Active involvement of Robol and Robo4 in filopodia formation and endothelial cell motility mediated via WASP and other actin nucleation-promoting factors

FASEB Journal

Volumn 23, Issue 2, 2009, Pages 513-522

  Sheldon, Helen ^a   Andre, Maud ^a   Legg, John A ^a,b   Heal, Paul ^a   Herbert, John M ^b   Sainson, Richard ^a   Sharma, Anshula S ^c   Kitajewski, Jan K ^c   Heath, Victoria L ^b   Bicknell, Roy ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Angiogenesis; Cell signaling; Roundabouts

Indexed keywords

ACTIN; GREEN FLUORESCENT PROTEIN; PROTEIN ROBO1; PROTEIN ROBO4; ROUNDABOUT RECEPTOR; UNCLASSIFIED DRUG; WISKOTT ALDRICH SYNDROME PROTEIN; CELL SURFACE RECEPTOR; IMMUNOGLOBULIN RECEPTOR; NERVE PROTEIN; ROBO4 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ARTICLE; CELL MOTILITY; CELL MOTION; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; ANIMAL; CELL CULTURE; CERCOPITHECUS; CYTOLOGY; GENETICS; METABOLISM; PROTEIN MULTIMERIZATION; PSEUDOPODIUM; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; ENDOTHELIAL CELLS; HUMANS; NERVE TISSUE PROTEINS; PROTEIN MULTIMERIZATION; PSEUDOPODIA; RECEPTORS, CELL SURFACE; RECEPTORS, IMMUNOLOGIC; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; WISKOTT-ALDRICH SYNDROME PROTEIN;

EID: 59649086084     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.07-098269     Document Type: Article

References (31)

