The divergent DSL ligand Dll3 does not activate Notch signaling but cell autonomously attenuates signaling induced by other DSL ligands

Journal of Cell Biology

Volumn 170, Issue 6, 2005, Pages 983-992

  Ladi, Ena ^a,c   Nichols, James T ^a   Ge, Weihong ^a   Miyamoto, Alison ^a   Yao, Christine ^a   Yang, Liang Tung ^a   Boulter, Jim ^a   Sun, Yi E ^a   Kintner, Chris ^b   Weinmaster, Gerry ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c University of California Berkeley   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

JAGGED1; LIGAND; NOTCH RECEPTOR; PROTEIN; PROTEIN DII3; PROTEIN LAG2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL ACTIVITY; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; BIOTINYLATION; CELL LINE; COCULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; GLYCOSYLTRANSFERASES; L CELLS (CELL LINE); LIGANDS; LUCIFERASES; MEMBRANE PROTEINS; MICE; MUTATION; NEURONS; NIH 3T3 CELLS; RATS; SIGNAL TRANSDUCTION; TUBULIN; XENOPUS LAEVIS;

XENOPUS LAEVIS;

EID: 24944501849     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200503113     Document Type: Article

References (54)

1. Ascano, J.M., L.J. Beverly, and A.J. Capobianco. 2003. The C-terminal PDZ-ligand of JAGGED1 is essential for cellular transformation. J. Biol. Chem. 278:8771-8779.
2. Barrantes, I.B., A.J. Elia, K. Wunsch, M.H. De Angelis, T.W. Mak, J. Rossant, R.A. Conlon, A. Gossler, and J.L. de la Pompa. 1999. Interaction between N signalling and Lunatic fringe during somite boundary formation in the mouse. Curr. Biol. 9:470-480.
3. Bulman, M.P., K. Kusumi, T.M. Frayling, C. McKeown, C. Garrett, E.S. Lander, R. Krumlauf, A.T. Hattersley, S. Ellard, and P.D. Turnpenny. 2000. Mutations in the human delta homologue, DLL3, cause axial skeletal defects in spondylocostal dysostosis. Nat. Genet. 24:438-441.
4. Bush, G., G. diSibio, A. Miyamoto, J.B. Denault, R. Leduc, and G. Weinmaster. 2001. Ligand-induced signaling in the absence of furin processing of N1. Dev. Biol. 229:494-502.
5. Campos, L.S., A.J. Duarte, T. Branco, and D. Henrique. 2001. mDll1 and mDll3 expression in the developing mouse brain: role in the establishment of the early cortex. J. Neurosci. Res. 64:590-598.
6. Chitnis, A., D. Henrique, J. Lewis, D. Ish-Horowicz, and C. Kintner. 1995. Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature. 375:761-766.
7. Daluiski, A., T. Engstrand, M.E. Bahamonde, L.W. Gamer, E. Agius, S.L. Stevenson, K. Cox, V. Rosen, and K.M. Lyons. 2001. Bone morphogenetic protein-3 is a negative regulator of bone density. Nat. Genet. 27:84-88.
8. de Celis, J.F., and S.J. Bray. 2000. The Abruptex domain of N regulates negative interactions between N, its ligands and Fringe. Development. 127:1291-1302
9. Dunwoodie, S.L., D. Henrique, S.M. Harrison, and R.S. Beddington. 1997. Mouse Dll3: a novel divergent Delta gene which may complement the function of other Delta homologues during early pattern formation in the mouse embryo. Development. 124:3065-3076.
10. Dunwoodie, S.L., M. Clements, D.B. Sparrow, X. Sa, R.A. Conlon, and R.S. Beddington. 2002. Axial skeletal defects caused by mutation in the spondylocostal dysplasia/pudgy gene Dll3 are associated with disruption of the segmentation clock within the presomitic mesoderm. Development. 129:1795-1806.
11. Ge, W., K. Martinowich, X. Wu, F. He, A. Miyamoto, G. Fan, G. Weinmaster, and Y.E. Sun. 2002. N signaling promotes astrogliogenesis via direct CSL-mediated glial gene activation. J. Neurosci. Res. 69:848-860.
12. Giudicelli, F., and J. Lewis. 2004. The vertebrate segmentation clock. Curr. Opin. Genet. Dev. 14:407-414.
13. Heitzler, P., and P. Simpson. 1993. Altered epidermal growth factor-like sequences provide evidence for a role of N as a receptor in cell fate decisions. Development. 117:1113-1123.
14. Henderson, S.T., D. Gao, S. Christensen, and J. Kimble. 1997. Functional domains of LAG-2, a putative signaling ligand for LIN-12 and GLP-1 receptors in Caenorhabditis elegans. Mol. Biol. Cell. 8:1751-1762.
