Regulation of Commissureless by the Ubiquitin Ligase DNedd4 Is Required for Neuromuscular Synaptogenesis in Drosophila melanogaster

REFERENCES

• Abriel, H., J. Loffing, J. F. Rebhun, J. H. Pratt, L. Schild, J. D. Horisberger, D. Rotin, and O. Staub. 1999. Defective regulation of the epithelial Na+ channel by Nedd4 in Liddle's syndrome. J. Clin. Investig. 103:667–673.
   PubMed Web of Science ®Google Scholar
• Bellen, H. J., and V. Budnik. 2000. The neuromuscular junction, p. 175–200. In W. Sullivan, M. Ashburner, and R. S. Hawley (ed.), Drosophila protocols. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Boll, W., H. Ohno, Z. Songyang, I. Rapoport, L. C. Cantley, J. S. Bonifacino, and T. Kirchhausen. 1996. Sequence requirements for the recognition of tyrosine-based endocytic signals by clathrin AP-2 complexes. EMBO J. 15:5789–5795.
   PubMedGoogle Scholar
• Brand, A. H., and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415.
   PubMed Web of Science ®Google Scholar
• Chen, H. I., and M. Sudol. 1995. The WW domain of Yes-associated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules. Proc. Natl. Acad. Sci. USA 92:7819–7823.
   PubMedGoogle Scholar
• Chen, X., B. Zhang, and J. A. Fischer. 2002. A specific protein substrate for a deubiquitinating enzyme: liquid facets is the substrate of Fat facets. Genes Dev. 16:289–294.
   PubMedGoogle Scholar
• Clemens, J. C., C. A. Worby, N. Simonson-Leff, M. Muda, T. Maehama, B. A. Hemmings, and J. E. Dixon. 2000. Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc. Natl. Acad. Sci. USA 97:6499–503.
   PubMed Web of Science ®Google Scholar
• Dunn, R., and L. Hicke. 2001. Multiple roles for Rsp5p-dependent ubiquitination at the internalization step of endocytosis. J. Biol. Chem. 276:25974–81.
   PubMedGoogle Scholar
• Galan, J. M., V. Moreau, B. Andre, C. Volland, and R. Haguenauer-Tsapis. 1996. Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J. Biol. Chem. 271:10946–52.
   PubMed Web of Science ®Google Scholar
• Georgiou, M., and G. Tear. 2003. The N-terminal and transmembrane domains of Commissureless are necessary for its function and trafficking within neurons. Mech. Dev. 120:1009–1019.
   PubMedGoogle Scholar
• Goodman, C. S., and C. Q. Doe. 1993. Embryonic development of the Drosophila central nervous system, p. 1131–1206. In M. Bate and A. Martinez-Arias (ed.), the development of Drosophila melanogaster, vol. 19. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Helliwell, S. B., S. Losko, and C. A. Kaiser. 2001. Components of a ubiquitin ligase complex specify polyubiquitination and intracellular trafficking of the general amino acid permease. J. Cell Biol. 153:649–662.
   PubMed Web of Science ®Google Scholar
• Henry, P. C., V. Kanelis, M. C. O'Brien, B. Kim, I. Gautschi, J. Forman-Kay, L. Schild, and D. Rotin. 2003. Affinity and specificity of interactions between Nedd4 isoforms and the epithelial Na+ channel. J. Biol. Chem. 278:20019–28.
   PubMedGoogle Scholar
• Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425–479.
   PubMed Web of Science ®Google Scholar
• Hicke, L., and R. Dunn. 2003. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19:141–172.
   PubMed Web of Science ®Google Scholar
• Hoang, B., and A. Chiba. 2001. Single-cell analysis of Drosophila larval neuromuscular synapses. Dev. Biol. 229:55–70.
   PubMedGoogle Scholar
• Johansen, J., M. E. Halpern, and H. Keshishian. 1989. Axonal guidance and the development of muscle fiber-specific innervation in Drosophila embryos. J. Neurosci. 9:4318–4332.
   PubMed Web of Science ®Google Scholar
• Kanelis, V., C. Bruce, N. Skrynnikov, D. Rotin, and J. D. Forman-Kay. 2006. Structure determinants for high affinity binding in a Nedd4 WW3* domain - Comm PY motif complex. Structure 14:543–553.
   PubMedGoogle Scholar
• Kanelis, V., D. Rotin, and J. D. Forman-Kay. 2001. Solution structure of a Nedd4 WW domain - ENaC peptide complex. Nat. Struct. Biol. 8:407–412.
   PubMedGoogle Scholar
• Kasanov, J., G. Pirozzi, A. J. Uveges, and B. K. Kay. 2001. Characterizing class I WW domains defines key specificity determinants and generates mutant domains with novel specificities. Chem. Biol. 8:231–241.
