Drosophila syndecan regulates tracheal cell migration by stabilizing Robo levels

EMBO Reports

Volumn 12, Issue 10, 2011, Pages 1039-1046

  Schulz, Joachim G ^a,b,c   Ceulemans, Helga ^a,c   Caussinus, Emmanuel ^d   Baietti, Maria F ^a,c   Affolter, Markus ^d   Hassan, Bassem A ^b,c   David, Guido ^a,c  

^a Laboratory of Glycobiology and Developmental Genetics   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d UNIVERSITY OF BASEL   (Switzerland)

Author keywords

cell migration; Drosophila; heparan sulphate; Robo; tracheal system

Indexed keywords

ROUNDABOUT RECEPTOR; SLIT PROTEIN; SYNDECAN;

ARTICLE; CELL FUSION; CELL MIGRATION; CYTOPLASM; DROSOPHILA; GENE INTERACTION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SIGNAL TRANSDUCTION; TRACHEA;

ANIMALS; BASE SEQUENCE; CELL MOVEMENT; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; GENE ORDER; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; PHENOTYPE; PROTEIN STABILITY; RECEPTORS, IMMUNOLOGIC; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SYNDECANS; TRACHEA;

EID: 80053571864     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.1038/embor.2011.153     Document Type: Article

References (35)

