Rumi Is a CAP10 Domain Glycosyltransferase that Modifies Notch and Is Required for Notch Signaling

Cell

Volumn 132, Issue 2, 2008, Pages 247-258

  Acar, Melih ^a   Jafar Nejad, Hamed ^a   Takeuchi, Hideyuki ^b   Rajan, Akhila ^a   Ibrani, Dafina ^a   Rana, Nadia A ^b   Pan, Hongling ^a   Haltiwanger, Robert S ^b   Bellen, Hugo J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

DEVBIO; PROTEINS; SIGNALING

Indexed keywords

CELL PROTEIN; EPIDERMAL GROWTH FACTOR; GLUCOSE; GLUCOSYLTRANSFERASE; GLYCOSYLTRANSFERASE; NOTCH RECEPTOR; PROTEIN RUMI; SERINE; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; DROSOPHILA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; SENSE ORGAN;

EID: 38649125625     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.12.016     Document Type: Article

References (70)

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. Bellen H.J., Levis R.W., Liao G., He Y., Carlson J.W., Tsang G., Evans-Holm M., Hiesinger P.R., Schulze K.L., Rubin G.M., et al. The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 167 (2004) 761-781
3. Bolos V., Grego-Bessa J., and de la Pompa J.L. Notch signaling in development and cancer. Endocr. Rev. 28 (2007) 339-363
4. Brou C., Logeat F., Gupta N., Bessia C., LeBail O., Doedens J.R., Cumano A., Roux P., Black R.A., and Israel A. A novel proteolytic cleavage involved in Notch signaling: the role of the disintegrin-metalloprotease TACE. Mol. Cell 5 (2000) 207-216
5. Bruckner K., Perez L., Clausen H., and Cohen S. Glycosyltransferase activity of Fringe modulates Notch-Delta interactions. Nature 406 (2000) 411-415
6. Carlson M.E., and Conboy I.M. Regulating the Notch pathway in embryonic, adult and old stem cells. Curr. Opin. Pharmacol. 7 (2007) 303-309
7. Chang Y.C., and Kwon-Chung K.J. Isolation, characterization, and localization of a capsule-associated gene, CAP10, of Cryptococcus neoformans. J. Bacteriol. 181 (1999) 5636-5643
8. Childress J.L., Acar M., Tao C., and Halder G. Lethal giant discs, a novel C2-domain protein, restricts notch activation during endocytosis. Curr. Biol. 16 (2006) 2228-2233
9. de Celis J.F., Bray S., and Garcia-Bellido A. Notch signalling regulates veinlet expression and establishes boundaries between veins and interveins in the Drosophila wing. Development 124 (1997) 1919-1928
10. De Strooper B. Aph-1, Pen-2, and Nicastrin with Presenilin generate an active gamma-Secretase complex. Neuron 38 (2003) 9-12
11. De Strooper B., Annaert W., Cupers P., Saftig P., Craessaerts K., Mumm J.S., Schroeter E.H., Schrijvers V., Wolfe M.S., Ray W.J., et al. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 398 (1999) 518-522
12. Emery G., Hutterer A., Berdnik D., Mayer B., Wirtz-Peitz F., Gaitan M.G., and Knoblich J.A. Asymmetric Rab 11 endosomes regulate delta recycling and specify cell fate in the Drosophila nervous system. Cell 122 (2005) 763-773
13. Gallagher C.M., and Knoblich J.A. The conserved c2 domain protein lethal (2) giant discs regulates protein trafficking in Drosophila. Dev. Cell 11 (2006) 641-653
14. Haines N., and Irvine K.D. Glycosylation regulates Notch signalling. Nat. Rev. Mol. Cell Biol. 4 (2003) 786-797
15. Hori K., Fostier M., Ito M., Fuwa T.J., Go M.J., Okano H., Baron M., and Matsuno K. Drosophila deltex mediates suppressor of Hairless-independent and late-endosomal activation of Notch signaling. Development 131 (2004) 5527-5537
