14. Hoang, M. V., Whelan, M. C. & Senger, D. R. Rho activity critically and selectively regulates endothelial cell organization during angiogenesis. Proc. Natl Acad. Sci. USA 101, 1874-1879 (2004).
15. Mavria, G. et al. ERK-MAPK signaling opposes Rho-kinase to promote endothelial cell survival and sprouting during angiogenesis. Cancer Cell 9, 33-44 (2006).
16. Cote, J. F. & Vuori, K. GEF what? Dock180 and related proteins help Rac to polarize cells in new ways. Trends Cell Biol. 17, 383-393 (2007).
17. Ueda, S., Fujimoto, S., Hiramoto, K., Negishi, M. & Katoh, H. Dock4 regulates dendritic development in hippocampal neurons. J. Neurosci. Res. 86, 3052-3061 (2008).
18. Katoh, H., Hiramoto, K. & Negishi, M. Activation of Rac1 by RhoG regulates cell migration. J. Cell Sci. 119, 56-65 (2006).
19. Kawada, K. et al. Cell migration is regulated by platelet-derived growth factor receptor endocytosis. Mol. Cell Biol. 29, 4508-4518 (2009).
20. Bishop, E. T. et al. An in vitro model of angiogenesis: basic features. Angiogenesis 3, 335-344 (1999).
21. Strilic, B. et al. The molecular basis of vascular lumen formation in the developing mouse aorta. Dev. Cell 17, 505-515 (2009).
22. Gadea, G., Sanz-Moreno, V., Self, A., Godi, A. & Marshall, C. J. DOCK10-mediated Cdc42 activation is necessary for amoeboid invasion of melanoma cells. Curr. Biol. 18, 1456-1465 (2008).
23. Lee, S. H. & Dominguez, R. Regulation of actin cytoskeleton dynamics in cells. Mol. Cells 29, 311-325 (2010).
24. Morton, W. M., Ayscough, K. R. & McLaughlin, P. J. Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat. Cell Biol. 2, 376-378 (2000).
25. Nobes, C. D. & Hall, A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62 (1995).
26. Katoh, H. & Negishi, M. RhoG activates Rac1 by direct interaction with the Dock180-binding protein Elmo. Nature 424, 461-464 (2003).
27. Hiramoto, K., Negishi, M. & Katoh, H. Dock4 is regulated by RhoG and promotes Rac-dependent cell migration. Exp. Cell Res. 312, 4205-4216 (2006).
28. Terasawa, M. et al. Dimerization of DOCK2 is essential for DOCK2-mediated Rac activation and lymphocyte migration. PLoS ONE 7, e46277 (2012).
29. Komander, D. et al. An alpha-helical extension of the ELMO1 pleckstrin homology domain mediates direct interaction to DOCK180 and is critical in Rac signaling. Mol. Biol. Cell 19, 4837-4851 (2008).
30. Hanawa-Suetsugu, K. et al. Structural basis for mutual relief of the Rac guanine nucleotide exchange factor DOCK2 and its partner ELMO1 from their autoinhibited forms. Proc. Natl Acad. Sci. USA 109, 3305-3310 (2012).
31. Fradelizi, J. et al. ActA and human zyxin harbour Arp2/3-independent actin-polymerization activity. Nat. Cell Biol. 3, 699-707 (2001).
32. Castellano, F. et al. Inducible recruitment of Cdc42 or WASP to a cell-surface receptor triggers actin polymerization and filopodium formation. Curr. Biol. 9, 351-360 (1999).
33. Wykoff, C. C. et al. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res. 60, 7075-7083 (2000).
34. Meller, N., Merlot, S. & Guda, C. CZH proteins: a new family of Rho-GEFs. J. Cell Sci. 118, 4937-4946 (2005).
35. Krugmann, S. et al. Cdc42 induces filopodia by promoting the formation of an IRSp53:Mena complex. Curr. Biol. 11, 1645-1655 (2001).
36. Woolner, S., Jacinto, A. & Martin, P. The small GTPase Rac plays multiple roles in epithelial sheet fusion-dynamic studies of Drosophila dorsal closure. Dev. Biol. 282, 163-173 (2005).
37. Demarco, R. S., Struckhoff, E. C. & Lundquist, E. A. The Rac GTP exchange factor TIAM-1 acts with CDC-42 and the guidance receptor UNC-40/DCC in neuronal protrusion and axon guidance. PLoS Genet. 8, e1002665 (2012).
38. Yang, J., Zhang, Z., Roe, S. M., Marshall, C. J. & Barford, D. Activation of Rho GTPases by DOCK exchange factors is mediated by a nucleotide sensor. Science 325, 1398-1402 (2009).
39. Nemethova, M., Auinger, S. & Small, J. V. Building the actin cytoskeleton: filopodia contribute to the construction of contractile bundles in the lamella. J. Cell Biol. 180, 1233-1244 (2008).
40. Graupera, M. et al. Angiogenesis selectively requires the p110alpha isoform of PI3K to control endothelial cell migration. Nature 453, 662-666 (2008).
41. Gambardella, L. et al. PI3K signaling through the dual GTPase-activating protein ARAP3 is essential for developmental angiogenesis. Sci. Signal. 3, ra76 (2010).
42. Namekata, K., Enokido, Y., Iwasawa, K. & Kimura, H. MOCA induces membrane spreading by activating Rac1. J. Biol. Chem. 279, 14331-14337 (2004).
43. Vigorito, E. et al. Immunological function in mice lacking the Rac-related GTPase RhoG. Mol. Cell Biol. 24, 719-729 (2004).
44. Samson, T. et al. The guanine-nucleotide exchange factor SGEF plays a crucial role in the formation of atherosclerosis. PLoS ONE 8, e55202 (2013).
45. Iruela-Arispe, M. L. & Davis, G. E. Cellular and molecular mechanisms of vascular lumen formation. Dev. Cell 16, 222-231 (2009).
46. Kamei, M. et al. Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 442, 453-456 (2006).
47. Herwig, L. et al. Distinct cellular mechanisms of blood vessel fusion in the zebrafish embryo. Curr. Biol. 21, 1942-1948 (2011).
48. Pelton, J. C., Wright, C. E., Leitges, M. & Bautch, V. L. Multiple endothelial cells constitute the tip of developing blood vessels and polarize to promote lumen formation. Development 141, 4121-4126 (2014).
49. Blum, Y. et al. Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Dev. Biol. 316, 312-322 (2008).
50. Pankov, R. et al. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170, 793-802 (2005).
51. Nishikimi, A. et al. Zizimin2: a novel, DOCK180-related Cdc42 guanine nucleotide exchange factor expressed predominantly in lymphocytes. FEBS Lett. 579, 1039-1046 (2005).
52. Vial, E., Sahai, E. & Marshall, C. J. ERK-MAPK signaling coordinately regulates activity of Rac1 and RhoA for tumor cell motility. Cancer Cell 4, 67-79 (2003).
53. Self, A. J. & Hall, A. Purification of recombinant Rho/Rac/G25K from Escherichia coli. Methods Enzymol. 256, 3-10 (1995).
54. Kaufman, M.H. Atlas of Mouse Development (Elsevier Academic Press, 1995).