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For cells to initiate and sustain a differentiated state, it is necessary that a 'memory' of this state is transmitted through mitosis to the daughter cells 1-3 . Mammalian switch/sucrose non-fermentable (SWI/SNF) complexes (also known as Brg1/Brg-associated factors, or BAF) control cell identity by modulating chromatin architecture to regulate gene expression 4-7 , but whether they participate in cell fate memory is unclear. Here we provide evidence that subunits of SWI/SNF act as mitotic bookmarks to safeguard cell identity during cell division. The SWI/SNF core subunits SMARCE1 and SMARCB1 are displaced from enhancers but are bound to promoters during mitosis, and we show that this binding is required for appropriate reactivation of bound genes after mitotic exit. Ablation of SMARCE1 during a single mitosis in mouse embryonic stem cells is sufficient to disrupt gene expression, impair the occupancy of several established bookmarks at a subset of their targets and cause aberrant neural differentiation. Thus, SWI/SNF subunit SMARCE1 has a mitotic bookmarking role and is essential for heritable epigenetic fidelity during transcriptional reprogramming.

Titel:	Mitotic bookmarking by SWI/SNF subunits.
Autor/in / Beteiligte Person:	Zhu, Z ; Chen, X ; Guo, A ; Manzano, T ; Walsh, PJ ; Wills, KM ; Halliburton, R ; Radko-Juettner, S ; Carter, RD ; Partridge, JF ; Green, DR ; Zhang, J ; Roberts, CWM
Link:	View record at Springer (Volltext)
Zeitschrift:	Nature, Jg. 618 (2023-06-01), Heft 7963, S. 180-187
Veröffentlichung:	Basingstoke : Nature Publishing Group ; <i>Original Publication</i>: London, Macmillan Journals ltd., 2023
Medientyp:	academicJournal
ISSN:	1476-4687 (electronic)
DOI:	10.1038/s41586-023-06085-6
Schlagwort:	Animals Mice Chromatin genetics Chromatin Assembly and Disassembly genetics Nuclear Proteins metabolism Transcription Factors metabolism Protein Subunits metabolism Mouse Embryonic Stem Cells metabolism Enhancer Elements, Genetic genetics Promoter Regions, Genetic genetics Cell Division genetics Cell Differentiation genetics Mitosis genetics Chromosomal Proteins, Non-Histone deficiency Chromosomal Proteins, Non-Histone genetics Chromosomal Proteins, Non-Histone metabolism Epigenesis, Genetic genetics
Sonstiges:	Nachgewiesen in: MEDLINE Sprachen: English Publication Type: Journal Article Language: English [Nature] 2023 Jun; Vol. 618 (7963), pp. 180-187. <i>Date of Electronic Publication: </i>2023 May 24. MeSH Terms: Cell Differentiation* / genetics ; Mitosis* / genetics ; Chromosomal Proteins, Non-Histone* / deficiency ; Chromosomal Proteins, Non-Histone* / genetics ; Chromosomal Proteins, Non-Histone* / metabolism ; Epigenesis, Genetic* / genetics ; Animals ; Mice ; Chromatin / genetics ; Chromatin Assembly and Disassembly / genetics ; Nuclear Proteins / metabolism ; Transcription Factors / metabolism ; Protein Subunits / metabolism ; Mouse Embryonic Stem Cells / metabolism ; Enhancer Elements, Genetic / genetics ; Promoter Regions, Genetic / genetics ; Cell Division / genetics Comments: Comment in: Signal Transduct Target Ther. 2023 Oct 4;8(1):380. (PMID: 37788985) References: Palozola, K. C. et al. Mitotic transcription and waves of gene reactivation during mitotic exit. Science 358, 119–122 (2017). (PMID: 28912132572789110.1126/science.aal4671) ; Reinberg, D. & Vales, L. D. Chromatin domains rich in inheritance. Science 361, 33–34 (2018). (PMID: 2997681510.1126/science.aat7871) ; Ming, X. et al. Kinetics and mechanisms of mitotic inheritance of DNA methylation and their roles in aging-associated methylome deterioration. Cell Res. 30, 980–996 (2020). (PMID: 