Netrin-dependent downregulation of Frazzled/DCC is required for the dissociation of the peripodial epithelium in Drosophila

Nature Communications

Volumn 4, Issue , 2013, Pages

  Manhire Heath, Rosemary ^a   Golenkina, Sofia ^a   Saint, Robert ^a,b   Murray, Michael J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MOESIN; NETRIN;

APOPTOSIS; BIOCHEMISTRY; CANCER; ENTOMOLOGY; FLY; GENE EXPRESSION; INHIBITION; PROTEIN; RNA; SECRETION; WING;

ARTICLE; CELL JUNCTION; CONTROLLED STUDY; DISSOCIATION; DOWN REGULATION; DROSOPHILA; ENDOCYTOSIS; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FORELIMB; GENOTYPE; NONHUMAN; PROTEIN DEGRADATION; RNA INTERFERENCE;

NETA;

ADHERENS JUNCTIONS; ANIMALS; DOWN-REGULATION; DROSOPHILA; EPITHELIUM; FEMALE; MEMBRANE PROTEINS; METAMORPHOSIS, BIOLOGICAL; NERVE GROWTH FACTORS; PROTEASOME ENDOPEPTIDASE COMPLEX; RECEPTORS, CELL SURFACE; TUMOR SUPPRESSOR PROTEINS; WING;

EID: 84889560920     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3790     Document Type: Article

References (42)

