Identification of the new GAGA transcription factor target genes during Drosophila melanogaster oogenesis | Vestnik Tomskogo gosudarstvennogo universiteta. Biologiya - Tomsk State University Journal of Biology. 2014. № 1 (25).

Identification of the new GAGA transcription factor target genes during Drosophila melanogaster oogenesis

D. melanogaster oogenesis, including dorsal appendage (DA) formation, is controlled by numerous genes and signaling pathways, e.g. EGFR, Notch, Wingless, Decapentaplegic (Dpp) pathways. Since these signaling pathways participate in the formation of many Drosophila organs and tissues and are evolutionary conserved, their regulation and relationships between themselves are well-studied. However, so far association of these pathways with the GAGA protein, taking part in the expression regulation of many Drosophila genes, has not been shown. In this paper, the association between the GAGA transcription factor and key components of the Dpp signaling pathway (decapentaplegic (dpp), thickveins (tkv), and saxophone (sax)) were studied. The dpp gene encodes ligand of the Dpp pathway, tkv and sax encode the type I receptors. This work was performed using combined computer-experimental approach, which included: (1) recognition of the GAGA binding sites in the regulatory regions of genes, using computational approach; (2) analysis of the genetic interaction of the Trl gene with the components of the Dpp signaling pathway; (3) analysis of the relative expression of the genes in the ovaries of wild type females and Trl mutants, using real-time PCR. As a result, in the regulatory regions of all analyzed genes, numerous GAGA binding sites, including experimentally verified and evolutionary conserved, were found. Besides, the genetic interaction of the Trl gene, encoding the GAGA protein, with the dpp, tkv, and sax genes during DA formation was demonstrated, i.e. an enhancement of the dpp, tkv and sax mutants, when the GAGA level was reduced. DAs of the eggs laid by the flies carrying both mutations on the Trl gene and dpp/ tkv/ sax gene were shortened, abnormal or had no paddles. At the same time DAs of the Trl/+, dpp/+, tkv/+, and sax/+ heterozygotes didn't have significant distinctions as compared with norm. Additionally, we investigated an alteration of the relative expression of the dpp, tkv and sax genes in the ovaries of wild type females and Trl/Trl mutants. As a result, it was found that only sax expression was reduced more than two-fold as compared with wild type. In the case of other genes, expression was changed insignificantly. Thus, in this manuscript we have shown that the GAGA transcription factor participates in the expression regulation of the sax gene during D. melanogaster oogenesis. Since the relative level of the mRNA of the dpp and tkv genes didn't change significantly when GAGA level was reduced, we suppose that GAGA can participate in the transcription regulation of the dpp and tkv genes at other stages of development/ in other Drosophila organs and tissues.

Download file

Counter downloads: 237

Keywords

GAGA, Drosophila, oogenesis, Dpp signaling pathway, Drosophila, GAGA, Trithorax-like, сигнальный путь Dpp, оогенез, Trithorax-like

Authors

Name	Organization	E-mail
Omelina Eugeniya S.	Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences	omelina@bionet.nsc.ru
Kokhanenko Alina A.	Tomsk State University	alinakokhanenko@gmail.com

Всего: 2

References

Pineyro D., Blanch M., Badal M., Kosoy A., Bernues J. GAGA factor repression of transcription is a rare event but the negative regulation of Trl is conserved in Drosophila species // Biochim Biophys Acta. 2013. Vol. 1829. P. 1056-1065.

Niepielko M.G., Ip K., Kanodia J.S., Lun D.S., Yakoby N. Evolution of BMP Signaling in Drosophila Oogenesis: A Receptor-Based Mechanism // Biophys. J. 2012. Vol. 102. P. 1722-1730.

Fritsch C., Lanfear R., Ray R.P. Rapid evolution of a novel signalling mechanism by concerted duplication and divergence of a BMP ligand and its extracellular modulators // Dev. Genes Evol. 2010. Vol. 220. P. 235-250.

Penton A., Chen Y., Staehling-Hampton K. et al. Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that Brk25D is a decapentaplegic receptor // Cell. 1194. Vol. 78. P. 239-250.

Singer M.A., Penton A., Twombly V., Hoffmann F.M., Gelbart W.M. Signaling through both type I DPP receptors is required for anterior-posterior patterning of the entire Drosophila wing // Development. 1997. Vol. 124. P. 79-89.

