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. 1998 Apr 1;17(7):2067–2078. doi: 10.1093/emboj/17.7.2067

Drosophila CtBP: a Hairy-interacting protein required for embryonic segmentation and hairy-mediated transcriptional repression.

G Poortinga 1, M Watanabe 1, S M Parkhurst 1
PMCID: PMC1170551  PMID: 9524128

Abstract

hairy is a Drosophila pair-rule segmentation gene that functions genetically as a repressor. To isolate protein components of Hairy-mediated repression, we used a yeast interaction screen and identified a Hairy-interacting protein, the Drosophila homolog of the human C-terminal-binding protein (CtBP). Human CtBP is a cellular phosphoprotein that interacts with the C-terminus of the adenovirus E1a oncoprotein and functions as a tumor suppressor. dCtBP also interacts with E1a in a directed yeast two-hybrid assay. We show that dCtBP interacts specifically and directly with a small, previously uncharacterized C-terminal region of Hairy. dCtBP activity appears to be specific to Hairy of the Hairy/Enhancer of split [E(spl)]/Dpn basic helix-loop-helix protein class. We identified a P-element insertion within the dCtBP transcription unit that fails to complement alleles of a known locus, l(3)87De. We demonstrate that dCtBP is essential for proper embryonic segmentation by analyzing embryos lacking maternal dCtBP activity. While Hairy is probably not the only segmentation gene interacting with dCtBP, we show dose-sensitive genetic interactions between dCtBP and hairy mutations.

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Selected References

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  1. Alifragis P., Poortinga G., Parkhurst S. M., Delidakis C. A network of interacting transcriptional regulators involved in Drosophila neural fate specification revealed by the yeast two-hybrid system. Proc Natl Acad Sci U S A. 1997 Nov 25;94(24):13099–13104. doi: 10.1073/pnas.94.24.13099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barolo S., Levine M. hairy mediates dominant repression in the Drosophila embryo. EMBO J. 1997 May 15;16(10):2883–2891. doi: 10.1093/emboj/16.10.2883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bender W., Spierer P., Hogness D. S. Chromosomal walking and jumping to isolate DNA from the Ace and rosy loci and the bithorax complex in Drosophila melanogaster. J Mol Biol. 1983 Jul 25;168(1):17–33. doi: 10.1016/s0022-2836(83)80320-9. [DOI] [PubMed] [Google Scholar]
  4. Bier E., Vaessin H., Younger-Shepherd S., Jan L. Y., Jan Y. N. deadpan, an essential pan-neural gene in Drosophila, encodes a helix-loop-helix protein similar to the hairy gene product. Genes Dev. 1992 Nov;6(11):2137–2151. doi: 10.1101/gad.6.11.2137. [DOI] [PubMed] [Google Scholar]
  5. Bossy B., Hall L. M., Spierer P. Genetic activity along 315 kb of the Drosophila chromosome. EMBO J. 1984 Nov;3(11):2537–2541. doi: 10.1002/j.1460-2075.1984.tb02169.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Botas J., Moscoso del Prado J., García-Bellido A. Gene-dose titration analysis in the search of trans-regulatory genes in Drosophila. EMBO J. 1982;1(3):307–310. doi: 10.1002/j.1460-2075.1982.tb01165.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Boyd J. M., Subramanian T., Schaeper U., La Regina M., Bayley S., Chinnadurai G. A region in the C-terminus of adenovirus 2/5 E1a protein is required for association with a cellular phosphoprotein and important for the negative modulation of T24-ras mediated transformation, tumorigenesis and metastasis. EMBO J. 1993 Feb;12(2):469–478. doi: 10.1002/j.1460-2075.1993.tb05679.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brown N. L., Sattler C. A., Markey D. R., Carroll S. B. hairy gene function in the Drosophila eye: normal expression is dispensable but ectopic expression alters cell fates. Development. 1991 Dec;113(4):1245–1256. doi: 10.1242/dev.113.4.1245. [DOI] [PubMed] [Google Scholar]
