Drosophila Neuralized Is a Ubiquitin Ligase that Promotes the Internalization and Degradation of Delta

Developmental Cell

Volumn 1, Issue 6, 2001, Pages 783-794

  Lai, Eric C ^a   Deblandre, Gisèle A ^b   Kintner, Chris ^b   Rubin, Gerald M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE PROTEINASE; DROSOPHILA PROTEIN; E6 ASSOCIATED PROTEIN; E6-ASSOCIATED PROTEIN; HOMEODOMAIN PROTEIN; HYBRID PROTEIN; LIGASE; MEMBRANE PROTEIN; MULTIENZYME COMPLEX; NERVE PROTEIN; NEU PROTEIN, DROSOPHILA; PROTEASOME; PROTEIN; UBIQUITIN; ZINC FINGER PROTEIN;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CELL LINE; CYTOLOGY; DROSOPHILA MELANOGASTER; EMBRYONIC STRUCTURES; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; FORELIMB; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; PHENOTYPE; PHOTORECEPTOR; PHYSIOLOGY; REPORTER GENE;

ANIMAL; CELL LINE; CYSTEINE ENDOPEPTIDASES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYONIC STRUCTURES; ENDOCYTOSIS; GENES, REPORTER; HOMEODOMAIN PROTEINS; HUMAN; LIGASES; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MULTIENZYME COMPLEXES; NERVE TISSUE PROTEINS; PHENOTYPE; PHOTORECEPTORS, INVERTEBRATE; RECOMBINANT FUSION PROTEINS; SUPPORT, NON-U.S. GOV'T; UBIQUITIN; WING; ZINC FINGERS;

EID: 0035651380     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1534-5807(01)00092-2     Document Type: Article

References (61)

