BAF complex-mediated chromatin relaxation is required for establishment of X chromosome inactivation.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
29 03 2022
Historique:
received: 10 01 2021
accepted: 10 03 2022
entrez: 30 3 2022
pubmed: 31 3 2022
medline: 14 4 2022
Statut: epublish

Résumé

The process of epigenetic silencing, while fundamentally important, is not yet completely understood. Here we report a replenishable female mouse embryonic stem cell (mESC) system, Xmas, that allows rapid assessment of X chromosome inactivation (XCI), the epigenetic silencing mechanism of one of the two X chromosomes that enables dosage compensation in female mammals. Through a targeted genetic screen in differentiating Xmas mESCs, we reveal that the BAF complex is required to create nucleosome-depleted regions at promoters on the inactive X chromosome during the earliest stages of establishment of XCI. Without this action gene silencing fails. Xmas mESCs provide a tractable model for screen-based approaches that enable the discovery of unknown facets of the female-specific process of XCI and epigenetic silencing more broadly.

Identifiants

pubmed: 35351876
doi: 10.1038/s41467-022-29333-1
pii: 10.1038/s41467-022-29333-1
pmc: PMC8964718
doi:

Substances chimiques

Chromatin 0
RNA, Long Noncoding 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1658

Informations de copyright

© 2022. The Author(s).

