Groucho. A Corepressor with Instructive Roles in Development

Current Topics in Developmental Biology

Volumn 98, Issue , 2012, Pages 65-96

  Turki Judeh, Wiam ^a   Courey, Albert J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chromatin; Dpp signaling; Groucho; Notch signaling; Transcriptional repression; Transducin like enhancer of split; Wg Wnt signaling

Indexed keywords

EID: 84856504995     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386499-4.00003-3     Document Type: Chapter

References (147)

1. Abed M., Barry K.C., Kenyagin D., et al. Degringolade, a SUMO-targeted ubiquitin ligase, inhibits Hairy/Groucho-mediated repression. EMBO J. 2011, 30:1289-1301.
2. Ajuria L., Nieva C., Winkler C., et al. Capicua DNA-binding sites are general response elements for RTK signaling in Drosophila. Development 2011, 138:915-924.
3. Allander S.V., Illei P.B., Chen Y., et al. Expression profiling of synovial sarcoma by cDNA microarrays: Association of ERBB2, IGFBP2, and ELF3 with epithelial differentiation. Am. J. Pathol. 2002, 161:1587-1595.
4. Allen T., van Tuyl M., Iyengar P., et al. Grg1 acts as a lung-specific oncogene in a transgenic mouse model. Cancer Res. 2006, 66:1294-1301.
5. Andrioli L.P., Oberstein A.L., Corado M.S., et al. Groucho-dependent repression by sloppy-paired 1 differentially positions anterior pair-rule stripes in the Drosophila embryo. Dev. Biol. 2004, 276:541-551.
6. Arnosti D.N. Multiple mechanisms of transcriptional repression in eukaryotes. Handb. Exp. Pharmacol. 2004, 66:33-67.
7. Aronson B.D., Fisher A.L., Blechman K., et al. Groucho-dependent and -independent repression activities of Runt domain proteins. Mol. Cell. Biol. 1997, 17:5581-5587.
8. Astigarraga S., Grossman R., Diaz-Delfin J., et al. A MAPK docking site is critical for downregulation of Capicua by Torso and EGFR RTK signaling. EMBO J. 2007, 26:668-677.
9. Bajoghli B. Evolution of the Groucho/Tle gene family: Gene organization and duplication events. Dev. Genes Evol. 2007, 217:613-618.
10. Bajoghli B., Aghaallaei N., Soroldoni D., et al. The roles of Groucho/Tle in left-right asymmetry and Kupffer's vesicle organogenesis. Dev. Biol. 2007, 303:347-361.
11. Barolo S., Stone T., Bang A.G., et al. Default repression and Notch signaling: Hairless acts as an adaptor to recruit the corepressors Groucho and dCtBP to Suppressor of Hairless. Genes Dev. 2002, 16:1964-1976.
12. Beagle B., Johnson G.V. AES/GRG5: More than just a dominant-negative TLE/GRG family member. Dev. Dyn. 2010, 239:2795-2805.
13. Berger S.L. The complex language of chromatin regulation during transcription. Nature 2007, 447:407-412.
14. Berk A.J. Activation of RNA polymerase II transcription. Curr. Opin. Cell Biol. 1999, 11:330-335.
15. Bienz M., Clevers H. Linking colorectal cancer to Wnt signaling. Cell 2000, 103:311-320.
16. Brantjes H., Roose J., van De Wetering M., et al. All Tcf HMG box transcription factors interact with Groucho-related co-repressors. Nucleic Acids Res. 2001, 29:1410-1419.
17. Buchberger J.R., Onishi M., Li G., et al. Sir3-nucleosome interactions in spreading of silent chromatin in Saccharomyces cerevisiae. Mol. Cell. Biol. 2008, 28:6903-6918.
18. Burks P.J., Isaacs H.V., Pownall M.E. FGF signalling modulates transcriptional repression by Xenopus groucho-related-4. Biol. Cell 2009, 101:301-308.
19. Buscarlet M., Stifani S. The 'Marx' of Groucho on development and disease. Trends Cell Biol. 2007, 17:353-361.
20. Buscarlet M., Hermann R., Lo R., et al. Cofactor-activated phosphorylation is required for inhibition of cortical neuron differentiation by Groucho/TLE1. PLoS One 2009, 4:e8107.
