The control of transcriptional memory by stable mitotic bookmarking.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
04 03 2022
04 03 2022
Historique:
received:
24
08
2021
accepted:
15
02
2022
entrez:
5
3
2022
pubmed:
6
3
2022
medline:
14
4
2022
Statut:
epublish
Résumé
To maintain cellular identities during development, gene expression profiles must be faithfully propagated through cell generations. The reestablishment of gene expression patterns upon mitotic exit is mediated, in part, by transcription factors (TF) mitotic bookmarking. However, the mechanisms and functions of TF mitotic bookmarking during early embryogenesis remain poorly understood. In this study, taking advantage of the naturally synchronized mitoses of Drosophila early embryos, we provide evidence that GAGA pioneer factor (GAF) acts as a stable mitotic bookmarker during zygotic genome activation. We show that, during mitosis, GAF remains associated to a large fraction of its interphase targets, including at cis-regulatory sequences of key developmental genes with both active and repressive chromatin signatures. GAF mitotic targets are globally accessible during mitosis and are bookmarked via histone acetylation (H4K8ac). By monitoring the kinetics of transcriptional activation in living embryos, we report that GAF binding establishes competence for rapid activation upon mitotic exit.
Identifiants
pubmed: 35246556
doi: 10.1038/s41467-022-28855-y
pii: 10.1038/s41467-022-28855-y
pmc: PMC8897465
doi:
Substances chimiques
Chromatin
0
Histones
0
Transcription Factors
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1176Subventions
Organisme : NIGMS NIH HHS
ID : R35 GM136298
Pays : United States
Informations de copyright
© 2022. The Author(s).
Références
Bellec, M., Radulescu, O. & Lagha, M. Remembering the past: mitotic bookmarking in a developing embryo. Curr. Opin. Syst. Biol. 11, 41–49 (2018).
pubmed: 30417158
pmcid: 6218673
doi: 10.1016/j.coisb.2018.08.003
Festuccia, N., Gonzalez, I., Owens, N. & Navarro, P. Mitotic bookmarking in development and stem cells. Development 144, 3633–3645 (2017).
pubmed: 29042475
doi: 10.1242/dev.146522
Elsherbiny, A. & Dobreva, G. Epigenetic memory of cell fate commitment. Curr. Opin. Cell Biol. 69, 80–87 (2021).
pubmed: 33535129
doi: 10.1016/j.ceb.2020.12.014
Raccaud, M. & Suter, D. M. Transcription factor retention on mitotic chromosomes: regulatory mechanisms and impact on cell fate decisions. FEBS Lett. 592, 878–887 (2017).
pubmed: 28862742
doi: 10.1002/1873-3468.12828
Raccaud, M. et al. Mitotic chromosome binding predicts transcription factor properties in interphase. Nat. Commun. 10, 1–16 (2019).
doi: 10.1038/s41467-019-08417-5
Cirillo, L. A. et al. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol. Cell 9, 279–289 (2002).
pubmed: 11864602
doi: 10.1016/S1097-2765(02)00459-8
Mazzocca, M., Colombo, E., Callegari, A. & Mazza, D. Transcription factor binding kinetics and transcriptional bursting: What do we really know? Curr. Opin. Struct. Biol. 71, 239–248 (2021).
pubmed: 34481381
doi: 10.1016/j.sbi.2021.08.002
Palozola, K. C. et al. Mitotic transcription and waves of gene reactivation during mitotic exit. Science 358, 119–122 (2017).
pubmed: 28912132
pmcid: 5727891
doi: 10.1126/science.aal4671
Zhang, H. et al. CTCF and transcription influence chromatin structure re-configuration after mitosis. Nat Commun 12, 5157 https://doi.org/10.1038/s41467-021-25418-5 (2021).