Références

Gendrel, A. V. & Heard, E. Fifty years of X-inactivation research. Development 138, 5049–5055 (2011).
pubmed: 22069183 doi: 10.1242/dev.068320
Jegu, T., Aeby, E. & Lee, J. T. The X chromosome in space. Nat. Rev. Genet 18, 377–389 (2017).
pubmed: 28479596 doi: 10.1038/nrg.2017.17
Disteche, C. M. & Berletch, J. B. X-chromosome inactivation and escape. J. Genet 94, 591–599 (2015).
pubmed: 26690513 pmcid: 4826282 doi: 10.1007/s12041-015-0574-1
Brockdorff, N. & Turner, B. M. Dosage compensation in mammals. Cold Spring Harb. Perspect. Biol. 7, a019406 (2015).
pubmed: 25731764 pmcid: 4355265 doi: 10.1101/cshperspect.a019406
Monk, M. & McLaren, A. X-chromosome activity in foetal germ cells of the mouse. J. Embryol. Exp. Morphol. 63, 75–84 (1981).
pubmed: 7310296
Tam, P. P., Zhou, S. X. & Tan, S. S. X-chromosome activity of the mouse primordial germ cells revealed by the expression of an X-linked lacZ transgene. Development 120, 2925–2932 (1994).
pubmed: 7607082 doi: 10.1242/dev.120.10.2925
Kratzer, P. G. & Chapman, V. M. X chromosome reactivation in oocytes of Mus caroli. Proc. Natl Acad. Sci. USA 78, 3093–3097 (1981).
pubmed: 6942418 pmcid: 319506 doi: 10.1073/pnas.78.5.3093
Brockdorff, N. et al. Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome. Nature 351, 329–331 (1991).
pubmed: 2034279 doi: 10.1038/351329a0
Brown, C. J. et al. The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 71, 527–542 (1992).
pubmed: 1423611 doi: 10.1016/0092-8674(92)90520-M
McHugh, C. A. et al. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature 521, 232–236 (2015).
pubmed: 25915022 pmcid: 4516396 doi: 10.1038/nature14443
Chu, C. et al. Systematic discovery of Xist RNA binding proteins. Cell 161, 404–416 (2015).
pubmed: 25843628 pmcid: 4425988 doi: 10.1016/j.cell.2015.03.025
Minajigi, A. et al. Chromosomes. A comprehensive Xist interactome reveals cohesin repulsion and an RNA-directed chromosome conformation. Science 349 (2015).
Keohane, A. M., O’Neill, L. P., Belyaev, N. D., Lavender, J. S. & Turner, B. M. X-Inactivation and histone H4 acetylation in embryonic stem cells. Dev. Biol. 180, 618–630 (1996).
pubmed: 8954732 doi: 10.1006/dbio.1996.0333
Heard, E. et al. Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation. Cell 107, 727–738 (2001).
pubmed: 11747809 doi: 10.1016/S0092-8674(01)00598-0
Zylicz, J. J. et al. The implication of early chromatin changes in X chromosome inactivation. Cell 176, 182–197 e123 (2019).
pubmed: 30595450 pmcid: 6333919 doi: 10.1016/j.cell.2018.11.041
Mak, W. et al. Mitotically stable association of polycomb group proteins eed and enx1 with the inactive x chromosome in trophoblast stem cells. Curr. Biol. 12, 1016–1020 (2002).
pubmed: 12123576 doi: 10.1016/S0960-9822(02)00892-8
Silva, J. et al. Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev. Cell 4, 481–495 (2003).
pubmed: 12689588 doi: 10.1016/S1534-5807(03)00068-6
Plath, K. et al. Role of histone H3 lysine 27 methylation in X inactivation. Science 300, 131–135 (2003).
pubmed: 12649488 doi: 10.1126/science.1084274
de Napoles, M. et al. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell 7, 663–676 (2004).
pubmed: 15525528 doi: 10.1016/j.devcel.2004.10.005
Fang, J., Chen, T., Chadwick, B., Li, E. & Zhang, Y. Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J. Biol. Chem. 279, 52812–52815 (2004).
pubmed: 15509584 doi: 10.1074/jbc.C400493200
Plath, K. et al. Developmentally regulated alterations in Polycomb repressive complex 1 proteins on the inactive X chromosome. J. Cell Biol. 167, 1025–1035 (2004).
pubmed: 15596546 pmcid: 2172612 doi: 10.1083/jcb.200409026
Schoeftner, S. et al. Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J. 25, 3110–3122 (2006).
pubmed: 16763550 pmcid: 1500994 doi: 10.1038/sj.emboj.7601187
Keniry, A. et al. Setdb1-mediated H3K9 methylation is enriched on the inactive X and plays a role in its epigenetic silencing. Epigenetics Chromatin 9, 16 (2016).
pubmed: 27195021 pmcid: 4870784 doi: 10.1186/s13072-016-0064-6