Horsfield J., Penton A., Secombe J. et al. Decapentaplegic is required for arrest in G1 phase during Drosophila eye development // Development. 1998. Vol. 125. P. 5069-5078.

de Celis J.F. Expression and function of decapentaplegic and thick veins during the differentiation of the veins in the Drosophila wing // Development. 1997. Vol. 124. P. 1007-1018.

Russo C.A., Takezaki N., Nei M. Molecular phylogeny and divergence times of drosophilid species // Mol. Biol. Evol. 1995. Vol. 12. P. 391-404.

Spencer F.A., Hoffmann F.M., Gelbart W.M. Decapentaplegic: A gene complex affecting morphogenesis in Drosophila melanogaster // Cell. 1982. Vol. 28. P. 451-461.

Arora K., Nusslein-Volhard C. Altered mitotic domains reveal fate map changes in Drosophila embryos mutant for zygotic dorsoventral patterning genes // Development. 1992. Vol. 114. P. 1003-1024.

Wharton K.A., Ray R.P., Findley S.D., Duncan H.E., Gelbart W.M. Molecular lesions associated with alleles of decapentaplegic identify residues necessary for TGF- BMP cell signaling in Drosophila melanogaster // Genetics. 1996. Vol. 142. P. 493-505.

Hartl D.L., Lozovskaya E.R. Genome evolution: between the nucleosome and the chromosome // EXS. 1994. Vol. 69. P. 579-592.

Shelton D.A., Stegman L., Hardison R. et al. Phylogenetic footprinting of hypersensitive site 3 of the betaglobin locus control region // Blood. 1997. Vol. 89. P. 3457-3469.

Bergman C.M., Kreitman M. Analysis of conserved noncoding DNA in Drosophila reveals similar constraints in intergenic and intronic sequences // Genome Res. 2001. Vol. 11. P. 1335-1345.

Gumucio D.L., Shelton D.A., Bailey W.J. et al. Phylogenetic footprinting reveals unexpected complexity in trans factor binding upstream from the epsilon-globin gene // Proc. Natl. Acad. Sci. USA. 1993. Vol. 90. P. 6018-6022.

Schotman H., Karhinen L., Rabouille C. Integrins mediate their unconventional, mechanical-stress-induced secretion via RhoA and PINCH in Drosophila // J Cell Sci. 2009. Vol. 122. P. 2662-2672.

Omelina E.S., Baricheva E.M., Oshchepkov D.Y., Merkulova T.I. Analysis and recognition of the GAGA transcription factor binding sites in Drosophila genes // Comput Biol. Chem. 2011. Vol. 35. P. 363-370.

Guild G.M., Connelly P.S., Shaw M.K., Tilney L.G. Actin filament cables in Drosophila nurse cells are composed of modules that slide passively past one another during dumping // J Cell Biol. 1997. Vol. 138. P. 783-797.

Karch F., Galloni M., Sipos L. et al. Mcp and Fab-7: molecular analysis of putative boundaries of cis-regulatory domains in the bithorax complex of Drosophila melanogaster // Nucleic Acids Res. 1994. Vol. 22. P. 3138-3146.

Oshchepkov D.Y., VityaevE.E., GrigorovichD.A., IgnatievaE.V., Khlebodarova T.M. SITE-CON: a tool for detecting conservative conformational and physicochemical properties in transcription factor binding site alignments and for site recognition // Nucleic Acids Res. 2004. Vol. 32. P. 208-212.

Огиенко А.А., Карагодин ДЛ., Павлова Н.В. и др. Молекулярно-генетическая характеристика новой гипоморфной мутации гена Trithorax-like и анализ ее влияния на оогенез Drosophila melanogaster // Онтогенез. 2008. Т. 39, № 2. С. 134-142.

Tsuneizumi K., Nakayama T., Kamoshida Y. et al. Daughters against dpp modulates dpp organizing activity in Drosophila wing development // Nature. 1997. Vol. 389. P. 627-631.

Dos-Santos N., Rubin T., ChalvetF., GandilleP., CremazyF., Leroy J., Boissonneau E., Theodore L. Drosophila retinal pigment cell death is regulated in a position-dependent manner by a cell memory gene // Int J Dev Biol. 2008. Vol. 52. P. 21-31.

Огиенко А.А., Карагодин ДЛ., Федорова С.А. и др. Анализ новой гипоморфной мутации гена Trithorax-like, влияющей на оогенез Drosophila melanogaster // Онтогенез. 2006. Т. 37, № 3. С. 157-166.

