Combinatorial expression patterns of individual TLE proteins during cell determination and differentiation suggest non-redundant functions for mammalian homologs of Drosophila Groucho

Development Growth and Differentiation

Volumn 40, Issue 2, 1998, Pages 133-146

  Yao, Jing ^a   Liu, Yanling ^a   Husain, Junaid ^a   Lo, Rita ^a   Palaparti, Anuradha ^a   Henderson, Janet ^b   Stifani, Stefano ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Cell determination; Groucho; Neurogenesis; Notch signaling; Transducin like Enhancer of split proteins

Indexed keywords

GROUCHO POTEIN; TRANSDUCIN; TRANSDUCIN LIKE ENHANCER PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL SPECIFICITY; DROSOPHILA; EMBRYO; IMMUNOHISTOCHEMISTRY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY; STRAIN DIFFERENCE;

ANIMALIA; INSECTA; MAMMALIA;

EID: 0031952854     PISSN: 00121592     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1440-169X.1998.00003.x     Document Type: Article

References (55)

1. Akazawa, C., Sasai, Y., Nakanishi, S & Kageyama, R. 1992. Molecular characterization of a rat negative regulator with a basic helix-loop-helix structure predominantly expressed in the developing nervous system J. Biol. Chem. 267. 21879-21885.
2. Alonso, M. C. & Cabrera, C. V. 1988. The achaete-scute gene complex of Drosophila melanogaster comprises four homologous genes. EMBO J. 7, 2585-2591.
3. Artavanis-Tsakonas, S. & Simpson, P. 1991 Choosing a cell fate: A view from the Notch locus. Trends Genet. 7, 403-408.
4. Bernier, S. M., Desiardins, J., Sullivan, A. K. & Goltzman, D. 1990. Establishment of an osseous cell line from fetal rat calvaria using an immunocytolytic method of cell selection: Characterization of the cell line and of derived clones J. Cell. Physiol. 145, 274-285.
5. Bernier, S. M. & Goltzman, D. 1993. Regulation of expression of the chondrocytic phenotype in a skeletal cell line (CFK2) in vitro. J. Bone Miner Res. 8, 475-484.
6. Bier, E., Vaessin, H., Younger-Shepherd, S., Jan, L. Y. & Jan Y. N. 1992. deadpan, an essential pan-neural gene in Drosophila, encodes a helix-loop-helix protein similar to the hairy gene product. Genes Dev. 6, 2137-2151.
7. Campos-Ortega, J. A. 1993. Mechanisms of early neurogenesis in Drosophila melanogaster. J. Neurobiol. 24, 1305-1327.
8. Campuzano, S. & Modolell, J. 1992. Patterning of the Drosophila nervous system: The achaete-scute gene complex. Trends Genet. 8, 202-208.
9. Caudy, M., Vaessin, H., Brand, M., Tuma, R., Jan, L. Y. & Jan, Y. N. 1988. daughterless, a gene essential for both neurogenesis and sex determination, has sequence similarities to myc and the achaete-scute complex. Cell 55, 1061-1067.
10. Chitnis, A. & Kintner, C. 1996. Sensitivity of proneural genes to lateral inhibition affects the pattern of primary neurons in Xenopus embryos. Development 122, 2295-2301.
11. Dawson, S. R., Turner, D. L., Weintraub, H. & Parkhurst, S. M. 1995. 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. 15, 6923-6931.
12. Dehni, G., Liu, Y., Husain, J. & Stifani, S. 1995. TLE expression correlates with mouse embryonic segmentation, neurogenesis, and epithelial determination. Mech. Dev. 53, 369-381.
13. Delidakis, C. & 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, 731-735.
14. Delidakis, C., Preiss, A., Hartley, D. A. & 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.
15. Feder, J. N., Jan, L. Y. & Jan, Y. N. 1993. 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. 13, 105-113.