Peters, A. H. et al. Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nat. Genet. 30, 77–80 (2002).
pubmed: 11740497 doi: 10.1038/ng789
Boggs, B. A. et al. Differentially methylated forms of histone H3 show unique association patterns with inactive human X chromosomes. Nat. Genet. 30, 73–76 (2002).
pubmed: 11740495 doi: 10.1038/ng787
Mermoud, J. E., Popova, B., Peters, A. H., Jenuwein, T. & Brockdorff, N. Histone H3 lysine 9 methylation occurs rapidly at the onset of random X chromosome inactivation. Curr. Biol. 12, 247–251 (2002).
pubmed: 11839280 doi: 10.1016/S0960-9822(02)00660-7
Splinter, E. et al. The inactive X chromosome adopts a unique three-dimensional conformation that is dependent on Xist RNA. Genes Dev. 25, 1371–1383 (2011).
pubmed: 21690198 pmcid: 3134081 doi: 10.1101/gad.633311
Giorgetti, L. et al. Structural organization of the inactive X chromosome in the mouse. Nature 535, 575–579 (2016).
pubmed: 27437574 pmcid: 5443622 doi: 10.1038/nature18589
Deng, X. et al. Bipartite structure of the inactive mouse X chromosome. Genome Biol. 16, 152 (2015).
pubmed: 26248554 pmcid: 4539712 doi: 10.1186/s13059-015-0728-8
Nora, E. P. et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485, 381–385 (2012).
pubmed: 22495304 pmcid: 3555144 doi: 10.1038/nature11049
Wang, C. Y., Jegu, T., Chu, H. P., Oh, H. J. & Lee, J. T. SMCHD1 merges chromosome compartments and assists formation of super-structures on the inactive X. Cell 174, 406–421 e425 (2018).
pubmed: 29887375 pmcid: 6475921 doi: 10.1016/j.cell.2018.05.007
Gdula, M. R. et al. The non-canonical SMC protein SmcHD1 antagonises TAD formation and compartmentalisation on the inactive X chromosome. Nat. Commun. 10, 30 (2019).
pubmed: 30604745 pmcid: 6318279 doi: 10.1038/s41467-018-07907-2
Jansz, N. et al. Smchd1 regulates long-range chromatin interactions on the inactive X chromosome and at Hox clusters. Nat. Struct. Mol. Biol. 25, 766–777 (2018).
pubmed: 30127357 doi: 10.1038/s41594-018-0111-z
Sado, T. et al. X inactivation in the mouse embryo deficient for Dnmt1: distinct effect of hypomethylation on imprinted and random X inactivation. Dev. Biol. 225, 294–303 (2000).
pubmed: 10985851 doi: 10.1006/dbio.2000.9823
Minkovsky, A. et al. The Mbd1-Atf7ip-Setdb1 pathway contributes to the maintenance of X chromosome inactivation. Epigenetics Chromatin 7, 12 (2014).
pubmed: 25028596 pmcid: 4099106 doi: 10.1186/1756-8935-7-12
Zvetkova, I. et al. Global hypomethylation of the genome in XX embryonic stem cells. Nat. Genet. 37, 1274–1279 (2005).
pubmed: 16244654 doi: 10.1038/ng1663
Ooi, S. K. et al. Dynamic instability of genomic methylation patterns in pluripotent stem cells. Epigenetics Chromatin 3, 17 (2010).
pubmed: 20868487 pmcid: 2954997 doi: 10.1186/1756-8935-3-17
Schulz, E. G. et al. The two active X chromosomes in female ESCs block exit from the pluripotent state by modulating the ESC signaling network. Cell Stem Cell 14, 203–216 (2014).
pubmed: 24506884 doi: 10.1016/j.stem.2013.11.022
Choi, J. et al. DUSP9 modulates DNA hypomethylation in female mouse pluripotent stem cells. Cell Stem Cell 20, 706–719 e707 (2017).
pubmed: 28366588 pmcid: 5524993 doi: 10.1016/j.stem.2017.03.002
Choi, J. et al. Prolonged Mek1/2 suppression impairs the developmental potential of embryonic stem cells. Nature 548, 219–223 (2017).
pubmed: 28746311 pmcid: 5905676 doi: 10.1038/nature23274
Yagi, M. et al. Derivation of ground-state female ES cells maintaining gamete-derived DNA methylation. Nature 548, 224–227 (2017).
pubmed: 28746308 doi: 10.1038/nature23286
Habibi, E. et al. Whole-genome bisulfite sequencing of two distinct interconvertible DNA methylomes of mouse embryonic stem cells. Cell Stem Cell 13, 360–369 (2013).
pubmed: 23850244 doi: 10.1016/j.stem.2013.06.002
Wu, H. et al. Cellular resolution maps of X chromosome inactivation: implications for neural development, function, and disease. Neuron 81, 103–119 (2014).
pubmed: 24411735 pmcid: 3950970 doi: 10.1016/j.neuron.2013.10.051