Zhang, H. et al. Chromatin structure dynamics during the mitosis-to-G1 phase transition. Nature 576, 158–162 (2019).
pubmed: 31776509
pmcid: 6895436
doi: 10.1038/s41586-019-1778-y
Kadauke, S. et al. Tissue-specific mitotic bookmarking by hematopoietic transcription factor GATA1. Cell 150, 725–737 (2012).
pubmed: 22901805
pmcid: 3425057
doi: 10.1016/j.cell.2012.06.038
Teves, S. S. et al. A stable mode of bookmarking by TBP recruits RNA polymerase II to mitotic chromosomes. eLife 7, 1–22 (2018).
doi: 10.7554/eLife.35621
Festuccia, N. et al. Mitotic binding of Esrrb marks key regulatory regions of the pluripotency network. Nat. Cell Biol. 18, 1139–1148 (2016).
pubmed: 27723719
doi: 10.1038/ncb3418
Pichon, X., Lagha, M., Mueller, F. & Bertrand, E. A growing toolbox to image gene expression in single cells: sensitive approaches for demanding challenges. Mol. Cell 71, 468–480 (2018).
pubmed: 30075145
doi: 10.1016/j.molcel.2018.07.022
Bertrand, E. et al. Localization of ASH1 mRNA particles in living yeast. Mol. Cell 2, 437–445 (1998).
pubmed: 9809065
doi: 10.1016/S1097-2765(00)80143-4
Zhao, R., Nakamura, T., Fu, Y., Lazar, Z. & Spector, D. L. Gene bookmarking accelerates the kinetics of post-mitotic transcriptional re-activation. Nat. Cell Biol. 13, 1295–1304 (2011).
pubmed: 21983563
pmcid: 3210065
doi: 10.1038/ncb2341
Muramoto, T., Müller, I., Thomas, G., Melvin, A. & Chubb, J. R. Methylation of H3K4 is required for inheritance of active transcriptional states. Curr. Biol. 20, 397–406 (2010).
pubmed: 20188556
doi: 10.1016/j.cub.2010.01.017
Ferraro, T. et al. Transcriptional memory in the Drosophila embryo. Curr. Biol. 26, 212–218 (2016).
pubmed: 26748851
doi: 10.1016/j.cub.2015.11.058
Vallot, A. & Tachibana, K. The emergence of genome architecture and zygotic genome activation. Curr. Opin. Cell Biol. 64, 50–57 (2020).
pubmed: 32220807
pmcid: 7374442
doi: 10.1016/j.ceb.2020.02.002
Schulz, K. N. & Harrison, M. M. Mechanisms regulating zygotic genome activation. Nat. Rev. Genet. 20, 221–234 (2019).
pubmed: 30573849
pmcid: 6558659
doi: 10.1038/s41576-018-0087-x
Zaret, K. S. & Mango, S. E. Pioneer transcription factors, chromatin dynamics, and cell fate control. Curr. Opin. Genet. Dev. 37, 76–81 (2016).
pubmed: 26826681
pmcid: 4914445
doi: 10.1016/j.gde.2015.12.003
Iwafuchi-Doi, M. & Zaret, K. S. Cell fate control by pioneer transcription factors. Development 143, 1833–1837 (2016).
pubmed: 27246709
pmcid: 6514407
doi: 10.1242/dev.133900
Zaret, K. S. Pioneering the chromatin landscape. Nat. Genet. 50, 167–169 (2018).
pubmed: 29374252
doi: 10.1038/s41588-017-0038-z
Larson, E. D., Marsh, A. J. & Harrison, M. M. Pioneering the developmental frontier. Mol. Cell 81, 1640–1650 (2021).
pubmed: 33689750
pmcid: 8052302
doi: 10.1016/j.molcel.2021.02.020
Zaret, K. S. Pioneer transcription factors initiating gene network changes. Annu. Rev. Genet. 54, 367–385 (2020).
pubmed: 32886547
pmcid: 7900943
doi: 10.1146/annurev-genet-030220-015007
Liang, H. L. et al. The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila. Nature 456, 400–403 (2008).
pubmed: 18931655
pmcid: 2597674
doi: 10.1038/nature07388
Sun, Y. et al. Zelda overcomes the high intrinsic nucleosome barrier at enhancers during Drosophila zygotic genome activation. Genome Res. 25, 1703–1714 (2015).
pubmed: 26335633
pmcid: 4617966
doi: 10.1101/gr.192542.115
Gaskill, M. M., Gibson, T. J., Larson, E. D. & Harrison, M. M. GAF is essential for zygotic genome activation and chromatin accessibility in the early Drosophila embryo. eLife 10, e66668 (2021).