16. Fisher, A. L., Ohsako, S. & Caudy, M. 1996. 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. 16, 2670-2677.
17. Grbavec, D. & Stifani, S. 1996. Molecular interaction between TLE1 and the carboxyl-terminal domain of HES-1 containing the WRPW motif. Biochem. Biophys. Res. Commun. 223, 701-705.
18. Guillemot, F., Lo, L. C., Johnson, J. E. et al 1993. Mammalian achaete-scute homologue 1 is required for early development of olfactory and autonomic neurons. Cell 75, 463-476.
19. Hartley, D. A., Preiss, A. & Artavanis-Tsakonas, S. 1988. A deduced gene product from the Drosophila neurogenic locus, Enhancer of split, shows homology to mammalian G-protein β subunit. Cell 55, 785-795.
20. Heitzler, P., Bourouis, M., Ruel, L., Carteret, C. & Simpson, P. 1996. Genes of the Enhancer of split and achaete-scute complexes are required for a regulatory loop between Notch and Delta during lateral signaling in Drosophila. Development 122, 161-171.
21. Herbertson, A. & Aubin, J. E. 1995. Dexamethasone alters the subpopulation make-up of rat bone marrow stromal cell cultures. J. Bone Miner. Res. 10, 285-294.
22. Husain, J., Lo, R., Grbavec, D. & Stifani, S. 1996. Affinity for the nuclear compartment and expression during cell differentiation implicate phosphorylated Groucho/TLE1 forms of higher molecular mass in nuclear functions. Biochem. J. 317, 523-531.
23. Ishibashi, M., Ang, S-L., Shiota, K., Nakanishi, S., Kageyama, R. & Guillemot, F. 1995. Targeted disruption of mammalian hairy and Enhancer of split homologue 1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev. 9, 3136-3148.
24. Ishibashi, M., Moriyoshi, K., Sasai, Y., Shiota, K., Nakanishi, S. & Kageyama, R. 1994. Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J. 13, 1799-1805.
25. Ishibashi, M., Sasai, Y., Nakanishi, S. & Kageyama, R. 1993. Molecular characterization of HES-2, a mammalian helix-loop-helix factor structurally related to Drosophila hairy and Enhancer of split. Eur. J. Biochem. 215, 645-652.
26. Jan, Y. N. & Jan, L. Y. 1994. Neural cell fate specification in Drosophila. Curr. Opin. Neurobiol. 4, 8-13.
27. Jarman, A. P., Grell, E. H., Ackerman, L. Y., Jan, L. Y. & Jan, Y. N. 1993. atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73, 1307-1321.
28. Jennings, B., Preiss, A., Delidakis, C. & Bray, S. 1994. The Notch signaling pathway is required for Enhancer of split bHLH protein expression during neurogenesis in the Drosophila embryo. Development 120, 3537-3548.
29. Jimenez, F. & Modolell, J. 1993. Neural fate specification in Drosophila. Curr. Opin. Gen. Dev. 3, 626-632.
30. Knust, E., Schrons, H., Grawe, F. & 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.
31. Koop, K. E., MacDonald, L. M. & Lobe, C. G. 1996. Transcripts of Grg4, a murine groucrto-related gene, are detected in adjacent tissues to other murine neurogenic gene homologues during embryonic development. Mech. Dev. 59, 73-87.
32. Lecourtois, M. & 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.
33. Lee, J. E., Hollenberg, S. M., Snider, L., Turner, D. L., Lipnick, N. & Weintraub, H. 1995. Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268, 836-844.
34. Leon, C. & Lobe, C. G. 1996. Grg3, a murine Groucho-related gene, is expressed in the developing nervous system and in mesenchyme-induced epithelial structures. Dev. Dyn. 208, 11-24.
35. Liu, Y., Dehni, G., Purcell, K. J. et al. 1996. Epithelial expression and chromosomal location of human TLE genes: Implications for Notch signaling and neoplasia. Genomics 31, 58-64.