Ciavatta, D., Kalantry, S., Magnuson, T. & Smithies, O. A DNA insulator prevents repression of a targeted X-linked transgene but not its random or imprinted X inactivation. Proc. Natl Acad. Sci. USA 103, 9958–9963 (2006).
pubmed: 16777957 pmcid: 1479543 doi: 10.1073/pnas.0603754103
Bauer, M. et al. Chromosome compartments on the inactive X guide TAD formation independently of transcription during X-reactivation. Nat. Commun. 12, 3499 (2021).
pubmed: 34108480 pmcid: 8190187 doi: 10.1038/s41467-021-23610-1
Pasque, V. et al. X chromosome reactivation dynamics reveal stages of reprogramming to pluripotency. Cell 159, 1681–1697 (2014).
pubmed: 25525883 pmcid: 4282187 doi: 10.1016/j.cell.2014.11.040
Sommer, C. A. et al. Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells 27, 543–549 (2009).
pubmed: 19096035 pmcid: 4848035 doi: 10.1634/stemcells.2008-1075
Takagi, N. & Sasaki, M. Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature 256, 640–642 (1975).
pubmed: 1152998 doi: 10.1038/256640a0
Marks, H. et al. The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149, 590–604 (2012).
pubmed: 22541430 pmcid: 3398752 doi: 10.1016/j.cell.2012.03.026
Maza, I. et al. Transient acquisition of pluripotency during somatic cell transdifferentiation with iPSC reprogramming factors. Nat. Biotechnol. 33, 769–774 (2015).
pubmed: 26098448 pmcid: 4500825 doi: 10.1038/nbt.3270
Ying, Q. L. et al. The ground state of embryonic stem cell self-renewal. Nature 453, 519–523 (2008).
pubmed: 18497825 pmcid: 5328678 doi: 10.1038/nature06968
Makhlouf, M. et al. A prominent and conserved role for YY1 in Xist transcriptional activation. Nat. Commun. 5, 4878 (2014).
pubmed: 25209548 doi: 10.1038/ncomms5878
Hasegawa, Y. et al. The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev. Cell 19, 469–476 (2010).
pubmed: 20833368 doi: 10.1016/j.devcel.2010.08.006
da Rocha, S. T. et al. Jarid2 is implicated in the initial Xist-induced targeting of PRC2 to the inactive X chromosome. Mol. Cell 53, 301–316 (2014).
pubmed: 24462204 doi: 10.1016/j.molcel.2014.01.002
Cooper, S. et al. Jarid2 binds mono-ubiquitylated H2A lysine 119 to mediate crosstalk between Polycomb complexes PRC1 and PRC2. Nat. Commun. 7, 13661 (2016).
pubmed: 27892467 pmcid: 5133711 doi: 10.1038/ncomms13661
Vizlin-Hodzic, D., Johansson, H., Ryme, J., Simonsson, T. & Simonsson, S. SAF-A has a role in transcriptional regulation of Oct4 in ES cells through promoter binding. Cell Reprogram 13, 13–27 (2011).
pubmed: 21235343 pmcid: 3030915 doi: 10.1089/cell.2010.0075
Donohoe, M. E., Zhang, L. F., Xu, N., Shi, Y. & Lee, J. T. Identification of a Ctcf cofactor, Yy1, for the X chromosome binary switch. Mol. Cell 25, 43–56 (2007).
pubmed: 17218270 doi: 10.1016/j.molcel.2006.11.017
Blewitt, M. E. et al. An N-ethyl-N-nitrosourea screen for genes involved in variegation in the mouse. Proc. Natl. Acad. Sci. USA 102, 7629–7634 (2005).
pubmed: 15890782 pmcid: 1140414 doi: 10.1073/pnas.0409375102
Daxinger, L. et al. An ENU mutagenesis screen identifies novel and known genes involved in epigenetic processes in the mouse. Genome Biol. 14, R96 (2013).
pubmed: 24025402 pmcid: 4053835 doi: 10.1186/gb-2013-14-9-r96
Ashe, A. et al. A genome-wide screen for modifiers of transgene variegation identifies genes with critical roles in development. Genome Biol. 9, R182 (2008).
pubmed: 19099580 pmcid: 2646286 doi: 10.1186/gb-2008-9-12-r182
Daxinger, L. et al. A forward genetic screen identifies eukaryotic translation initiation factor 3, subunit H (eIF3h), as an enhancer of variegation in the mouse. G3 (Bethesda) 2, 1393–1396 (2012).
doi: 10.1534/g3.112.004036
Harten, S. K. et al. The first mouse mutants of D14Abb1e (Fam208a) show that it is critical for early development. Mamm. Genome 25, 293–303 (2014).
pubmed: 24781204 pmcid: 4105592 doi: 10.1007/s00335-014-9516-0
Whitelaw, N. C. et al. Reduced levels of two modifiers of epigenetic gene silencing, Dnmt3a and Trim28, cause increased phenotypic noise. Genome Biol. 11, R111 (2010).