  9. Brown N. L., Sattler C. A., Paddock S. W., Carroll S. B. Hairy and emc negatively regulate morphogenetic furrow progression in the Drosophila eye. Cell. 1995 Mar 24;80(6):879–887. doi: 10.1016/0092-8674(95)90291-0. [DOI] [PubMed] [Google Scholar]
  10. Carroll S. B., Scott M. P. Zygotically active genes that affect the spatial expression of the fushi tarazu segmentation gene during early Drosophila embryogenesis. Cell. 1986 Apr 11;45(1):113–126. doi: 10.1016/0092-8674(86)90543-x. [DOI] [PubMed] [Google Scholar]
  11. Chinnadurai G. Adenovirus E1a as a tumor-suppressor gene. Oncogene. 1992 Jul;7(7):1255–1258. [PubMed] [Google Scholar]
  12. Chou T. B., Noll E., Perrimon N. Autosomal P[ovoD1] dominant female-sterile insertions in Drosophila and their use in generating germ-line chimeras. Development. 1993 Dec;119(4):1359–1369. doi: 10.1242/dev.119.4.1359. [DOI] [PubMed] [Google Scholar]
  13. Chou T. B., Perrimon N. Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics. 1992 Jul;131(3):643–653. doi: 10.1093/genetics/131.3.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cooley L., Kelley R., Spradling A. Insertional mutagenesis of the Drosophila genome with single P elements. Science. 1988 Mar 4;239(4844):1121–1128. doi: 10.1126/science.2830671. [DOI] [PubMed] [Google Scholar]
  15. Dawson S. R., Turner D. L., Weintraub H., Parkhurst S. M. Specificity for the hairy/enhancer of split basic helix-loop-helix (bHLH) proteins maps outside the bHLH domain and suggests two separable modes of transcriptional repression. Mol Cell Biol. 1995 Dec;15(12):6923–6931. doi: 10.1128/mcb.15.12.6923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Delidakis C., Artavanis-Tsakonas S. The Enhancer of split [E(spl)] locus of Drosophila encodes seven independent helix-loop-helix proteins. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8731–8735. doi: 10.1073/pnas.89.18.8731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Feder J. N., Jan L. Y., Jan Y. N. A rat gene with sequence homology to the Drosophila gene hairy is rapidly induced by growth factors known to influence neuronal differentiation. Mol Cell Biol. 1993 Jan;13(1):105–113. doi: 10.1128/mcb.13.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Feder J. N., Li L., Jan L. Y., Jan Y. N. Genomic cloning and chromosomal localization of HRY, the human homolog to the Drosophila segmentation gene, hairy. Genomics. 1994 Mar 1;20(1):56–61. doi: 10.1006/geno.1994.1126. [DOI] [PubMed] [Google Scholar]
  19. Fisher A. L., Ohsako S., Caudy M. The WRPW motif of the hairy-related basic helix-loop-helix repressor proteins acts as a 4-amino-acid transcription repression and protein-protein interaction domain. Mol Cell Biol. 1996 Jun;16(6):2670–2677. doi: 10.1128/mcb.16.6.2670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Fujita S. C., Zipursky S. L., Benzer S., Ferrús A., Shotwell S. L. Monoclonal antibodies against the Drosophila nervous system. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7929–7933. doi: 10.1073/pnas.79.24.7929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gausz J., Hall L. M., Spierer A., Spierer P. Molecular Genetics of the ROSY-ACE Region of DROSOPHILA MELANOGASTER. Genetics. 1986 Jan;112(1):65–78. doi: 10.1093/genetics/112.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Giebel B., Campos-Ortega J. A. Functional dissection of the Drosophila enhancer of split protein, a suppressor of neurogenesis. Proc Natl Acad Sci U S A. 1997 Jun 10;94(12):6250–6254. doi: 10.1073/pnas.94.12.6250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Golic K. G. Site-specific recombination between homologous chromosomes in Drosophila. Science. 1991 May 17;252(5008):958–961. doi: 10.1126/science.2035025. [DOI] [PubMed] [Google Scholar]
  24. Gray S., Cai H., Barolo S., Levine M. Transcriptional repression in the Drosophila embryo. Philos Trans R Soc Lond B Biol Sci. 1995 Sep 29;349(1329):257–262. doi: 10.1098/rstb.1995.0111. [DOI] [PubMed] [Google Scholar]