1. Seeger, M., Tear, G., Ferres-Marco, D., and Goodman, C. S. (1993) Mutations affecting growth cone guidance in Drosophila genes necessary for guidance toward or away from the midline. Neuron 10, 409-426
2. Kidd, T., Brose, K., Mitchell, K.J., Fetter, R. D., Tessier-Lavigne, M., Goodman, C. S., and Tear, G. (1998) Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92, 205-215
3. Huminiecki, L., Gorn, M., Suchting, S., Poulsom, R., and Bicknell, R. (2002) Magic Roundabout is a new member of the Roundabout receptor family that is endothelial specific and expressed at sites of active angiogenesis. Genomics 79, 547-552
4. Legg, J. A., Herbert, J. M. J., Clissold, P., and Bicknell, R. (2008) Slits and Roundabouts in cancer, tumour angiogenesis and endothelial cell migration. Angiogenesis 11, 13-21
5. Herbert, J. M., Stekel, D., Sanderson, S., Heath, V. L., Bicknell, R. (2008) A novel method of differential gene expression analysis using multiple cDNA libraries applied to the identification of tumour endothelial genes. BMC Genomics 7, 153-174
6. Wang, B., Xiao, Y., Ding, B. B., Zhang, N., Yuan, X., Gui, L., Qian, K. X., Duan, S., Chen, Z., Rao, Y., and Geng, J. G. (2003) Induction of tumour angiogenesis by Slit-Robo signalling and inhibition of cancer growth by blocking Robo activity. Cancer Cell 4, 19-29
7. Park, K. W., Morrison, C. M., Sorensen, L. K., Jones, C. A., Rao, Y., Chien, C. B., Wu, J. Y., Urness, L. D., and Li, D. Y. (2003) Robo4 is a vascular-specific receptor that inhibits endothelial cell migration. Dev. Biol. 261, 251-267
8. Bedell, V. M., Yeo, S. Y., Park, K. W., Chung, J., Seth, P., Shivalingappa, V., Zhao, J., Obara, T., Sukhatme, V. P., Drummond, I. A., Li, D. Y., and Ramchandran, R. (2005) Roundabout4 is essential for angiogenesis in vivo. Proc. Natl. Acad. Sci. U. S. A. 102, 6373-6378
9. Kaur, S., Castellone, M. D., Bedell, V. M., Konar, M., Gutkind, J. S., and Ramchandran, R. (2006) Robo4 signalling in endothelial cells implies attractive guidance mechanisms. J. Biol. Chem. 281, 11347-11356
10. 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
11. Seth, P., Lin, Y., Hanai, J., Shivalingappa, V., Duyao, M. P., and Sukhatme, V. P. (2005) Magic Roundabout, a tumour endothelial marker: expression and signalling. Biochem. Biophys. Res. Commun. 332, 533-541
12. Hohenester, E., Hussain, S., and Howitt, J. A. (2006) Interaction of the guidance molecule Slit with cellular receptors. Biochem. Soc. Trans. 34, 418-421
13. Morlot, C., Thielens, N. M., Ravelli, R. B., Hemrika, W., Romijn, R. A., Gros, P., Cusack, S., and McCarthy, A. A. (2007) Structural insights into the Slit-Robo complex. Proc. Natl. Acad. Sci. U. S. A. 104, 14923-14928
14. Millard, T. H., Behrendt, B., Launay, S., Fütterer, K., and Machesky, L. M. (2003) Identification and charaterisation of a novel human isoform of Arp2/3 complex subunit p16-ARC/ARPC5. Cell Motil. Cytoskelet. 54, 81-90
15. Reynolds, A., Leake, D., Boese, Q., Scaringe, S., Marshall, W. S., and Khvorova, A. (2004) Rational siRNA design for RNA interference. Nat. Biotechnol. 22, 326-330
16. Nguyen Ba-Charvet, K. T., Brose, K., Ma, L., Wang, K. H., Marillat, V., Sotelo, C., Tessier-Lavigne, M., and Chédotal, A. (2001) Diversity and specificity of actions of Slit2 proteolytic fragments in axon guidance. J. Neurosci. 21, 4281-4289
17. Sledz, C. A., Holko, M., de Veer, M. J., Silverman, R. H., and Williams, B. R. (2003) Activation of the interferon system by short-interfering RNAs. Nat. Cell Biol. 5, 834-839
18. Derry, J. M., Ochs, H. D., and Francke, U. (1994) Isolation of a novel gene mutated in Wiskott-Aldrich syndrome. Cell 78, 635-644
19. Hivert, B., Liu, Z., Chuang, C. Y., Doherty, P., and Sundaresan, V. (2002) Robo1 and Robo2 are homophilic binding molecules that promote axonal growth. Mol. Cell Neurosci. 21, 534-545
20. Sabatier, C., Plump, A. S., Le Ma, Brose, K., Tamada, A., Murakami, F., Lee, E. Y., Tessier-Lavigne, M. (2004) The divergent Robo family protein rig-1/Robo3 is a negative regulator of Slit responsiveness required for midline crossing by commisural axons. Cell 117, 157-169
21. Howitt, J. A., Clout, N. J., and Hohenester, E. (2004) Binding site for Robo receptors revealed by dissection of the leucine-rich repeat region of Slit. EMBO J. 23, 4406-4412
22. Stein, E., and Tessier-Lavigne, M. (2001) Hierarchical organization of guidance receptors: silencing of netrin attaraction by Slit through a robo/DCC receptor complex. Science 291, 1928-1939
23. Krugmann, S., Jordens, I., Gevaert, K., Driessens, M., Vandekerckhove, J., and Hall, A. (2001) Cdc42 induces filopodia by promoting the formation of an IRSp53: Mena complex. Curr. Biol. 11, 1645-1655
24. Martinez-Quiles, N. M., Rhotagi, R., Anton, I. M., Medina, M., Saville, S. P., Miki, H., Yamaguchi, H., Takenawa, T., Hartwig, J. H., Geha, R. S., and Ramesh, N. (2001) WIP regulates N-WASP-mediated actin polymerization and filopodium formation. Nat. Cell Biol. 3, 484-491
25. Miki, H., Miura, K., and Takenawa, T. (1996) N-WASP, a novel actin-depolymerizing protein, regulates the cortical cytoskeletal rearragement in a PIP2-dependent manner downstream of tyrosine kinases. EMBO J. 15, 5326-5335
26. Kessels, M. M., and Qualmann, B. (2002) Syndapins integrate N-WASP in receptor-mediated endocytosis. EMBO J. 21, 6083-6094
27. Kessels, M. M., and Qualmann, B. (2006) Syndapin oligomers interconnect the machineries for endocytic vesicle formation and actin polymerization. J. Biol. Chem. 281, 13285-13299
28. Suchting, S., Heal, P., Tahtis, K., Stewart, L. M., and Bicknell, R. (2005) Soluble Robo4 receptor inhibits in vivo angiogenesis and endothelial cell migration. FASEB J. 19, 121-123
29. Lundström, A., Gallio, M., Englund, C., Steneberg, P., Hemphälä, J., Aspenström, P., Keleman, K., Falileeva, L., Dickson, B. J., and Samakovlis, C. (2004) Vilse, a conserved Rac/Cdc42 GAP mediating Robo repulsion in tracheal cells and axons. Genes Dev. 18, 2161-2171
30. Hu, H., Li, M., Labrador, J. P., McEwen, J., Lai, E. C., Goodman, C. S., and Bashaw, G. J. (2005) Cross GTPase-activating protein (CrossGAP)/Vilse links the Roundabout receptor to Rac to regulate midline repulsion. Proc. Natl. Acad. Sci. U. S. A. 102, 4613-4618
31. Wong, K., Ren, X. R., Huang, Y. Z., Xie, Y., Liu, G., Saito, H., Tang, H., Wen, L., Brady-Kalnay, S. M., Mei, L., Wu, J. Y., Xiong, W. C., and Rao, Y. (2001) Signal transduction in neuronal migration: roles of the GTPase activating proteins and small GTPase Cdc42 in the Slit-Robo pathway. Cell 107, 209-221