32581343778502410.1038/s41422-020-0359-9) ; Wilson, B. G. & Roberts, C. W. SWI/SNF nucleosome remodellers and cancer. Nat. Rev. Cancer 11, 481–492 (2011). (PMID: 2165481810.1038/nrc3068) ; Lessard, J. et al. An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55, 201–215 (2007). (PMID: 17640523267411010.1016/j.neuron.2007.06.019) ; Ho L, R. J. et al. An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc. Natl Acad. Sci. USA 106, 5181–5186 (2009). (PMID: 19279220265439610.1073/pnas.0812889106) ; Alver, B. H. et al. The SWI/SNF chromatin remodelling complex is required for maintenance of lineage specific enhancers. Nat. Commun. 8, 14648 (2017). (PMID: 28262751534348210.1038/ncomms14648) ; PARSONS, G. G. & SPENCER, C. A. Mitotic repression of RNA polymerase II transcription is accompanied by release of transcription elongation complexes. Mol. Cell. Biol. 17, 5791–5802 (1997). (PMID: 931563723242710.1128/MCB.17.10.5791) ; Naumova, N. et al. Organization of the mitotic chromosome. Science 342, 948–953 (2013). (PMID: 24200812404046510.1126/science.1236083) ; Zhang, H. et al. Chromatin structure dynamics during the mitosis-to-G1 phase transition. Nature 576, 158–162 (2019). (PMID: 31776509689543610.1038/s41586-019-1778-y) ; Antonin, W. & Neumann, H. Chromosome condensation and decondensation during mitosis. Curr. Opin. Cell Biol. 40, 15–22 (2016). (PMID: 2689513910.1016/j.ceb.2016.01.013) ; Muchardt, C., Reyes, J. C., Bourachot, B., Leguoy, E. & Yaniv, M. The hbrm and BRG-1 proteins, components of the human SNF/SWI complex, are phosphorylated and excluded from the condensed chromosomes during mitosis. EMBO J. 15, 3394–3402 (1996). (PMID: 867084145190310.1002/j.1460-2075.1996.tb00705.x) ; Sif, S., Stukenberg, P. T., Kirschner, M. W. & Kingston, R. E. Mitotic inactivation of a human SWI/SNF chromatin remodeling complex. Genes Dev. 12, 2842–2851 (1998). (PMID: 974486131716410.1101/gad.12.18.2842) ; Gurley, L. R., Walters, R. A. & Tobey, R. A. Cell cycle-specific changes in histone phosphorylation associated with cell proliferation and chromosome condensation. J. Cell Biol. 60, 356–364 (1974). (PMID: 4855902210916110.1083/jcb.60.2.356) ; Festuccia, N. et al. Transcription factor activity and nucleosome organization in mitosis. Genome Res. 29, 250–260 (2019). (PMID: 30655337636081610.1101/gr.243048.118) ; Teves, S. S. et al. A dynamic mode of mitotic bookmarking by transcription factors. eLife 5, e22280 (2016). (PMID: 27855781515652610.7554/eLife.22280) ; Deluz, C. et al. A role for mitotic bookmarking of SOX2 in pluripotency and differentiation. Genes Dev. 30, 2538–2550 (2016). (PMID: 27920086515966810.1101/gad.289256.116) ; Liu, Y. et al. Widespread mitotic bookmarking by histone marks and transcription factors in pluripotent stem cells. Cell Rep. 19, 1283–1293 (2017). (PMID: 28514649549501710.1016/j.celrep.2017.04.067) ; Festuccia, N., Gonzalez, I., Owens, N. & Navarro, P. Mitotic bookmarking in development and stem cells. Development 144, 3633–3645 (2017). (PMID: 2904247510.1242/dev.146522) ; Skene, P. J., Henikoff, J. G. & Henikoff, S. Targeted in situ genome-wide profiling with high efficiency for low cell numbers. Nat. Protoc. 13, 1006–1019 (2018). (PMID: 2965105310.1038/nprot.2018.015) ; de Dieuleveult, M. et al. Genome-wide nucleosome specificity and function of chromatin remodellers in ES cells. Nature 530, 113–116 (2016). (PMID: 26814966487111710.1038/nature16505) ; Magana-Acosta, M. & Valadez-Graham, V. Chromatin remodelers in the 3D nuclear compartment. Front. Genet. 