The characterization of zebrafish antimorphic mib alleles reveals that Mib and Mind bomb-2 (Mib2) function redundantly

Developmental Biology

Volumn 305, Issue 1, 2007, Pages 14-27

  Zhang, Chengjin ^a   Li, Qing ^a   Lim, Chiaw Hwee ^a   Qiu, Xuehui ^a   Jiang, Yun Jin ^a  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

Delta; E3 ligase; Endocytosis; mib alleles; Mib homologs; Notch

Indexed keywords

CELL PROTEIN; MUTANT PROTEIN; NOTCH RECEPTOR; PROTEIN MIB; PROTEIN MIB2; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STRAIN COS7; EMBRYO; EMBRYO DEVELOPMENT; ENDOCYTOSIS; GENE; GENE CONTROL; MIB GENE; MIB2 GENE; MISSENSE MUTATION; NONHUMAN; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; NULL ALLELE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ZEBRA FISH;

DANIO RERIO;

EID: 34247262037     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.01.034     Document Type: Article

References (84)

1. Artavanis-Tsakonas S., Rand M.D., and Lake R.J. Notch signaling: cell fate control and signal integration in development. Science 284 (1999) 770-776
2. Bardin A.J., and Schweisguth F. Bearded family members inhibit Neuralized-mediated endocytosis and signaling activity of Delta in Drosophila. Dev. Cell 10 (2006) 245-255
3. Bessho Y., Sakata R., Komatsu S., Shiota K., Yamada S., and Kageyama R. Dynamic expression and essential functions of Hes7 in somite segmentation. Genes Dev. 15 (2001) 2642-2647
4. Bessho Y., Hirata H., Masamizu Y., and Kageyama R. Periodic repression by the bHLH factor Hes7 is an essential mechanism for the somite segmentation clock. Genes Dev. 17 (2003) 1451-1456
5. Bisson S.A., Ujack E.E., and Robbins S.M. Isolation and characterization of a novel, transforming allele of the c-Cbl proto-oncogene from a murine macrophage cell line. Oncogene 21 (2002) 3677-3687
6. Blader P., Fischer N., Gradwohl G., Guillemont F., and Strähle U. The activity of neurogenin1 is controlled by local cues in the zebrafish embryo. Development 124 (1997) 4557-4569
7. Castro B., Barolo S., Bailey A.M., and Posakony J.W. Lateral inhibition in proneural clusters: cis-regulatory logic and default repression by Suppressor of Hairless. Development 132 (2005) 3333-3344
8. Chen W., and Corliss D.C. Three modules of zebrafish Mind bomb work cooperatively to promote Delta ubiquitination and endocytosis. Dev. Biol. 267 (2004) 361-373
9. Chen M.S., Obar R.A., Schroeder C.C., Austin T.W., Poodry C.A., Wadsworth S.C., and Vallee R.B. Multiple forms of Dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature 351 (1991) 583-586
10. Chitnis A. Why is Delta endocytosis required for effective activation of Notch?. Dev. Dyn. 235 (2006) 886-894
11. Cornell R.A., and Eisen J.S. Delta/Notch signaling promotes formation of zebrafish neural crest by repressing Neurogenin 1 function. Development 129 (2002) 2639-2648
12. Culi J., and Modolell J. Proneural gene self-stimulation in neural precursors: an essential mechanism for sense organ development that is regulated by Notch signaling. Genes Dev. 12 (1998) 2036-2047
13. Dale J.K., Maroto M., Dequeant M.L., Malapert P., McGrew M., and Pourquié O. Periodic notch inhibition by lunatic fringe underlies the chick segmentation clock. Nature 421 (2003) 275-278
14. Deblandre G.A., Lai E.C., and Kintner C. Xenopus Neuralized is a ubiquitin ligase that interacts with XDelta1 and regulates Notch signaling. Dev. Cell 1 (2001) 795-806
15. Fjose A., Izpisúa-Belmonte J.-C., Fromental-Ramain C., and Duboule D. Expression of the zebrafish gene hlx-1 in the prechordal plate and during CNS development. Development 120 (1994) 71-81
16. Gajewski M., Sieger D., Alt B., Leve C., Hans S., Wolff C., Rohr K.B., and Tautz D. Anterior and posterior waves of cyclic her1 gene expression are differentially regulated in the presomitic mesoderm of zebrafish. Development 130 (2003) 4269-4278
17. Geling A., Steiner H., Willem M., Bally-Cuif L., and Haass C. A γ-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep. 3 (2002) 688-694
