Drosophila Epsin mediates a select endocytic pathway that DSL ligands must enter to activate Notch

Development

Volumn 131, Issue 21, 2004, Pages 5367-5380

  Wang, Weldong ^a   Struhl, Gary ^a  

^a Columbia Univ Coll of Phys/Surg ^*  (United States)

Author keywords

Delta; Drosophila; DSL Notch signaling; Endocytosis; Epsin Liquid facets(Lqf); Mono ubiquitination

Indexed keywords

ADAPTOR PROTEIN; CLATHRIN; EPSIN; LIGAND; LOW DENSITY LIPOPROTEIN RECEPTOR; NOTCH RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL SUBPOPULATION; COATED PIT; CONTROLLED STUDY; DROSOPHILA; ENDOCYTOSIS; GENE ACTIVATION; GENETIC CONSERVATION; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; UBIQUITINATION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CALCIUM-BINDING PROTEINS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CHOLESTEROL, LDL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOCYTOSIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGANDS; MEMBRANE PROTEINS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; UBIQUITIN; VESICULAR TRANSPORT PROTEINS; WING;

ANIMALIA;

EID: 9444297354     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01413     Document Type: Article

References (53)

1. Baonza, A. and Freeman, M. (2001). Notch signalling and the initiation of neural development in the Drosophila eye. Development 128, 3889-3898.
2. Basler, K. and Struhl, G. (1994). Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208-214.
3. Blair, S. S. (2000). Notch signaling: Fringe really is a glycosyltransferase. Curr. Biol. 10, R608-R612.
4. Cadavid, A. L., Ginzel, A. and Fischer, J. A. (2000). The function of the Drosophila fat facets deubiquitinating enzyme in limiting photoreceptor cell number is intimately associated with endocytosis. Development 127, 1727-1736.
5. Calleja, M., Moreno, E., Pelaz, S. and Morata, G. (1996). Visualization of gene expression in living adult Drosophila. Science 274, 252-255.
6. Chen, C. M. and Struhl, G. (1999). Wingless transduction by the Frizzled and Frizzled proteins of Drosophila. Development 126, 5441-5452.
7. Chen, H., Fre, S., Slepnev, V. I., Capua, M. R., Takei, K., Butler, M. H., di Flore, P. P. and de Catailli, P. (1998). Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature 394, 793-797.
8. Chen, W. J., Goldstein, J. L. and Brown, M. S. (1990). NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J. Biol. Chem. 265, 3116-3123.
9. de Celis, J. F. and Bray, S. (1997). Feed-back mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing. Development 124, 3241-3251.
10. Deblandre, G. A., Lai, E. C. and Kintner, C. (2001). Xenopus neuralized is a ubiquitin ligase that interacts with XDelta1 and regulates Notch signaling. Dev. Cell 1, 795-806.
11. Drake, M. T., Downs, M. A. and Traub, L. M. (2000). Epsin binds to clathrin by associating directly with the clathrin-terminal domain. Evidence for cooperative binding through two discrete sites. J. Biol. Chem. 275, 6479-6489.
12. Fleming, R. J., Gu, Y. and Hukriede, N. A. (1997). Serrate-mediated activation of Notch is specifically blocked by the product of the gene fringe in the dorsal compartment of the Drosophila wing imaginal disc. Development 124, 2973-2981.
13. Ford, M. G., Mills, I. G., Peter, B. J., Vallis, Y., Praefcke, G. J., Evans, P. R. and McMahon, H. T. (2002). Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366.
14. Greenwald, I. (1998). LIN-12/Notch signaling: lessons from worms and flies. Genes Dev. 12, 1751-1762.
15. Grimm, S. and Pflugfelder, G. O. (1996). Control of the gene optomotor-blind in Drosophila wing development by decapentaplegic and wingless. Science 271, 1601-1604.
16. Hicke, L. and Dunn, R. (2003). Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19, 141-172.
17. Hofmann, K. and Falquet, L. (2001). A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem. Sci. 26, 347-350.
18. Irvine, K. D. and Vogt, T. F. (1997). Dorsal-ventral signaling in limb development. Curr. Opin. Cell Biol. 9, 867-876.
19. Itoh, M., Kim, C. H., Palardy, G., Oda, T., Jiang, Y. J., Maust, D., Yeo, S. Y., Lorick, K., Wright, G. J., Ariza-McNaughton, L. et al. (2003). Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev. Cell 4 67-82.
20. Jiang, J. and Struhl, G. (1995). Protein kinase A and hedgehog signaling in Drosophila limb development. Cell 80, 563-572.
21. Kooh, P. J., Fehon, R. G. and Muskavitch, M. A. (1993). Implications of dynamic patterns of Delta and Notch expression for cellular interactions during Drosophila development. Development 117, 493-507.
22. Lai, E. C., Deblandre, G. A., Kintner, C. and Rubin, G. M. (2001). Drosophila neuralized is a ubiquitin ligase that promotes the internalization and degradation of delta. Dev. Cell 1, 783-794.
23. Le Borgne, R. and Schweisguth, F. (2003a). Unequal segregation of Neuralized biases Notch activation during asymmetric cell division. Dev. Cell 5, 139-148.
24. Le Borgne, R. and Schweisguth, F. (2003b). Notch signaling: endocytosis makes delta signal better. Curr. Biol. 13 R273-R275.
25. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461.
26. Lloyd, T. E., Atkinson, R., Wu, M. N., Zhou, Y., Pennetta, G. and Bellen, H. J. (2002). Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108, 261-269.
27. Lopez-Schier, H. and St Johnston, D. (2001). Delta signaling from the germ line controls the proliferation and differentiation of the somatic follicle cells during Drosophila oogenesis. Genes Dev. 15, 1393-1405.
28. Matter, K., Whitney, J. A., Yamamoto, E. M. and Mellman, I. (1993). Common signals control low density lipoprotein receptor sorting in endosomes and the Golgi complex of MDCK cells. Cell 74, 1053-1064.
29. Micchelli, C. A., Rulifson, E. J. and Blair, S. S. (1997). The function and regulation of cut expression on the wing margin of Drosophila: Notch, Wingless and a dominant negative role for Delta and Serrate. Development 124, 1485-1495.
30. Mills, I. G., Praefcke, G. J., Vallis, Y., Peter, B. J., Olesen, L. E., Gallop, J. L., Butler, P. J., Evans, P. R. and McMahon, H. T. (2003). EpsinR: an AP1/clathrin interacting protein involved in vesicle trafficking. J. Cell Biol. 160, 213-222.
31. Mishra, S. K., Keyel, P. A., Hawryluk, M. J., Agostinelli, N. R., Watkins, S. C. and Traub, L. M. (2002). Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J. 21, 4915-4926.
32. Mumm, J. S. and Kopan, R. (2000). Notch signaling: from the outside in. Dev. Biol. 228, 151-165.
33. Nellen, D., Burke, R., Struhl, G. and Basler, K. (1996). Direct and long-range action of a DPP morphogen gradient. Cell 85, 357-368.
34. Nolo, R., Abbott, L. A. and Bellen, H. J. (2000). Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 102, 349-362.
35. Overstreet, E., Chen, X., Wendland, B. and Fischer, J. A. (2003). Either part of a Drosophila epsin protein, divided after the ENTH domain, functions in endocytosis of delta in the developing eye. Curr. Biol. 13, 854-860.
36. Owen, D. J., Vallis, Y., Noble, M. E., Hunter, J. B., Dafforn, T. R., Evans, P. R. and McMahon, H. T. (1999). A structural explanation for the binding of multiple ligands by the alpha-adaptin appendage domain. Cell 97, 805-815.
37. Panin, V. M., Papayannopoulos, V., Wilson, R. and Irvine, K. D. (1997). Fringe modulates Notch-ligand interactions. Nature 387, 908-912.
38. Parks, A. L., Klueg, K. M., Stout, J. R. and Muskavitch, M. A. (2000). Ligand endocytosis drives receptor dissociation and activation in the Notch pathway. Development 127, 1373-1385.
39. Pavlopoulos, E., Pitsouli, C., Klueg, K. M., Muskavitch, M. A., Moschonas, N. K. and Delidakis, C. (2001). neuralized Encodes a peripheral membrane protein involved in delta signaling and endocytosis. Dev. Cell 1, 807-816.
40. Rosenthal, J. A., Chen, H., Slepnev, V. I., Pellegrini, L., Salcini, A. E., di Fiore, P. P. and de Camilli, P. (1999). The epsins define a family of proteins that interact with components of the clathrin coat and contain a new protein module. J. Biol. Chem. 274, 33959-33965.
41. Schweisguth, F. (2004). Notch signaling activity. Curr. Biol. 14, R129-R138.
42. Seugnet, L., Simpson, P. and Haenlin, M. (1997). Requirement for dynamin during Notch signaling in Drosophila neurogenesis. Dev. Biol. 192, 585-598.
43. Shih, S. C., Katzmann, D. J., Schnell, J. D., Sutanto, M., Emr, S. D. and Hicke, L. (2002). Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat. Cell Biol. 4, 389-393.
44. Struhl, G. and Greenwald, I. (1999). Presenilin is required for activity and nuclear access of Notch in Drosophila. Nature 398, 522-525.
45. Struhl, G. and Adachi, A. (2000). Requirements for presenilin-dependent cleavage of notch and other transmembrane proteins. Mol. Cell 6, 625-636.
46. Struhl, G. and Greenwald, I. (2001). Presenilin-mediated transmembrane cleavage is required for Notch signal transduction in Drosophila. Proc. Natl. Acad. Sci. USA 98, 229-234.
47. Sun, X. and Artavanis-Tsakonas, S. (1996). The intracellular deletions of Delta and Serrate define dominant negative forms of the Drosophila Notch ligands. Development 122, 2465-2474.
48. Terrell, J., Shih, S., Dunn, R. and Hicke, L. (1998). A function for monoubiquitination in the internalization of a G protein-coupled receptor. Mol. Cell 1, 193-202.
49. Vervoort, M., Crozatier, M., Valle, D. and Vincent, A. (1999). The COE transcription factor Collier is a mediator of short-range Hedgehog-induced patterning of the Drosophila wing. Curr. Biol. 9, 632-639.
50. Wendland, B. (2002). Epsins: adaptors in endocytosis? Nat. Rev. Mol. Cell Biol. 3, 971-977.
51. Wendland, B., Steece, K. E. and Emr, S. D. (1999). Yeast epsins contain an essential N-terminal ENTH domain, bind clathrin and are required for endocytosis. EMBO J. 18, 4383-4393.
52. Yeh, E., Dermer, M., Commisso, C., Zhou, L., McGlade, C. J. and Boulianne, G. L. (2001). Neuralized functions as an E3 ubiquitin ligase during Drosophila development. Curr. Biol. 11 1675-1679.
53. Zecca, M., Basler, K. and Struhl, G. (1996). Direct and long-range action of a wingless morphogen gradient. Cell 87, 833-844.