36. Ma, Q., Kintner, C. & Anderson, D. J. 1996. Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87, 43-52.
37. Mallo, M., Franco del Amo, F. & Gridley, T. 1993. Cloning and developmental expression of Grg, a mouse gene related to the groucho transcript of the Drosophila Enhancer of split complex. Mech. Dev. 42, 67-76.
38. Mallo, M., Gendron-Maguire, M., Harbison, M. L. & Gridley, T. 1995. Protein characterization and targeted disruption of Grg, a mouse gene related to the groucho transcript of the Drosophila Enhancer of split Complex. Dev. Dyn. 204, 338-347.
39. McBurney, M. W., Reuhl, K. R., Ally, A. I., Nasipuri, S., Bell, J. C. & Craig, J. 1988. Differentiation and maturation of embryonal carcinoma-derived neurons in cell culture. J. Neurosci. 8, 1063-1073.
40. McConnell, S. K. 1995. Construction of the cerebral cortex: neurogenesis and fate determination. Neuron 15, 761-768.
41. Miyasaka, H., Choudhury, B. K., Hou, E. W. & Li, S. S-L. 1993. Molecular cloning and expression of mouse and human cDNA encoding AES and ESG proteins with strong similarity to Drosophila enhancer of split groucho protein. Eur. J. Biochem. 216, 343-352.
42. 2 phase cells. Biochem. Biophys. Res. Commun. 207, 1029-1037.
43. Nakayama, H., Liu, Y., Stifani, S. & Cross, J. C. 1997. Developmental restriction of Mash-2 expression in trophoblast correlates with potential activation of the Notch-2 pathway. Dev. Genet 21, 21-30.
44. Ohsako, S., Hyer, J., Panganiban, G., Oliver, I. & Caudy, M. 1994. hairy function as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. Genes Dev. 8, 2743-2755.
45. Paroush, Z., Finley, R. L., Kidd, T. et al. 1994. Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins. Cell 79, 805-815.
46. Pflugrad, A., Meir, J. Y. J., Barnes, T. M. & Miller, D. M. III. 1997. The Groucho-like transcription factor UNC-37 functions with the neural specificity gene unc-4 to govern motor neuron identity in C. elegans. Development 124, 1699-1709.
47. Preiss, A., Hartley, D. A. & Artavanis-Tsakonas, S. 1988. The molecular genetics of Enhancer of split, a gene required for embryonic neural development in Drosophila. EMBO J. 7, 3917-3927.
48. Rakic, P. 1988. Dividing up the neocortex. Science 241, 170-176.
49. Rudnicki, M. A. & McBurney, M. W. 1987. Cell culture methods and induction of differentiation of embryonal carcinoma cell lines. In Teratocarcinomas and Embryonic Stem Cells: A Practical Approach (Ed. E. J. Robertson), pp. 19-49. IRL Press, Oxford.
50. Ruit, K. G., Elliott, J. L., Osborne, P. A., Yan, Q. & Snider, W. D. 1992. Selective dependence of mammalian dorsal root ganglion neurons on nerve growth factor during embryonic development. Neuron 8, 573-587.
51. Rushlow, C. A., Hogan, A., Pinchin, S. M., Howe, K. R., Lardelli, M. T. & Ish-Horowicz, D. 1989. The Drosophila hairy protein acts in both segmentation and bristle patterning and shows homology to N-myc. EMBO J. 8, 3095-3103.
52. Sasai, Y., Kageyama, R., Tagawa, Y., Shigemoto, R. & Nakanishi, S. 1992. Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev. 5, 2620-2634.
53. Schmidt, C. J. & Sladek, T. E. 1993. A rat homolog of the Drosophila Enhancer of split (groucho) locus lacking WD-40 repeats. J. Biol. Chem. 268, 25 681-25 686.
54. Schrons, H., Knust, E. & 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.
55. Stifani, S., Blaumueller, C. M., Redhead, N. J., Hill, R. E. & Artavanis-Tsakonas, S. 1992. Human homologs of a Drosophila Enhancer of split gene product define a novel family of nuclear proteins. Nature Genet. 2, 119-127.