21. Cai H.N., Arnosti D.N., Levine M. Long-range repression in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 1996, 93:9309-9314.
22. Cai Y., Brophy P.D., Levitan I., et al. Groucho suppresses Pax2 transactivation by inhibition of JNK-mediated phosphorylation. EMBO J. 2003, 22:5522-5529.
23. Canon J., Banerjee U. In vivo analysis of a developmental circuit for direct transcriptional activation and repression in the same cell by a Runx protein. Genes Dev. 2003, 17:838-843.
24. Cavallo R.A., Cox R.T., Moline M.M., et al. Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 1998, 395:604-608.
25. Chen G., Courey A.J. Groucho/TLE family proteins and transcriptional repression. Gene 2000, 249:1-16.
26. Chen G., Nguyen P.H., Courey A.J. A role for Groucho tetramerization in transcriptional repression. Mol. Cell. Biol. 1998, 18:7259-7268.
27. Chen G., Fernandez J., Mische S., et al. A functional interaction between the histone deacetylase Rpd3 and the corepressor groucho in Drosophila development. Genes Dev. 1999, 13:2218-2230.
28. Choi C.Y., Kim Y.H., Kwon H.J., et al. The homeodomain protein NK-3 recruits Groucho and a histone deacetylase complex to repress transcription. J. Biol. Chem. 1999, 274:33194-33197.
29. Choi C.Y., Kim Y.H., Kim Y.O., et al. Phosphorylation by the DHIPK2 protein kinase modulates the corepressor activity of Groucho. J. Biol. Chem. 2005, 280:21427-21436.
30. Chouard T. Structural biology: Breaking the protein rules. Nature 2011, 471:151-153.
31. Choudhury B.K., Kim J., Kung H.F., et al. Cloning and developmental expression of Xenopus cDNAs encoding the Enhancer of split groucho and related proteins. Gene 1997, 195:41-48.
32. Cinnamon E., Paroush Z. Context-dependent regulation of Groucho/TLE-mediated repression. Curr. Opin. Genet. Dev. 2008, 18:435-440.
33. Cinnamon E., Helman A., Ben-Haroush Schyr R., et al. Multiple RTK pathways downregulate Groucho-mediated repression in Drosophila embryogenesis. Development 2008, 135:829-837.
34. Courey A.J., Jia S. Transcriptional repression: The long and the short of it. Genes Dev. 2001, 15:2786-2796.
35. Dawson S.R., Turner D.L., Weintraub H., et al. 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, 15:6923-6931.
36. de Celis J.F., Bray S., Garcia-Bellido A. Notch signalling regulates veinlet expression and establishes boundaries between veins and interveins in the Drosophila wing. Development 1997, 124:1919-1928.
37. Delidakis C., Preiss A., Hartley D.A., et al. Two genetically and molecularly distinct functions involved in early neurogenesis reside within the Enhancer of split locus of Drosophila melanogaster. Genetics 1991, 129:803-823.
38. Dubnicoff T., Valentine S.A., Chen G., et al. Conversion of dorsal from an activator to a repressor by the global corepressor Groucho. Genes Dev. 1997, 11:2952-2957.
39. Dunker A.K., Cortese M.S., Romero P., et al. Flexible nets. The roles of intrinsic disorder in protein interaction networks. FEBS J. 2005, 272:5129-5148.
40. Eberhard D., Jimenez G., Heavey B., et al. Transcriptional repression by Pax5 (BSAP) through interaction with corepressors of the Groucho family. EMBO J. 2000, 19:2292-2303.
41. Edmondson D.G., Roth S.Y. Interactions of transcriptional regulators with histones. Methods 1998, 15:355-364.
42. Edmondson D.G., Smith M.M., Roth S.Y. Repression domain of the yeast global repressor Tup1 interacts directly with histones H3 and H4. Genes Dev. 1996, 10:1247-1259.
43. Edmondson D.G., Zhang W., Watson A., et al. In vivo functions of histone acetylation/deacetylation in Tup1p repression and Gcn5p activation. Cold Spring Harb. Symp. Quant. Biol. 1998, 63:459-468.