  25. Gray S., Levine M. Transcriptional repression in development. Curr Opin Cell Biol. 1996 Jun;8(3):358–364. doi: 10.1016/s0955-0674(96)80010-x. [DOI] [PubMed] [Google Scholar]
  26. Harding K., Rushlow C., Doyle H. J., Hoey T., Levine M. Cross-regulatory interactions among pair-rule genes in Drosophila. Science. 1986 Aug 29;233(4767):953–959. doi: 10.1126/science.3755551. [DOI] [PubMed] [Google Scholar]
  27. Herschbach B. M., Johnson A. D. Transcriptional repression in eukaryotes. Annu Rev Cell Biol. 1993;9:479–509. doi: 10.1146/annurev.cb.09.110193.002403. [DOI] [PubMed] [Google Scholar]
  28. Hilliker A. J., Clark S. H., Chovnick A., Gelbart W. M. Cytogenetic analysis of the chromosomal region immediately adjacent to the rosy locus in Drosophila melanogaster. Genetics. 1980 May;95(1):95–110. doi: 10.1093/genetics/95.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hollenberg S. M., Sternglanz R., Cheng P. F., Weintraub H. Identification of a new family of tissue-specific basic helix-loop-helix proteins with a two-hybrid system. Mol Cell Biol. 1995 Jul;15(7):3813–3822. doi: 10.1128/mcb.15.7.3813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hooper K. L., Parkhurst S. M., Ish-Horowicz D. Spatial control of hairy protein expression during embryogenesis. Development. 1989 Nov;107(3):489–504. doi: 10.1242/dev.107.3.489. [DOI] [PubMed] [Google Scholar]
  31. Hoshijima K., Kohyama A., Watakabe I., Inoue K., Sakamoto H., Shimura Y. Transcriptional regulation of the Sex-lethal gene by helix-loop-helix proteins. Nucleic Acids Res. 1995 Sep 11;23(17):3441–3448. doi: 10.1093/nar/23.17.3441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Howard K., Ingham P. Regulatory interactions between the segmentation genes fushi tarazu, hairy, and engrailed in the Drosophila blastoderm. Cell. 1986 Mar 28;44(6):949–957. doi: 10.1016/0092-8674(86)90018-8. [DOI] [PubMed] [Google Scholar]
  33. Hurlin P. J., Quéva C., Koskinen P. J., Steingrímsson E., Ayer D. E., Copeland N. G., Jenkins N. A., Eisenman R. N. Mad3 and Mad4: novel Max-interacting transcriptional repressors that suppress c-myc dependent transformation and are expressed during neural and epidermal differentiation. EMBO J. 1995 Nov 15;14(22):5646–5659. doi: 10.1002/j.1460-2075.1995.tb00252.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ingham P. W., Pinchin S. M., Howard K. R., Ish-Horowicz D. Genetic Analysis of the Hairy Locus in DROSOPHILA MELANOGASTER. Genetics. 1985 Nov;111(3):463–486. doi: 10.1093/genetics/111.3.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ingham P. W. The molecular genetics of embryonic pattern formation in Drosophila. Nature. 1988 Sep 1;335(6185):25–34. doi: 10.1038/335025a0. [DOI] [PubMed] [Google Scholar]
  36. Ip Y. T., Hemavathy K. Drosophila development. Delimiting patterns by repression. Curr Biol. 1997 Apr 1;7(4):R216–R218. doi: 10.1016/s0960-9822(06)00104-7. [DOI] [PubMed] [Google Scholar]
  37. Ip Y. T., Park R. E., Kosman D., Bier E., Levine M. The dorsal gradient morphogen regulates stripes of rhomboid expression in the presumptive neuroectoderm of the Drosophila embryo. Genes Dev. 1992 Sep;6(9):1728–1739. doi: 10.1101/gad.6.9.1728. [DOI] [PubMed] [Google Scholar]
  38. Ish-Horowicz D., Pinchin S. M. Pattern abnormalities induced by ectopic expression of the Drosophila gene hairy are associated with repression of ftz transcription. Cell. 1987 Nov 6;51(3):405–415. doi: 10.1016/0092-8674(87)90636-2. [DOI] [PubMed] [Google Scholar]
  39. Ishibashi M., Sasai Y., Nakanishi S., Kageyama R. Molecular characterization of HES-2, a mammalian helix-loop-helix factor structurally related to Drosophila hairy and Enhancer of split. Eur J Biochem. 1993 Aug 1;215(3):645–652. doi: 10.1111/j.1432-1033.1993.tb18075.x. [DOI] [PubMed] [Google Scholar]
  40. Jiang J., Kosman D., Ip Y. T., Levine M. The dorsal morphogen gradient regulates the mesoderm determinant twist in early Drosophila embryos. Genes Dev. 1991 Oct;5(10):1881–1891. doi: 10.1101/gad.5.10.1881. [DOI] [PubMed] [Google Scholar]