Moshe, A. & Kaplan, T. Genome-wide search for Zelda-like chromatin signatures identifies GAF as a pioneer factor in early fly development. Epigenetics Chromatin 10, 1–14 (2017).
doi: 10.1186/s13072-017-0141-5
Schulz, K. N. et al. Zelda is differentially required for chromatin accessibility, transcription factor binding, and gene expression in the early Drosophila embryo. Genome Res. 25, 1715–1726 (2015).
Dufourt, J. et al. Temporal control of gene expression by the pioneer factor Zelda through transient interactions in hubs. Nat. Commun. 9, 1–13 (2018).
doi: 10.1038/s41467-018-07613-z
Raff, J. W., Kellum, R. & Alberts, B. The Drosophila GAGA transcription factor is associated with specific regions of heterochromatin throughout the cell cycle. EMBO J. 13, 5977–5983 (1994).
pubmed: 7813435
pmcid: 395573
doi: 10.1002/j.1460-2075.1994.tb06943.x
Chetverina, D., Erokhin, M. & Schedl, P. GAGA factor: a multifunctional pioneering chromatin protein. Cell. Mol. Life Sci. 78, 4125–4141 (2021).
pubmed: 33528710
doi: 10.1007/s00018-021-03776-z
Srivastava, A., Kumar, A. S. & Mishra, R. K. Vertebrate GAF/ThPOK: emerging functions in chromatin architecture and transcriptional regulation. Cell. Mol. Life Sci. 75, 623–633 (2018).
pubmed: 28856379
doi: 10.1007/s00018-017-2633-7
Hendrix, D. A., Hong, J. W., Zeitlinger, J., Rokhsar, D. S. & Levine, M. S. Promoter elements associated with RNA Pol II stalling in the Drosophila embryo. Proc. Natl Acad. Sci. USA 105, 7762–7767 (2008).
pubmed: 18505835
pmcid: 2396556
doi: 10.1073/pnas.0802406105
Li, J. & Gilmour, D. S. Distinct mechanisms of transcriptional pausing orchestrated by GAGA factor and M1BP, a novel transcription factor. EMBO J. 32, 1829–1841 (2013).
pubmed: 23708796
pmcid: 3981175
doi: 10.1038/emboj.2013.111
Fuda, N. J. et al. GAGA factor maintains nucleosome-free regions and has a role in RNA polymerase II recruitment to promoters. PLoS Genet. 11, 1–22 (2015).
doi: 10.1371/journal.pgen.1005108
Judd, J., Duarte, F. M. & Lis, J. T. Pioneer-like factor GAF cooperates with PBAP (SWI/SNF) and NURF (ISWI) to regulate transcription. Genes Dev. 35, 147–156 (2021).
pubmed: 33303640
pmcid: 7778264
doi: 10.1101/gad.341768.120
Foe, V. E., Odell, G. M. & Edgar, B. A. Mitosis and morphogenesis in the Drosophila embryo: point and counterpoint. In The Development of Drosophila melanogaster. (eds. Bate, M. & Martinez Arias, A.) 149–300 (Cold Spring Harb. Lab. Press, 1993).
Auer, J. M. T. et al. Of numbers and movement—understanding transcription factor pathogenesis by advanced microscopy. DMM Dis. Model. Mech. 13, dmm046516 (2021).
