Antagonism of Notch signaling activity by members of a novel protein family encoded by the Bearded and Enhancer of split gene complexes

Development

Volumn 127, Issue 2, 2000, Pages 291-306

  Lai, Eric C ^a   Bodner, Ruth ^a   Kavaler, Joshua ^a,b   Freschi, Gina ^a   Posakony, James W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MIDDLEBURY COLLEGE   (United States)

Author keywords

Amphipathic helix; Brd family; Drosophila melanogaster; Neurogenesis; Notch signaling; Sensory organ development

Indexed keywords

NOTCH RECEPTOR; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FATE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; ENHANCER REGION; EYE DEVELOPMENT; GENE LOCATION; GENE OVEREXPRESSION; MULTIGENE FAMILY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FAMILY; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SENSORY SYSTEM;

3' UNTRANSLATED REGIONS; AMINO ACID SEQUENCE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINEAGE; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; INSECT PROTEINS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR SEQUENCE DATA; NUCLEIC ACID HYBRIDIZATION; PHENOTYPE; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, NOTCH; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

ANIMALIA; DROSOPHILA MELANOGASTER; HEXAPODA; MELANOGASTER; METAZOA;

EID: 0033982518     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (72)

1. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25. 3389-3402.
2. Artavanis-Tsakonas, S., Rand, M. D. and Lake, R. J. (1999). Notch signaling: Cell fate control and signal integration in development. Science 284, 770-776.
3. Bailey, A. M. and Posakony, J. W. (1995). Suppressor of Hairless directly activates transcription of Enhancer of split Complex genes in response to Notch receptor activity. Genes Dev. 9, 2609-2622.
4. Bang, A. G. and Posakony, J. W. (1992). The Drosophila gene Hairless encodes a novel basic protein that controls alternative cell fates in adult sensory organ development. Genes Dev. 6, 1752-1769.
5. 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 Der. 3, 1288-1300.
6. Benson, D. A., Boguski, M. S., Lipman, D. J., Ostell, J., Ouellette, B. F., Rapp, B. A. and Wheeler, D. L. (1999). GenBank. Nucl. Acids Res. 27, 12-17.
7. Bier, K., Vaessin, H., Shepherd, S., Lee, K., McCall, K., Barbel, S., Ackerman, L., Carretto, R., Uemura, T., Grell, E. et al. (1989). Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 3, 1273-1287.
8. Blackman, R. K., Sanicola, M., Raftery, L. A., Gillevet, T. and Gelbart, W. M. (1991). An extensive 3′ cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-β family in Drosophila. Development 111, 657-666.
9. Brand, A. H., Manoukian, A. S. and Perrimon, N. (1994). Ectopic expression in Drosophila. Methods Cell Biol. 44, 635-654.
10. 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.
11. Brown, N. H. and Kafatos, F. C. (1988). Functional cDNA libraries from Drosophila embryos. J. Mol. Biol. 203, 425-437.
12. Cabrera, C. V. and Alonso, M. C. (1991). Transcriptional activation by heterodimers of the achaete-scute and daughterless gene products of Drosophila. EMBO J. 10, 2965-2973.
13. 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.
14. Capdevila, J. and Guerrero, I. (1994). Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J. 13, 4459-4468.
15. Cubas, P., de Celis, J.-F., Campuzano, S. and Modolell, J. (1991). Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc. Genes Dev. 5, 996-1008.
16. de Celis, J. F., Bray, S. and Garcia-Bellido, A. (1997). Notch signalling regulates veinlet expression and establishes boundaries between veins and interveins in the Drosophila wing. Development 124, 1919-1928.
17. Delidakis, C. and Artavanis-Tsakonas, S. (1992). The Enhancer of split [E(spl)] locus of Drosophila encodes seven independent helix-loop-helix proteins. Proc. Natl. Acad. Sci. USA 89, 8731-8735.
18. Delidakis, C., Preiss, A., Hartley, D. A. and Artavanis-Tsakonas, S. (1991). Two genetically and molecularly distinct functions involved in early neurogenesis reside within the Enhancer of split locus of Drosophila melanogaster. Genetics 129, 803-823.
19. Eastman, D. S., Slee, R., Skoufos, E., Bangalore, L., Bray, S. and Delidakis, C. (1997). Synergy between Suppressor of Hairless and Notch in regulation of Enhancer of split mγ and mδ expression. Mol. Cell. Biol. 17, 5620-5628.
20. FlyBase. (1998). FlyBase - A Drosophila database. Nucl. Acids Res. 26, 85-88.
21. Fortini, M. K. and Artavanis-Tsakonas, S. (1994). The Suppressor of Hairless protein participates in Notch receptor signaling. Cell 79, 273-282.
