Brinker possesses multiple mechanisms for repression because its primary co-repressor, Groucho, may be unavailable in some cell types

Development (Cambridge)

Volumn 140, Issue 20, 2013, Pages 4256-4265

  Upadhyai, Priyanka ^a   Campbell, Gerard ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Brinker; Co repressor; CtBP; Groucho; Repression

Indexed keywords

ARTICLE; BRINKER GENE; DROSOPHILA; EGG SHELL; GENE REPRESSION; GENETIC ENGINEERING; GROUCHO GENE; MUTANT; NONHUMAN; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; REPRESSOR GENE;

BRINKER; CO-REPRESSOR; CTBP; GROUCHO; REPRESSION;

ALCOHOL OXIDOREDUCTASES; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CO-REPRESSOR PROTEINS; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKOUT TECHNIQUES; MUTATION; OOGENESIS; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, INVERTEBRATE PEPTIDE; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; WING;

EID: 84884949943     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.099366     Document Type: Article

References (65)

1. Alexandre, C., Lecourtois, M. and Vincent, J. (1999). Wingless and Hedgehog pattern Drosophila denticle belts by regulating the production of short-range signals. Development 126, 5689-5698.
2. Barolo, S. and Levine, M. (1997). hairy mediates dominant repression in the Drosophila embryo. EMBO J. 16, 2883-2891.
3. Barolo, S., Carver, L. A. and Posakony, J. W. (2000). GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. Biotechniques 29, 726, 728, 730, 732.
4. Barolo, S., Stone, T., Bang, A. G. and Posakony, J. W. (2002). Default repression and Notch signaling: Hairless acts as an adaptor to recruit the corepressors Groucho and dCtBP to Suppressor of Hairless. Genes Dev. 16, 1964-1976.
5. Barrio, R. and de Celis, J. F. (2004). Regulation of spalt expression in the Drosophila wing blade in response to the Decapentaplegic signaling pathway. Proc. Natl. Acad. Sci. USA 101, 6021-6026.
6. Bejsovec, A. and Martinez Arias, A. (1991). Roles of wingless in patterning the larval epidermis of Drosophila. Development 113, 471-485.
7. Berg, C. A. (2005). The Drosophila shell game: patterning genes and morphological change. Trends Genet. 21, 346-355.
8. Bianchi-Frias, D., Orian, A., Delrow, J. J., Vazquez, J., Rosales-Nieves, A. E. and Parkhurst, S. M. (2004). Hairy transcriptional repression targets and cofactor recruitment in Drosophila. PLoS Biol. 2, e178.
9. Campbell, G. and Tomlinson, A. (1999). Transducing the Dpp morphogen gradient in the wing of Drosophila: regulation of Dpp targets by brinker. Cell 96, 553-562.
10. Chen, Y. and Schüpbach, T. (2006). The role of brinker in eggshell patterning. Mech. Dev. 123, 395-406.
11. Chen, G., Fernandez, J., Mische, S. and Courey, A. J. (1999). A functional interaction between the histone deacetylase Rpd3 and the corepressor groucho in Drosophila development. Genes Dev. 13, 2218-2230.
12. Choi, C. Y., Kim, Y. H., Kim, Y. O., Park, S. J., Kim, E. A., Riemenschneider, W., Gajewski, K., Schulz, R. A. and Kim, Y. (2005). Phosphorylation by the DHIPK2 protein kinase modulates the corepressor activity of Groucho. J. Biol. Chem. 280, 21427-21436.
13. Cinnamon, E., Helman, A., Ben-Haroush Schyr, R., Orian, A., Jiménez, G. and Paroush, Z. (2008). Multiple RTK pathways downregulate Groucho-mediated repression in Drosophila embryogenesis. Development 135, 829-837.
14. del Álamo Rodríguez, D., Terriente Felix, J. and Díaz-Benjumea, F. J. (2004). The role of the T-box gene optomotor-blind in patterning the Drosophila wing. Dev. Biol. 268, 481-492.
15. Golembo, M., Raz, E. and Shilo, B. Z. (1996). The Drosophila embryonic midline is the site of Spitz processing, and induces activation of the EGF receptor in the ventral ectoderm. Development 122, 3363-3370.
16. Gong, W. J. and Golic, K. G. (2003). Ends-out, or replacement, gene targeting in Drosophila. Proc. Natl. Acad. Sci. USA 100, 2556-2561.
17. Gromöller, A. and Lehming, N. (2000). Srb7p is a physical and physiological target of Tup1p. EMBO J. 19, 6845-6852.
18. Hasson, P., Müller, B., Basler, K. and Paroush, Z. (2001). Brinker requires two corepressors for maximal and versatile repression in Dpp signalling. EMBO J. 20, 5725-5736.