Bhat K.M., Farkas G., Karch F., Gyurkovics H., Gausz J., Schedl P. The GAGA factor is required in the early Drosophila embryo not only for transcriptional regulation but also for nuclear division // Development. 1996. Vol. 122. P. 1113-1124.

Kumar S. Remote homologue identification of Drosophila GAGA factor in mouse // Bioin-formation. 2011. Vol. 7. P. 29-32.

Matharu N.K., Hussain T., Sankaranarayanan R., Mishra R.K. Vertebrate homologue of Drosophila GAGA factor // J. Mol. Biol. 2010. Vol. 400. P. 434-447.

Mulholland N.M., King I.F., Kingston R.E. Regulation of polycomb group complexes by the sequence-specific DNA binding proteins Zeste and GAGA // Genes Dev. 2003. Vol. 17. P. 2741-2746.

Schwyter D.H., Huang J.D., Dubnicoff T., CoureyA.J. The decapentaplegic core promoter region plays an integral role in the spatial control of transcription // Mol. Cell. Biol. 1995. Vol. 15. P. 3960-3968.

Schuettengruber B., ChourroutD., VervoortM., Leblanc B., Cavalli G. Genome regulation by polycomb and trithorax proteins // Cell. 2007. Vol. 128. P. 735-745.

Ringrose L., ParoR. Polycomb/Trithorax response elements and epigenetic memory of cell identity // Development. 2007. Vol. 134. P. 223-232.

Espinas M.L., Canudas S., Fanti L. et al. The GAGA factor of Drosophila interacts with SAP18, a Sin3-associated polypeptide // EMBO Rep. 2000. Vol. 1. P. 253-259.

Hagstrom K., Muller M., Schedl P. A Polycomb and GAGA dependent silencer adjoins the Fab-7 boundary in the Drosophila bithorax complex // Genetics. 1997. Vol. 146. P. 1365-1380.

Hur M.W., Laney J.D., Jeon S.H., Ali J., Biggin M.D. Zeste maintains repression of Ubx transgenes: support for a new model of polycomb repression // Development. 2002. Vol. 129. P. 1339-1343.

Mahmoudi T., Zuijderduijn L.M., Mohd-Sarip A., Verrijzer C.P. GAGA facilitates binding of Pleiohomeotic to a chromatinized Polycomb response element // Nucleic Acids Res. 2003. Vol. 31. P. 4147-4156.

Brown J.L., Mucci D., WhiteleyM. et al. The Drosophila polycomb group gene pleiohomeotic encodes a DNA binding protein with homology to the transcription factor YY1 // Mol. Cell. 1998. Vol. 1. P. 1057-1064.

Berger N., Dubreucq B. Evolution goes GAGA: GAGA binding proteins across kingdoms // Biochim Biophys Acta. 2012. Vol. 1819. P. 863-868.

Fuda N.J., Lis J.T. A new player in Pol II pausing // EMBO J. 2013. Vol. 32. P. 1796-1798.

Hendrix D.A., Hong J.W., Zeitlinger J. et al. Promoter elements associated with RNA Pol II stalling in the Drosophila embryo // Proc Natl Acad Sci USA. 2013. Vol. 105. P. 7762-7767.

Kerrigan L.A., Croston G.E., Lira L.M., Kadonaga J.T. Sequence-specific transcriptional antirepression of the Drosophila Kruppel gene by the GAGA factor // J Biol Chem. 1991. Vol. 266. P. 574-582.

Wilkins R.C., Lis J.T. DNA distortion and multimerization: novel functions of the glutamine-rich domain of GAGA factor // J Mol Biol. 1999. Vol. 285. P. 515-525.

O'Brien T., Wilkins R.C., Giardina C., Lis J.T. Distribution of GAGA protein on Drosophila genes in vivo // Genes & development. 1995. Vol. 9. P. 1098-1110.

Shimojima T., Okada M., Nakayama T. et al. Drosophila FACT contributes to Hox gene expression through physical and functional interactions with GAGA factor // Genes & development. 2003. Vol. 17. P. 1605-1616.

Lee C., LiX., Hechmer A., Eisen M. et al. NELF and GAGA factor are linked to promoter-proximal pausing at many genes in Drosophila // Mol Cell Biol. 2008. Vol. 28. P. 3290-3300.