   PubMed Web of Science ®Google Scholar
• Katz, M., K. Shtiegman, P. Tal-Or, L. Yakir, Y. Mosesson, D. Harari, Y. Machluf, H. Asao, T. Jovin, K. Sugamura, and Y. Yarden. 2002. Ligand-independent degradation of epidermal growth factor receptor involves receptor ubiquitylation and Hgs, an adaptor whose ubiquitin-interacting motif targets ubiquitylation by Nedd4. Traffic 3:740–751.
   PubMedGoogle Scholar
• Katzmann, D. J., M. Babst, and S. D. Emr. 2001. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106:145–155.
   PubMed Web of Science ®Google Scholar
• Keleman, K., S. Rajagopalan, D. Cleppien, D. Teis, K. Paiha, L. A. Huber, G. M. Technau, and B. J. Dickson. 2002. Comm sorts robo to control axon guidance at the Drosophila midline. Cell 110:415–427.
   PubMed Web of Science ®Google Scholar
• Keleman, K., C. Ribeiro, and B. J. Dickson. 2005. Comm function in commissural axon guidance: cell-autonomous sorting of Robo in vivo. Nat. Neurosci. 8:156–163.
   PubMed Web of Science ®Google Scholar
• Keshishian, H., A. Chiba, T. N. Chang, M. S. Halfon, E. W. Harkins, J. Jarecki, L. Wang, M. Anderson, S. Cash, M. E. Halpern, et al. 1993. Cellular mechanisms governing synaptic development in Drosophila melanogaster. J. Neurobiol. 24:757–787.
   PubMedGoogle Scholar
• Kikonyogo, A., F. Bouamr, M. L. Vana, Y. Xiang, A. Aiyar, C. Carter, and J. Leis. 2001. Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells. Proc. Natl. Acad. Sci. USA 98:11199–204.
   PubMed Web of Science ®Google Scholar
• Kobayashi, T., E. Stang, K. S. Fang, P. de Moerloose, R. G. Parton, and J. Gruenberg. 1998. A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392:193–197.
   PubMed Web of Science ®Google Scholar
• Leventis, P. A., B. M. Chow, B. A. Stewart, B. Iyengar, A. R. Campos, and G. L. Boulianne. 2001. Drosophila amphiphysin is a post-synaptic protein required for normal locomotion but not endocytosis. Traffic 2:839–850.
   PubMedGoogle Scholar
• Lifton, R. P., A. G. Gharavi, and D. S. Geller. 2001. Molecular mechanisms of human hypertension. Cell 104:545–556.
   PubMed Web of Science ®Google Scholar
• Lloyd, T. E., R. Atkinson, M. N. Wu, Y. Zhou, G. Pennetta, and H. J. Bellen. 2002. Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108:261–269.
   PubMed Web of Science ®Google Scholar
• Mosesson, Y., K. Shtiegman, M. Katz, Y. Zwang, G. Vereb, J. Szollosi, and Y. Yarden. 2003. Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J. Biol. Chem. 278:21323–6.
   PubMed Web of Science ®Google Scholar
• Myat, A., P. Henry, V. McCabe, L. Flintoft, D. Rotin, and G. Tear. 2002. Drosophila Nedd4, a ubiquitin ligase, is recruited by Commissureless to control cell surface levels of the roundabout receptor. Neuron 35:447–459.
   PubMedGoogle Scholar
• Owen, D. J., and P. R. Evans. 1998. A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282:1327–1332.
   PubMed Web of Science ®Google Scholar
• Patel, N. H. 1994. Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. Methods Cell Biol. 44:445–487.
   PubMed Web of Science ®Google Scholar
• Plant, P. J., F. Lafont, S. Lecat, P. Verkade, K. Simons, and D. Rotin. 2000. Apical membrane targeting of Nedd4 is mediated by an association of its C2 domain with annexin XIIIb. J. Cell Biol. 149:1473–1484.
   PubMed Web of Science ®Google Scholar
• Plant, P. J., H. Yeger, O. Staub, P. Howard, and D. Rotin. 1997. The C2 domain of the ubiquitin protein ligase Nedd4 mediates Ca2+-dependent plasma membrane localization. J. Biol. Chem. 272:32329–36.
   PubMedGoogle Scholar
• Polo, S., S. Sigismund, M. Faretta, M. Guidi, M. R. Capua, G. Bossi, H. Chen, P. De Camilli, and P. P. Di Fiore. 2002. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416:451–455.
   PubMedGoogle Scholar
• Rose, D., and A. Chiba. 2000. Synaptic target recognition at Drosophila neuromuscular junctions. Microsc. Res. Tech. 49:3–13.
   PubMedGoogle Scholar
• Rotin, D., O. Staub, and R. Haguenauer-Tsapis. 2000. Ubiquitination and endocytosis of plasma membrane proteins: role of Nedd4/Rsp5p family of ubiquitin-protein ligases. J. Membr. Biol. 176:1–17.
   PubMed Web of Science ®Google Scholar
• Sakata, T., H. Sakaguchi, L. Tsuda, A. Higashitani, T. Aigaki, K. Matsuno, and S. Hayashi. 2004. Drosophila Nedd4 regulates endocytosis of notch and suppresses its ligand-independent activation. Curr. Biol. 14:2228–2236.