19. Hasson, P., Egoz, N., Winkler, C., Volohonsky, G., Jia, S., Dinur, T., Volk, T., Courey, A. J. and Paroush, Z. (2005). EGFR signaling attenuates Grouchodependent repression to antagonize Notch transcriptional output. Nat. Genet. 37, 101-105.
20. Hong, S. H. and Privalsky, M. L. (2000). The SMRT corepressor is regulated by a MEK-1 kinase pathway: inhibition of corepressor function is associated with SMRT phosphorylation and nuclear export. Mol. Cell. Biol. 20, 6612-6625.
21. Huang, J., Zhou, W., Watson, A. M., Jan, Y. N. and Hong, Y. (2008). Efficient ends-out gene targeting in Drosophila. Genetics 180, 703-707.
22. Huang, J., Zhou, W., Dong, W., Watson, A. M. and Hong, Y. (2009). Directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering. Proc. Natl. Acad. Sci. USA 106, 8284-8289.
23. Jaźwińska, A., Rushlow, C. and Roth, S. (1999a). The role of brinker in mediating the graded response to Dpp in early Drosophila embryos. Development 126, 3323-3334.
24. Jaźwińska, A., Kirov, N., Wieschaus, E., Roth, S. and Rushlow, C. (1999b). The Drosophila gene brinker reveals a novel mechanism of Dpp target gene regulation. Cell 96, 563-573.
25. Jennings, B. H. and Ish-Horowicz, D. (2008). The Groucho/TLE/Grg family of transcriptional co-repressors. Genome Biol. 9, 205.
26. Jennings, B. H., Wainwright, S. M. and Ish-Horowicz, D. (2008). Differential in vivo requirements for oligomerization during Groucho-mediated repression. EMBO Rep. 9, 76-83.
27. Keller, S. A., Mao, Y., Struffi, P., Margulies, C., Yurk, C. E., Anderson, A. R., Amey, R. L., Moore, S., Ebels, J. M., Foley, K. et al. (2000). dCtBP-dependent and-independent repression activities of the Drosophila Knirps protein. Mol. Cell. Biol. 20, 7247-7258.
28. Kim, J. H., Cho, E. J., Kim, S. T. and Youn, H. D. (2005). CtBP represses p300-mediated transcriptional activation by direct association with its bromodomain. Nat. Struct. Mol. Biol. 12, 423-428.
29. Kühnlein, R. P., Frommer, G., Friedrich, M., Gonzalez-Gaitan, M., Weber, A., Wagner-Bernholz, J. F., Gehring, W. J., Jäckle, H. and Schuh, R. (1994). spalt encodes an evolutionarily conserved zinc finger protein of novel structure which provides homeotic gene function in the head and tail region of the Drosophila embryo. EMBO J. 13, 168-179.
30. Kühnlein, R. P., Brönner, G., Taubert, H. and Schuh, R. (1997). Regulation of Drosophila spalt gene expression. Mech. Dev. 66, 107-118.
31. Lammel, U., Meadows, L. and Saumweber, H. (2000). Analysis of Drosophila salivary gland, epidermis and CNS development suggests an additional function of brinker in anterior-posterior cell fate specification. Mech. Dev. 92, 179-191.
32. Lee, J. R., Urban, S., Garvey, C. F. and Freeman, M. (2001). Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila. Cell 107, 161-171.
33. Lin, X., Sun, B., Liang, M., Liang, Y. Y., Gast, A., Hildebrand, J., Brunicardi, F. C., Melchior, F. and Feng, X. H. (2003). Opposed regulation of corepressor CtBP by SUMOylation and PDZ binding. Mol. Cell 11, 1389-1396.
34. Martinez, C. A. and Arnosti, D. N. (2008). Spreading of a corepressor linked to action of long-range repressor hairy. Mol. Cell. Biol. 28, 2792-2802.
35. Minami, M., Kinoshita, N., Kamoshida, Y., Tanimoto, H. and Tabata, T. (1999). brinker is a target of Dpp in Drosophila that negatively regulates Dppdependent genes. Nature 398, 242-246.
36. Nagel, A. C. and Preiss, A. (2011). Fine tuning of Notch signaling by differential co-repressor recruitment during eye development of Drosophila. Hereditas 148, 77-84.
37. Nagel, A. C., Krejci, A., Tenin, G., Bravo-Patiño, A., Bray, S., Maier, D. and Preiss, A. (2005). Hairless-mediated repression of notch target genes requires the combined activity of Groucho and CtBP corepressors. Mol. Cell. Biol. 25, 10433-10441.
38. Nibu, Y., Zhang, H. and Levine, M. (1998a). Interaction of short-range repressors with Drosophila CtBP in the embryo. Science 280, 101-104.
39. Nibu, Y., Zhang, H., Bajor, E., Barolo, S., Small, S. and Levine, M. (1998b). dCtBP mediates transcriptional repression by Knirps, Krüppel and Snail in the Drosophila embryo. EMBO J. 17, 7009-7020.
40. Orian, A., Delrow, J. J., Rosales Nieves, A. E., Abed, M., Metzger, D., Paroush, Z., Eisenman, R. N. and Parkhurst, S. M. (2007). A Myc-Groucho complex integrates EGF and Notch signaling to regulate neural development. Proc. Natl. Acad. Sci. USA 104, 15771-15776.