1. Artavanis-Tsakonas S., Rand M.D., Lake R.J. Notch signaling. cell fate control and signal integration in development Science. 284:1999;770-776.
2. Baker N.E., Yu S.-Y. The R8-photoreceptor equivalence group in Drosophila. fate choice precedes regulated Delta transcription and is independent of Notch gene dose Mech. Dev. 74:1998;3-14.
3. Barolo S., Carver L.A., Posakony J.W. GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. Biotechniques. 29:2000;726-732.
4. Bellen H.J., O'Kane C.J., Wilson C., Grossniklaus U., Pearson R.K., Gehring W.J. P-element-mediated enhancer detection. a versatile method to study development in Drosophila Genes Dev. 3:1989;1288-1300.
5. Bonifacino J., Weissman A. Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu. Rev. Cell Dev. Biol. 14:1998;19-57.
6. Boulianne G.L., de la Concha A., Campos-Ortega J.A., Jan L.Y., Jan Y.N. The Drosophila neurogenic gene neuralized encodes a novel protein and is expressed in precursors of larval and adult neurons. EMBO J. 10:1991;2975-2983.
7. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 118:1993;401-415.
8. Capdevila J., Guerrero I. Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J. 13:1994;4459-4468.
9. Casci T., Vinos J., Freeman M. Sprouty, an intracellular inhibitor of Ras signaling. Cell. 96:1999;655-665.
10. Corbin V., Michelson A.M., Abmayr S.M., Neel V., Alcamo E., Maniatis T., Young M.W. A role for the Drosophila neurogenic genes in mesoderm formation. Cell. 67:1991;311-323.
11. Damke H., Baba T., Van der Bliek A., Schmidt S.L. Clathrin-independent pinocytosis is induced in cells over-expressing a temperature-sensitive mutant of dynamin. J. Cell Biol. 131:1995;69-80.
12. Deblandre G.A., Lai E.C., Kintner C. Xenopus Neuralized is a ubiquitin ligase that interacts with XDelta1 and regulates Notch signaling. Dev. Cell. 1:2001;795-806. this issue
13. Freeman M. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell. 87:1996;651-660.
14. Hartenstein A.Y., Rugendorff A., Tepass U., Hartenstein V. The function of the neurogenic genes during epithelial development in the Drosophila embryo. Development. 116:1992;1203-1220.
15. Heitzler P., Simpson P. The choice of cell fate in the epidermis of Drosophila. Cell. 64:1991;1083-1092.
16. Heitzler P., Simpson P. Altered epidermal growth factor-like sequences provide evidence for a role of Notch as a receptor in cell fate decisions. Development. 117:1993;1113-1123.
17. Heitzler P., Bourouis M., Ruel L., Carteret C., Simpson P. Genes of the Enhancer of split and achaete-scute complexes are required for a regulatory loop between Notch and Delta during lateral signalling in Drosophila. Development. 122:1996;161-171.
18. Hicke L. A new ticket for entry into budding vesicles-ubiquitin. Cell. 106:2001;527-530.
19. Hicke L., Riezman H. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell. 84:1996;277-287.
20. Hinz U., Giebel B., Campos-Ortega J.A. The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell. 76:1994;77-87.
21. Hu G., Zhang S., Vidal M., La Baer J., Xu T., Fearon E. Mammalian homologs of seven in absentia regulate DCC via the ubiquitin-proteasome pathway. Genes Dev. 11:1997;2701-2714.
22. Huppert S.S., Jacobsen T.L., Muskavitch M.A. Feedback regulation is central to Delta-Notch signalling required for Drosophila wing vein morphogenesis. Development. 124:1997;3283-3291.
23. Jackson P.K., Eldridge A.G., Freed E., Furstenthal L., Hsu J.Y., Kaiser B.K., Reimann J.D. The lore of the RINGS. substrate recognition and catalysis by ubiquitin ligases Trends Cell Biol. 10:2000;429-439.
24. Jacobsen T.L., Brennan K., Arias A.M., Muskavitch M.A.T. Cis-interactions between Delta and Notch modulate neurogenic signaling in Drosophila. Development. 125:1998;4531-4540.
25. Jeffers M., Taylor G., Weidner K., Omura S., Vande Woude G.F. Degradation of the Met kinase receptor by the ubiquitin-proteasome pathway. Mol. Cell. Biol. 17:1997;799-802.
26. Joazeiro C., Weissman A.M. RING finger proteins. mediators of ubiquitin ligase activity Cell. 102:2000;549-552.
27. Joazeiro C., Wing S., Huang H.-K., Leverson J., Hunter T., Liu Y.-C. The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science. 286:1999;309-312.
28. Klueg K.M., Parody T.R., Muskavitch M.A. Complex proteolytic processing acts on Delta, a transmembrane ligand for Notch, during Drosophila development. Mol. Biol. Cell. 9:1998;1709-1723.
29. Kooh P.J., Fehon R.G., Muskavitch M.A. Implications of dynamic patterns of Delta and Notch expression for cellular interactions during Drosophila development. Development. 117:1993;493-507.
30. Lai E.C., Rubin G.M. neuralized functions cell-autonomously to regulate a subset of Notch-dependent processes during adult Drosophila development. Dev. Biol. 231:2001;217-233. a.
31. Lai E.C., Rubin G.M. neuralized is essential for a subset of Notch pathway-dependent cell fate decisions during Drosophila eye development. Proc. Natl. Acad. Sci. USA. 98:2001;5637-5642. b.
32. Lehmann R., Jiménez F., Dietrich U., Campos-Ortega J. On the phenotype and development of mutants of early neurogenesis in Drosophila melanogaster. Roux's Arch. Dev. Biol. 192:1983;62-74.
33. Leverson J.D., Joazeiro C.A., Page A.M., Huang H.K., Hieter P., Hunter T. The APC11 RING-H2 finger mediates E2-dependent ubiquitination. Mol. Biol. Cell. 11:2000;2315-2325.
