Polycomb repressive complexes 1 and 2 are each essential for maintenance of X inactivation in extra-embryonic lineages.


Journal

Nature cell biology
ISSN: 1476-4679
Titre abrégé: Nat Cell Biol
Pays: England
ID NLM: 100890575

Informations de publication

Date de publication:
Jan 2023
Historique:
received: 28 04 2021
accepted: 08 11 2022
pubmed: 13 1 2023
medline: 25 1 2023
entrez: 12 1 2023
Statut: ppublish

Résumé

In female mammals, one of the two X chromosomes becomes inactivated during development by X-chromosome inactivation (XCI). Although Polycomb repressive complex (PRC) 1 and PRC2 have both been implicated in gene silencing, their exact roles in XCI during in vivo development have remained elusive. To this end, we have studied mouse embryos lacking either PRC1 or PRC2. Here we demonstrate that the loss of either PRC has a substantial impact on maintenance of gene silencing on the inactive X chromosome (Xi) in extra-embryonic tissues, with overlapping yet different genes affected, indicating potentially independent roles of the two complexes. Importantly, a lack of PRC1 does not affect PRC2/H3K27me3 accumulation and a lack of PRC2 does not impact PRC1/H2AK119ub1 accumulation on the Xi. Thus PRC1 and PRC2 contribute independently to the maintenance of XCI in early post-implantation extra-embryonic lineages, revealing that both Polycomb complexes can be directly involved and differently deployed in XCI.

Identifiants

pubmed: 36635505
doi: 10.1038/s41556-022-01047-y
pii: 10.1038/s41556-022-01047-y
doi:

Substances chimiques

Polycomb Repressive Complex 1 EC 2.3.2.27
Polycomb Repressive Complex 2 EC 2.1.1.43
Polycomb-Group Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

134-144

Subventions

Organisme : MEXT | JST | Precursory Research for Embryonic Science and Technology (PRESTO)
ID : JPMJPR11SE
Organisme : MEXT | Japan Science and Technology Agency (JST)
ID : 17H06426
Organisme : MEXT | JST | Core Research for Evolutional Science and Technology (CREST)
ID : 13417643
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : ANR-11-LABX-0044