44. Fisher A.L., Caudy M. Groucho proteins: Transcriptional corepressors for specific subsets of DNA-binding transcription factors in vertebrates and invertebrates. Genes Dev. 1998, 12:1931-1940.
45. 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, 16:2670-2677.
46. Flores-Saaib R.D., Courey A.J. Analysis of Groucho-histone interactions suggests mechanistic similarities between Groucho- and Tup1-mediated repression. Nucleic Acids Res. 2000, 28:4189-4196.
47. Flores-Saaib R.D., Jia S., Courey A.J. Activation and repression by the C-terminal domain of Dorsal. Development 2001, 128:1869-1879.
48. Flowers E.B., Poole R.J., Tursun B., et al. The Groucho ortholog UNC-37 interacts with the short Groucho-like protein LSY-22 to control developmental decisions in C. elegans. Development 2010, 137:1799-1805.
49. Gao X., Chandra T., Gratton M.O., et al. HES6 acts as a transcriptional repressor in myoblasts and can induce the myogenic differentiation program. J. Cell Biol. 2001, 154:1161-1171.
50. Gasperowicz M., Otto F. Mammalian Groucho homologs: Redundancy or specificity?. J. Cell. Biochem. 2005, 95:670-687.
51. Goldstein R.E., Jimenez G., Cook O., et al. Huckebein repressor activity in Drosophila terminal patterning is mediated by Groucho. Development 1999, 126:3747-3755.
52. Gray S., Levine M. Short-range transcriptional repressors mediate both quenching and direct repression within complex loci in Drosophila. Genes Dev. 1996, 10:700-710.
53. Gray S., Levine M. Transcriptional repression in development. Curr. Opin. Cell Biol. 1996, 8:358-364.
54. Grbavec D., Stifani S. Molecular interaction between TLE1 and the carboxyl-terminal domain of HES-1 containing the WRPW motif. Biochem. Biophys. Res. Commun. 1996, 223:701-705.
55. Grbavec D., Lo R., Liu Y., et al. Transducin-like Enhancer of split 2, a mammalian homologue of Drosophila Groucho, acts as a transcriptional repressor, interacts with Hairy/Enhancer of split proteins, and is expressed during neuronal development. Eur. J. Biochem. 1998, 258:339-349.
56. Gromoller A., Lehming N. Srb7p is a physical and physiological target of Tup1p. EMBO J. 2000, 19:6845-6852.
57. Guichard A., Biehs B., Sturtevant M.A., et al. rhomboid and Star interact synergistically to promote EGFR/MAPK signaling during Drosophila wing vein development. Development 1999, 126:2663-2676.
58. Hasson P., Paroush Z. Crosstalk between the EGFR and other signalling pathways at the level of the global transcriptional corepressor Groucho/TLE. Br. J. Cancer 2006, 94:771-775.
59. Hasson P., Muller B., Basler K., et al. Brinker requires two corepressors for maximal and versatile repression in Dpp signalling. EMBO J. 2001, 20:5725-5736.
60. Hasson P., Egoz N., Winkler C., et al. EGFR signaling attenuates Groucho-dependent repression to antagonize Notch transcriptional output. Nat. Genet. 2005, 37:101-105.
61. Hecht A., Laroche T., Strahl-Bolsinger S., et al. Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: A molecular model for the formation of heterochromatin in yeast. Cell 1995, 80:583-592.
62. Helman A., Cinnamon E., Mezuman S., et al. Phosphorylation of Groucho mediates RTK feedback inhibition and prolonged pathway target gene expression. Curr. Biol. 2011, 21:1102-1110.
63. Hoppe G.J., Tanny J.C., Rudner A.D., et al. Steps in assembly of silent chromatin in yeast: Sir3-independent binding of a Sir2/Sir4 complex to silencers and role for Sir2-dependent deacetylation. Mol. Cell. Biol. 2002, 22:4167-4180.
64. Huang Y. Transcriptional silencing in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Nucleic Acids Res. 2002, 30:1465-1482.
65. Imai Y., Kurokawa M., Tanaka K., et al. TLE, the human homolog of groucho, interacts with AML1 and acts as a repressor of AML1-induced transactivation. Biochem. Biophys. Res. Commun. 1998, 252:582-589.
