Zelda Binding in the Early Embryo Marks Regions Subsequently Activated at the Maternal-to-Zygotic Transition
The earliest stages of development in most metazoans are driven by maternally deposited proteins and mRNAs, with widespread transcriptional activation of the zygotic genome occurring hours after fertilization, at a period known as the maternal-to-zygotic transition (MZT). In Drosophila, the MZT is preceded by the transcription of a small number of genes that initiate sex determination, patterning, and other early developmental processes; and the zinc-finger protein Zelda (ZLD) plays a key role in their transcriptional activation. To better understand the mechanisms of ZLD activation and the range of its targets, we used chromatin immunoprecipitation coupled with high-throughput sequencing (ChIP-Seq) to map regions bound by ZLD before (mitotic cycle 8), during (mitotic cycle 13), and after (late mitotic cycle 14) the MZT. Although only a handful of genes are transcribed prior to mitotic cycle 10, we identified thousands of regions bound by ZLD in cycle 8 embryos, most of which remain bound through mitotic cycle 14. As expected, early ZLD-bound regions include the promoters and enhancers of genes transcribed at this early stage. However, we also observed ZLD bound at cycle 8 to the promoters of roughly a thousand genes whose first transcription does not occur until the MZT and to virtually all of the thousands of known and presumed enhancers bound at cycle 14 by transcription factors that regulate patterned gene activation during the MZT. The association between early ZLD binding and MZT activity is so strong that ZLD binding alone can be used to identify active promoters and regulatory sequences with high specificity and selectivity. This strong early association of ZLD with regions not active until the MZT suggests that ZLD is not only required for the earliest wave of transcription but also plays a major role in activating the genome at the MZT.
Vyšlo v časopise:
Zelda Binding in the Early Embryo Marks Regions Subsequently Activated at the Maternal-to-Zygotic Transition. PLoS Genet 7(10): e32767. doi:10.1371/journal.pgen.1002266
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002266
Souhrn
The earliest stages of development in most metazoans are driven by maternally deposited proteins and mRNAs, with widespread transcriptional activation of the zygotic genome occurring hours after fertilization, at a period known as the maternal-to-zygotic transition (MZT). In Drosophila, the MZT is preceded by the transcription of a small number of genes that initiate sex determination, patterning, and other early developmental processes; and the zinc-finger protein Zelda (ZLD) plays a key role in their transcriptional activation. To better understand the mechanisms of ZLD activation and the range of its targets, we used chromatin immunoprecipitation coupled with high-throughput sequencing (ChIP-Seq) to map regions bound by ZLD before (mitotic cycle 8), during (mitotic cycle 13), and after (late mitotic cycle 14) the MZT. Although only a handful of genes are transcribed prior to mitotic cycle 10, we identified thousands of regions bound by ZLD in cycle 8 embryos, most of which remain bound through mitotic cycle 14. As expected, early ZLD-bound regions include the promoters and enhancers of genes transcribed at this early stage. However, we also observed ZLD bound at cycle 8 to the promoters of roughly a thousand genes whose first transcription does not occur until the MZT and to virtually all of the thousands of known and presumed enhancers bound at cycle 14 by transcription factors that regulate patterned gene activation during the MZT. The association between early ZLD binding and MZT activity is so strong that ZLD binding alone can be used to identify active promoters and regulatory sequences with high specificity and selectivity. This strong early association of ZLD with regions not active until the MZT suggests that ZLD is not only required for the earliest wave of transcription but also plays a major role in activating the genome at the MZT.
Zdroje
1. NewportJKirschnerM 1982 A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30 687 696
2. TadrosWLipshitzHD 2009 The maternal-to-zygotic transition: a play in two acts. Development 136 3033 3042
3. FoeVEAlbertsBM 1983 Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci 61 31 70
4. AndersonKVLengyelJA 1979 Rates of synthesis of major classes of RNA in Drosophila embryos. Dev Biol 70 217 231
5. McKnightSLMillerOLJr 1976 Ultrastructural patterns of RNA synthesis during early embryogenesis of Drosophila melanogaster. Cell 8 305 319
6. PritchardDKSchubigerG 1996 Activation of transcription in Drosophila embryos is a gradual process mediated by the nucleocytoplasmic ratio. Genes Dev 10 1131 1142
7. ten BoschJRBenavidesJAClineTW 2006 The TAGteam DNA motif controls the timing of Drosophila pre-blastoderm transcription. Development 133 1967 1977
8. De RenzisSElementoOTavazoieSWieschausEF 2007 Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol 5 e117 doi:10.1371/journal.pbio.0050117