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Lyon, M. F. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190, 372–373 (1961).
doi: 10.1038/190372a0
Żylicz, J. J. & Heard, E. Molecular mechanisms of facultative heterochromatin formation: an X-chromosome perspective. Annu. Rev. Biochem. 89, 255–282 (2020).
doi: 10.1146/annurev-biochem-062917-012655
Brockdorff, N. et al. The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell 71, 515–526 (1992).
doi: 10.1016/0092-8674(92)90519-I
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).
doi: 10.1016/0092-8674(92)90520-M
Ku, M. et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 4, e1000242 (2008).
doi: 10.1371/journal.pgen.1000242
Lock, L. F., Takagi, N. & Martin, G. R. Methylation of the Hprt gene on the inactive X occurs after chromosome inactivation. Cell 48, 39–46 (1987).
doi: 10.1016/0092-8674(87)90353-9
Gendrel, A.-V. et al. Smchd1-dependent and -independent pathways determine developmental dynamics of CpG island methylation on the inactive X chromosome. Dev. Cell 23, 265–279 (2012).
doi: 10.1016/j.devcel.2012.06.011
Chu, C. et al. Systematic discovery of Xist RNA binding proteins. Cell 161, 404–416 (2015).
doi: 10.1016/j.cell.2015.03.025
McHugh, C. A. et al. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature 521, 232–236 (2015).
doi: 10.1038/nature14443
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).
doi: 10.1016/j.celrep.2015.06.067
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).
doi: 10.1016/j.celrep.2015.06.053
Dossin, F. et al. SPEN integrates transcriptional and epigenetic control of X-inactivation. Nature 578, 455–460 (2020).
doi: 10.1038/s41586-020-1974-9
Brockdorff, N. Polycomb complexes in X chromosome inactivation. Philos. Trans. R. Soc. Lond. B 372, 20170021 (2017).
doi: 10.1098/rstb.2017.0021
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).
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).
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).
doi: 10.1016/j.devcel.2004.10.005
Dixon-McDougall, T. & Brown, C. J. Independent domains for recruitment of PRC1 and PRC2 by human XIST. PLoS Genet. 17, e1009123 (2021).
doi: 10.1371/journal.pgen.1009123
Wang, H. et al. Role of histone H2A ubiquitination in Polycomb silencing. Nature 431, 873–878 (2004).
doi: 10.1038/nature02985
Gao, Z. et al. PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes. Mol. Cell 45, 344–356 (2012).
doi: 10.1016/j.molcel.2012.01.002
Cao, R. et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298, 1039–1043 (2002).
doi: 10.1126/science.1076997
Wang, J. et al. Imprinted X inactivation maintained by a mouse Polycomb group gene. Nat. Genet. 28, 371–375 (2001).
doi: 10.1038/ng574
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 (2017).
doi: 10.1016/j.molcel.2017.11.013
Almeida, M. et al. PCGF3/5–PRC1 initiates Polycomb recruitment in X chromosome inactivation. Science 356, 1081–1084 (2017).
doi: 10.1126/science.aal2512
Nesterova, T. et al. Systematic allelic analysis defines the interplay of key pathways in X chromosome inactivation. Nat. Commun. 10, 3129 (2019).
doi: 10.1038/s41467-019-11171-3
Endoh, M. et al. Polycomb group proteins Ring1A/B are functionally linked to the core transcriptional regulatory circuitry to maintain ES cell identity. Development 135, 1513–1524 (2008).
doi: 10.1242/dev.014340
Okamoto, I., Otte, A. P., Allis, C. D., Reinberg, D. & Heard, E. Epigenetic dynamics of imprinted X inactivation during early mouse development. Science 303, 644–649 (2004).
doi: 10.1126/science.1092727
Borensztein, M. et al. Xist-dependent imprinted X inactivation and the early developmental consequences of its failure. Nat. Struct. Mol. Biol. 24, 226–233 (2017).
doi: 10.1038/nsmb.3365
Corbel, C., Diabangouaya, P., Gendrel, A. V., Chow, J. C. & Heard, E. Unusual chromatin status and organization of the inactive X chromosome in murine trophoblast giant cells. Development 140, 861–872 (2013).
doi: 10.1242/dev.087429
Takagi, N. & Abe, K. Detrimental effects of two active X chromosomes on early mouse development. Development 109, 189–201 (1990).
doi: 10.1242/dev.109.1.189
Mugford, J. W., Yee, D. & Magnuson, T. Failure of extra-embryonic progenitor maintenance in the absence of dosage compensation. Development 139, 2130–2138 (2012).
doi: 10.1242/dev.076497
Sakata, Y. et al. Defects in dosage compensation impact global gene regulation in the mouse trophoblast. Development 144, 2784–2797 (2017).
Corbel, C. & Heard, E. Transcriptional analysis by nascent RNA FISH of in vivo trophoblast giant cells or in vitro short-term cultures of ectoplacental cone explants. J. Vis. Exp. 114, e54386 (2016).
Takada, T. et al. Mouse inter-subspecific consomic strains for genetic dissection of quantitative complex traits. Genome Res. 18, 500–508 (2008).
doi: 10.1101/gr.7175308
Su, I. H. et al. Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat. Immunol. 4, 124–131 (2003).
doi: 10.1038/ni876
Sugishita, H. et al. Variant PCGF1-PRC1 links PRC2 recruitment with differentiation-associated transcriptional inactivation at target genes. Nat. Commun. 12, 5341 (2021).
doi: 10.1038/s41467-021-24894-z
Farcas, A. M. et al. KDM2B links the Polycomb repressive complex 1 (PRC1) to recognition of CpG islands. eLife 18, e00205 (2012).
doi: 10.7554/eLife.00205
Andergassen, D., Smith, Z. D., Kretzmer, H., Rinn, J. L. & Meissner, A. Diverse epigenetic mechanisms maintain parental imprints within the embryonic and extraembryonic lineages. Dev. Cell 56, 2995–3005 (2021).
doi: 10.1016/j.devcel.2021.10.010
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).
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).
doi: 10.1038/ncomms13661
Dorbrinić, P., Szczurek, A. T. & Klose, R. J. PRC1 drives Polycomb-mediated gene repression by controlling transcription initiation and burst frequency. Nat. Struct. Mol. Biol. 28, 811–824 (2021).
doi: 10.1038/s41594-021-00661-y
Jadhav, U. et al. Replicational dilution of H3K27me3 in mammalian cells and the role of poised promoters. Mol. Cell 78, 141–151 (2020).
doi: 10.1016/j.molcel.2020.01.017
Li, H. Exploring single-sample SNP and INDEL calling with whole-genome de novo assembly. Bioinformatics 28, 1838–1844 (2012).
doi: 10.1093/bioinformatics/bts280
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv https://doi.org/10.48550/arXiv.1303.3997 (2013)
Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
doi: 10.1093/bioinformatics/btp352
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
doi: 10.1093/bioinformatics/btp324
Takahashi, S. et al. Genome-wide stability of the DNA replication program in single mammalian cells. Nat. Genet. 51, 529–540 (2019).
doi: 10.1038/s41588-019-0347-5
Perry, J., Palmer, S., Gabriel, A. & Ashworth, A. A short pseudoautosomal region in laboratory mice. Genome Res. 11, 1826–1832 (2001).
doi: 10.1101/gr.203001
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet J. 17, 10–12 (2011).
doi: 10.14806/ej.17.1.200
Magoc, T. & Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011).
doi: 10.1093/bioinformatics/btr507
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
doi: 10.1093/bioinformatics/btq033
Kent, W. J. et al. The Human Genome Browser at UCSC. Genome Res. 12, 996–1006 (2002).
doi: 10.1101/gr.229102
Degner, J. F. et al. Effect of read-mapping biases on detecting allele-specific expression from RNA-sequencing data. Bioinformatics 25, 3207–3212 (2009).
doi: 10.1093/bioinformatics/btp579
Trapnell, C. et al. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511–515 (2010).
doi: 10.1038/nbt.1621