66. Jan Y., Matter M., Pai J.T., et al. A mitochondrial protein, Bit1, mediates apoptosis regulated by integrins and Groucho/TLE corepressors. Cell 2004, 116:751-762.
67. Jennings B.H., Ish-Horowicz D. The Groucho/TLE/Grg family of transcriptional co-repressors. Genome Biol. 2008, 9:205.
68. Jennings B.H., Pickles L.M., Wainwright S.M., et al. Molecular recognition of transcriptional repressor motifs by the WD domain of the Groucho/TLE corepressor. Mol. Cell 2006, 22:645-655.
69. Jennings B.H., Wainwright S.M., Ish-Horowicz D. Differential in vivo requirements for oligomerization during Groucho-mediated repression. EMBO Rep. 2008, 9:76-83.
70. Jimenez G., Paroush Z., Ish-Horowicz D. Groucho acts as a corepressor for a subset of negative regulators, including Hairy and Engrailed. Genes Dev. 1997, 11:3072-3082.
71. Jimenez G., Verrijzer C.P., Ish-Horowicz D. A conserved motif in goosecoid mediates groucho-dependent repression in Drosophila embryos. Mol. Cell. Biol. 1999, 19:2080-2087.
72. Jimenez G., Guichet A., Ephrussi A., et al. Relief of gene repression by torso RTK signaling: Role of capicua in Drosophila terminal and dorsoventral patterning. Genes Dev. 2000, 14:224-231.
73. Ju B.G., Solum D., Song E.J., et al. Activating the PARP-1 sensor component of the groucho/TLE1 corepressor complex mediates a CaMKinase IIdelta-dependent neurogenic gene activation pathway. Cell 2004, 119:815-829.
74. Kawamura A., Koshida S., Hijikata H., et al. Groucho-associated transcriptional repressor ripply1 is required for proper transition from the presomitic mesoderm to somites. Dev. Cell 2005, 9:735-744.
75. Kondow A., Hitachi K., Ikegame T., et al. Bowline, a novel protein localized to the presomitic mesoderm, interacts with Groucho/TLE in Xenopus. Int. J. Dev. Biol. 2006, 50:473-479.
76. Kornberg R.D. Mediator and the mechanism of transcriptional activation. Trends Biochem. Sci. 2005, 30:235-239.
77. Kuchin S., Carlson M. Functional relationships of Srb10-Srb11 kinase, carboxy-terminal domain kinase CTDK-I, and transcriptional corepressor Ssn6-Tup1. Mol. Cell. Biol. 1998, 18:1163-1171.
78. Kuo D., Nie M., De Hoff P., et al. A SUMO-Groucho Q domain fusion protein: Characterization and in vivo Ulp1-mediated cleavage. Protein Expr. Purif. 2011, 76:65-71.
79. Lee W., Andrews B.C., Faust M., et al. Hipk is an essential protein that promotes Notch signal transduction in the Drosophila eye by inhibition of the global co-repressor Groucho. Dev. Biol. 2009, 325:263-272.
80. Li S.S. Structure and function of the Groucho gene family and encoded transcriptional corepressor proteins from human, mouse, rat, Xenopus, Drosophila and nematode. Proc. Natl. Sci. Counc. Republ. Chin. B 2000, 24:47-55.
81. Li L.M., Arnosti D.N. Long- and short-range transcriptional repressors induce distinct chromatin states on repressed genes. Curr. Biol. 2011, 21:406-412.
82. Li D., Roberts R. WD-repeat proteins: Structure characteristics, biological function, and their involvement in human diseases. Cell. Mol. Life Sci. 2001, 58:2085-2097.
83. Li X., Romero P., Rani M., et al. Predicting protein disorder for N-, C-, and internal regions. Genome Inform. Ser. Workshop Genome Inform. 1999, 10:30-40.
84. Linderson Y., Eberhard D., Malin S., et al. Corecruitment of the Grg4 repressor by PU.1 is critical for Pax5-mediated repression of B-cell-specific genes. EMBO Rep. 2004, 5:291-296.