1. Affolter M, Caussinus E (2008) Tracheal branching morphogenesis in Drosophila: new insights into cell behaviour and organ architecture. Development 135: 2055-2064 (Pubitemid 352015141)
2. Affolter M, Zeller R, Caussinus E (2009) Tissue remodelling through branching morphogenesis. Nat Rev Mol Cell Biol 10: 831-842
3. Beauvais DM, Ell BJ, McWhorter AR, Rapraeger AC (2009) Syndecan-1 regulates alphavbeta3 and alphavbeta5 integrin activation during angiogenesis and is blocked by synstatin, a novel peptide inhibitor. J Exp Med 206: 691-705
4. Chanana B, Steigemann P, Jackle H, Vorbruggen G (2009) Reception of Slit requires only the chondroitin-sulphate-modified extracellular domain of Syndecan at the target cell surface. Proc Natl Acad Sci USA 106: 11984-11988
5. Chen E, Hermanson S, Ekker SC (2004) Syndecan-2 is essential for angiogenic sprouting during zebrafish development. Blood 103: 1710-1719 (Pubitemid 38268963)
6. De Smet F, Segura I, De Bock K, Hohensinner PJ, Carmeliet P (2009) Mechanisms of vessel branching: filopodia on endothelial tip cells lead the way. Arterioscler Thromb Vasc Biol 29: 639-649
7. Dedkov EI, Thomas MT, Sonka M, Yang F, Chittenden TW, Rhodes JM, Simons M, Ritman EL, Tomanek RJ (2007) Synectin/syndecan-4 regulate coronary arteriolar growth during development. Dev Dyn 236: 2004-2010 (Pubitemid 47076029)
8. Englund C, Steneberg P, Falileeva L, Xylourgidis N, Samakovlis C (2002) Attractive and repulsive functions of Slit are mediated by different receptors in the Drosophila trachea. Development 129: 4941-4951 (Pubitemid 35355912)
9. Epstein EA, Martin JM, O'Connor MB (2002) Genetics of the sara and syndecan region. A Dros Res Conf 43: 445A
10. Ghabrial A, Luschnig S, Metzstein MM, Krasnow MA (2003) Branching morphogenesis of the Drosophila tracheal system. Annu Rev Cell Dev Biol 19: 623-647 (Pubitemid 37487363)
11. Ghabrial AS, Krasnow MA (2006) Social interactions among epithelial cells during tracheal branching morphogenesis. Nature 441: 746-749 (Pubitemid 43865219)
12. Johnson KG, Ghose A, Epstein E, Lincecum J, O'Connor MB, Van Vactor D (2004) Axonal heparan sulfate proteoglycans regulate the distribution and efficiency of the repellent slit during midline axon guidance. Curr Biol 14: 499-504 (Pubitemid 38431285)
13. Jones CA et al (2009) Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nat Cell Biol 11: 1325-1331
14. Keleman K, Rajagopalan S, Cleppien D, Teis D, Paiha K, Huber LA, Technau GM, Dickson BJ (2002) Comm sorts robo to control axon guidance at the Drosophila midline. Cell 110: 415-427 (Pubitemid 35232286)
15. Keleman K, Ribeiro C, Dickson BJ (2005) Comm function in commissural axon guidance: cell-autonomous sorting of Robo in vivo. Nat Neurosci 8: 156-163 (Pubitemid 40194045)
16. Kidd T, Russell C, Goodman CS, Tear G (1998) Dosage-sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron 20: 25-33 (Pubitemid 28078346)
17. Kramer SG, Kidd T, Simpson JH, Goodman CS (2001) Switching repulsion to attraction: changing responses to slit during transition in mesoderm migration. Science 292: 737-740 (Pubitemid 32385546)
18. Kreuger J, Perez L, Giraldez AJ, Cohen SM (2004) Opposing activities of Dally-like glypican at high and low levels of Wingless morphogen activity. Dev Cell 7: 503-512 (Pubitemid 39341836)
19. Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451-461 (Pubitemid 29159845)
20. Lin X, Wei G, Shi Z, Dryer L, Esko JD, Wells DE, Matzuk MM (2000) Disruption of gastrulation and heparan sulfate biosynthesis in EXT1-deficient mice. Dev Biol 224: 299-311 (Pubitemid 30661012)
21. Lu P, Werb Z (2008) Patterning mechanisms of branched organs. Science 322: 1506-1509
22. Myat A, Henry P, McCabe V, Flintoft L, Rotin D, Tear G (2002) Drosophila Nedd4, a ubiquitin ligase, is recruited by Commissureless to control cell surface levels of the roundabout receptor. Neuron 35: 447-459 (Pubitemid 34879945)
23. Palacios F, Price L, Schweitzer J, Collard JG, D'Souza-Schorey C (2001) An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J 20: 4973-4986 (Pubitemid 32848649)
24. Phng LK, Gerhardt H (2009) Angiogenesis: a team effort coordinated by notch. Dev Cell 16: 196-208
25. Rhiner C, Gysi S, Frohli E, Hengartner MO, Hajnal A (2005) Syndecan regulates cell migration axon guidance in C. elegans. Development 132: 4621-4633 (Pubitemid 41632239)
26. Rong YS, Titen SW, Xie HB, Golic MM, Bastiani M, Bandyopadhyay P, Olivera BM, Brodsky M, Rubin GM, Golic KG (2002) Targeted mutagenesis by homologous recombination in D. melanogaster. Genes Dev 16: 1568-1581 (Pubitemid 34686337)
27. Sabe H (2003) Requirement for Arf6 in cell adhesion, migration, and cancer cell invasion. J Biochem 134: 485-489 (Pubitemid 37442870)
28. Samakovlis C, Manning G, Steneberg P, Hacohen N, Cantera R, Krasnow MA (1996) Genetic control of epithelial tube fusion during Drosophila tracheal development. Development 122: 3531-3536 (Pubitemid 26395994)
29. Schulz JG, David G, Hassan BA (2009) A novel method for tissue-specific RNAi rescue in Drosophila. Nucleic Acids Res 37: e93
30. Spring J, Paine-Saunders SE, Hynes RO, Bernfield M (1994) Drosophila syndecan: conservation of a cell-surface heparan sulfate proteoglycan. Proc Natl Acad Sci USA 91: 3334-3338 (Pubitemid 24130231)
31. Steigemann P, Molitor A, Fellert S, Jackle H, Vorbruggen G (2004) Heparan sulfate proteoglycan syndecan promotes axonal and myotube guidance by slit/robo signaling. Curr Biol 14: 225-230 (Pubitemid 38215350)
32. Tanaka-Matakatsu M, Uemura T, Oda H, Takeichi M, Hayashi S (1996) Cadherin-mediated cell adhesion and cell motility in Drosophila trachea regulated by the transcription factor Escargot. Development 122: 3697-3705 (Pubitemid 27033866)
33. Tkachenko E, Lutgens E, Stan RV, Simons M (2004) Fibroblast growth factor 2 endocytosis in endothelial cells proceed via syndecan-4-dependent activation of Rac1 and a Cdc42-dependent macropinocytic pathway. J Cell Sci 117: 3189-3199 (Pubitemid 39139905)
34. Uv A, Cantera R, Samakovlis C (2003) Drosophila tracheal morphogenesis: intricate cellular solutions to basic plumbing problems. Trends Cell Biol 13: 301-309 (Pubitemid 36638797)
35. Zimmermann P, Zhang Z, Degeest G, Mortier E, Leenaerts I, Coomans C, Schulz JG, N'Kuli F, Courtoy PJ, David G (2005) Syndecan recycling is controlled by syntenin-PIP2 interaction and Arf6. Dev Cell 9: 377-388 (Pubitemid 41235807)