Li J., Liu Y., Rhee H.S., Ghosh S.K.B. et al. Kinetic competition between elongation rate and binding of NELF controls promoter proximal pausing // Mol Cell. 2013. Vol. 5. P. 711-722.

ShoplandL.S., Hirayoshi K., Fernandes M., Lis J.T. HSF access to heat shock elements in vivo depends critically on promoter architecture defined by GAGA factor, TFIID, and RNA polymerase II binding sites // Genes Dev. 1995. Vol. 9. P. 2756-2769.

Tsukiyama T., Wu C. Purification and properties of an ATP-dependent nucleosome remodeling factor // Cell. 1995. Vol. 83. P. 1011-1020.

Tsukiyama T., Becker P.B., Wu C. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding binding of GAGA transcription factor // Nature (London). 1994. Vol. 367. P. 525-532.

Farkas G., Leibovitch B.A., Elgin S.C. Chromatin organization and transcriptional control of gene expression in Drosophila // Gene. 2000. Vol. 253. P. 117-136.

Lee H., Kraus K.W., Wolfner M.F., Lis J.T. DNA sequence requirements for generating paused polymerase at the start of hsp70 // Genes & Development. 1992. Vol. 6. P. 284-295.

Nakayama T., Nishioka K., Dong YX., Shimojima T., Hirose S. Drosophila GAGA factor directs histone H3.3 replacement that prevents the heterochromatin spreading // Genes Dev. 2007. Vol. 21. P. 552-561.

Okada M., Hirose S. Chromatin remodeling mediated by Drosophila GAGA factor and ISWI activates fushi tarazu gene transcription in vitro // Mol. Cell. Biol. 1998. Vol. 18. P. 2455-2461.

Wilkins R.C., Lis J.T. Dynamics of potentiation and activation: GAGA factor and its role in heat shock gene regulation // Nucleic Acids Res. 1997. Vol. 25. P. 3963-3968.

Shi Y., Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus // Cell. 2003. Vol. 113. P. 685-700.

Омелина Е.С., Павлова Н.В., Огиенко А.А., Баричева Э.М. Для формирования дор-зальных выростов хориона Drosophila melanogaster требуется белок GAGA // Докл. Биохим. Биофиз. 2011. Т. 436, № 5. С. 696-698.

Letsou A., Arora K., Wrana J.L. Drosophila Dpp signaling is mediated by the punt gene product: a dual ligand-binding type II receptor of the TGF beta receptor family // Cell. 1995. Vol. 80. P. 899-908.

Ruberte E., Marty T., Nellen D., AffolterM., Basler K. An absolute requirement for both the Type II and Type I receptors, punt and thick veins, for Dpp signaling in vivo // Cell. 1995. Vol. 80. P. 889-897.

Xie T., FinelliA., PadgettR.W. The Drosophila saxophone gene: a serine-threonine kinase receptor of the TGF-superfamily // Science. 1994. Vol. 263. P. 1756-1759.

Brummel T., Twombly V., Marques G., Wrana J.L. et al. Characterization and relationship of dpp receptors encoded by the saxophone and thick veins genes in Drosophila // Cell. 1994. Vol. 78. P. 251-261.

Derynck R. TGF-beta-receptor-mediated signaling // Trends Biochem. Sci. 1994. Vol. 19. P. 548-553.

Nellen D., AffolterM., Basler K. Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic // Cell. 1994. Vol. 78. P. 225-237.

Berg C.A. The Drosophila shell game: patterning genes and morphological change // Trends Genet. 2005. Vol. 21. P. 346-355.

Омелина Е.С., Баричева Э.М. Основные компоненты генной сети, контролирующей развитие дорзальных выростов хориона яиц Drosophila melanogaster // Онтогенез. 2011. Т. 43, № 3. С. 163-174.

Twombly V., Blackman R.K., Jin H. The TGF-beta signaling pathway is essential for Drosophila oogenesis // Development. 1996. Vol. 122. P. 1555-1565.

Zhao D., Woolner S., Bownes M. The Mirror transcription factor links signaling pathways in Drosophila oogenesis // Dev Genes Evol. 2000. Vol. 210. P. 449-457.

Padgett R.W., Reiss M. TGFbeta superfamily signaling: notes from the desert // Develop ment. 2007. Vol. 134. P. 3565-3569.

Berg C.A. Tube formation in Drosophila egg chambers // Tissue Eng. Part A. 2008. Vol. 14. P. 1479-1488.