Auteurs

Osamu Masui (O)

Laboratory for Developmental Genetics, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
Department of Cellular and Molecular Medicine, Graduate School of Medicine, Chiba University, Chiba, Japan.

Catherine Corbel (C)

Unité de Génétique et Biologie du Développement, Institut Curie, PSL Research University, CNRS UMR 3215, INSERM U934, Paris, France.

Koji Nagao (K)

Department of Biological Sciences, Graduate School of Science, Osaka University, Toyonaka, Japan.

Takaho A Endo (TA)

Laboratory for Integrative Genomics, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.

Fuyuko Kezuka (F)

Laboratory for Developmental Genetics, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.

Patricia Diabangouaya (P)

Unité de Génétique et Biologie du Développement, Institut Curie, PSL Research University, CNRS UMR 3215, INSERM U934, Paris, France.

Manabu Nakayama (M)

Laboratory of Medical Omics Research, Kazusa DNA Research Institute, Kisarazu, Japan.

Mami Kumon (M)

Laboratory for Developmental Genetics, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.

Yoko Koseki (Y)

Laboratory for Developmental Genetics, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.

Chikashi Obuse (C)

Department of Biological Sciences, Graduate School of Science, Osaka University, Toyonaka, Japan.

Haruhiko Koseki (H)

Laboratory for Developmental Genetics, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan. haruhiko.koseki@riken.jp.
Department of Cellular and Molecular Medicine, Graduate School of Medicine, Chiba University, Chiba, Japan. haruhiko.koseki@riken.jp.

Edith Heard (E)

Unité de Génétique et Biologie du Développement, Institut Curie, PSL Research University, CNRS UMR 3215, INSERM U934, Paris, France. edith.heard@embl.org.
Collège de France, Paris, France. edith.heard@embl.org.
European Molecular Biology Laboratory (EMBL), Directors' research unit, Heidelberg, Germany. edith.heard@embl.org.

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