pubmed: 21092094 pmcid: 3156950 doi: 10.1186/gb-2010-11-11-r111
Youngson, N. A. et al. No evidence for cumulative effects in a Dnmt3b hypomorph across multiple generations. Mamm. Genome 24, 206–217 (2013).
pubmed: 23636699 doi: 10.1007/s00335-013-9451-5
Blewitt, M. & Whitelaw, E. The use of mouse models to study epigenetics. Cold Spring Harb. Perspect. Biol. 5, a017939 (2013).
pubmed: 24186070 pmcid: 3809579 doi: 10.1101/cshperspect.a017939
Chong, S. et al. Modifiers of epigenetic reprogramming show paternal effects in the mouse. Nat. Genet. 39, 614–622 (2007).
pubmed: 17450140 pmcid: 3199608 doi: 10.1038/ng2031
Blewitt, M. E. et al. SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat. Genet. 40, 663–669 (2008).
pubmed: 18425126 doi: 10.1038/ng.142
Kaeser, M. D., Aslanian, A., Dong, M. Q., Yates, J. R. 3rd & Emerson, B. M. BRD7, a novel PBAF-specific SWI/SNF subunit, is required for target gene activation and repression in embryonic stem cells. J. Biol. Chem. 283, 32254–32263 (2008).
pubmed: 18809673 pmcid: 2583284 doi: 10.1074/jbc.M806061200
Fazzio, T. G., Huff, J. T. & Panning, B. An RNAi screen of chromatin proteins identifies Tip60-p400 as a regulator of embryonic stem cell identity. Cell 134, 162–174 (2008).
pubmed: 18614019 pmcid: 4308735 doi: 10.1016/j.cell.2008.05.031
Ho, L. 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).
pubmed: 19279220 pmcid: 2654396 doi: 10.1073/pnas.0812889106
Schick, S. et al. Acute BAF perturbation causes immediate changes in chromatin accessibility. Nat. Genet. 53, 269–278 (2021).
pubmed: 33558760 doi: 10.1038/s41588-021-00777-3
Schick, S. et al. Systematic characterization of BAF mutations provides insights into intracomplex synthetic lethalities in human cancers. Nat. Genet 51, 1399–1410 (2019).
pubmed: 31427792 pmcid: 6952272 doi: 10.1038/s41588-019-0477-9
Ng, K. et al. A system for imaging the regulatory noncoding Xist RNA in living mouse embryonic stem cells. Mol. Biol. Cell 22, 2634–2645 (2011).
pubmed: 21613549 pmcid: 3135487 doi: 10.1091/mbc.e11-02-0146
Rodermund, L. et al. Time-resolved structured illumination microscopy reveals key principles of Xist RNA spreading. Science 372 (2021).
Moindrot, B. et al. A pooled shRNA screen identifies Rbm15, Spen, and Wtap as factors required for Xist rna-mediated silencing. Cell Rep. 12, 562–572 (2015).
pubmed: 26190105 pmcid: 4534822 doi: 10.1016/j.celrep.2015.06.053
Hadjantonakis, A. K., Gertsenstein, M., Ikawa, M., Okabe, M. & Nagy, A. Non-invasive sexing of preimplantation stage mammalian embryos. Nat. Genet. 19, 220–222 (1998).
pubmed: 9662390 doi: 10.1038/893
Hadjantonakis, A. K., Cox, L. L., Tam, P. P. & Nagy, A. An X-linked GFP transgene reveals unexpected paternal X-chromosome activity in trophoblastic giant cells of the mouse placenta. Genesis 29, 133–140 (2001).
pubmed: 11252054 doi: 10.1002/gene.1016
Csankovszki, G., Nagy, A. & Jaenisch, R. Synergism of Xist RNA, DNA methylation, and histone hypoacetylation in maintaining X chromosome inactivation. J. Cell Biol. 153, 773–784 (2001).
pubmed: 11352938 pmcid: 2192370 doi: 10.1083/jcb.153.4.773
Mohandas, T., Sparkes, R. S. & Shapiro, L. J. Reactivation of an inactive human X chromosome: evidence for X inactivation by DNA methylation. Science 211, 393–396 (1981).
pubmed: 6164095 doi: 10.1126/science.6164095
Graves, J. A. 5-azacytidine-induced re-expression of alleles on the inactive X chromosome in a hybrid mouse cell line. Exp. Cell Res. 141, 99–105 (1982).
pubmed: 6180921 doi: 10.1016/0014-4827(82)90072-6
Royce-Tolland, M. E. et al. The A-repeat links ASF/SF2-dependent Xist RNA processing with random choice during X inactivation. Nat. Struct. Mol. Biol. 17, 948–954 (2010).
pubmed: 20657585 pmcid: 4336797 doi: 10.1038/nsmb.1877
Jegu, T. et al. Xist RNA antagonizes the SWI/SNF chromatin remodeler BRG1 on the inactive X chromosome. Nat. Struct. Mol. Biol. 26, 96–109 (2019).
pubmed: 30664740 pmcid: 6421574 doi: 10.1038/s41594-018-0176-8