15. Henrique, D., E. Hirsinger, J. Adam, I. Le Roux, O. Pourquie, D. Ish-Horowicz, and J. Lewis. 1997. Maintenance of neuroepithelial progenitor cells by Delta-N signalling in the embryonic chick retina. Curr. Biol. 7:661-670.
16. Hermanson, O., K. Jepsen, and M.G. Rosenfeld. 2002. N-CoR controls differentiation of neural stem cells into astrocytes. Nature. 419:934-939.
17. Hicks, C., S.H. Johnston, G. diSibio, A. Collazo, T.F. Vogt, and G. Weinmaster. 2000. Fringe differentially modulates Jagged1 and Delta1 signalling through N1 and N2. Nat. Cell Biol. 2:515-520.
18. Hicks, C., E. Ladi, C. Lindsell, J. Hsieh, S. Hayward, A. Collazo, and G. Weinmaster. 2002. A secreted Delta1-Fc fusion protein functions both as an activator and inhibitor of Notch1 signaling. J. Neurosci. Res. 68:655-667.
19. Hsieh, J.J., T. Henkel, P. Salmon, E. Robey, M.G. Peterson, and S.D. Hayward. 1996. Truncated mammalian N1 activates CBF1/RBPJk-repressed genes by a mechanism resembling that of Epstein-Barr virus EBNA2. Mol. Cell. Biol. 16:952-959.
20. Hukriede, N.A., Y. Gu, and R.J. Fleming. 1997. A dominant-negative form of Serrate acts as a general antagonist of N activation. Development. 124:3427-3437.
21. Itoh, M., C.H. Kim, G. Palardy, T. Oda, Y.J. Jiang, D. Maust, S.Y. Yeo, K. Lorick, G.J. Wright, L. Ariza-McNaughton, et al. 2003. Mind bomb is a ubiquitin ligase that is essential for efficient activation of N signaling by Delta. Dev. Cell. 4:67-82.
22. Jacobsen, T.L., K. Brennan, A.M. Arias, and M.A. Muskavitch. 1998. Cis-interactions between Delta and N modulate neurogenic signalling in Drosophila. Development. 125:4531-4540.
23. Kiyota, T., and T. Kinoshita. 2004. The intracellular domain of X-Serrate-1 is cleaved and suppresses primary neurogenesis in Xenopus laevis. Mech. Dev. 121:573-585.
24. Krebs, L.T., M.L. Deftos, M.J. Bevan, and T. Gridley. 2001. The Nrarp gene encodes an ankyrin-repeat protein that is transcriptionally regulated by the N signaling pathway. Dev. Biol. 238:110-119.
25. Kusumi, K., E.S. Sun, A.W. Kerrebrock, R.T. Bronson, D.C. Chi, M.S. Bulotsky, J.B. Spencer, B.W. Birren, W.N. Frankel, and E.S. Lander. 1998. The mouse pudgy mutation disrupts Delta homologue Dll3 and initiation of early somite boundaries. Nat. Genet. 19:274-278.
26. Kusumi, K., M.S. Mimoto, K.L. Covello, R.S. Beddington, R. Krumlauf, and S.L. Dunwoodie. 2004. Dll3 pudgy mutation differentially disrupts dynamic expression of somite genes. Genesis. 39:115-121.
27. Le Borgne, R., A. Bardin, and F. Schweisguth. 2005. The roles of receptor and ligand endocytosis in regulating N signaling. Development. 132:1751-1762.
28. Lewis, J. 1996. Neurogenic genes and vertebrate neurogenesis. Curr. Opin. Neurobiol. 6:3-10.
29. Lindsell, C.E., C.J. Shawber, J. Boulter, and G. Weinmaster. 1995. Jagged: a mammalian ligand that activates N1. Cell. 80:909-917.
30. Logeat, F., C. Bessia, C. Brou, O. LeBail, S. Jarriault, N. Seiday, and A. Israel. 1998. The N1 receptor is cleaved constitutively by a furin-like convertase. Proc. Natl. Acad. Sci. 95:8108-8112.
31. Morrison, S.J., S.E. Perez, Z. Qiao, J.M. Verdi, C. Hicks, G. Weinmaster, and D.J. Anderson. 2000. Transient N activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell. 101:499-510.
32. Mumm, J.S., and R. Kopan. 2000. N signaling: from the outside in. Dev. Biol. 228:151-165.
33. Nofziger, D., A. Miyamoto, K.M. Lyons, and G. Weinmaster. 1999. N signaling imposes two distinct blocks in the differentiation of C2C12 myoblasts. Development. 126:1689-1702.
34. Panin, V.M., L. Shao, L. Lei, D.J. Moloney, K.D. Irvine, and R.S. Haltiwanger. 2002. Notch ligands are substrates for protein O- fucosyltransferase-1 and Fringe. J. Biol. Chem. 277:29945-29952.
35. Pfister, S., G.K. Przemeck, J.K. Gerber, J. Beckers, J. Adamski, and M. Hrabe de Angelis. 2003. Interaction of the MAGUK family member Acvrinp1 and the cytoplasmic domain of the N ligand Delta1. J. Mol. Biol. 333:229-235.