9. HarrisonMMBotchanMRClineTW 2010 Grainyhead and Zelda compete for binding to the promoters of the earliest-expressed Drosophila genes. Dev Biol 345 248 255
10. LiangHLNienCYLiuHYMetzsteinMMKirovN 2008 The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila. Nature 456 400 403
11. StaudtNFellertSChungHRJackleHVorbruggenG 2006 Mutations of the Drosophila zinc finger-encoding gene vielfaltig impair mitotic cell divisions and cause improper chromosome segregation. Mol Biol Cell 17 2356 2365
12. LiXYMacArthurSBourgonRNixDPollardDA 2008 Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol 6 e27 doi:10.1371/journal.pbio.0060027
13. LangmeadBTrapnellCPopMSalzbergSL 2009 Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10 R25
14. BaileyTLElkanC 1994 Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2 28 36
15. BarashYElidanGFriedmanNKaplanT 2003 Modeling dependencies in protein-DNA binding sites. Proceedings of the seventh annual international conference on Research in computational molecular biology Berlin, Germany ACM 28 37
16. PavesiGMereghettiPMauriGPesoleG 2004 Weeder Web: discovery of transcription factor binding sites in a set of sequences from co-regulated genes. Nucleic Acids Res 32 W199 203
17. LottSEVillaltaJESchrothGPLuoSTonkinLA 2011 Noncanonical Compensation of the Zygotic X Transcription in Early Drosophila melanogaster Development Revealed through Single-Embryo RNA-Seq. PLoS Biol 9 e1000590 doi:10.1371/journal.pbio.100059
18. MacArthurSLiXYLiJBrownJBChuHC 2009 Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions. Genome Biol 10 R80
19. KaplanTLiX-ySaboPJThomasSStamatoyannopoulosJA 2011 Quantitative Models of the Mechanisms That Control Genome-Wide Patterns of Transcription Factor Binding during Early Drosophila Development. PLoS Genet 7 e1001290 doi:10.1371/journal.pgen.1001290
20. ThomasSLiXYSaboPJSandstromRBThurmanRE 2011 Dynamic reprogramming of chromatin accessibility during Drosophila embryo development. Genome Biol 12 R43
21. TweedieSAshburnerMFallsKLeylandPMcQuiltonP 2009 FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res 37 D555 559
22. LiXYThomasSSaboPJEisenMBStamatoyannopoulosJA 2011 The role of chromatin accessibility in directing the widespread, overlapping patterns of Drosophila transcription factor binding. Genome Biol 12 R34
23. BradleyRKLiXYTrapnellCDavidsonSPachterL 2010 Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related Drosophila species. PLoS Biol 8 e1000343 doi:10.1371/journal.pbio.1000343
24. YangJTanCDarkenRSWilsonPAKleinPS 2002 Beta-catenin/Tcf-regulated transcription prior to the midblastula transition. Development 129 5743 5752
25. BlytheSAChaSWTadjuidjeEHeasmanJKleinPS 2010 beta-Catenin primes organizer gene expression by recruiting a histone H3 arginine 8 methyltransferase, Prmt2. Dev Cell 19 220 231
26. GualdiRBossardPZhengMHamadaYColemanJR 1996 Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control. Genes Dev 10 1670 1682
27. CirilloLALinFRCuestaIFriedmanDJarnikM 2002 Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol Cell 9 279 289
28. Gaspar-MaiaAAlajemAMeshorerERamalho-SantosM 2011 Open chromatin in pluripotency and reprogramming. Nature reviews Mol Cell Biol 12 36 47
29. BultmanSJGebuhrTCPanHSvobodaPSchultzRM 2006 Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev 20 1744 1754
30. VastenhouwNLZhangYWoodsIGImamFRegevA 2010 Chromatin signature of embryonic pluripotency is established during genome activation. Nature 464 922 926
31. BernsteinBEMikkelsenTSXieXKamalMHuebertDJ 2006 A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125 315 326
32. MikkelsenTSKuMJaffeDBIssacBLiebermanE 2007 Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448 553 560
33. Rada-IglesiasABajpaiRSwigutTBrugmannSAFlynnRA 2011 A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470 279 283
34. SchuettengruberBGanapathiMLeblancBPortosoMJaschekR 2009 Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos. PLoS Biol 7 e1000013 doi:10.1371/journal.pbio.1000013
35. AkkersRCvan HeeringenSJJacobiUGJanssen-MegensEMFrancoijsKJ 2009 A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus embryos. Dev Cell 17 425 434
36. TsurumiAXiaFLiJLarsonKLafranceR 2011 STAT Is an Essential Activator of the Zygotic Genome in the Early Drosophila Embryo. PLoS Genet 7 e1002086 doi:10.1371/journal.pgen.1002086
37. PeterlinBMPriceDH 2006 Controlling the elongation phase of transcription with P-TEFb. Mol Cell 23 297 305
38. RemusDBeallELBotchanMR 2004 DNA topology, not DNA sequence, is a critical determinant for Drosophila ORC-DNA binding. The EMBO journal 23 897 907
39. RoySErnstJKharchenkoPVKheradpourPNegreN 2010 Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330 1787 1797
40. MacAlpineHKGordanRPowellSKHarteminkAJMacAlpineDM 2010 Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res 20 201 211
41. CapaldiAPKaplanTLiuYHabibNRegevA 2008 Structure and function of a transcriptional network activated by the MAPK Hog1. Nat Genet 40 1300 1306
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 10
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