22. Freeman, M. (1996). Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87, 651-660.
23. Frise, K., Knoblich, J. A., Younger-Shepherd, S., Jan, L. Y. and Jan, Y. N. (1996). The Drosophila Numb protein inhibits signaling of the Notch receptor during cell-cell interaction in sensory organ lineage. Proc. Natl. Acad. Sci. USA 93, 11925-11932.
24. Furukawa, T., Kobayakawa, Y., Tamura, K., Kimura, K., Kawaichi, M., Tanimura, T. and Honjo, T. (1995). Suppressor of Hairless, the Drosophila homologue of RBP-Jκ, transactivates the neurogenic gene E(spl)m8. Jpn. J. Genet. 70, 505-524.
25. Furukawa, T., Maruyania, S., Kawaichi, M. and Honjo, T. (1992) The Drosophila homolog of the immunoglobulin recombination signal-binding protein regulates peripheral nervous system development. Cell 69, 1191-1197.
26. Gho, M., Bellaïche, Y. and Schweisguth, F. (1999). Revisiting the Drosophila microchaete lineage: a novel intrinsically asymmetric cell division generates a glial cell. Development 126, 3573-3584.
27. Greenwald, I. (1998). LIN-12/Notch signaling: lessons from worms and flies. Genes Dev. 12, 1751-1762.
28. Ha, I., Wightman, B. and Ruvkun, G. (1996). A bulged lin-4/lin-14 RNA duplex is sufficient for Caenorhahditis elegans lin-14 temporal gradient formation. Genes & Dev. 10, 3041-3050.
29. Hartenstein, V. and Posakony, J. W. (1989). Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development 107, 389-405.
30. Hartenslein, V. and Posakony, J. W. (1990). A dual function of the Notch gene in Drosophila sensillum development. Dev. Biol. 142, 13-30.
31. Harvey, D., Hong, L., Evans-Holm, M., Pendleton, J., Su, C., Brokstein, P., Lewis, S. and Rubin, G. M. (1998) BDGP/HHMI Drosophila EST Project.
32. Hinz, U., Giebel, B. and Campos-Ortega, J. A. (1994). The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell 76, 77-87.
33. Jarriault, S., Brou, C., Logeat, F., Schroeter, E. H., Kopan, R. and Israel, A. (1995). Signalling downstream of activated mammalian Notch. Nuture 377, 355-358.
34. Kavaler, J., Fu, W., Duan, H., Noll, M. and Posakony, J. W. (1999). An essential role for the Drosophila Fax2 homolog in the differentiation of adult sensory organs. Development 126, 2261-2272.
35. Kimble, J. and Simpson, P. (1997). The LIN-12/Notch signaling pathway and its regulation. Ann. Rev. Cell Dev. Biol. 13, 333-361.
36. Klämbt, C., Knust, E., Tietze, K. and Campos-Ortega, J. (1989). Closely related transcripts encoded by the neurogenic gene complex Enhancer of split of Drosophila melanogaster. EMBO J. 8, 203-210.
37. Knust, E., Schrons, H., Grawe, F. and Campos-Ortega, J. A. (1992). Seven genes of the Enhancer of split complex of Drosophila melanogaster encode helix-loop-helix proteins. Genetics 132, 505-518.
38. Kopczynski, C. C., Noordermeer, J. N., Serano, T. L., Chen, W. Y., Pendleton, J. D., Lewis, S., Goodman, C. S. and Rubin, G. M. (1998). A high throughput screen to identify secreted and transmembrane proteins involved in Drosophila embryogenesis. Proc. Natl. Acad. Sci. USA 95, 9973-9973.
39. Kramatschek, B. and Campos-Ortega, J. A. (1994). Neuroectodermal transcription of the Drosophila neurogenic genes E(spl) and HLH-m5 is regulated by proneural genes. Development 120, 815-826.
40. Lai, E. C., Burks, C. and Posakony, J. W. (1998). The K box, a conserved 3′ UTR sequence motif, negatively regulates accumulation of Enhancer of split Complex transcripts. Development 125, 4077-4088.
41. Lai, E. C. and Posakony, J. W. (1997). The Bearded box, a novel 3′ UTR sequence motif, mediates negative post-transcriptional regulation of Bearded and Enhancer of split Complex gene expression. Development 124, 4847-4856.
42. Lai, E. C. and Posakony, J. W. (1998). Regulation of Drosophila neurogcnesis by RNA:RNA duplexes? Cell 93, 1103-1104.
43. Lecourtois, M. and Schweisguth, F. (1995). 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, 2598-2608.
44. Levilen, M. W., Lai, E. C. and Posakony, J. W. (1997). The Drosophila gene Bearded encodes a novel small protein and shares 3′ UTR sequence motifs with multiple Enhancer of split Complex genes. Development 124, 4039-4051.
45. Leviten, M. W. and Posakony, J. W. (1996). Gain-of-funclion alleles of Bearded interfere with alternative cell fate decisions in Drosophila adult sensory organ development. Dev. Biol. 176, 264-283.
46. Milan, M., Diaz-Benjumea, F. J. and Cohen, S. M. (1998). Beadex encodes an LMO protein that regulates Apterous LIM-homeodomnain activity in Drosophila wing development: a model for LMO oncogene function. Genes Dev. 12, 2912-2920.