16. Hu Y., Ye Y., and Fortini M.E. Nicastrin is required for gamma-secretase cleavage of the Drosophila Notch receptor. Dev. Cell 2 (2002) 69-78
17. Jaekel R., and Klein T. The Drosophila Notch inhibitor and tumor suppressor gene lethal (2) giant discs encodes a conserved regulator of endosomal trafficking. Dev. Cell 11 (2006) 655-669
18. Jafar-Nejad H., Andrews H.K., Acar M., Bayat V., Wirtz-Peitz F., Mehta S.Q., Knoblich J.A., and Bellen H.J. Sec15, a component of the exocyst, promotes notch signaling during the asymmetric division of Drosophila sensory organ precursors. Dev. Cell 9 (2005) 351-363
19. Jarriault S., Brou C., Logeat F., Schroeter E.H., Kopan R., and Israel A. Signalling downstream of activated mammalian Notch. Nature 377 (1995) 355-358
20. Joutel A., Corpechot C., Ducros A., Vahedi K., Chabriat H., Mouton P., Alamowitch S., Domenga V., Cecillion M., Marechal E., et al. Notch3 mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia. Nature 383 (1996) 707-710
21. Kidd S., and Lieber T. Furin cleavage is not a requirement for Drosophila Notch function. Mech. Dev. 115 (2002) 41-51
22. Lai E.C. Notch signaling: control of cell communication and cell fate. Development 131 (2004) 965-973
23. Lai E.C., and Orgogozo V. A hidden program in Drosophila peripheral neurogenesis revealed: fundamental principles underlying sensory organ diversity. Dev. Biol. 269 (2004) 1-17
24. Le Borgne R. Regulation of Notch signalling by endocytosis and endosomal sorting. Curr. Opin. Cell Biol. 18 (2006) 213-222
25. Le Borgne R., Bardin A., and Schweisguth F. The roles of receptor and ligand endocytosis in regulating Notch signaling. Development 132 (2005) 1751-1762
26. Lecourtois M., and Schweisguth F. The neurogenic suppressor of hairless DNA-binding protein mediates the transcriptional activation of the enhancer of split complex genes triggered by Notch signaling. Genes Dev. 9 (1995) 2598-2608
27. Lee T., and Luo L. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 24 (2001) 251-254
28. Li L., Krantz I.D., Deng Y., Genin A., Banta A.B., Collins C.C., Qi M., Trask B.J., Kuo W.L., Cochran J., et al. Alagille syndrome is caused by mutations in human Jagged1, which encodes a ligand for Notch1. Nat. Genet. 16 (1997) 243-251
29. Lieber T., Kidd S., and Young M.W. kuzbanian-mediated cleavage of Drosophila Notch. Genes Dev. 16 (2002) 209-221
30. Luo Y., Koles K., Vorndam W., Haltiwanger R.S., and Panin V.M. Protein O-fucosyltransferase 2 adds O-fucose to thrombospondin type 1 repeats. J. Biol. Chem. 281 (2006) 9393-9399
31. Luo Y., Nita-Lazar A., and Haltiwanger R.S. Two distinct pathways for O-fucosylation of epidermal growth factor-like or thrombospondin type 1 repeats. J. Biol. Chem. 281 (2006) 9385-9392
32. Malecki M.J., Sanchez-Irizarry C., Mitchell J.L., Histen G., Xu M.L., Aster J.C., and Blacklow S.C. Leukemia-associated mutations within the NOTCH1 heterodimerization domain fall into at least two distinct mechanistic classes. Mol. Cell. Biol. 26 (2006) 4642-4651
33. Manseau L., Baradaran A., Brower D., Budhu A., Elefant F., Phan H., Philp A.V., Yang M., Glover D., Kaiser K., et al. GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev. Dyn. 209 (1997) 310-322