34. Li S., Li Y., Carthew R.W., Lai Z.C. Photoreceptor cell differentiation requires regulated proteolysis of the transcriptional repressor Tramtrack. Cell. 90:1997;469-478.
35. Lieber T., Kidd S., Alcamo E., Corbin V., Young M.W. Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal transduction and may point to a novel function for Notch in nuclei. Genes Dev. 7:1993;1949-1965.
36. Lorick K.L., Jensen J.P., Fang S., Ong A., Hatakeyama S., Weissman A. RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc. Natl. Acad. Sci. USA. 96:1999;11364-11369.
37. Martin-Bermundo M.D., Carmena A., Jimenez F. Neurogenic genes control gene expression at the transcriptional level in early neurogenesis and in mesectoderm specification. Development. 121:1995;219-224.
38. Micchelli C.A., Rulifson E.J., Blair S.S. 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. 124:1997;1485-1495.
39. Mimnaugh E., Chavany C., Neckers L. Polyubiquitination and proteasomal degradation of the p185(c-erb-2) receptor protein tyrosine kinase induced by geldanamycin. J. Biol. Chem. 271:1996;22796-22801.
40. Mori S., Tanaka K., Omura S., Saito Y. Degradation process of ligand-stimulated platelet-derived growth factor β-receptor involves ubiquitin-proteasome proteolytic pathway. J. Biol. Chem. 270:1995;29447-29452.
41. Nakamura H., Yoshida M., Tsuiki H., Ito K., Ueno M., Nakao M., Oka K., Tada M., Kochi M., Kuratsu J.et al. Identification of a human homolog of the Drosophila neuralized gene within the 10q25.1 malignant astrocytoma deletion region. Oncogene. 16:1998;1009-1019.
42. Neufeld T.P., Tang A.H., Rubin G.M. A genetic screen to identify components of the sina signaling pathway in Drosophila eye development. Genetics. 148:1998;277-286.
43. Parks A.L., Turner R., Muskavitch M.A.T. Relationships between complex Delta expression and the specification of retinal cell fates during Drosophila eye development. Mech. Dev. 50:1995;201-216.
44. Parks A., Klueg K., Stout J., Muskavitch M.A. Ligand endocytosis drives receptor dissociation and activation in the Notch pathway. Development. 127:2000;1373-1385.
45. Poodry C.A. shibire, a neurogenic mutant of Drosophila. Dev. Biol. 138:1990;464-472.
46. Price B.D., Chang Z., Smith R., Bockheim S., Laughon A. The Drosophila neuralized gene encodes a C3HC4 zinc finger. EMBO J. 12:1993;2411-2418.
47. Rebay I., Fleming R.J., Fehon R.G., Cherbas L., Cherbas P., Artavanis-Tsakonas S. Specific EGF repeats of Notch mediate interactions with Delta and Serrate. implications for Notch as a multifunctional receptor Cell. 67:1991;687-699.
48. Rotin D., Staub O., Haguenauer-Tsapis R. Ubiquitination and endocytosis of plasma membrane proteins. role of Nedd4/Rsp5p family of ubiquitin-protein ligases J. Membr. Biol. 176:2000;1-17.
49. Ruan Y., Tecott L., Jiang M.-M., Jan L.Y., Jan Y.N. Ethanol hypersensitivity and olfactory discrimination defect in mice lacking a homolog of Drosophila neuralized. Proc. Natl. Acad. Sci. USA. 98:2001;9907-9912.
50. Saville J., Belote J.M. Identification of an essential gene, l(3)73Ai, with a dominant temperature-sensitive lethal allele, encoding a Drosophila proteasome subunit. Proc. Natl. Acad. Sci. USA. 90:1993;8842-8846.
51. Schrons H., Knust E., Campos-Ortega J.A. The Enhancer of split complex and adjacent genes in the 96F region of Drosophila melanogaster are required for segregation of neural and epidermal progenitor cells. Genetics. 132:1992;481-503.
52. Schweisguth F. Dominant-negative mutation in the B2 and B6 proteasome-subunit genes affect alternative cell fate decisions in the Drosophila sense organ lineage. Proc. Natl. Acad. Sci. USA. 96:1999;11382-11386.
53. Seugnet L., Simpson P., Haenlin M. Requirement for dynamin during Notch signaling in Drosophila neurogenesis. Dev. Biol. 192:1997;585-598.
54. Staehling-Hampton K., Jackson P., Clark M., Brand A.H., Hoffman F.M. Specificity of bone morphogenetic protein-related factors. cell fate and gene expression changes in Drosophila embryos induced by decapentaplegic but not 60A Cell Growth Differ. 5:1994;585-593.
55. Staub O., Gautschi I., Ishikawa T., Breitschopf K., Ciechanover A., Schild L., Rotin D. Regulation of stability and function of the epithelial Na-channel (ENaC) by ubiquitination. EMBO J. 16:1997;6325-6336.
56. Strous G., van Kerkhof P., Govers R., Ciechanover A., Schwartz A. The ubiquitin conjugation system is required for ligand-induced endocytosis and degradation of the growth hormone receptor. EMBO J. 15:1996;3806-3812.
57. Struhl G., Adachi A. Nuclear access and action of Notch in vivo. Cell. 93:1998;649-660.
58. Sun X., Artavanis-Tsakonas S. The intracellular deletions of Delta and Serrate define dominant negative forms of the Drosophila Notch ligands. Development. 122:1996;2465-2474.
59. Tang A.H., Neufeld T.P., Kwan E., Rubin G.M. PHYL acts to down-regulate TTK88, a transcriptional repressor of neuronal cell fates, by a SINA-dependent mechanism. Cell. 90:1997;459-467.
60. Wiley H., Herbst J., Walsh B., Lauffenburger D., Rosenfeld M.G., Gill G. The role of tyrosine kinase activity in endocytosis compartmentation, and down-regulation of the epidermal growth factor receptor. J. Biol. Chem. 266:1991;11083-11094.
61. Yeh E., Zhou L., Rudzik N., Boulianne G.L. Neuralized functions cell autonomously to regulate Drosophila sense organ development. EMBO J. 19:2000;4827-4837.