36. Sakamoto, K., O. Ohara, M. Takagi, S. Takeda, and K. Katsube. 2002. Intracellular cell-autonomous association of N and its ligands: a novel mechanism of N signal modification. Dev. Biol. 241:313-326.
37. Sanchez-Irizarry, C., A.C. Carpenter, A.P. Weng, W.S. Pear, J.C. Aster, and S.C. Blacklow. 2004. N subunit heterodimerization and prevention of ligand-independent proteolytic activation depend, respectively, on a novel domain and the LNR repeats. Mol. Cell. Biol. 24:9265-9273.
38. Serth, K., K. Schuster-Gossler, R. Cordes, and A. Gossler. 2003. Transcriptional oscillation of Lunatic fringe is essential for somitogenesis. Genes Dev. 17:912-925.
39. Shimizu, K., S. Chiba, K. Kumano, N. Hosoya, T. Takahashi, Y. Kanda, Y. Hamada, Y. Yazaki, and H. Hirai. 1999. Mouse Jagged1 physically interacts with N2 and other N receptors. Assessment by quantitative methods. J. Biol. Chem. 274:32961-32969.
40. Shutter, J.R., S. Scully, W. Fan, W.G. Richards, J. Kitajewski, G.A. Deblandre, C.R. Kintner, and K.L. Stark. 2000. Dll4, a novel N ligand expressed in arterial endothelium. Genes Dev. 14:1313-1318.
41. Six, E., D. Ndiaye, Y. Laabi, C. Brou, N. Gupta-Rossi, A. Israel, and F. Logeat. 2003. The N ligand Delta1 is sequentially cleaved by an ADAM protease and gamma-secretase. Proc. Natl. Acad. Sci. USA. 100:7638-7643.
42. Sparrow, D.B., M. Clements, S.L. Withington, A.N. Scott, J. Novotny, D. Sillence, K. Kusumi, R.S. Beddington, and S.L. Dunwoodie. 2002. Diverse requirements for N signalling in mammals. Int. J. Dev. Biol. 46:365-374.
43. Sun, Y., M. Nadal-Vicens, S. Misono, M.Z. Lin, A. Zubiaga, X. Hua, G. Fan, and M.E. Greenberg. 2001. Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell. 104:365-376.
44. Takahashi, Y., T. Inoue, A. Gossler, and Y. Saga. 2003. Feedback loops comprising Dll1, Dll3 and Mesp2, and differential involvement of Psen1 are essential for rostrocaudal patterning of somites. Development. 130:4259-4268.
45. Turner, D.L., and H. Weintraub. 1994. Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev. 8:1434-1447.
46. Turnpenny, P.D., N. Whittock, J. Duncan, S. Dunwoodie, K. Kusumi, and S. Ellard. 2003. Novel mutations in DLL3, a somitogenesis gene encoding a ligand for the N signalling pathway, cause a consistent pattern of abnormal vertebral segmentation in spondylocostal dysostosis. J. Med. Genet. 40:333-339.
47. Vinos, J., and M. Freeman. 2000. Evidence that Argos is an antagonistic ligand of the EGF receptor. Oncogene. 19:3560-3562.
48. Weinmaster, G. 2000. N signal transduction: a real rip and more. Curr. Opin. Genet. Dev. 10:363-369.
49. Weinmaster, G., and C. Kintner. 2003. Modulation of notch signaling during somitogenesis. Annu. Rev. Cell Dev. Biol. 19:367-395.
50. Weng, A.P., A.A. Ferrando, W. Lee, J.P. Morris IV, L.B. Silverman, C. Sanchez-Irizarry, S.C. Blacklow, A.T. Look, and J.C. Aster. 2004. Activating mutations of N1 in human T cell acute lymphoblastic leukemia. Science. 306:269-271.
51. Wettstein, D.A., D.L. Turner, and C. Kintner. 1997. The Xenopus homolog of Drosophila Suppressor of Hairless mediates N signaling during primary neurogenesis. Development. 124:693-702.
52. Wright, G.J., J.D. Leslie, L. Ariza-McNaughton, and J. Lewis. 2004. Delta proteins and MAGI proteins: an interaction of N ligands with intracellular scaffolding molecules and its significance for zebrafish development. Development. 131:5659-5669.
53. Yang, L.T., J.T. Nichols, C. Yao, J.O. Manilay, E.A. Robey, and G. Weinmaster. 2004. Fringe glycosyltransferases differentially modulate N1 proteolysis induced by Delta1 and Jagged1. Mol. Biol. Cell. 16:927-942.
54. Zhang, N., C.R. Norton, and T. Gridley. 2002. Segmentation defects of N pathway mutants and absence of a synergistic phenotype in lunatic fringe/ radical fringe double mutant mice. Genesis. 33:21-28.