Lay, F. D., Kelly, T. K. & Jones, P. A. Nucleosome occupancy and methylome sequencing (NOMe-seq). Methods Mol. Biol. 1708, 267–284 (2018).
pubmed: 29224149 doi: 10.1007/978-1-4939-7481-8_14
Kelly, T. K. et al. Genome-wide mapping of nucleosome positioning and DNA methylation within individual DNA molecules. Genome Res. 22, 2497–2506 (2012).
pubmed: 22960375 pmcid: 3514679 doi: 10.1101/gr.143008.112
Taberlay, P. C., Statham, A. L., Kelly, T. K., Clark, S. J. & Jones, P. A. Reconfiguration of nucleosome-depleted regions at distal regulatory elements accompanies DNA methylation of enhancers and insulators in cancer. Genome Res. 24, 1421–1432 (2014).
pubmed: 24916973 pmcid: 4158760 doi: 10.1101/gr.163485.113
Argelaguet, R. et al. Multi-omics profiling of mouse gastrulation at single-cell resolution. Nature 576, 487–491 (2019).
pubmed: 31827285 pmcid: 6924995 doi: 10.1038/s41586-019-1825-8
Ohhata, T. et al. Dynamics of transcription-mediated conversion from euchromatin to facultative heterochromatin at the Xist promoter by Tsix. Cell Rep. 34, 108912 (2021).
pubmed: 33789104 doi: 10.1016/j.celrep.2021.108912
Minkovsky, A. et al. A high-throughput screen of inactive X chromosome reactivation identifies the enhancement of DNA demethylation by 5-aza-2’-dC upon inhibition of ribonucleotide reductase. Epigenetics Chromatin 8, 42 (2015).
pubmed: 26468331 pmcid: 4604769 doi: 10.1186/s13072-015-0034-4
Lessing, D. et al. A high-throughput small molecule screen identifies synergism between DNA methylation and Aurora kinase pathways for X reactivation. Proc. Natl Acad. Sci. USA 113, 14366–14371 (2016).
pubmed: 28182563 pmcid: 5167172 doi: 10.1073/pnas.1617597113
Bhatnagar, S. et al. Genetic and pharmacological reactivation of the mammalian inactive X chromosome. Proc. Natl. Acad. Sci. USA 111, 12591–12598 (2014).
pubmed: 25136103 pmcid: 4156765 doi: 10.1073/pnas.1413620111
Sripathy, S. et al. Screen for reactivation of MeCP2 on the inactive X chromosome identifies the BMP/TGF-beta superfamily as a regulator of XIST expression. Proc. Natl Acad. Sci. USA 114, 1619–1624 (2017).
pubmed: 28143937 pmcid: 5321041 doi: 10.1073/pnas.1621356114
Li, W. et al. Genome-wide RNAi screen identify melanoma-associated antigen Mageb3 involved in X chromosome inactivation. J. Mol. Biol. 430, 2734–2746 (2018).
pubmed: 29800566 doi: 10.1016/j.jmb.2018.05.031
Chan, K. M., Zhang, H., Malureanu, L., van Deursen, J. & Zhang, Z. Diverse factors are involved in maintaining X chromosome inactivation. Proc. Natl Acad. Sci. USA 108, 16699–16704 (2011).
pubmed: 21940502 pmcid: 3189073 doi: 10.1073/pnas.1107616108
Monfort, A. et al. Identification of Spen as a crucial factor for xist function through forward genetic screening in haploid embryonic stem cells. Cell Rep. 12, 554–561 (2015).
pubmed: 26190100 pmcid: 4530576 doi: 10.1016/j.celrep.2015.06.067
Mashtalir, N. et al. Modular organization and assembly of SWI/SNF family chromatin remodeling complexes. Cell 175, 1272e1220 (2018).
doi: 10.1016/j.cell.2018.09.032
Wang, W. et al. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J. 15, 5370–5382 (1996).
pubmed: 8895581 pmcid: 452280 doi: 10.1002/j.1460-2075.1996.tb00921.x
Wang, W. et al. Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev. 10, 2117–2130 (1996).
pubmed: 8804307 doi: 10.1101/gad.10.17.2117
Han, D. et al. SRG3, a core component of mouse SWI/SNF complex, is essential for extra-embryonic vascular development. Dev. Biol. 315, 136–146 (2008).
pubmed: 18206867 doi: 10.1016/j.ydbio.2007.12.024
Bultman, S. et al. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol. Cell 6, 1287–1295 (2000).
pubmed: 11163203 doi: 10.1016/S1097-2765(00)00127-1
Kidder, B. L., Palmer, S. & Knott, J. G. SWI/SNF-Brg1 regulates self-renewal and occupies core pluripotency-related genes in embryonic stem cells. Stem Cells 27, 317–328 (2009).
pubmed: 19056910 doi: 10.1634/stemcells.2008-0710