11, 600615 (2020). (PMID: 33329746767339210.3389/fgene.2020.600615) ; Festuccia, N. et al. Mitotic binding of Esrrb marks key regulatory regions of the pluripotency network. Nat. Cell Biol. 18, 1139–1148 (2016). (PMID: 2772371910.1038/ncb3418) ; Lodato, M. A. et al. SOX2 co-occupies distal enhancer elements with distinct POU factors in ESCs and NPCs to specify cell state. PLoS Genet. 9, e1003288 (2013). (PMID: 23437007357874910.1371/journal.pgen.1003288) ; Wang, X. et al. BRD9 defines a SWI/SNF sub-complex and constitutes a specific vulnerability in malignant rhabdoid tumors. Nat. Commun. 10, 1881 (2019). (PMID: 31015438647905010.1038/s41467-019-09891-7) ; Michel, B. C. et al. A non-canonical SWI/SNF complex is a synthetic lethal target in cancers driven by BAF complex perturbation. Nat. Cell Biol. 20, 1410–1420 (2018). (PMID: 30397315669838610.1038/s41556-018-0221-1) ; Owens, N. et al. CTCF confers local nucleosome resiliency after DNA replication and during mitosis. eLife 8, e47898 (2019). (PMID: 31599722684464510.7554/eLife.47898) ; Pelham-Webb, B. et al. H3K27ac bookmarking promotes rapid post-mitotic activation of the pluripotent stem cell program without impacting 3D chromatin reorganization. Mol. Cell 81, 1732–1748.e1738 (2021). (PMID: 33730542805229410.1016/j.molcel.2021.02.032) ; Hsiung, C. C. et al. Genome accessibility is widely preserved and locally modulated during mitosis. Genome Res. 25, 213–225 (2015). (PMID: 25373146431529510.1101/gr.180646.114) ; Glotzer, M., Murray, A. W. & Kirschner, M. W. Cyclin is degraded by the ubiquitin pathway. Nature 349, 132–138 (1991). (PMID: 184603010.1038/349132a0) ; Ran, F. A. et al. Genome engineering using the CRISPR–Cas9 system. Nat. Protoc. 8, 2281–2308 (2013). (PMID: 24157548396986010.1038/nprot.2013.143) ; Kadauke, S. et al. Tissue-specific mitotic bookmarking by hematopoietic transcription factor GATA1. Cell 150, 725–737 (2012). (PMID: 22901805342505710.1016/j.cell.2012.06.038) ; Kim, J., Chu, J., Shen, X., Wang, J. & Orkin, S. H. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 132, 1049–1061 (2008). (PMID: 1835881610.1016/j.cell.2008.02.039) ; Jao, C. Y. & Salic, A. Exploring RNA transcription and turnover in vivo by using click chemistry. Proc. Natl Acad. Sci. USA 105, 15779–15784 (2008). (PMID: 18840688257291710.1073/pnas.0808480105) ; Hsiung, C. C.-S. et al. A hyperactive transcriptional state marks genome reactivation at the mitosis–G1 transition. Genes Dev. 30, 1423–1439 (2016). (PMID: 27340175492686510.1101/gad.280859.116) ; Yesbolatova, A. et al. The auxin-inducible degron 2 technology provides sharp degradation control in yeast, mammalian cells, and mice. Nat. Commun. 11, 5701 (2020). (PMID: 33177522765900110.1038/s41467-020-19532-z) ; King, H. W. & Klose, R. J. The pioneer factor OCT4 requires the chromatin remodeller BRG1 to support gene regulatory element function in mouse embryonic stem cells. eLife 6, e22631 (2017). (PMID: 28287392540050410.7554/eLife.22631) ; Gatchalian, J. et al. A non-canonical BRD9-containing BAF chromatin remodeling complex regulates naive pluripotency in mouse embryonic stem cells. Nat. Commun. 9, 5139 (2018). (PMID: 30510198627744410.1038/s41467-018-07528-9) ; Caravaca, J. M. et al. Bookmarking by specific and nonspecific binding of FoxA1 pioneer factor to mitotic chromosomes. Genes Dev. 27, 251–260 (2013). (PMID: 23355396357651110.1101/gad.206458.112) ; Asenjo, HelenaG. et al. Polycomb regulation is coupled to cell cycle transition in pluripotent stem cells. Sci. Adv. 6, eaay4768 (2020). (PMID: 32181346705632010.1126/sciadv.aay4768) ; Pauklin, S. & Vallier, L. The cell-cycle state of stem cells determines cell fate propensity. Cell 155, 135–147 (2013). (PMID: 24074866389874610.1016/j.cell.2013.08.031) ; Hodges, H. C. et al. Dominant-negative SMARCA4 mutants alter the accessibility landscape of tissue-unrestricted enhancers. Nat. Struct. Mol. Biol. 25, 61–72 (2018). (PMID: 2932327210.1038/s41594-017-0007-3) ; Stanton, B. Z. et al. Smarca4 ATPase mutations disrupt direct eviction of PRC1 from chromatin. Nat. Genet. 