The GAGA Factor Regulatory Network: Identification of GAGA Factor Associated Proteins

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2017 Mar 16

PMID 28296955

Citations 27

Authors

Dmitry Lomaev

Anna Mikhailova

Maksim Erokhin

Alexander V Shaposhnikov

James J Moresco

Tatiana Blokhina

Daniel Wolle

Tsutomu Aoki

Vladimir Ryabykh

John R Yates 3rd

Yulii V Shidlovskii

Pavel Georgiev

Paul Schedl

Darya Chetverina

Affiliations

Soon will be listed here.

Abstract

The Drosophila GAGA factor (GAF) has an extraordinarily diverse set of functions that include the activation and silencing of gene expression, nucleosome organization and remodeling, higher order chromosome architecture and mitosis. One hypothesis that could account for these diverse activities is that GAF is able to interact with partners that have specific and dedicated functions. To test this possibility we used affinity purification coupled with high throughput mass spectrometry to identify GAF associated partners. Consistent with this hypothesis the GAF interacting network includes a large collection of factors and complexes that have been implicated in many different aspects of gene activity, chromosome structure and function. Moreover, we show that GAF interactions with a small subset of partners is direct; however for many others the interactions could be indirect, and depend upon intermediates that serve to diversify the functional capabilities of the GAF protein.

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References

Soeller W, Oh C, Kornberg T . Isolation of cDNAs encoding the Drosophila GAGA transcription factor. Mol Cell Biol. 1993; 13(12):7961-70. PMC: 364868. DOI: 10.1128/mcb.13.12.7961-7970.1993. View

Okada M, Hirose S . Chromatin remodeling mediated by Drosophila GAGA factor and ISWI activates fushi tarazu gene transcription in vitro. Mol Cell Biol. 1998; 18(5):2455-61. PMC: 110625. DOI: 10.1128/MCB.18.5.2455. View

Gause M, Morcillo P, Dorsett D . Insulation of enhancer-promoter communication by a gypsy transposon insert in the Drosophila cut gene: cooperation between suppressor of hairy-wing and modifier of mdg4 proteins. Mol Cell Biol. 2001; 21(14):4807-17. PMC: 87172. DOI: 10.1128/MCB.21.14.4807-4817.2001. View

Negre N, Hennetin J, Sun L, Lavrov S, Bellis M, White K . Chromosomal distribution of PcG proteins during Drosophila development. PLoS Biol. 2006; 4(6):e170. PMC: 1440717. DOI: 10.1371/journal.pbio.0040170. View

Erokhin M, Elizarev P, Parshikov A, Schedl P, Georgiev P, Chetverina D . Transcriptional read-through is not sufficient to induce an epigenetic switch in the silencing activity of Polycomb response elements. Proc Natl Acad Sci U S A. 2015; 112(48):14930-5. PMC: 4672805. DOI: 10.1073/pnas.1515276112. View

Faucheux M, Roignant J, Netter S, Charollais J, Antoniewski C, Theodore L . batman Interacts with polycomb and trithorax group genes and encodes a BTB/POZ protein that is included in a complex containing GAGA factor. Mol Cell Biol. 2003; 23(4):1181-95. PMC: 141128. DOI: 10.1128/MCB.23.4.1181-1195.2003. View

Guruharsha K, Rual J, Zhai B, Mintseris J, Vaidya P, Vaidya N . A protein complex network of Drosophila melanogaster. Cell. 2011; 147(3):690-703. PMC: 3319048. DOI: 10.1016/j.cell.2011.08.047. View

Zollman S, Godt D, Prive G, Couderc J, Laski F . The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc Natl Acad Sci U S A. 1994; 91(22):10717-21. PMC: 45093. DOI: 10.1073/pnas.91.22.10717. View

Bardwell V, Treisman R . The POZ domain: a conserved protein-protein interaction motif. Genes Dev. 1994; 8(14):1664-77. DOI: 10.1101/gad.8.14.1664. View

10.

Horard B, Tatout C, Poux S, Pirrotta V . Structure of a polycomb response element and in vitro binding of polycomb group complexes containing GAGA factor. Mol Cell Biol. 2000; 20(9):3187-97. PMC: 85613. DOI: 10.1128/MCB.20.9.3187-3197.2000. View

11.

Shimojima T, Okada M, Nakayama T, Ueda H, Okawa K, Iwamatsu A . Drosophila FACT contributes to Hox gene expression through physical and functional interactions with GAGA factor. Genes Dev. 2003; 17(13):1605-16. PMC: 196133. DOI: 10.1101/gad.1086803. View

12.

Weber J, Taxman D, Lu Q, Gilmour D . Molecular architecture of the hsp70 promoter after deletion of the TATA box or the upstream regulation region. Mol Cell Biol. 1997; 17(7):3799-808. PMC: 232231. DOI: 10.1128/MCB.17.7.3799. View

13.

Bonchuk A, Denisov S, Georgiev P, Maksimenko O . Drosophila BTB/POZ domains of "ttk group" can form multimers and selectively interact with each other. J Mol Biol. 2011; 412(3):423-36. DOI: 10.1016/j.jmb.2011.07.052. View

14.

Fuda N, Guertin M, Sharma S, Danko C, Martins A, Siepel A . GAGA factor maintains nucleosome-free regions and has a role in RNA polymerase II recruitment to promoters. PLoS Genet. 2015; 11(3):e1005108. PMC: 4376892. DOI: 10.1371/journal.pgen.1005108. View

15.

Schwartz Y, Pirrotta V . A new world of Polycombs: unexpected partnerships and emerging functions. Nat Rev Genet. 2013; 14(12):853-64. DOI: 10.1038/nrg3603. View

16.

Kvon E, Stampfel G, Yanez-Cuna J, Dickson B, Stark A . HOT regions function as patterned developmental enhancers and have a distinct cis-regulatory signature. Genes Dev. 2012; 26(9):908-13. PMC: 3347788. DOI: 10.1101/gad.188052.112. View

17.

Hagstrom K, Muller M, Schedl P . A Polycomb and GAGA dependent silencer adjoins the Fab-7 boundary in the Drosophila bithorax complex. Genetics. 1997; 146(4):1365-80. PMC: 1208081. DOI: 10.1093/genetics/146.4.1365. View

18.

Kellner W, Van Bortle K, Li L, Ramos E, Takenaka N, Corces V . Distinct isoforms of the Drosophila Brd4 homologue are present at enhancers, promoters and insulator sites. Nucleic Acids Res. 2013; 41(20):9274-83. PMC: 3814382. DOI: 10.1093/nar/gkt722. View

19.

Reddy B, Bajpe P, Bassett A, Moshkin Y, Kozhevnikova E, Bezstarosti K . Drosophila transcription factor Tramtrack69 binds MEP1 to recruit the chromatin remodeler NuRD. Mol Cell Biol. 2010; 30(21):5234-44. PMC: 2953047. DOI: 10.1128/MCB.00266-10. View

20.

Nakayama T, Shimojima T, Hirose S . The PBAP remodeling complex is required for histone H3.3 replacement at chromatin boundaries and for boundary functions. Development. 2012; 139(24):4582-90. DOI: 10.1242/dev.083246. View