   PubMed Web of Science ®Google Scholar
• Schild, L., Y. Lu, I. Gautschi, E. Schneeberger, R. P. Lifton, and B. C. Rossier. 1996. Identification of a PY motif in the epithelial Na channel subunits as a target sequence for mutations causing channel activation found in Liddle syndrome. EMBO J. 15:2381–2387.
   PubMed Web of Science ®Google Scholar
• Schmid, A., A. Chiba, and C. Q. Doe. 1999. Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126:4653–4689.
   PubMed Web of Science ®Google Scholar
• Shishido, E., M. Takeichi, and A. Nose. 1998. Drosophila synapse formation: regulation by transmembrane protein with Leu-rich repeats, CAPRICIOUS. Science 280:2118–2121.
   PubMed Web of Science ®Google Scholar
• Soetens, O., J. O. De Craene, and B. Andre. 2001. Ubiquitin is required for sorting to the vacuole of the yeast general amino acid permease, Gap1. J. Biol. Chem. 276:43949–57.
   PubMedGoogle Scholar
• Soubeyran, P., K. Kowanetz, I. Szymkiewicz, W. Y. Langdon, and I. Dikic. 2002. Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature 416:183–187.
   PubMed Web of Science ®Google Scholar
• Staub, O., S. Dho, P. Henry, J. Correa, T. Ishikawa, J. McGlade, and D. Rotin. 1996. WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na+ channel deleted in Liddle's syndrome. EMBO J. 15:2371–2380.
   PubMed Web of Science ®Google Scholar
• Stewart, B. A., H. L. Atwood, J. J. Renger, J. Wang, and C. F. Wu. 1994. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J. Comp. Physiol. A 175:179–191.
   PubMed Web of Science ®Google Scholar
• Taniguchi, H., E. Shishido, M. Takeichi, and A. Nose. 2000. Functional dissection of drosophila capricious: its novel roles in neuronal pathfinding and selective synapse formation. J. Neurobiol. 42:104–116.
   PubMedGoogle Scholar
• Tear, G., R. Harris, S. Sutaria, K. Kilomanski, C. S. Goodman, and M. A. Seeger. 1996. Commissureless controls growth cone guidance across the CNS midline in Drosophila and encodes a novel membrane protein. Neuron 16:501–514.
   PubMedGoogle Scholar
• Umemiya, T., E. Takasu, M. Takeichi, T. Aigaki, and A. Nose. 2002. Forked end: a novel transmembrane protein involved in neuromuscular specificity in drosophila identified by gain-of-function screening. J. Neurobiol. 51:205–214.
   PubMedGoogle Scholar
• Vecchione, A., A. Marchese, P. Henry, D. Rotin, and A. Morrione. 2003. The Grb10/Nedd4 complex regulates ligand-induced ubiquitination and stability of the insulin-like growth factor I receptor. Mol. Cell. Biol. 23:3363–3372.
   PubMed Web of Science ®Google Scholar
• Wang, G., J. M. McCaffery, B. Wendland, S. Dupre, R. Haguenauer-Tsapis, and J. M. Huibregtse. 2001. Localization of the Rsp5p ubiquitin-protein ligase at multiple sites within the endocytic pathway. Mol. Cell. Biol. 21:3564–3575.
   PubMed Web of Science ®Google Scholar
• Wang, W., and G. Struhl. 2004. Drosophila Epsin mediates a select endocytic pathway that DSL ligands must enter to activate Notch. Development 131:5367–5380.
   PubMedGoogle Scholar
• Wilkin, M. B., A. M. Carbery, M. Fostier, H. Aslam, S. L. Mazaleyrat, J. Higgs, A. Myat, D. A. Evans, M. Cornell, and M. Baron. 2004. Regulation of notch endosomal sorting and signaling by Drosophila Nedd4 family proteins. Curr. Biol. 14:2237–2244.
   PubMed Web of Science ®Google Scholar
• Wolf, B., M. A. Seeger, and A. Chiba. 1998. Commissureless endocytosis is correlated with initiation of neuromuscular synaptogenesis. Development 125:3853–3863.
   PubMedGoogle Scholar
• Wucherpfennig, T., M. Wilsch-Brauninger, and M. Gonzalez-Gaitan. 2003. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol. 161:609–624.
   PubMed Web of Science ®Google Scholar
• Yasuda, J., M. Nakao, Y. Kawaoka, and H. Shida. 2003. Nedd4 regulates egress of Ebola virus-like particles from host cells. J. Virol. 77:9987–9992.
   PubMed Web of Science ®Google Scholar
• Yoshihara, M., M. B. Rheuben, and Y. Kidokoro. 1997. Transition from growth cone to functional motor nerve terminal in Drosophila embryos. J. Neurosci. 17:8408–8426.
   PubMedGoogle Scholar