41. Paroush, Z., Finley, R. L., Jr, Kidd, T., Wainwright, S. M., Ingham, P. W., Brent, R. and Ish-Horowicz, D. (1994). Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins. Cell 79, 805-815.
42. Payankaulam, S. and Arnosti, D. N. (2009). Groucho corepressor functions as a cofactor for the Knirps short-range transcriptional repressor. Proc. Natl. Acad. Sci. USA 106, 17314-17319.
43. Poortinga, G., Watanabe, M. and Parkhurst, S. M. (1998). Drosophila CtBP: a Hairy-interacting protein required for embryonic segmentation and hairymediated transcriptional repression. EMBO J. 17, 2067-2078.
44. Rong, Y. S. and Golic, K. G. (2000). Gene targeting by homologous recombination in Drosophila. Science 288, 2013-2018.
45. Saller, E., Kelley, A. and Bienz, M. (2002). The transcriptional repressor Brinker antagonizes Wingless signaling. Genes Dev. 16, 1828-1838.
46. Sanson, B. (2001). Generating patterns from fields of cells. Examples from Drosophila segmentation. EMBO Rep. 2, 1083-1088.
47. Shi, Y., Sawada, J., Sui, G., Affar, B., Whetstine, J. R., Lan, F., Ogawa, H., Luke, M. P., Nakatani, Y. and Shi, Y. (2003). Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 422, 735-738.
48. Shravage, B. V., Altmann, G., Technau, M. and Roth, S. (2007). The role of Dpp and its inhibitors during eggshell patterning in Drosophila. Development 134, 2261-2271.
49. Sivasankaran, R., Vigano, M. A., Müller, B., Affolter, M. and Basler, K. (2000). Direct transcriptional control of the Dpp target omb by the DNA binding protein Brinker. EMBO J. 19, 6162-6172.
50. Struffi, P. and Arnosti, D. N. (2005). Functional interaction between the Drosophila knirps short range transcriptional repressor and RPD3 histone deacetylase. J. Biol. Chem. 280, 40757-40765.
51. Struffi, P., Corado, M., Kulkarni, M. and Arnosti, D. N. (2004). Quantitative contributions of CtBP-dependent and-independent repression activities of Knirps. Development 131, 2419-2429.
52. Subramanian, T. and Chinnadurai, G. (2003). Association of class I histone deacetylases with transcriptional corepressor CtBP. FEBS Lett. 540, 255-258.
53. Szüts, D., Freeman, M. and Bienz, M. (1997). Antagonism between EGFR and Wingless signalling in the larval cuticle of Drosophila. Development 124, 3209-3219.
54. Tautz, D. and Pfeifle, C. (1989). 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 98, 81-85.
55. Winkler, C. J., Ponce, A. and Courey, A. J. (2010). Groucho-mediated repression may result from a histone deacetylase-dependent increase in nucleosome density. PLoS ONE 5, e10166.
56. Winter, S. E. and Campbell, G. (2004). Repression of Dpp targets in the Drosophila wing by Brinker. Development 131, 6071-6081.
57. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
58. Yang, L., Meng, F., Ma, D., Xie, W. and Fang, M. (2013). Bridging Decapentaplegic and Wingless signaling in Drosophila wings through repression of naked cuticle by Brinker. Development 140, 413-422.
59. Zeng, W., Wharton, K. A., Jr, Mack, J. A., Wang, K., Gadbaw, M., Suyama, K., Klein, P. S. and Scott, M. P. (2000). naked cuticle encodes an inducible antagonist of Wnt signalling. Nature 403, 789-795.
60. Zhang, H. and Emmons, S. W. (2002). Caenorhabditis elegans unc-37/groucho interacts genetically with components of the transcriptional mediator complex. Genetics 160, 799-803.
61. Zhang, H. and Levine, M. (1999). Groucho and dCtBP mediate separate pathways of transcriptional repression in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 96, 535-540.
62. Zhang, H., Levine, M. and Ashe, H. L. (2001). Brinker is a sequence-specific transcriptional repressor in the Drosophila embryo. Genes Dev. 15, 261-266.
63. Zhao, L. J., Subramanian, T., Zhou, Y. and Chinnadurai, G. (2006). Acetylation by p300 regulates nuclear localization and function of the transcriptional corepressor CtBP2. J. Biol. Chem. 281, 4183-4189.
64. Zhou, W., Huang, J., Watson, A. M. and Hong, Y. (2012). W:Neo: a novel dualselection marker for high efficiency gene targeting in Drosophila. PLoS ONE 7, e31997.
65. Ziv, O., Suissa, Y., Neuman, H., Dinur, T., Geuking, P., Rhiner, C., Portela, M., Lolo, F., Moreno, E. and Gerlitz, O. (2009). The co-regulator dNAB interacts with Brinker to eliminate cells with reduced Dpp signaling. Development 136, 1137-1145.