Steffen, P. A. et al. Quantitative in vivo analysis of chromatin binding of Polycomb and Trithorax group proteins reveals retention of ASH1 on mitotic chromatin. Nucleic Acids Res. 41, 5235–5250 (2013).
pubmed: 23580551
pmcid: 3664806
doi: 10.1093/nar/gkt217
Elsner, M. et al. Spatiotemporal dynamics of the COPI vesicle machinery. EMBO Rep. 4, 1000–1004 (2003).
pubmed: 14502225
pmcid: 1326400
doi: 10.1038/sj.embor.embor942
Elf, J., Li, G.-W. & Xie, X. S. Probing transcription factor dynamics at the single-molecule level in a living cell. Science 316, 1191 LP–1191194 (2007).
doi: 10.1126/science.1141967
Tang, X. et al. Kinetic principles underlying pioneer function of GAGA transcription factor in live cells. Preprint at bioRxiv https://doi.org/10.1101/2021.10.21.465351 (2021).
Mir, M. et al. Dense bicoid hubs accentuate binding along the morphogen gradient. Genes Dev. 31, 1784–1794 (2017).
pubmed: 28982761
pmcid: 5666676
doi: 10.1101/gad.305078.117
Mir, M. et al. Dynamic multifactor hubs interact transiently with sites of active transcription in drosophila embryos. eLife 7, 1–27 (2018).
doi: 10.7554/eLife.40497
Farrell, J. A. & O’Farrell, P. H. From egg to gastrula: how the cell cycle is remodeled during the drosophila mid-blastula transition. Annu. Rev. Genet. 48, 269–294 (2014).
pubmed: 25195504
pmcid: 4484755
doi: 10.1146/annurev-genet-111212-133531
Hendzel, M. J. et al. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348–360 (1997).
pubmed: 9362543
doi: 10.1007/s004120050256
Follmer, N. E., Wani, A. H. & Francis, N. J. A polycomb group protein is retained at specific sites on chromatin in mitosis. PLoS Genet. 8, e1003135 (2012).
Koenecke, N., Johnston, J., He, Q., Meier, S. & Zeitlinger, J. Drosophila poised enhancers are generated during tissue patterning with the help of repression. Genome Res. 27, 64–74 (2017).
pubmed: 27979994
pmcid: 5204345
doi: 10.1101/gr.209486.116
Hug, C. B., Grimaldi, A. G., Kruse, K. & Vaquerizas, J. M. Chromatin architecture emerges during zygotic genome activation independent of transcription. Cell 169, 216–228.e19 (2017).
pubmed: 28388407
doi: 10.1016/j.cell.2017.03.024
Nègre, N. et al. A comprehensive map of insulator elements for the Drosophila genome. PLoS Genet. 6, e1000814 (2010).
Kvon, E. Z. et al. Genome-scale functional characterization of Drosophila developmental enhancers in vivo. Nature 512, 91–95 (2014).
pubmed: 24896182
doi: 10.1038/nature13395
Blythe, S. A. & Wieschaus, E. F. Establishment and maintenance of heritable chromatin structure during early Drosophila embryogenesis. Elife 5, 1–21 (2016).
doi: 10.7554/eLife.20148
Adkins, N. L., Hagerman, T. A. & Georgel, P. GAGA protein: a multi-faceted transcription factor. Biochem. Cell Biol. 84, 559–567 (2006).
pubmed: 16936828
doi: 10.1139/o06-062
Li, X. Y., Harrison, M. M., Villalta, J. E., Kaplan, T. & Eisen, M. B. Establishment of regions of genomic activity during the Drosophila maternal to zygotic transition. eLife 3, 1–20 (2014).
doi: 10.7554/eLife.03737
Lott, S. E. et al. Noncanonical compensation of zygotic X transcription in early Drosophila melanogaster development revealed through single-embryo RNA-Seq. PLoS Biol. 9, e1000590 (2011).