47. Murre, C., McCaw, P. S., Vaessin, H., Caudy, M., Jan, L. Y., Jan, V. N., Cabrera, C. V., Buskin, J. N., Hauschka, S. D., Lassar, A. B. et al (1989). Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58, 537-544.
48. Nakao, K. and Campos-Ortega, J. A. (1996). Persistent expression of genes of the Enhancer of split complex suppresses neural development in Drosophila. Neuron 16, 275-286.
49. Nellesen, D. T., Lai, E. C. and Posakony, J. W. (1999). Discrete enhancer elements mediate selective responsiveness of Enhancer of split Complex genes to common transcriptional activators. Dev. Biol. 213, 33-53.
50. Parks, A. L. and Muskavitch, M. A. (1993). Delta function is required for bristle organ determination and morphogenesis in Drosophila. Dev. Biol. 157, 484-496.
51. Phelps, C. B. and Brand, A. H. (1998). Ectopic gene expression in Drosophila using GAL4 system. Methods 14, 367-379.
52. Posakony, J. W. (1994). Nature versus nurture: asymmetric cell divisions in Drosophila bristle development. Cell 76, 415-418.
53. Preiss, A., Hartley, D. A. and Artavanis-Tsakonas, S. (1988). The molecular genetics of Enhancer of split, a gene required for embryonic neural development in Dmsophila. EMBO J. 7, 3917-3927.
54. 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.
55. Romani, S., Campuzano, S., Macagno, E. R. and Modolell, J. (1989). Expression of achaete and acute genes in Drosophila imaginal discs and their function in sensory organ development. Genes Dev. 3, 997-1007.
56. Rørth, P., Szabo, K., Bailey, A., Laverty, T., Rehm, J., Rubin, G. M., Weigmann, K., Milan, M., Benes, V., Ansorge, W. et al. (1998). Systematic gain-of-function genetics in Drosophila. Development 125, 1049-1057.
57. Rubin, G. M. and Spradling, A. C. (1982). Genetic transformation of Dmsophila with transposable element vectors. Science 218, 348-353.
58. Schmid, K. J. and Tautz, D. (1997). A screen for fast evolving genes from Drosophila. Proc. Natl. Acad. Sci. USA 94, 9746-9750.
59. Schrons, H., Knust, E. and Campos-Ortega, J. A. (1992). 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, 481-503.
60. Schweisguth, F. and Posakony, J. W. (1992). Suppressor of Hairless, the Drosophila homolog of the mouse recombination signal-binding protein gene, controls sensory organ cell fates. Cell 69, 1199-1212.
61. Schweisguth, F. and Posakony, J. W. (1994). Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis. Development 120, 1433-1441.
62. Segrest, J. P., De Loof, H., Dohlman, J. G., Brouillette, C. G. and Anantharamaiah, G. M. (1990). Amphipathic helix motif: Classes and properties. Proteins 8, 103-117.
63. Singson, A., Leviten, M. W., Bang, A. G., Hua, X. H. and Posakony, J. W. (1994). Direct downstream targets of proneural activators in the imaginal disc include genes involved in lateral inhibitory signaling. Genes Dev. 8, 2058-2071.
64. Skeath, J. B. and Carroll, S. B. (1991). Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev. 5, 984-995.
65. Sturtevant, M. A., Roark, M. and Bier, E. (1993). The Drosophila rhomboid gene mediates the localized formation of wing veins and interacts genetically with components of the EGF-R signaling pathway. Genes Dev. 7, 961-973.
66. Tamura, K., Taniguchi, Y., Minoguchi, S., Sakai, T., Tun, T., Furukawa, T. and Honjo, T. (1995). Physical interaction between a novel domain of the receptor Notch and the transcription factor RBP-Jκ/Su(H). Curr. Biol. 5, 1416-1423.
67. Tun, T., Hamaguchi, Y., Matsunami, N., Furukawa, T., Honjo, T. and Kawaichi, M. (1994). Recognition sequence of a highly conserved DNA binding protein RBP-Jκ. Nucleic Acids Res. 22, 965-971.
68. Van Doren, M., Ellis, H. M. and Posakony, J. W. (1991). The Drosophila extramacrochaetae protein antagonizes sequence-specific DNA binding by daughterless/achaete-scute protein complexes. Development 113, 245-255.
69. Van Doren, M., Powell, P. A., Pasternak, D., Singson, A. and Posakony, J. W. (1992). Spatial regulation of proneural gene activity: auto- and cross-activation of achaete is antagonized by extramacrochaetae. Genes Dev. 6, 2592-2605.
70. Wurmbach, E., Wech, I. and Preiss, A. (1999). The Enhancer of split complex of Drosophila melanogaster harbors three classes of Notch responsive genes. Mech. Dev. 80, 171-180.
71. Zeng, C., Younger-Shepherd, S., Jan, L. Y. and Jan, Y. N. (1998). Delta and Serrate are redundant Notch ligands required for asymmetric cell divisions within the Drosophila sensory organ lineage. Genes Dev. 12, 1086-1091.
72. Ziemer, A., Tietze, K., Knust, E. and Campos-Ortega, J. (1988). Genetic-analysis of Enhancer of split, a locus involved in neurogenesis in Drosophila melanogaster. Genetics 119, 63-74.