34. Moloney D.J., Panin V.M., Johnston S.H., Chen J., Shao L., Wilson R., Wang Y., Stanley P., Irvine K.D., Haltiwanger R.S., et al. Fringe is a glycosyltransferase that modifies Notch. Nature 406 (2000) 369-375
35. Moloney D.J., Shair L.H., Lu F.M., Xia J., Locke R., Matta K.L., and Haltiwanger R.S. Mammalian Notch1 is modified with two unusual forms of O-linked glycosylation found on epidermal growth factor-like modules. J. Biol. Chem. 275 (2000) 9604-9611
36. Mumm J.S., Schroeter E.H., Saxena M.T., Griesemer A., Tian X., Pan D.J., Ray W.J., and Kopan R. A ligand-induced extracellular cleavage regulates gamma-secretase-like proteolytic activation of Notch1. Mol. Cell 5 (2000) 197-206
37. Nita-Lazar A., and Haltiwanger R.S. Methods for analysis of O-linked modifications on epidermal growth factor-like and thrombospondin type 1 repeats. Methods Enzymol. 417 (2006) 93-111
38. Oda T., Elkahloun A.G., Pike B.L., Okajima K., Krantz I.D., Genin A., Piccoli D.A., Meltzer P.S., Spinner N.B., Collins F.S., et al. Mutations in the human Jagged1 gene are responsible for Alagille syndrome. Nat. Genet. 16 (1997) 235-242
39. Okabayashi K., Hasegawa A., and Watanabe T. Microreview: Capsule-associated genes of Cryptococcus neoformans. Mycopathologia 163 (2007) 1-8
40. Okajima T., and Irvine K.D. Regulation of notch signaling by o-linked fucose. Cell 111 (2002) 893-904
41. Okajima T., Xu A., and Irvine K.D. Modulation of notch-ligand binding by protein O-fucosyltransferase 1 and fringe. J. Biol. Chem. 278 (2003) 42340-42345
42. Okajima T., Xu A., Lei L., and Irvine K.D. Chaperone activity of protein O-fucosyltransferase 1 promotes notch receptor folding. Science 307 (2005) 1599-1603
43. Pan D., and Rubin G.M. Kuzbanian controls proteolytic processing of Notch and mediates lateral inhibition during Drosophila and vertebrate neurogenesis. Cell 90 (1997) 271-280
44. Panin V.M., Papayannopoulos V., Wilson R., and Irvine K.D. Fringe modulates Notch-ligand interactions. Nature 387 (1997) 908-912
45. Parks A.L., Klueg K.M., Stout J.R., and Muskavitch M.A. Ligand endocytosis drives receptor dissociation and activation in the Notch pathway. Development 127 (2000) 1373-1385
46. Patil C., and Walter P. Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr. Opin. Cell Biol. 13 (2001) 349-355
47. Rampal R., Li A.S., Moloney D.J., Georgiou S.A., Luther K.B., Nita-Lazar A., and Haltiwanger R.S. Lunatic fringe, manic fringe, and radical fringe recognize similar specificity determinants in O-fucosylated epidermal growth factor-like repeats. J. Biol. Chem. 280 (2005) 42454-42463
48. Ricketts L.M., Dlugosz M., Luther K.B., Haltiwanger R.S., and Majerus E.M. O-fucosylation is required for ADAMTS13 secretion. J. Biol. Chem. 282 (2007) 17014-17023
49. Ryoo H.D., Domingos P.M., Kang M.J., and Steller H. Unfolded protein response in a Drosophila model for retinal degeneration. EMBO J. 26 (2007) 242-252
50. Sasaki N., Sasamura T., Ishikawa H.O., Kanai M., Ueda R., Saigo K., and Matsuno K. Polarized exocytosis and transcytosis of Notch during its apical localization in Drosophila epithelial cells. Genes Cells 12 (2007) 89-103
51. Sasamura T., Sasaki N., Miyashita F., Nakao S., Ishikawa H.O., Ito M., Kitagawa M., Harigaya K., Spana E., Bilder D., et al. neurotic, a novel maternal neurogenic gene, encodes an O-fucosyltransferase that is essential for Notch-Delta interactions. Development 130 (2003) 4785-4795