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. 20, 3187–3197 (2000).
pubmed: 10757803
pmcid: 85613
doi: 10.1128/MCB.20.9.3187-3197.2000
Koenecke, N., Johnston, J., Gaertner, B., Natarajan, M. & Zeitlinger, J. Genome-wide identification of Drosophila dorso-ventral enhancers by differential histone acetylation analysis. Genome Biol. 17, 1–19 (2016).
doi: 10.1186/s13059-016-1057-2
Schuettengruber, B., Bourbon, H. M., Di Croce, L. & Cavalli, G. Genome regulation by polycomb and trithorax: 70 years and counting. Cell 171, 34–57 (2017).
pubmed: 28938122
doi: 10.1016/j.cell.2017.08.002
Mahmoudi, T., Katsani, K. R. & Verrijzer, C. P. GAGA can mediate enhancer function in trans by linking two separate DNA molecules. EMBO J. 21, 1775–1781 (2002).
pubmed: 11927561
pmcid: 125945
doi: 10.1093/emboj/21.7.1775
Ogiyama, Y., Schuettengruber, B., Papadopoulos, G. L., Chang, J. M. & Cavalli, G. Polycomb-dependent chromatin looping contributes to gene silencing during Drosophila development. Mol. Cell 71, 73–88.e5 (2018).
pubmed: 30008320
doi: 10.1016/j.molcel.2018.05.032
Ghavi-Helm, Y. et al. Enhancer loops appear stable during development and are associated with paused polymerase. Nature 512, 96–100 (2014).
pubmed: 25043061
doi: 10.1038/nature13417
Trullo, A., Dufourt, J. & Lagha, M. MitoTrack, a user-friendly semi-automatic software for lineage tracking in living embryos. Bioinformatics 36, 1300–1302 (2020).
pubmed: 31580394
Rieder, L. E. et al. Histone locus regulation by the Drosophila dosage compensation adaptor protein CLAMP. Genes Dev. 31, 1494–1508 (2017).
pubmed: 28838946
pmcid: 5588930
doi: 10.1101/gad.300855.117
Dufourt, J. et al. Spatio-temporal requirements for transposable element piRNA-mediated silencing during Drosophila oogenesis. Nucleic Acids Res. 42, 2512–2524 (2014).
pubmed: 24288375
doi: 10.1093/nar/gkt1184
Orphanides, G., LeRoy, G., Chang, C. H., Luse, D. S. & Reinberg, D. FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92, 105–116 (1998).
pubmed: 9489704
doi: 10.1016/S0092-8674(00)80903-4
Kwon, S. Y., Jang, B. & Badenhorst, P. The ISWI chromatin remodelling factor NURF is not required for mitotic male X chromosome organisation. microPublication Biol. 2–7 (2021).
Deluz, C. et al. A role for mitotic bookmarking of SOX2 in pluripotency and differentiation. Genes Dev. 30, 2538–2550 (2016).
pubmed: 27920086
pmcid: 5159668
doi: 10.1101/gad.289256.116
Espinás, M. L. et al. The N-terminal POZ domain of GAGA mediates the formation of oligomers that bind DNA with high affinity and specificity. J. Biol. Chem. 274, 16461–16469 (1999).
pubmed: 10347208
doi: 10.1074/jbc.274.23.16461
Van Steensel, B., Delrow, J. & Bussemaker, H. J. Genomewide analysis of Drosophila GAGA factor target genes reveals context-dependent DNA binding. Proc. Natl Acad. Sci. USA 100, 2580–2585 (2003).
pubmed: 12601174
pmcid: 151383
doi: 10.1073/pnas.0438000100
Behera, V. et al. Interrogating histone acetylation and BRD4 as mitotic bookmarks of transcription. Cell Rep. 27, 400–415.e5 (2019).
pubmed: 30970245
pmcid: 6664437
doi: 10.1016/j.celrep.2019.03.057
Liu, Y. et al. Widespread mitotic bookmarking by histone marks and transcription factors in pluripotent stem cells. Cell Rep. 19, 1283–1293 (2017).
pubmed: 28514649
pmcid: 5495017
doi: 10.1016/j.celrep.2017.04.067
Samata, M. et al. Intergenerationally maintained histone H4 lysine 16 acetylation is instructive for future gene activation. Cell 182, 127–144.e23 (2020).
pubmed: 32502394
doi: 10.1016/j.cell.2020.05.026
Lagha, M., Bothma, J. P. & Levine, M. Mechanisms of transcriptional precision in animal development. Trends Genet. 28, 409–416 (2012).