49, 282–288 (2017). (PMID: 2794179510.1038/ng.3735) ; Schick, S. et al. Acute BAF perturbation causes immediate changes in chromatin accessibility. Nat. Genet. 53, 269–278 (2021). (PMID: 33558760761408210.1038/s41588-021-00777-3) ; Rosen, O. R. et al. The C-terminal SET domains of ALL-1 and TRITHORAX interact with the INI1 and SNR1 proteins, components of the SWI/SNF complex. Proc. Natl Acad. Sci. USA 95, 4152–4157 (1998). (PMID: 10.1073/pnas.95.8.4152) ; Hsiao, P. W., Fryer, C. J., Trotter, K. W., Wang, W. & Archer, T. K. BAF60a mediates critical interactions between nuclear receptors and the BRG1 chromatin-remodeling complex for transactivation. Mol. Cell. Biol. 23, 6210–6220 (2003). (PMID: 1291734218092810.1128/MCB.23.17.6210-6220.2003) ; Abranches, E. et al. Neural differentiation of embryonic stem cells in vitro: a road map to neurogenesis in the embryo. PLoS ONE 4, e6286 (2009). (PMID: 19621087270944810.1371/journal.pone.0006286) ; Hiroshi Kawasaki, K. M. et al. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28, 31–40 (2000). (PMID: 10.1016/S0896-6273(00)00083-0) ; Panamarova, M. et al. The BAF chromatin remodelling complex is an epigenetic regulator of lineage specification in the early mouse embryo. Development 143, 1271–1283 (2016). (PMID: 269529874852518) ; Ginno, P. A., Burger, L., Seebacher, J., Iesmantavicius, V. & Schubeler, D. Cell cycle-resolved chromatin proteomics reveals the extent of mitotic preservation of the genomic regulatory landscape. Nat. Commun. 9, 4048 (2018). (PMID: 30279501616860410.1038/s41467-018-06007-5) ; Djeghloul, D. et al. Identifying proteins bound to native mitotic ESC chromosomes reveals chromatin repressors are important for compaction. Nat. Commun. 11, 4118 (2020). (PMID: 32807789743186110.1038/s41467-020-17823-z) ; Liu, N. et al. Direct promoter repression by BCL11A controls the fetal to adult hemoglobin switch. Cell 173, 430–442.e417 (2018). (PMID: 29606353588933910.1016/j.cell.2018.03.016) ; Valencia, A. M. et al. Recurrent SMARCB1 mutations reveal a nucleosome acidic patch interaction site that potentiates mSWI/SNF complex chromatin remodeling. Cell 179, 1342–1356.e23 (2019). ; Mashtalir, N. et al. A structural model of the endogenous human BAF complex informs disease mechanisms. Cell 183, 802–817.e824 (2020). (PMID: 33053319771717710.1016/j.cell.2020.09.051) ; Zhu, Z. et al. PHB associates with the HIRA complex to control an epigenetic-metabolic circuit in human ESCs. Cell Stem Cell 20, 274–289.e277 (2017). (PMID: 2793921710.1016/j.stem.2016.11.002) ; Hnisz, D. et al. Super-enhancers in the control of cell identity and disease. Cell 155, 934–947 (2013). (PMID: 2411984310.1016/j.cell.2013.09.053) Grant Information: R01 AI123322 United States AI NIAID NIH HHS; F31 CA261150 United States CA NCI NIH HHS; R01 CA216391 United States CA NCI NIH HHS; R01 CA113794 United States CA NCI NIH HHS; P30 CA021765 United States CA NCI NIH HHS; R01 CA172152 United States CA NCI NIH HHS Substance Nomenclature: 0 (Chromatin) ; 0 (Nuclear Proteins) ; 0 (Transcription Factors) ; 0 (Smarce1 protein, mouse) ; EC 3.6.1.- (Smarca4 protein, mouse) ; 0 (Smarcb1 protein, mouse) ; 0 (SWI-SNF-B chromatin-remodeling complex) ; 0 (Chromosomal Proteins, Non-Histone) ; 0 (Protein Subunits) Entry Date(s): Date Created: 20230524 Date Completed: 20230605 Latest Revision: 20231202 Update Code: 20231215 PubMed Central ID: PMC10303083

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Mitotic bookmarking by SWI/SNF subunits.