52. Sasamura T., Ishikawa H.O., Sasaki N., Higashi S., Kanai M., Nakao S., Ayukawa T., Aigaki T., Noda K., Miyoshi E., et al. The O-fucosyltransferase O-fut1 is an extracellular component that is essential for the constitutive endocytic trafficking of Notch in Drosophila. Development 134 (2007) 1347-1356
53. Schweisguth F. Notch signaling activity. Curr. Biol. 14 (2004) R129-R138
54. Shao L., and Haltiwanger R.S. O-fucose modifications of epidermal growth factor-like repeats and thrombospondin type 1 repeats: unusual modifications in unusual places. Cell. Mol. Life Sci. 60 (2003) 241-250
55. Shao L., Luo Y., Moloney D.J., and Haltiwanger R. O-glycosylation of EGF repeats: identification and initial characterization of a UDP-glucose: protein O-glucosyltransferase. Glycobiology 12 (2002) 763-770
56. Shao L., Moloney D.J., and Haltiwanger R. Fringe modifies O-fucose on mouse Notch1 at epidermal growth factor-like repeats within the ligand-binding site and the Abruptex region. J. Biol. Chem. 278 (2003) 7775-7782
57. Shi S., and Stanley P. Protein O-fucosyltransferase 1 is an essential component of Notch signaling pathways. Proc. Natl. Acad. Sci. USA 100 (2003) 5234-5239
58. Staehling-Hampton K., Jackson P.D., Clark M.J., Brand A.H., and Hoffmann 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
59. Struhl G., and Adachi A. Nuclear access and action of notch in vivo. Cell 93 (1998) 649-660
60. Struhl G., and Greenwald I. Presenilin is required for activity and nuclear access of Notch in Drosophila. Nature 398 (1999) 522-525
61. Struhl G., Fitzgerald K., and Greenwald I. Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell 74 (1993) 331-345
62. Teng Y., Liu Q., Ma J., Liu F., Han Z., Wang Y., and Wang W. Cloning, expression and characterization of a novel human CAP10-like gene hCLP46 from CD34(+) stem/progenitor cells. Gene 371 (2006) 7-15
63. Tepass U., Gruszynski-DeFeo E., Haag T.A., Omatyar L., Torok T., and Hartenstein V. shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev. 10 (1996) 672-685
64. Wang L.W., Dlugosz M., Somerville R.P., Raed M., Haltiwanger R.S., and Apte S.S. O-Fucosylation of thrombospondin type 1 repeats in ADAMTS like-1/punctin-1 regulates secretion: Implications for the ADAMTS superfamily. J. Biol. Chem. 282 (2007) 17024-17031
65. Wang W., and Struhl G. Drosophila Epsin mediates a select endocytic pathway that DSL ligands must enter to activate Notch. Development 131 (2004) 5367-5380
66. 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
67. Wang Y., and Spellman M.W. Purification and characterization of a GDP-fucose:polypeptide fucosyltransferase from Chinese hamster ovary cells. J. Biol. Chem. 273 (1998) 8112-8118
68. Wang Y., Shao L., Shi S., Harris R.J., Spellman M.W., Stanley P., and Haltiwanger R.S. Modification of epidermal growth factor-like repeats with O-fucose. Molecular cloning and expression of a novel GDP-fucose protein O-fucosyltransferase. J. Biol. Chem. 276 (2001) 40338-40345
69. Ye Y., Lukinova N., and Fortini M.E. Neurogenic phenotypes and altered Notch processing in Drosophila Presenilin mutants. Nature 398 (1999) 525-529
70. Zhai R.G., Hiesinger P.R., Koh T.W., Verstreken P., Schulze K.L., Cao Y., Jafar-Nejad H., Norga K.K., Pan H., Bayat V., et al. Mapping Drosophila mutations with molecularly defined P element insertions. Proc. Natl. Acad. Sci. USA 100 (2003) 10860-10865