  41. Jiménez G., Pinchin S. M., Ish-Horowicz D. In vivo interactions of the Drosophila Hairy and Runt transcriptional repressors with target promoters. EMBO J. 1996 Dec 16;15(24):7088–7098. [PMC free article] [PubMed] [Google Scholar]
  42. Klämbt C., Knust E., Tietze K., Campos-Ortega J. A. Closely related transcripts encoded by the neurogenic gene complex enhancer of split of Drosophila melanogaster. EMBO J. 1989 Jan;8(1):203–210. doi: 10.1002/j.1460-2075.1989.tb03365.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Knust E., Schrons H., Grawe F., Campos-Ortega J. A. Seven genes of the Enhancer of split complex of Drosophila melanogaster encode helix-loop-helix proteins. Genetics. 1992 Oct;132(2):505–518. doi: 10.1093/genetics/132.2.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Laherty C. D., Yang W. M., Sun J. M., Davie J. R., Seto E., Eisenman R. N. Histone deacetylases associated with the mSin3 corepressor mediate mad transcriptional repression. Cell. 1997 May 2;89(3):349–356. doi: 10.1016/s0092-8674(00)80215-9. [DOI] [PubMed] [Google Scholar]
  45. Moran E. DNA tumor virus transforming proteins and the cell cycle. Curr Opin Genet Dev. 1993 Feb;3(1):63–70. doi: 10.1016/s0959-437x(05)80342-9. [DOI] [PubMed] [Google Scholar]
  46. Mozer B., Marlor R., Parkhurst S., Corces V. Characterization and developmental expression of a Drosophila ras oncogene. Mol Cell Biol. 1985 Apr;5(4):885–889. doi: 10.1128/mcb.5.4.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Murre C., McCaw P. S., Baltimore D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell. 1989 Mar 10;56(5):777–783. doi: 10.1016/0092-8674(89)90682-x. [DOI] [PubMed] [Google Scholar]
  48. Murre C., McCaw P. S., Vaessin H., Caudy M., Jan L. Y., Jan Y. N., Cabrera C. V., Buskin J. N., Hauschka S. D., Lassar A. B. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell. 1989 Aug 11;58(3):537–544. doi: 10.1016/0092-8674(89)90434-0. [DOI] [PubMed] [Google Scholar]
  49. Mymryk J. S. Tumour suppressive properties of the adenovirus 5 E1A oncogene. Oncogene. 1996 Oct 17;13(8):1581–1589. [PubMed] [Google Scholar]
  50. Oellers N., Dehio M., Knust E. bHLH proteins encoded by the Enhancer of split complex of Drosophila negatively interfere with transcriptional activation mediated by proneural genes. Mol Gen Genet. 1994 Sep 1;244(5):465–473. doi: 10.1007/BF00583897. [DOI] [PubMed] [Google Scholar]
  51. Ohsako S., Hyer J., Panganiban G., Oliver I., Caudy M. Hairy function as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. Genes Dev. 1994 Nov 15;8(22):2743–2755. doi: 10.1101/gad.8.22.2743. [DOI] [PubMed] [Google Scholar]
  52. Parkhurst S. M., Bopp D., Ish-Horowicz D. X:A ratio, the primary sex-determining signal in Drosophila, is transduced by helix-loop-helix proteins. Cell. 1990 Dec 21;63(6):1179–1191. doi: 10.1016/0092-8674(90)90414-a. [DOI] [PubMed] [Google Scholar]
  53. Parkhurst S. M. Groucho: making its Marx as a transcriptional co-repressor. Trends Genet. 1998 Apr;14(4):130–132. doi: 10.1016/s0168-9525(98)01407-3. [DOI] [PubMed] [Google Scholar]
  54. Parkhurst S. M., Ish-Horowicz D. wimp, a dominant maternal-effect mutation, reduces transcription of a specific subset of segmentation genes in Drosophila. Genes Dev. 1991 Mar;5(3):341–357. doi: 10.1101/gad.5.3.341. [DOI] [PubMed] [Google Scholar]
  55. Paroush Z., Finley R. L., Jr, Kidd T., Wainwright S. M., Ingham P. W., Brent R., Ish-Horowicz D. Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins. Cell. 1994 Dec 2;79(5):805–815. doi: 10.1016/0092-8674(94)90070-1. [DOI] [PubMed] [Google Scholar]
  56. Perrimon N., Lanjuin A., Arnold C., Noll E. Zygotic lethal mutations with maternal effect phenotypes in Drosophila melanogaster. II. Loci on the second and third chromosomes identified by P-element-induced mutations. Genetics. 1996 Dec;144(4):1681–1692. doi: 10.1093/genetics/144.4.1681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Roth S. Y. Chromatin-mediated transcriptional repression in yeast. Curr Opin Genet Dev. 1995 Apr;5(2):168–173. doi: 10.1016/0959-437x(95)80004-2. [DOI] [PubMed] [Google Scholar]