18. Gigliani F., Longo F., Gaddini L., and Battaglia P.A. Interactions among the bHLH domains of the proteins encoded by the Enhancer of split and achaete-scute gene complexes of Drosophila. Mol. Gen. Genet. 251 (1996) 628-634
19. Gupta-Rossi N., Six E., LeBail O., Logeat F., Chastagner P., Olry A., Israël A., and Brou C. Monoubiquitination and endocytosis direct γ-secretase cleavage of activated Notch receptor. J. Cell Biol. 166 (2004) 73-83
20. Haddon C., Jiang Y.-J., Smithers L., and Lewis J. Delta-Notch signalling and the patterning of sensory cell differentiation in the zebrafish ear: evidence from the mind bomb mutant. Development 125 (1998) 4637-4644
21. Harder T., Scheiffele P., Verkade P., and Simons K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141 (1998) 929-942
22. Hashizume R., Fukuda M., Maeda I., Nishikawa H., Oyake D., Yabuki Y., Ogata H., and Ohta T. The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J. Biol. Chem. 276 (2001) 14537-14540
23. Heitzler P., Bourouis M., Ruel L., Carteret C., and 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
24. Henry C.A., Urban M.K., Dill K.K., Merlie J.P., Page M.F., Kimmel C.B., and Amacher S.L. Two linked hairy/Enhancer of split-related zebrafish genes, her1 and her7, function together to refine alternating somite boundaries. Development 129 (2002) 3693-3704
25. Hicke L. A new ticket for entry into budding vesicles-ubiquitin. Cell 106 (2001) 527-530
26. Holley S.A., Jülich D., Rauch G.J., Geisler R., and Nüsslein-Volhard C. her1 and the notch pathway function within the oscillator mechanism that regulates zebrafish somitogenesis. Development 129 (2002) 1175-1183
27. Hu G., and Fearon E.R. Siah-1 N-terminal RING domain is required for proteolysis function, and C-terminal sequences regulate oligomerization and binding to target proteins. Mol. Cell. Biol. 19 (1999) 724-732
28. Huppert S.S., Ilagan M.X., De Strooper B., and Kopan R. Analysis of Notch function in presomitic mesoderm suggests a γ-secretase-independent role for presenilins in somite differentiation. Dev. Cell 8 (2005) 677-688
29. 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., Weissman A.M., Lewis J., Chandrasekharappa S.C., and Chitnis A.B. Mind bomb is a ubiquitin ligase that is essential for efficient activation of notch signaling by delta. Dev. Cell 4 (2003) 67-82
30. Jehn B.M., Dittert I., Beyer S., von der Mark K., and Bielke W. c-Cbl binding and ubiquitin-dependent lysosomal degradation of membrane-associated Notch1. J. Biol. Chem. 277 (2002) 8033-8040
31. Jiang Y.-J., Brand M., Heisenberg C.-P., Beuchle D., Furutani-Seiki M., Kelsh R.N., Warga R.M., Granato M., Haffter P., Hammerschmidt M., Kane D.A., Mullins M.C., Odenthal J., van Eeden F.J.M., and Nüsslein-Volhard C. Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio. Development 123 (1996) 205-216
32. Jiang Y.-J., Aerne B.L., Smithers L., Haddon C., Ish-Horowicz D., and Lewis J. Notch signalling and the synchronization of the somite segmentation clock. Nature 408 (2000) 475-479
33. Jin Y., Blue E.K., Dixon S., Shao Z., and Gallagher P.J. A death-associated protein kinase (DAPK)-interacting protein, DIP-1, is an E3 ubiquitin ligase that promotes tumor necrosis factor-induced apoptosis and regulates the cellular levels of DAPK. J. Biol. Chem. 277 (2002) 46980-46986
34. Jülich D., Lim C.H., Round J., Nicolaije C., Schroeder J., Davies A., Tübingen 2000 Screen Consortium, Geisler R., Lewis J., Jiang Y.-J., and Holley S.A. beamter/deltaC and the role of Notch ligands in the zebrafish somite segmentation, hindbrain neurogenesis and hypochord differentiation. Dev. Biol. 286 (2005) 391-404
35. Juven-Gershon T., Shifman O., Unger T., Elkeles A., Haupt Y., and Oren M. The Mdm2 oncoprotein interacts with the cell fate regulator Numb. Mol. Cell. Biol. 18 (1998) 3974-3982
36. Kageyama R., and Ohtsuka T. The Notch-Hes pathway in mammalian neural development. Cell Res. 9 (1999) 179-188
37. Kelsh R.N., Schmid B., and Eisen J.S. Genetic analysis of melanophore development in zebrafish embryos. Dev. Biol. 225 (2000) 277-293
38. Kim C.H., Ueshima E., Muraoka O., Tanaka H., Yeo S.Y., Huh T.L., and Miki N. Zebrafish elav/HuC homologue as a very early neuronal marker. Neurosci. Lett. 216 (1996) 109-112
39. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., and Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203 (1995) 253-310
40. Koo B.-K., Yoon K.-J., Yoo K.-W., Lim H.-S., Song R., So J.-H., Kim C.-H., and Kong Y.-Y. Mind bomb-2 is an E3 ligase for Notch ligand. J. Biol. Chem. 280 (2005) 22335-22342
41. Korzh V., Edlund T., and Thor S. Zebrafish primary neurons initiate expression of the LIM homeodomain protein Isl-1 at the end of gastrulation. Development 118 (1993) 417-425
42. Kumar S., Talis A.L., and Howley P.M. Identification of HHR23A as a substrate for E6-associated protein-mediated ubiquitination. J. Biol. Chem. 274 (1999) 18785-18792
43. Lai E.C., Deblandre G.A., Kintner C., and Rubin G.M. Drosophila Neuralized is a ubiquitin ligase that promotes the internalization and degradation of Delta. Dev. Cell 1 (2001) 783-794
44. Lai E.C., Roegiers F., Qin X., Jan Y.N., and Rubin G.M. The ubiquitin ligase Drosophila Mind bomb promotes Notch signaling by regulating the localization and activity of Serrate and Delta. Development 13 (2005) 2333-2343
45. Lamar E., Deblandre G., Wettstein D., Gawantka V., Pollet N., Niehrs C., and Kintner C. Nrarp is a novel intracellular component of the Notch signaling pathway. Genes Dev. 15 (2001) 1885-1899
46. Latimer A.J., Dong X., Markov Y., and Appel B. Delta-Notch signaling induces hypochord development in zebrafish. Development 129 (2002) 2555-2563
47. Le Borgne R., Bardin A., and Schweisguth F. The roles of receptor and ligand endocytosis in regulating Notch signaling. Development 132 (2005) 1751-1762
48. Le Borgne R., Remaud S., Hamel S., and Schweisguth F. Two distinct E3 ubiquitin ligases have complementary functions in the regulation of delta and serrate signaling in Drosophila. PLoS Biol. 3 (2005) e96
49. Ma M., and Jiang Y.-J. Jagged2a-Notch signaling mediates cell fate choice in zebrafish pronephric duct. PLoS Genet. 3 (2007) e18
50. Ma Q., Kintner C., and Anderson D.J. Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87 (1996) 43-52
51. Maquat L.E. Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat. Rev. Mol. Cell Biol. 5 (2004) 89-99
52. Mumm J.S., and Kopan R. Notch signaling: from the outside in. Dev. Biol. 228 (2000) 151-165
53. Nie J., McGill M.A., Dermer M., Dho S.E., Wolting C.D., and McGlade C.J. LNX functions as a RING type E3 ubiquitin ligase that targets the cell fate determinant Numb for ubiquitin-dependent degradation. EMBO J. 21 (2002) 93-102
54. Oates A.C., and Ho R.K. Hairy/E(spl)-related (Her) genes are central components of the segmentation oscillator and display redundancy with the Delta/Notch signaling pathway in the formation of anterior segmental boundaries in the zebrafish. Development 129 (2002) 2929-2946
55. Parks A.L., Klueg K.M., Stout J.R., and Muskavitch M.A.T. Ligand endocytosis drives receptor dissociation and activation in the Notch pathway. Development 127 (2000) 1373-1385
56. Pavlopoulos E., Pitsouli C., Klueg K.M., Muskavitch M.A.T., Moschonas N.K., and Delidakis C. neuralized encodes a peripheral membrane protein involved in Delta signaling and endocytosis. Dev. Cell 1 (2001) 807-816
57. Pickart C.M. Ubiquitin enters the new millennium. Mol. Cell 8 (2001) 499-504
58. Pitsouli C., and Delidakis C. The interplay between DSL proteins and ubiquitin ligases in Notch signaling. Development 132 (2005) 4041-4050
59. Poodry C.A. shibire, a neurogenic mutant of Drosophila. Dev. Biol. 138 (1990) 464-472
60. Pourquié O. The segmentation clock: converting embryonic time into spatial pattern. Science 301 (2003) 328-330
61. Qiu L., Joazeiro C., Fang N., Wang H.Y., Elly C., Altman Y., Fang D., Hunter T., and Liu Y.C. Recognition and ubiquitination of Notch by Itch, a Hect-type E3 ubiquitin ligase. J. Biol. Chem. 275 (2000) 35734-35737
62. Qiu X., Xu H., Haddon C., Lewis J., and Jiang Y.-J. Sequence and embryonic expression of three zebrafish fringe genes, lunatic fringe, radical fringe, and manic fringe. Dev. Dyn. 231 (2004) 621-630
63. Rida P.C.G., Le Minh N., and Jiang Y.-J. A Notch feeling of somite segmentation and beyond. Dev. Biol. 265 (2004) 2-22