pubmed: 22513408
pmcid: 4257495
doi: 10.1016/j.tig.2012.03.006
Bentovim, L., Harden, T. T. & DePace, A. H. Transcriptional precision and accuracy in development: from measurements to models and mechanisms. Dev 144, 3855–3866 (2017).
doi: 10.1242/dev.146563
Matharu, N. K., Yadav, S., Kumar, M. & Mishra, R. K. Role of vertebrate GAGA associated factor (vGAF) in early development of zebrafish. Cells Dev. 166, 203682 (2021).
pubmed: 33994355
doi: 10.1016/j.cdev.2021.203682
Dufourt, J. et al. Imaging translation dynamics in live embryos reveals spatial heterogeneities. Science 372, 840–844 (2021).
pubmed: 33927056
doi: 10.1126/science.abc3483
Venken, K. J. T., He, Y., Hoskins, R. A. & Bellen, H. J. P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314, 1747–1751 (2006).
pubmed: 17138868
doi: 10.1126/science.1134426
Michelman-Ribeiro, A. et al. Direct measurement of association and dissociation rates of DNA binding in live cells by fluorescence correlation spectroscopy. Biophys. J. 97, 337–346 (2009).
pubmed: 19580772
pmcid: 2711375
doi: 10.1016/j.bpj.2009.04.027
Escoffre, J. M., Hubert, M., Teissié, J., Rols, M. P. & Favard, C. Evidence for electro-induced membrane defects assessed by lateral mobility measurement of a GPI anchored protein. Eur. Biophys. J. 43, 277–286 (2014).
pubmed: 24781652
doi: 10.1007/s00249-014-0961-1
Axelrod, D., Koppel, D. E., Schlessinger, J., Elson, E. & Webb, W. W. Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 16, 1055–1069 (1976).
pubmed: 786399
pmcid: 1334945
doi: 10.1016/S0006-3495(76)85755-4
Yguerabide, J., Schmidt, J. A. & Yguerabide, E. E. Lateral mobility in membranes as detected by fluorescence recovery after photobleaching. Biophys. J. 40, 69–75 (1982).
pubmed: 7139035
pmcid: 1328974
doi: 10.1016/S0006-3495(82)84459-7
Müller, P., Schwille, P. & Weidemann, T. PyCorrFit-generic data evaluation for fluorescence correlation spectroscopy. Bioinformatics 30, 2532–2533 (2014).
pubmed: 24825612
pmcid: 4147890
doi: 10.1093/bioinformatics/btu328
Dertinger, T. et al. The optics and performance of dual-focus fluorescence correlation spectroscopy. Opt. Express 16, 14353 (2008).
pubmed: 18794971
doi: 10.1364/OE.16.014353
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pubmed: 22388286
pmcid: 3322381
doi: 10.1038/nmeth.1923
Fenouil, R. et al. Pasha: a versatile R package for piling chromatin HTS data. Bioinformatics 15, 2528–2530 (2016).
doi: 10.1093/bioinformatics/btw206
Ramírez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160–W165 (2016).
pubmed: 27079975
pmcid: 4987876
doi: 10.1093/nar/gkw257
Pimmett, V. L. et al. Quantitative imaging of transcription in living Drosophila embryos reveals the impact of core promoter motifs on promoter state dynamics. Nat. Commun. 12, 4504 (2021).
pubmed: 34301936
pmcid: 8302612
doi: 10.1038/s41467-021-24461-6
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
doi: 10.1038/nmeth.2019
Garavís, M. et al. The structure of an endogenous Drosophila centromere reveals the prevalence of tandemly repeated sequences able to form i-motifs. Sci. Rep. 5, 1–10 (2015).
doi: 10.1038/srep13307
Bantignies, F. & Cavalli, G. Topological organization of Drosophila Hox genes using DNA fluorescent in situ hybridization. Methods Mol. Biol. 1196, 103–120 (2014).
pubmed: 25151160
doi: 10.1007/978-1-4939-1242-1_7