Ligand endocytosis drives receptor dissociation and activation in the Notch pathway

Development

Volumn 127, Issue 7, 2000, Pages 1373-1385

  Parks, Annette L ^a,b   Klueg, Kristin M ^a   Stout, Jane R ^a   Muskavitch, Marc A T ^a  

^a INDIANA UNIVERSITY   (United States)

^b EXELIXIS INC   (United States)

Author keywords

Delta; Drosophila; Endocytosis; Notch; Signal transduction

Indexed keywords

CELL PROTEIN; LIGAND;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; DISSOCIATION; DROSOPHILA; ENDOCYTOSIS; FEMALE; IMAGINAL DISC; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; RECEPTOR BINDING; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; CELL LINE; DNA PRIMERS; DROSOPHILA; DROSOPHILA PROTEINS; DYNAMINS; ENDOCYTOSIS; GENES, INSECT; GTP PHOSPHOHYDROLASES; INSECT PROTEINS; LIGANDS; MEMBRANE PROTEINS; MUTATION; RECEPTORS, NOTCH; RETINA; SIGNAL TRANSDUCTION; WING;

ANIMALIA; ARACHNIDA; HEXAPODA;

EID: 0034051852     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (70)

1. Artavanis-Tsakonas, S. (1997). Alagille syndrome - a notch up for the Notch receptor. Nat. Genet. 16, 212-213.
2. Artavanis-Tsakonas, S., Rand, M. D. and Lake, R. J. (1999). Notch signalling: Cell fate control and signal integration in development. Science 284, 770-775.
3. Ashburner, M. (1989). Appendix C: Mounting and embedding media. In Drosophila: A Laboratory Manual, vol. 2 (ed. 337). New York: Cold Spring Harbor Laboratory Press.
4. Bellen, H. J., O'Kane, C. J., Wilson, C., Grossniklaus, U., Pearson, R. K. and Gehring, W. J. (1989). P-element mediated enhancer detection; a versatile method to study development in Drosophila. Genes Dev. 3, 1288-1300.
5. Blaumueller, C. M., Qi, H., Zagouras, P. and Artavanis-Tsakonas, S. (1997). Intracellular cleavage of Notch leads to a heterodimeric receptor on the plasma membrane. Cell 90, 281-291.
6. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
7. Bray, S. (1998). A Notch affair. Cell 93, 499-503.
8. Cagan, R. L. and Ready, D. F. (1989). Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev. 3, 1099-1112.
9. Chan, Y.-M. and Jan, Y. N. (1998). Roles for proteolysis and trafficking in Notch maturation and signal transduction. Cell 94, 423-426.
10. Chitnis, A., Henrique, D., Lewis, J., Ish-Horowicz, D. and Kintner, C. (1995). Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 375, 761-766.
11. de Celis, J. F., Bray, S. and García-Bellido, A. (1997). Notch signalling regulates veinlet expression and establishes boundaries between veins and interveins in the Drosophila wing. Development 124, 1919-1928.
12. Diederich, R. J., Matsuno, K., Hing, H. and Artavanis-Tsakonas, S. (1994). Cytosolic interaction between deltex and Notch ankyrin repeats implicates deltex in the Notch signalling pathway. Development 120, 473-481.
13. Egan, S. E., St-Pierre, B. and Leow, C. C. (1998). Notch receptors, partners, and regulators: from conserved domains to powerful functions. Curr. Top. Microbiol. Immunol. 228, 274-324.
14. Ellisen, L. W., Bird, J., West, D. C., Soreng, A. L., Reynolds, T. C., Smith, S. D. and Sklar, J. (1991). TAN-I, the human homolog of the Drosophila Notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 66, 649-661.
15. Fehon, R. G., Kooh, P. J., Rebay, I., Regan, C. L., Xu, T., Muskavitch, M. A. T. and Artavanis-Tsakonas, S. (1990). Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF homologous genes in Drosophila. Cell 61, 523-534.
16. 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.
17. Gallyas, F., Göres, T. and Merchenthaler, I. (1982). High-grade intensification of the end-product of the diaminobenzidine reaction for peroxidase histochemistry. J. Histochem. Cytochem. 30, 183-184.
18. Greenwald, I. (1998). LIN-12/Notch signaling: lessons from worms and flies. Genes Dev. 124, 1751-1762.
19. Haenlin, M., Kramatschek, B. and Campos-Ortega, J. A. (1990). The pattern of transcription of the neurogenic gene Delta of Drosophila melanogaster. Development 110, 905-914.
20. Heldin, C.-H. (1995). Dimerization of cell surface receptors in signal transduction. Cell 80, 213-223.
21. Henderson, S. T., Gao, D., Christenson, S. and Kimble, J. (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.
22. Huppert, S. S., Jacobsen, T. L. and Muskavitch, M. A. T. (1997). Feedback regulation is central to Delta-Notch signalling required for Drosophila wing vein morphogenesis. Development 124, 3283-3291.