1. Thiery, J. P., Acloque, H., Huang, R. Y. J. & Nieto, M. A. Epithelialmesenchymal transitions in development and disease. Cell 139, 871-890 (2009
2. Kalluri, R. & Weinberg, R. A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119, 1420-1428 (2009
3. Yang, J. & Weinberg, R. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818-829 (2008 (Pubitemid 351757205)
4. Nakaya, Y. & Sheng, G. Epithelial to mesenchymal transition during gastrulation: an embryological view. Development 50, 755-766 (2008
5. Leptin, M. & Grunewald, B. Cell shape changes during gastrulation in Drosophila. Development 110, 73-84 (1990
6. Clark, I. B. N., Muha, V., Klingseisen, A., Leptin, M. & Muller, H.-A. J. Fibroblast growth factor signalling controls successive cell behaviours during mesoderm layer formation in Drosophila. Development 138, 2705-2715 (2011
7. Campbell, K., Whissell, G., Franch-Marro, X., Batlle, E. & Casanova, J. Specific GATA factors act as conserved inducers of an endodermal-EMT. Dev. Cell 21, 1051-1061 (2011
8. Srivastava, A., Pastor-Pareja, J. C., Igaki, T., Pagliarini, R. & Xu, T. Basement membrane remodeling is essential for Drosophila disc eversion and tumor invasion. Proc. Natl Acad. Sci. USA 104, 2721-2726 (2007 (Pubitemid 46327946)
9. Pastor-Pareja, J. C., Grawe, F., Martn-Blanco, E. & Garca-Bellido, A. Invasive cell behavior during Drosophila imaginal disc eversion is mediated by the JNK signaling cascade. Dev. Cell 7, 387-399 (2004 (Pubitemid 39232974)
10. Aldaz, S., Escudero, L. M. & Freeman, M. Live imaging of Drosophila imaginal disc development. PNAS 107, 14217-14222 (2010
11. Sun, K. L. W., Correia, J. P. & Kennedy, T. E. Netrins: versatile extracellular cues with diverse functions. Development 138, 2153-2169 (2011
12. Mazelin, L. et al. Netrin-1 controls colorectal tumorigenesis by regulating apoptosis. Nature 431, 80-84 (2004 (Pubitemid 39215111)
13. Mehlen, P. et al. The DCC gene product induces apoptosis by a mechanism requiring receptor proteolysis. Nature 395, 801-804 (1998 (Pubitemid 28485447)
14. Harris, R., Sabatelli, L. M. & Seeger, M. A. Guidance cues at the Drosophila CNS midline: identification and characterization of two Drosophila Netrin/ UNC-6 homologs. Neuron 17, 217-228 (1996 (Pubitemid 26296149)
15. Mitchell, K. J. et al. Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 17, 203-215 (1996 (Pubitemid 26296148)
16. Castets, M. et al. DCC constrains tumour progression via its dependence receptor activity. Nature 482, 534-537 (2011
17. Vanzomeren-Dohm, A., Sarro, J., Flannery, E. & Duman-Scheel, M. The Drosophila Netrin receptor frazzled/DCC functions as an invasive tumor suppressor. BMC Dev. Biol. 11, 41 (2011
18. Brankatschk, M. & Dickson, B. J. Netrins guide Drosophila commissural axons at short range. Nat. Neurosci. 9, 188-194 (2006 (Pubitemid 43164541)
19. Martn-Blanco, E. et al. puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev. 12, 557-570 (1998
20. Guillermet, C. & Mandaron, P. In vitro imaginal disc development and moulting hormone. J. Embryol. Exp. Morphol. 57, 107-118 (1980 (Pubitemid 10074504)
21. Brock, A. R. et al. Transcriptional regulation of Profilin during wound closure in Drosophila larvae. J. Cell Sci. 125, 5667-5676 (2012
22. Kolodziej, P. A. et al. frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 87, 197-204 (1996 (Pubitemid 26358998)
23. Duffy, J. GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis. 34, 1-15 (2002
24. Zhang, J. et al. Thirty-one flavors of Drosophila rab proteins. Genetics 176, 1307-1322 (2007 (Pubitemid 46961123)
25. Gorvel, J. P., Chavrier, P., Zerial, M. & Gruenberg, J. rab5 controls early endosome fusion in vitro. Cell 64, 915-925 (1991 (Pubitemid 121001179)
26. Bucci, C. et al. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70, 715-728 (1992
27. Hicke, L. Ubiquitin-dependent internalization and down-regulation of plasma membrane proteins. FASEB J. 11, 1215 (1997
28. Stang, E., Johannessen, L. E., Knardal, S. L. & Madshus, I. H. Polyubiquitination of the epidermal growth factor receptor occurs at the plasma membrane upon ligand-induced activation. J. Biol. Chem. 275, 13940-13947 (2000 (Pubitemid 30257471)
29. Hu, G. et al. Mammalian homologs of seven in absentia regulate DCC via the ubiquitin-proteasome pathway. Genes Dev. 11, 2701-2714 (1997 (Pubitemid 27452393)
30. Kim, T.-H. et al. Netrin induces down-regulation of its receptor, Deleted in Colorectal Cancer, through the ubiquitin-proteasome pathway in the embryonic cortical neuron. J. Neurochem. 95, 1-8 (2005 (Pubitemid 41384420)
31. Piper, M., Salih, S., Weinl, C., Holt, C. & Harris, W. Endocytosis-dependent desensitization and protein synthesis-dependent resensitization in retinal growth cone adaptation. Nat. Neurosci. 8, 179-186 (2005 (Pubitemid 40194048)
32. Campbell, D. S. & Holt, C. E. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32, 1013-1026 (2001 (Pubitemid 34075393)
33. Speck, O., Hughes, S. C., Noren, N. K., Kulikauskas, R. M. & Fehon, R. G. Moesin functions antagonistically to the Rho pathway to maintain epithelial integrity. Nature 421, 83-87 (2003 (Pubitemid 36077089)
34. Antoine-Bertrand, J., Ghogha, A., Luangrath, V., Bedford, F. K. & Lamarche- Vane, N. The activation of ezrin-radixin-moesin proteins is regulated by netrin-1 through Src kinase and RhoA/Rho kinase activities and mediates netrin-1-induced axon outgrowth. Mol. Biol. Cell 22, 3734-3746 (2011
35. Chuong, C. M., Jiang, T. X., Yin, E. & Widelitz, R. B. cDCC (chicken homologue to a gene deleted in colorectal carcinoma) is an epithelial adhesion molecule expressed in the basal cells and involved in epithelial-mesenchymal interaction. Dev. Biol. 164, 383-397 (1994 (Pubitemid 24269227)
36. Martn, M. et al. DCC regulates cell adhesion in human colon cancer derived HT-29 cells and associates with ezrin. Eur. J. Cell Biol. 85, 769-783 (2006
37. Fitamant, J. et al. Netrin-1 expression confers a selective advantage for tumor cell survival in metastatic breast cancer. Proc. Natl Acad. Sci. USA 105, 4850-4855 (2008 (Pubitemid 351753835)
38. Dumartin, L. et al. Netrin-1 mediates early events in pancreatic adenocarcinoma progression, acting on tumor and endothelial cells. Gastroenterology 138, 1595-1606 1606.e1591-1598 (2010
39. Arakawa, H. Netrin-1 and its receptors in tumorigenesis. Nat. Rev. Cancer 4, 978-986 (2004
40. Pallavi, S. K. & Shashidhara, L. S. Egfr/Ras pathway mediates interactions between peripodial and disc proper cells in Drosophila wing discs. Development 130, 4931-4941 (2003 (Pubitemid 37321875)
41. Edwards, K. A., Demsky, M., Montague, R. A., Weymouth, N. & Kiehart, D. P. GFP-Moesin illuminates actin cytoskeleton dynamics in living tissue and demonstrates cell shape changes during morphogenesis in Drosophila. Dev. Biol. 191, 103-117 (1997 (Pubitemid 27519708)
42. Albrecht, S., Altenhein, B. & Paululat, A. The transmembrane receptor Uncoordinated5 (Unc5) is essential for heart lumen formation in Drosophila melanogaster. Dev. Biol. 350, 89-100 (2011