Godzilla-dependent transcytosis promotes Wingless signalling in Drosophila wing imaginal discs

Nature Cell Biology

Volumn 18, Issue 4, 2016, Pages 451-457

  Yamazaki, Yasuo ^a   Palmer, Lucy ^b   Alexandre, Cyrille ^b   Kakugawa, Satoshi ^b   Beckett, Karen ^b   Gaugue, Isabelle ^c   Palmer, Ruth H ^a   Vincent, Jean Paul ^b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^c INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GODZILLA PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; WNT1 PROTEIN; DROSOPHILA PROTEIN; GODZILLA PROTEIN, DROSOPHILA; GREEN FLUORESCENT PROTEIN; UBIQUITIN PROTEIN LIGASE; WG PROTEIN, DROSOPHILA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; CONTROLLED STUDY; DROSOPHILA; ENDOCYTOSIS; ENDOSOME; IMAGINAL DISC; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSCYTOSIS; WING; ANIMAL; CONFOCAL MICROSCOPY; DROSOPHILA MELANOGASTER; EMBRYOLOGY; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; METABOLISM; RNA INTERFERENCE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOSOMES; GREEN FLUORESCENT PROTEINS; IMAGINAL DISCS; IN SITU HYBRIDIZATION, FLUORESCENCE; MICROSCOPY, CONFOCAL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCYTOSIS; UBIQUITIN-PROTEIN LIGASES; WINGS, ANIMAL; WNT1 PROTEIN;

EID: 84961219058     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3325     Document Type: Article

References (32)

1. Tuma, P. L., & Hubbard, A. L. Transcytosis: crossing cellular barriers. Physiol. Rev. 83, 871-932 (2003
2. Wilkie, G. S., & Davis, I. Drosophila wingless and pair-rule transcripts localize apically by dynein-mediated transport of RNA particles. Cell 105, 209-219 (2001
3. Simmonds, A. J., dos Santos, G., Livne-Bar, I., & Krause, H. M. Apical localization of wingless transcripts is required for wingless signaling. Cell 105, 197-207 (2001
4. Strigini, M., & Cohen, S. M. Wingless gradient formation in the Drosophila wing. Curr. Biol. 10, 293-300 (2000
5. Wu, J., Klein, T. J., & Mlodzik, M. Subcellular localization of frizzled receptors, mediated by their cytoplasmic tails, regulates signaling pathway specificity. PLoS Biol. 2, E158 (2004
6. Baena-Lopez, L. A., Alexandre, C., Mitchell, A., Pasakarnis, L., & Vincent, J. P. Accelerated homologous recombination and subsequent genome modification in Drosophila. Development 140, 4818-4825 (2013
7. Couso, J. P., Bishop, S. A., & Martinez Arias, A. The wingless signalling pathway and the patterning of the wing margin in Drosophila. Development 120, 621-636 (1994
8. Van der Bliek, A. M., & Meyerowitz, E. M. Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351, 411-414 (1991
9. Kicheva, A., et al. Kinetics of morphogen gradient formation. Science 315, 521-525 (2007
10. Zecca, M., Basler, K., & Struhl, G. Direct and long-range action of a wingless morphogen gradient. Cell 87, 833-844 (1996
11. Alexandre, C., Baena-Lopez, A., & Vincent, J.-P. Patterning and growth control by membrane-tethered Wingless. Nature 505, 180-185 (2014
12. Mertens, G., Van der Schueren, B., van den Berghe, H., & David, G. Heparan sulfate expression in polarized epithelial cells: the apical sorting of glypican (GPI-anchored proteoglycan) is inversely related to its heparan sulfate content. J. Cell Biol. 132, 487-497 (1996
13. Gallet, A., Staccini-Lavenant, L., & Therond, P. P. Cellular trafficking of the glypican Dally-like is required for full-strength Hedgehog signaling and wingless transcytosis. Dev. Cell 14, 712-725 (2008
14. Han, C., Yan, D., Belenkaya, T. Y., & Lin, X. Drosophila glypicans Dally and Dally-like shape the extracellular Wingless morphogen gradient in the wing disc. Development 132, 667-679 (2005
15. Bnziger, C., et al. Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell 125, 509-522 (2006
16. Bartscherer, K., Pelte, N., Ingelfinger, D., & Boutros, M. Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell 125, 523-533 (2006
17. Goodman, R. M., et al. Sprinter: a novel transmembrane protein required for Wg secretion and signaling. Development 133, 4901-4911 (2006
18. Coombs, G. S. WLS-dependent secretion of WNT3A requires Ser209 acylation and vacuolar acidification. J. Cell Sci. 123, 3357-3367 (2010
19. Herr, P., & Basler, K. Porcupine-mediated lipidation is required for Wnt recognition by Wls. Dev. Biol. 361, 392-402 (2012
20. Yamamoto, H., et al. The apical and basolateral secretion of Wnt11 and Wnt3a in polarized epithelial cells is regulated by different mechanisms. J. Cell Sci. 126, 2931-2943 (2013
21. Yu, J., et al. WLS retrograde transport to the endoplasmic reticulum during Wnt secretion. Dev. Cell 29, 277-291 (2014
22. Yamazaki, Y., et al. Goliath family E3 ligases regulate the recycling endosome pathway via VAMP3 ubiquitylation. EMBO J. 32, 524-537 (2013
23. Seto, E. S., & Bellen, H. J. Internalization is required for proper Wingless signaling in Drosophila melanogaster. J. Cell Biol. 173, 95-106 (2006
24. Rulifson, E. J., & Blair, S. S. Notch regulates wingless expression and is not required for reception of the paracrine wingless signal during wing margin neurogenesis in Drosophila. Development 121, 2813-2824 (1995
25. Kakugawa, S., et al. Notum deacylates Wnt proteins to suppress signalling activity. Nature 519, 187-192 (2015
26. Oshima, K., & Fehon, R. G. Analysis of protein dynamics within the septate junction reveals a highly stable core protein complex that does not include the basolateral polarity protein Discs large. J. Cell Sci. 124, 2861-2871 (2011
27. Cadigan, K. M., Fish, M. P., Rulifson, E. J., & Nusse, R. Wingless repression of Drosophila frizzled 2 expression shapes the Wingless morphogen gradient in the wing. Cell 93, 767-777 (1998
28. Callejo, A., et al. Dispatched mediates Hedgehog basolateral release to form the longrange morphogenetic gradient in the Drosophila wing disk epithelium. Proc. Natl Acad. Sci. USA 108, 12591-12598 (2011
29. De Lau, W., Peng, W. C., Gros, P., & Clevers, H. The R-spondin/Lgr5/Rnf43 module: regulator of Wnt signal strength. Genes Dev. 28, 305-316 (2014
30. Zhang, Y., et al. RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and Wnt signalling. Nat. Cell Biol. 13, 623-629 (2011
31. Bhattacharya, S., et al. Members of the synaptobrevin/vesicle-associated membrane protein (VAMP) family in Drosophila are functionally interchangeable in vivo for neurotransmitter release and cell viability. Proc. Natl Acad. Sci. USA 99, 13867-13872 (2002
32. Franch-Marro, X., et al. Glypicans shunt the Wingless signal between local signalling and further transport. Development 132, 659-666 (2005