  58. Rushlow C. A., Hogan A., Pinchin S. M., Howe K. M., Lardelli M., Ish-Horowicz D. The Drosophila hairy protein acts in both segmentation and bristle patterning and shows homology to N-myc. EMBO J. 1989 Oct;8(10):3095–3103. doi: 10.1002/j.1460-2075.1989.tb08461.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Sasai Y., Kageyama R., Tagawa Y., Shigemoto R., Nakanishi S. Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev. 1992 Dec;6(12B):2620–2634. doi: 10.1101/gad.6.12b.2620. [DOI] [PubMed] [Google Scholar]
  60. Schaeper U., Boyd J. M., Verma S., Uhlmann E., Subramanian T., Chinnadurai G. Molecular cloning and characterization of a cellular phosphoprotein that interacts with a conserved C-terminal domain of adenovirus E1A involved in negative modulation of oncogenic transformation. Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10467–10471. doi: 10.1073/pnas.92.23.10467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sollerbrant K., Chinnadurai G., Svensson C. The CtBP binding domain in the adenovirus E1A protein controls CR1-dependent transactivation. Nucleic Acids Res. 1996 Jul 1;24(13):2578–2584. doi: 10.1093/nar/24.13.2578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Spierer P., Spierer A., Bender W., Hogness D. S. Molecular mapping of genetic and chromomeric units in Drosophila melanogaster. J Mol Biol. 1983 Jul 25;168(1):35–50. doi: 10.1016/s0022-2836(83)80321-0. [DOI] [PubMed] [Google Scholar]
  63. Spradling A. C., Stern D. M., Kiss I., Roote J., Laverty T., Rubin G. M. Gene disruptions using P transposable elements: an integral component of the Drosophila genome project. Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):10824–10830. doi: 10.1073/pnas.92.24.10824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Stroumbakis N. D., Li Z., Tolias P. P. RNA- and single-stranded DNA-binding (SSB) proteins expressed during Drosophila melanogaster oogenesis: a homolog of bacterial and eukaryotic mitochondrial SSBs. Gene. 1994 Jun 10;143(2):171–177. doi: 10.1016/0378-1119(94)90093-0. [DOI] [PubMed] [Google Scholar]
  65. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
  66. Tietze K., Oellers N., Knust E. Enhancer of splitD, a dominant mutation of Drosophila, and its use in the study of functional domains of a helix-loop-helix protein. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):6152–6156. doi: 10.1073/pnas.89.13.6152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Török T., Tick G., Alvarado M., Kiss I. P-lacW insertional mutagenesis on the second chromosome of Drosophila melanogaster: isolation of lethals with different overgrowth phenotypes. Genetics. 1993 Sep;135(1):71–80. doi: 10.1093/genetics/135.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Van Doren M., Bailey A. M., Esnayra J., Ede K., Posakony J. W. Negative regulation of proneural gene activity: hairy is a direct transcriptional repressor of achaete. Genes Dev. 1994 Nov 15;8(22):2729–2742. doi: 10.1101/gad.8.22.2729. [DOI] [PubMed] [Google Scholar]
  69. Vojtek A. B., Hollenberg S. M., Cooper J. A. Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell. 1993 Jul 16;74(1):205–214. doi: 10.1016/0092-8674(93)90307-c. [DOI] [PubMed] [Google Scholar]
  70. Wainwright S. M., Ish-Horowicz D. Point mutations in the Drosophila hairy gene demonstrate in vivo requirements for basic, helix-loop-helix, and WRPW domains. Mol Cell Biol. 1992 Jun;12(6):2475–2483. doi: 10.1128/mcb.12.6.2475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. de Celis J. F., de Celis J., Ligoxygakis P., Preiss A., Delidakis C., Bray S. Functional relationships between Notch, Su(H) and the bHLH genes of the E(spl) complex: the E(spl) genes mediate only a subset of Notch activities during imaginal development. Development. 1996 Sep;122(9):2719–2728. doi: 10.1242/dev.122.9.2719. [DOI] [PubMed] [Google Scholar]

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