23. Jacobsen, T. L., Brennan, K., Arias, A. M. and Muskavitch, M. A. T. (1998). Cis-interactions between Delta and Notch modulate neurogenic signalling in Drosophila. Development 125, 4531-4540.
24. Jarriault, S., Brou, C., Logeat, F., Schroeter, E. H., Kopan, R. and Israel, A. (1995). Signalling downstream of activated mammalian Notch. Nature 377, 355-358.
25. Jen, W. C., Wettstein, D., Turner, D., Chitnis, A. and Kintner, C. (1997). The Notch ligand, X-Delta-2, mediates segmentation of the paraxial mesoderm in Xenopus embryos. Development 124, 1169-1178.
26. Jiang, R., Lan, Y., Chapman, H. D., Shawber, C., Norton, C. R., Serreze, D. V., Weinmaster, G. and Gridley, T. (1998). Defects in limb, craniofacial, and thymic development in Jagged2 mutant mice. Genes Dev. 12, 1046-1057.
27. Kimble, J., Henderson, S. and Crittenden, S. (1998). Notch/Lin-12 signaling: transduction by regulated protein slicing. Trends Biochem. Sci. 23, 353-357.
28. Klein, T. and Arias, A. M. (1998). Interactions among Delta. Serrate and Fringe modulate Notch activity during Drosophila wing development. Development 125, 2951-2962.
29. Klueg, K. M. and Muskavitch, M. A. T. (1999). Ligand-receptor interactions and trans-endocytosis of Delta, Serrate and Notch: members of the Notch signalling pathway in Drosophila. J. Cell Sci. 112, 3289-3297.
30. Klueg, K. M., Parody, T. R. and Muskavitch, M. A. T. (1998). Complex proteolytic processing acts on Delta, a transmembrane ligand for Notch, during Drosophila development. Mol. Biol. Cell 9, 1709-1723.
31. Kooh, P. J., Fehon, R. G. and Muskavitch, M. A. T. (1993). Implications of dynamic patterns of Delta and Notch expression for cellular interactions during Drosophila development. Development 117, 493-507.
32. Kopan, R., Schroeter, E. H., Weintraub, H. and Nye, J. S. (1996). Signal transduction by activated mNotch: importance of proteolytic processing and its regulation by the extracellular domain. Proc. Natl. Acad. Sci. USA 93, 1683-1688.
33. Kopczynski, C. C., Alton, A. K., Fechtel, K., Kooh, P. J. and Muskavitch, M. A. (1988). Delta, a Drosophila neurogenic gene, is transcriptionally complex and encodes a protein related to blood coagulation factors and epidermal growth factors of vertebrates. Genes Dev. 2, 1723-1735.
34. Krämer, H. and Phistry, M. (1996). Mutations in the Drosophila hook gene inhibit endocytosis of the Boss transmembrane ligand into multivesicular bodies. J. Cell Biol. 133, 1205-1216.
35. Krämer, H. and Phistry, M. (1999). Genetic analysis of hook, a gene required for endocytic trafficking in Drosophila. Genetics 151, 675-684.
36. Lecourtois, M. and Schweisguth, F. (1998). Indirect evidence for Delta-dependent intracellular processing of Notch in Drosophila embryos. Curr. Biol. 8, 771-774.
37. Lieber, T., Kidd, S., Alcamo, E., Corbin, V. and Young, M. W. (1993). 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, 1949-1961.
38. Lieber, T., Wesley, C., Alcamo, E., Hassel, B., Krane, J., Campos-Ortega, J. A. and Young, M. W. (1992). Single amino acid substitutions in EGF-like elements of Notch and Delta modify Drosophila development and affect cell adhesion in vitro. Neuron 9, 847-859.
39. Lindsley, D. L. and Zimm, G. G. (1992). The Genome of Drosophila melanogaster. New York: Academic Press.
40. Liposits, Z. S., Sétáló, G. Y. and Lerkó, B. F. (1984). Application of the silver-gold intensified 3,3-diaminobenzidine chromatin to the light and electron microscopic detection of the luteinizing hormone-releasing hormone system of the rat brain. Neurosci. 13, 513-525.
41. Lissemore, J. L. and Starmer, W. T. (1999). Phylogenetic analysis of vertebrate and invertebrate Delta/Serrate/LAG-2 (DSL) proteins. Molec. Phylog. Evol. 11, 308-319.
42. Logeat, F., Bessia, C., Brou, B., LeBail, O., Jarriault, S., Seidah, N. G. and Israel, A. (1998). The Notch1 receptor is cleaved constitutively by a furin-like convertase. Proc. Natl. Acad. Sci. USA 95, 8108-8112.
43. McNiven, M. A. (1998). Dynamin: A molecular motor with pinchase action. Cell 94, 151-154.
44. Mumm, J. S., Schroeter, E. H., Saxena, M. T., Tian, X., Griesemer, A., Ray, W. J. and Kopan, R. (2000). Ligand induced 'ectodomain shedding' regulates gamma-secretase-like proteolytic activation of Notch1. Mol. Cell. in press.