85. Lindsley D.L., Grell E.H. Genetic Variations of Drosophila melanogaster. Carnegie Institution of Washington Publication 1968, 627.
86. Liu Z., Karmarkar V. Groucho/Tup1 family co-repressors in plant development. Trends Plant Sci. 2008, 13:137-144.
87. Lund A.H., van Lohuizen M. RUNX: A trilogy of cancer genes. Cancer Cell 2002, 1:213-215.
88. Lutterbach B., Westendorf J.J., Linggi B., et al. A mechanism of repression by acute myeloid leukemia-1, the target of multiple chromosomal translocations in acute leukemia. J. Biol. Chem. 2000, 275:651-656.
89. Malave T.M., Dent S.Y. Transcriptional repression by Tup1-Ssn6. Biochem. Cell Biol. 2006, 84:437-443.
90. Malik S., Roeder R.G. The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation. Nat. Rev. Genet. 2010, 11:761-772.
91. Mallo M., Franco del Amo F., Gridley T. Cloning and developmental expression of Grg, a mouse gene related to the groucho transcript of the Drosophila Enhancer of split complex. Mech. Dev. 1993, 42:67-76.
92. Mannervik M., Levine M. The Rpd3 histone deacetylase is required for segmentation of the Drosophila embryo. Proc. Natl. Acad. Sci. USA 1999, 96:6797-6801.
93. Mannervik M., Nibu Y., Zhang H., et al. Transcriptional coregulators in development. Science 1999, 284:606-609.
94. Martinez C.A., Arnosti D.N. Spreading of a corepressor linked to action of long-range repressor hairy. Mol. Cell. Biol. 2008, 28:2792-2802.
95. Miyasaka H., Choudhury B.K., Hou E.W., et al. 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. 1993, 216:343-352.
96. Morin P.J. Beta-catenin signaling and cancer. Bioessays 1999, 21:1021-1030.
97. Muhr J., Andersson E., Persson M., et al. Groucho-mediated transcriptional repression establishes progenitor cell pattern and neuronal fate in the ventral neural tube. Cell 2001, 104:861-873.
98. Muller B., Hartmann B., Pyrowolakis G., et al. Conversion of an extracellular Dpp/BMP morphogen gradient into an inverse transcriptional gradient. Cell 2003, 113:221-233.
99. Nagel A.C., Krejci A., Tenin G., et al. Hairless-mediated repression of notch target genes requires the combined activity of Groucho and CtBP corepressors. Mol. Cell. Biol. 2005, 25:10433-10441.
100. Nakayama H., Liu Y., Stifani S., et al. Developmental restriction of Mash-2 expression in trophoblast correlates with potential activation of the notch-2 pathway. Dev. Genet. 1997, 21:21-30.
101. Nellen D., Burke R., Struhl G., et al. Direct and long-range action of a DPP morphogen gradient. Cell 1996, 85:357-368.
102. Nie M., Xie Y., Loo J.A., et al. Genetic and proteomic evidence for roles of Drosophila SUMO in cell cycle control, Ras signaling, and early pattern formation. PLoS One 2009, 4:e5905.
103. Nuthall H.N., Husain J., McLarren K.W., et al. Role for Hes1-induced phosphorylation in Groucho-mediated transcriptional repression. Mol. Cell. Biol. 2002, 22:389-399.
104. Nuthall H.N., Joachim K., Palaparti A., et al. A role for cell cycle-regulated phosphorylation in Groucho-mediated transcriptional repression. J. Biol. Chem. 2002, 277:51049-51057.
105. Nuthall H.N., Joachim K., Stifani S. Phosphorylation of serine 239 of Groucho/TLE1 by protein kinase CK2 is important for inhibition of neuronal differentiation. Mol. Cell. Biol. 2004, 24:8395-8407.
106. Palaparti A., Baratz A., Stifani S. The Groucho/transducin-like enhancer of split transcriptional repressors interact with the genetically defined amino-terminal silencing domain of histone H3. J. Biol. Chem. 1997, 272:26604-26610.
107. Papamichos-Chronakis M., Conlan R.S., Gounalaki N., et al. Hrs1/Med3 is a Cyc8-Tup1 corepressor target in the RNA polymerase II holoenzyme. J. Biol. Chem. 2000, 275:8397-8403.