64. Sakata T., Sakaguchi H., Tsuda L., Higashitani A., Aigaki T., Matsuno K., and Hayashi S. Drosophila Nedd4 regulates endocytosis of Notch and suppresses its ligand-independent activation. Curr. Biol. 14 (2004) 2228-2236
65. Schier A.F., Neuhauss S.C., Harvey M., Malicki J., Solnica-Krezel L., Stainier D.Y., Zwartkruis F., Abdelilah S., Stemple D.L., Rangini Z., Yang H., and Driever W. Mutations affecting the development of the embryonic zebrafish brain. Development 123 (1996) 165-178
66. Schweisguth F. Dominant-negative mutation in the β2 and β6 proteasome subunit genes affect alternative cell fate decisions in the Drosophila sense organ lineage. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 11382-11386
67. Seugnet L., Simpson P., and Haenlin M. Requirement for dynamin during Notch signaling in Drosophila neurogenesis. Dev. Biol. 192 (1997) 585-598
68. Sharp D.A., Kratowicz S.A., Sank M.J., and George D.L. Stabilization of the MDM2 oncoprotein by interaction with the structurally related MDMX protein. J. Biol. Chem. 274 (1999) 38189-38196
69. Sieger D., Tautz D., and Gajewski M. The role of Suppressor of Hairless in Notch mediated signalling during zebrafish somitogenesis. Mech. Dev. 120 (2003) 1083-1094
70. Smithers L., Haddon C., Jiang Y.-J., and Lewis J. Sequence and embryonic expression of deltaC in the zebrafish. Mech. Dev. 90 (2000) 119-123
71. Stad R., Little N.A., Xirodimas D.P., Frenk R., van der Eb A.J., Lane D.P., Saville M.K., and Jochemsen A.G. Mdmx stabilizes p53 and Mdm2 via two distinct mechanisms. EMBO Rep. 2 (2001) 1029-1034
72. Susini L., Passer B.J., Amzallag-Elbaz N., Juven-Gershon T., Prieur S., Privat N., Tuynder M., Gendron M.-C., Israël A., Amson R., Oren M., and Telerman A. Siah-1 binds and regulates the function of Numb. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 15067-15072
73. Takeuchi T., Heng H.H., Ye C.J., Liang S.B., Iwata J., Sonobe H., and Ohtsuki Y. Down-regulation of a novel actin-binding molecule, skeletrophin, in malignant melanoma. Am. J. Pathol. 163 (2003) 1395-1404
74. Takeuchi T., Adachi Y., and Ohtsuki Y. Skeletrophin, a novel ubiquitin ligase to the intracellular region of Jagged-2, is aberrantly expressed in multiple myeloma. Am. J. Pathol. 166 (2005) 1817-1826
75. Takeuchi T., Adachi Y., Sonobe H., Furihata M., and Ohtsuki Y. A ubiquitin ligase, skeletrophin, is a negative regulator of melanoma invasion. Oncogene 25 (2006) 7059-7069
76. Takke C., and Campos-Ortega J.A. her1, a zebrafish pair-rule like gene, acts downstream of notch signalling to control somite development. Development 126 (1999) 3005-3014
77. Takke C., Dornseifer P., von Weizsäcker E., and Campos-Ortega J.A. her4, a zebrafish homologue of the Drosophila neurogenic gene E(spl), is a target of NOTCH signalling. Development 126 (1999) 1811-1821
78. van der Bliek A.M., and Meyerowitz E.M. Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351 (1991) 411-414
79. Wang W., and Struhl G. Distinct roles for Mind bomb, Neuralized and Epsin in mediating DSL endocytosis and signaling in Drosophila. Development 132 (2005) 2883-2894
80. Weissman A.M. Themes and variations on ubiquitylation. Nat. Rev., Mol. Cell Biol. 2 (2001) 169-178
81. Wettstein D.A., Turner D.L., and Kintner C. The Xenopus homolog of Drosophila Suppressor of Hairless mediates Notch signaling during primary neurogenesis. Development 124 (1997) 693-702
82. Wilkin M.B., Carbery A.M., Fostier M., Aslam H., Mazaleyrat S.L., Higgs J., Myat A., Evans D.A., Cornell M., and Baron M. Regulation of Notch endosomal sorting and signaling by Drosophila Nedd4 family proteins. Curr. Biol. 14 (2004) 2237-2244
83. Wu G., Lyapina S., Das I., Li J., Gurney M., Pauley A., Chui I., Deshaies R.J., and Kitajewski J. SEL-10 is an inhibitor of notch signaling that targets notch for ubiquitin-mediated protein degradation. Mol. Cell. Biol. 21 (2001) 7403-7415
84. Zhang C., Li Q., and Jiang Y.-J. Zebrafish Mib and Mib2 are mutual E3 ubiquitin ligases with common and specific Delta substrates. J. Mol. Biol. 366 (2007) 1115-1128