Pintacuda, G. et al. hnRNPK recruits PCGF3/5-PRC1 to the Xist RNA B-repeat to establish polycomb-mediated chromosomal silencing. Mol. Cell 68, 955–969 e910 (2017).
pubmed: 29220657 pmcid: 5735038 doi: 10.1016/j.molcel.2017.11.013
Dossin, F. et al. SPEN integrates transcriptional and epigenetic control of X-inactivation. Nature 578, 455–460 (2020).
pubmed: 32025035 pmcid: 7035112 doi: 10.1038/s41586-020-1974-9
Farley, F. W., Soriano, P., Steffen, L. S. & Dymecki, S. M. Widespread recombinase expression using FLPeR (flipper) mice. Genesis 28, 106–110 (2000).
pubmed: 11105051 doi: 10.1002/1526-968X(200011/12)28:3/4<106::AID-GENE30>3.0.CO;2-T
Majewski, I. J. et al. Polycomb repressive complex 2 (PRC2) restricts hematopoietic stem cell activity. PLoS Biol. 6, e93 (2008).
pubmed: 18416604 pmcid: 2292752 doi: 10.1371/journal.pbio.0060093
Jansz, N. et al. Smchd1 Targeting to the Inactive X Is Dependent on the Xist-HnrnpK-PRC1 Pathway. Cell Rep. 25, 1912–1923 e1919 (2018).
pubmed: 30428357 doi: 10.1016/j.celrep.2018.10.044
Kinkel, S. A. et al. Jarid2 regulates hematopoietic stem cell function by acting with polycomb repressive complex 2. Blood 125, 1890–1900 (2015).
pubmed: 25645357 pmcid: 4424268 doi: 10.1182/blood-2014-10-603969
Majewski, I. J. et al. Opposing roles of polycomb repressive complexes in hematopoietic stem and progenitor cells. Blood 116, 731–739 (2010).
pubmed: 20445021 doi: 10.1182/blood-2009-12-260760
Gayen, S., Maclary, E., Buttigieg, E., Hinten, M. & Kalantry, S. A primary role for the Tsix lncRNA in maintaining random X-chromosome inactivation. Cell Rep. 11, 1251–1265 (2015).
pubmed: 25981039 pmcid: 4449283 doi: 10.1016/j.celrep.2015.04.039
Nefzger, C. M., Alaei, S., Knaupp, A. S., Holmes, M. L. & Polo, J. M. Cell surface marker mediated purification of iPS cell intermediates from a reprogrammable mouse model. J. Vis. Exp. 6, e51728 (2014).
Nefzger, C. M. et al. A versatile strategy for isolating a highly enriched population of intestinal stem cells. Stem Cell Rep. 6, 321–329 (2016).
doi: 10.1016/j.stemcr.2016.01.014
Krueger, F. Available at: http://www.bioinformatics.babraham.ac.uk/projects/trim_galore/ .
Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105–1111 (2009).
pubmed: 19289445 pmcid: 2672628 doi: 10.1093/bioinformatics/btp120
Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015).
pubmed: 25751142 pmcid: 4655817 doi: 10.1038/nmeth.3317
Krueger, F. & Andrews, S. R. SNPsplit: Allele-specific splitting of alignments between genomes with known SNP genotypes. F1000Res 5, 1479 (2016).
pubmed: 27429743 pmcid: 4934512 doi: 10.12688/f1000research.9037.1
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).
pubmed: 19910308 doi: 10.1093/bioinformatics/btp616
McCarthy, D. J., Chen, Y. & Smyth, G. K. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 40, 4288–4297 (2012).
pubmed: 22287627 pmcid: 3378882 doi: 10.1093/nar/gks042
Law, C. W., Chen, Y., Shi, W. & Smyth, G. K. voom: precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 15, R29 (2014).
pubmed: 24485249 pmcid: 4053721 doi: 10.1186/gb-2014-15-2-r29
Alhamdoosh, M. et al. Easy and efficient ensemble gene set testing with EGSEA. F1000Res 6, 2010 (2017).
pubmed: 29333246 pmcid: 5747338 doi: 10.12688/f1000research.12544.1
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
Chaumeil, J., Augui, S., Chow, J. C. & Heard, E. Combined immunofluorescence, RNA fluorescent in situ hybridization, and DNA fluorescent in situ hybridization to study chromatin changes, transcriptional activity, nuclear organization, and X-chromosome inactivation. Methods Mol. Biol. 463, 297–308 (2008).
pubmed: 18951174 doi: 10.1007/978-1-59745-406-3_18
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
Wutz, A. & Jaenisch, R. A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation. Mol. Cell 5, 695–705 (2000).
pubmed: 10882105 doi: 10.1016/S1097-2765(00)80248-8
Krueger, F. & Andrews, S. R. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27, 1571–1572 (2011).
pubmed: 21493656 pmcid: 3102221 doi: 10.1093/bioinformatics/btr167