108. Paroush Z., Finley R.L., Kidd T., et al. Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins. Cell 1994, 79:805-815.
109. Paroush Z., Wainwright S.M., Ish-Horowicz D. Torso signalling regulates terminal patterning in Drosophila by antagonising Groucho-mediated repression. Development 1997, 124:3827-3834.
110. Payankaulam S., Arnosti D.N. Groucho corepressor functions as a cofactor for the Knirps short-range transcriptional repressor. Proc. Natl. Acad. Sci. USA 2009, 106:17314-17319.
111. Payankaulam S., Li L.M., Arnosti D.N. Transcriptional repression: Conserved and evolved features. Curr. Biol. 2010, 20:R764-R771.
112. Pflugrad A., Meir J.Y., Barnes T.M., et al. The Groucho-like transcription factor UNC-37 functions with the neural specificity gene unc-4 to govern motor neuron identity in C. elegans. Development 1997, 124:1699-1709.
113. Pickles L.M., Roe S.M., Hemingway E.J., et al. Crystal structure of the C-terminal WD40 repeat domain of the human Groucho/TLE1 transcriptional corepressor. Structure 2002, 10:751-761.
114. Pinto M., Lobe C.G. Products of the grg (Groucho-related gene) family can dimerize through the amino-terminal Q domain. J. Biol. Chem. 1996, 271:33026-33031.
115. Radivojac P., Obradovic Z., Brown C.J., et al. Prediction of boundaries between intrinsically ordered and disordered protein regions. Pac. Symp. Biocomput. 2003, 8:216-227.
116. Radman-Livaja M., Ruben G., Weiner A., et al. Dynamics of Sir3 spreading in budding yeast: Secondary recruitment sites and euchromatic localization. EMBO J. 2011, 30:1012-1026.
117. Ratnaparkhi G.S., Jia S., Courey A.J. Uncoupling dorsal-mediated activation from dorsal-mediated repression in the Drosophila embryo. Development 2006, 133:4409-4414.
118. Redd M.J., Arnaud M.B., Johnson A.D. A complex composed of tup1 and ssn6 represses transcription in vitro. J. Biol. Chem. 1997, 272:11193-11197.
119. Romero P., Obradovic Z., Dunker K. Sequence data analysis for long disordered regions prediction in the calcineurin family. Genome Inform. Ser. Workshop Genome Inform. 1997, 8:110-124.
120. Romero P., Obradovic Z., Li X., et al. Sequence complexity of disordered protein. Proteins 2001, 42:38-48.
121. Roose J., Molenaar M., Peterson J., et al. The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 1998, 395:608-612.
122. Rorive S., Maris C., Debeir O., et al. Exploring the distinctive biological characteristics of pilocytic and low-grade diffuse astrocytomas using microarray gene expression profiles. J. Neuropathol. Exp. Neurol. 2006, 65:794-807.
123. Ruebel K.H., Leontovich A.A., Jin L., et al. Patterns of gene expression in pituitary carcinomas and adenomas analyzed by high-density oligonucleotide arrays, reverse transcriptase-quantitative PCR, and protein expression. Endocrine 2006, 29:435-444.
124. Rusche L.N., Kirchmaier A.L., Rine J. Ordered nucleation and spreading of silenced chromatin in Saccharomyces cerevisiae. Mol. Biol. Cell 2002, 13:2207-2222.
125. Schmidt C.J., Sladek T.E. A rat homolog of the Drosophila enhancer of split (groucho) locus lacking WD-40 repeats. J. Biol. Chem. 1993, 268:25681-25686.
126. Sekiya T., Zaret K.S. Repression by Groucho/TLE/Grg proteins: Genomic site recruitment generates compacted chromatin in vitro and impairs activator binding in vivo. Mol. Cell 2007, 28:291-303.
127. Sharief F.S., Tsoi S.C., Li S.S. cDNA cloning and genomic organization of enhancer of split groucho gene from nematode Caenorhabditis elegans. Biochem. Mol. Biol. Int. 1997, 43:327-337.
128. Shilo B.Z. Flies over Crete: Drosophila molecular biology. Kolymbari, Crete, July 12-18, 1998. EMBO J. 1998, 17:6769-6771.
129. Sivasankaran R., Vigano M.A., Muller B., et al. Direct transcriptional control of the Dpp target omb by the DNA binding protein Brinker. EMBO J. 2000, 19:6162-6172.
130. Song H., Hasson P., Paroush Z., et al. Groucho oligomerization is required for repression in vivo. Mol. Cell. Biol. 2004, 24:4341-4350.
131. Stifani S., Blaumueller C.M., Redhead N.J., et al. Human homologs of a Drosophila Enhancer of split gene product define a novel family of nuclear proteins. Nat. Genet. 1992, 2:119-127.
132. Swingler T.E., Bess K.L., Yao J., et al. The proline-rich homeodomain protein recruits members of the Groucho/Transducin-like enhancer of split protein family to co-repress transcription in hematopoietic cells. J. Biol. Chem. 2004, 279:34938-34947.
133. Terry J., Saito T., Subramanian S., et al. TLE1 as a diagnostic immunohistochemical marker for synovial sarcoma emerging from gene expression profiling studies. Am. J. Surg. Pathol. 2007, 31:240-246.
134. Thirunavukkarasu K., Mahajan M., McLarren K.W., et al. Two domains unique to osteoblast-specific transcription factor Osf2/Cbfa1 contribute to its transactivation function and its inability to heterodimerize with Cbfbeta. Mol. Cell. Biol. 1998, 18:4197-4208.
135. Tolkunova E.N., Fujioka M., Kobayashi M., et al. Two distinct types of repression domain in engrailed: One interacts with the groucho corepressor and is preferentially active on integrated target genes. Mol. Cell. Biol. 1998, 18:2804-2814.
136. Treitel M.A., Carlson M. Repression by SSN6-TUP1 is directed by MIG1, a repressor/activator protein. Proc. Natl. Acad. Sci. USA 1995, 92:3132-3136.
137. Tzamarias D., Struhl K. Distinct TPR motifs of Cyc8 are involved in recruiting the Cyc8-Tup1 corepressor complex to differentially regulated promoters. Genes Dev. 1995, 9:821-831.
138. Valentine S.A., Chen G., Shandala T., et al. Dorsal-mediated repression requires the formation of a multiprotein repression complex at the ventral silencer. Mol. Cell. Biol. 1998, 18:6584-6594.
139. Villanueva C.J., Waki H., Godio C., et al. TLE3 is a dual-function transcriptional coregulator of adipogenesis. Cell Metab. 2011, 13:413-427.
140. Weng A.P., Ferrando A.A., Lee W., et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 2004, 306:269-271.
141. Winkler C.J., Ponce A., Courey A.J. Groucho-mediated repression may result from a histone deacetylase-dependent increase in nucleosome density. PLoS One 2010, 5:e10166.
142. Xue B., Dunbrack R.L., Williams R.W., et al. PONDR-FIT: A meta-predictor of intrinsically disordered amino acids. Biochim. Biophys. Acta 2010, 1804:996-1010.
143. Yamagata T., Maki K., Mitani K. Runx1/AML1 in normal and abnormal hematopoiesis. Int. J. Hematol. 2005, 82:1-8.
144. Yao J., Liu Y., Husain J., et al. Combinatorial expression patterns of individual TLE proteins during cell determination and differentiation suggest non-redundant functions for mammalian homologs of Drosophila Groucho. Dev. Growth Differ. 1998, 40:133-146.
145. Yao J., Liu Y., Lo R., et al. Disrupted development of the cerebral hemispheres in transgenic mice expressing the mammalian Groucho homologue transducin-like-enhancer of split 1 in postmitotic neurons. Mech. Dev. 2000, 93:105-115.
146. Zhang H., Emmons S.W. Caenorhabditis elegans unc-37/groucho interacts genetically with components of the transcriptional mediator complex. Genetics 2002, 160:799-803.
147. Zhu C.C., Dyer M.A., Uchikawa M., et al. Six3-mediated auto repression and eye development requires its interaction with members of the Groucho-related family of co-repressors. Development 2002, 129:2835-2849.