45. Muskavitch, M. A. T. (1994). Delta-Notch signaling and Drosophila cell fate choice. Dev. Biol. 166, 415-430.
46. Parks, A. L., Huppert, S. S. and Muskavitch, M. A. T. (1997). The dynamics of neurogenic signalling underlying bristle development in Drosophila melanogaster. Mech. Dev. 63, 61-74.
47. Parks, A. L. and Muskavitch, M. A. T. (1993). Delta function is required for bristle organ determination and morphogenesis in Drosophila. Dev. Biol. 157, 484-496.
48. Parks, A. L., Turner, F. R. and Muskavitch, M. A. T. (1995). Relationships between complex Delta expression and the specification of retinal cell fates during Drosophila eye development. Mech. Dev. 50, 201-216.
49. Parody, T. R. (1998). Structure-function analysis of Delta in vivo. PhD Thesis. Indiana University, Bloomington, IN, USA.
50. Parody, T. R. and Muskavitch, M. A. T. (1993). The pleiotropic function of Delta during postembryonic development of Drosophila melanogaster. Genetics 135, 527-539.
51. Poodry, C. A. (1990). shibire, a neurogenic mutant of Drosophila. Dev. Biol. 138, 464-472.
52. 15: A pleiotropic mutation affecting larval and adult locomotion and development. Dev. Biol. 32, 373-386.
53. Qi, H., Rand, M. D., Wu, X., Sestan, N., Wang, W., Rakic, P., Xu, T. and Artavanis-Tsakonas, S. (1999). Processing of the Notch ligand Delta by the metalloprotease Kuzbanian. Science 283, 91-94.
54. Rebay, I., Fleming, R. J., Fehon, R. G., Cherbas, L. F., Cherbas, P. T. and Artavanis-Tsakonas, S. (1991). Specific EGF repeats of Notch mediate interactions with Delta and Serrate: implications for Notch as a multifunctional receptor. Cell 67, 687-699.
55. Rooke, J., Pan, D., Xu, T. and Rubin, G. M. (1996). KUZ, a conserved metalloprotease-disintegrin protein with two roles in Drosophila neurogenesis. Science 273, 1227-1231.
56. Schmid, S. L., McNiven, M. A. and Camilli, P. D. (1998). Dynamin and its partners: a progress report. Curr. Opin. Cell Biol. 10, 504-512.
57. Schneider, I. (1972). Cell lines derived from late embryonic stages of Drosophila melanogaster. J. Embryol. Exp. Morph. 27, 353-365.
58. Schroeter, E. H., Kissinger, J. A. and Kopan, R. (1998). Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393, 382-386.
59. Seugnet, L., Simpson, P. and Haenlin, M. (1997). Requirement for dynamin during Notch signalling in Drosophila neurogenesis. Dev. Biol. 192, 585-598.
60. Shellenbarger, D. L., and Mohler, J. D. (1978). Temperature sensitive periods and autonomy of pleiotropic effects of I(I)Ntsl, a conditional Notch lethal in Drosophila. Dev. Biol. 62, 432-446.
61. Shepard, S. B. (1941). A genetic and molecular analysis of interactions between the Drosophila melanogaster neurogenic genes Delta and Notch. PhD Thesis, Indiana University, Bloomington, IN, USA.
62. Sotillos, S., Roch, F. and Campuzano, S. (1997). The metalloprotease-disintegrin Kuzbanian participates in Notch activation during growth and patterning of Drosophila imaginal discs. Development 124, 4769-4779.
63. Staehling-Hampton, K., Jackson, P. D., Clark, M. J., Brand, A. H. and Hoffmann, F. M. (1994). 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, 585-593.
64. Struhl, G. and Adachi, A. (1998). Nuclear access and action of Notch in vivo. Cell 93, 649-660.
65. 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.
66. Sun, X. and Artavanis-Tsakonas, S. (1997). Secreted forms of DELTA and SERRATE define antagonists of Notch signaling in Drosophila. Development 124, 3439-3448.
67. Vässin, H., Bremer, K. A., Knust, E. and Campos-Ortega, J. A. (1987). The neurogenic gene Delta of Drosophila melanogaster is expressed in neurogenic territories and encodes a putative transmembrane protein with EGF-like repeats. EMBO J. 6, 3431-3440.
68. Wen, C., Metzstein, M. M. and Greenwald, I. (1997). Sup-17, a Caenorhabditis elegans ADAM protein related to Drosophila KUZBANIAN, and its role in LIN12/NOTCH signalling. Development 124, 4759-4767.
69. Woods, D. F. and Poodry, C. A. (1983). Cell surface proteins of Drosophila. Dev. Biol. 96, 23-31.
70. Xue, Y., Gao, X., Lindsell, C. E., Norton, C. R., Chang, B., Hicks, C., Gendron-Maguire, M., Rand, E. B., Weinmaster, G. and Gridley, T. (1999). Embryonic lethality and vascular defects in mice lacking the Notch ligand Jaggedl. Hum. Mol. Genet. 8, 723-730.