Auteurs

Andrew Keniry (A)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia. keniry@wehi.edu.au.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia. keniry@wehi.edu.au.

Natasha Jansz (N)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Linden J Gearing (LJ)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Iromi Wanigasuriya (I)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Joseph Chen (J)

Department of Anatomy and Developmental Biology, Monash University, Clayton, VIC, Australia.
Development and Stem Cells Program, Monash Biomedicine Discovery Institute, Clayton, VIC, Australia.
Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria, Australia.

Christian M Nefzger (CM)

Department of Anatomy and Developmental Biology, Monash University, Clayton, VIC, Australia.
The University of Queensland, Institute for Molecular Bioscience, St Lucia, QLD, Australia.

Peter F Hickey (PF)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Quentin Gouil (Q)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Joy Liu (J)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Kelsey A Breslin (KA)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.

Megan Iminitoff (M)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Tamara Beck (T)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.

Andres Tapia Del Fierro (A)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Lachlan Whitehead (L)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Andrew Jarratt (A)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Sarah A Kinkel (SA)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Phillippa C Taberlay (PC)

School of Medicine, College of Health and Medicine, University of Tasmania, Hobart, TAS, Australia.

Tracy Willson (T)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Miha Pakusch (M)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.

Matthew E Ritchie (ME)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Douglas J Hilton (DJ)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia.

Jose M Polo (JM)

Department of Anatomy and Developmental Biology, Monash University, Clayton, VIC, Australia.
Development and Stem Cells Program, Monash Biomedicine Discovery Institute, Clayton, VIC, Australia.
Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria, Australia.

Marnie E Blewitt (ME)

The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, Australia. blewitt@wehi.edu.au.
The Department of Medical Biology, University of Melbourne, Parkville, VIC, Australia. blewitt@wehi.edu.au.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH