Smchd1 Targeting to the Inactive X Is Dependent on the Xist-HnrnpK-PRC1 Pathway

Cell Reports - Tập 25 - Trang 1912-1923.e9 - 2018
Natasha Jansz1,2, Tatyana Nesterova3, Andrew Keniry1,2, Megan Iminitoff1, Peter F. Hickey1,2, Greta Pintacuda3, Osamu Masui4, Simon Kobelke5, Niall Geoghegan1,2, Kelsey A. Breslin1, Tracy A. Willson1, Kelly Rogers1,2, Graham F. Kay6, Archa H. Fox5, Haruhiko Koseki4, Neil Brockdorff3, James M. Murphy1,2, Marnie E. Blewitt1,2,7
1The Walter and Eliza Hall Institute of Medical Research, 1G Royal Parade, Parkville, Melbourne, VIC 3052, Australia
2Department of Medical Biology, University of Melbourne, Melbourne, VIC 3010, Australia
3Developmental Epigenetics, Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK
4Centre for Integrative Medical Sciences, RIKEN Yokohama Institute, 1-7-22, Suehiro-cho, Tsurumi, Yokohama, Kanagawa 230-0045, Japan
5School of Human Sciences, The University of Western Australia, Crawley, WA, 6009, Australia
6QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia
7Department of Genetics, University of Melbourne, Melbourne, VIC 3010, Australia

Tài liệu tham khảo

Almeida, 2017, PCGF3/5-PRC1 initiates Polycomb recruitment in X chromosome inactivation, Science, 356, 1081, 10.1126/science.aal2512 Ball, 2015, SIMcheck: a toolbox for successful super-resolution structured illumination microscopy, Sci. Rep., 5, 15915, 10.1038/srep15915 Bentley, 2011, Recognition of UbcH5c and the nucleosome by the Bmi1/Ring1b ubiquitin ligase complex, EMBO J., 30, 3285, 10.1038/emboj.2011.243 Blewitt, 2008, SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation, Nat. Genet., 40, 663, 10.1038/ng.142 Brideau, 2015, Independent mechanisms target SMCHD1 to trimethylated histone H3 lysine 9-modified chromatin and the inactive X chromosome, Mol. Cell. Biol., 35, 4053, 10.1128/MCB.00432-15 Brockdorff, 2017, Polycomb complexes in X chromosome inactivation, Philos. Trans. R. Soc. Lond. B Biol. Sci., 372, 20170021, 10.1098/rstb.2017.0021 Brockdorff, 1992, 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, 10.1016/0092-8674(92)90519-I Brown, 1991, A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome, Nature, 349, 38, 10.1038/349038a0 Buchwald, 2006, Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1b, EMBO J., 25, 2465, 10.1038/sj.emboj.7601144 Calés, 2008, Inactivation of the polycomb group protein Ring1B unveils an antiproliferative role in hematopoietic cell expansion and cooperation with tumorigenesis associated with Ink4a deletion, Mol. Cell. Biol., 28, 1018, 10.1128/MCB.01136-07 Cao, 2002, Role of histone H3 lysine 27 methylation in Polycomb-group silencing, Science, 298, 1039, 10.1126/science.1076997 Chaumeil, 2008, 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, 10.1007/978-1-59745-406-3_18 Chen, 2015, Genome-wide binding and mechanistic analyses of Smchd1-mediated epigenetic regulation, Proc. Natl. Acad. Sci. USA, 112, E3535, 10.1073/pnas.1504232112 Corcoran, 2011, PARalyzer: definition of RNA binding sites from PAR-CLIP short-read sequence data, Genome Biol., 12, R79, 10.1186/gb-2011-12-8-r79 del Mar Lorente, 2000, Loss- and gain-of-function mutations show a polycomb group function for Ring1A in mice, Development, 127, 5093, 10.1242/dev.127.23.5093 Dickins, 2005, Probing tumor phenotypes using stable and regulated synthetic microRNA precursors, Nat. Genet., 37, 1289, 10.1038/ng1651 Dow, 2012, A pipeline for the generation of shRNA transgenic mice, Nat. Protoc., 7, 374, 10.1038/nprot.2011.446 Elderkin, 2007, A phosphorylated form of Mel-18 targets the Ring1B histone H2A ubiquitin ligase to chromatin, Mol. Cell, 28, 107, 10.1016/j.molcel.2007.08.009 Endoh, 2008, Polycomb group proteins Ring1A/B are functionally linked to the core transcriptional regulatory circuitry to maintain ES cell identity, Development, 135, 1513, 10.1242/dev.014340 Endoh, 2012, Histone H2A mono-ubiquitination is a crucial step to mediate PRC1-dependent repression of developmental genes to maintain ES cell identity, PLoS Genet., 8, e1002774, 10.1371/journal.pgen.1002774 Eskeland, 2010, Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination, Mol. Cell, 38, 452, 10.1016/j.molcel.2010.02.032 Gdula, 2018, The non-canonical SMC protein SmcHD1 antagonises TAD formation on the inactive X chromosome, bioRxiv Gendrel, 2012, Smchd1-dependent and -independent pathways determine developmental dynamics of CpG island methylation on the inactive X chromosome, Dev. Cell, 23, 265, 10.1016/j.devcel.2012.06.011 Gendrel, 2013, Epigenetic functions of smchd1 repress gene clusters on the inactive X chromosome and on autosomes, Mol. Cell. Biol., 33, 3150, 10.1128/MCB.00145-13 Hafner, 2010, PAR-CliP--a method to identify transcriptome-wide the binding sites of RNA binding proteins, J. Vis. Exp., 2034 Hasegawa, 2010, The matrix protein hnRNP U is required for chromosomal localization of Xist RNA, Dev. Cell, 19, 469, 10.1016/j.devcel.2010.08.006 Heinz, 2010, Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities, Mol. Cell, 38, 576, 10.1016/j.molcel.2010.05.004 Jansz, 2018, Long-range chromatin interactions on the inactive X and at Hox clusters are regulated by the non-canonical SMC protein Smchd1, bioRxiv Kay, 1993, Expression of Xist during mouse development suggests a role in the initiation of X chromosome inactivation, Cell, 72, 171, 10.1016/0092-8674(93)90658-D Kelsey, 2015, Impact of flanking chromosomal sequences on localization and silencing by the human non-coding RNA XIST, Genome Biol., 16, 208, 10.1186/s13059-015-0774-2 Kim, 2013, TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions, Genome Biol., 14, R36, 10.1186/gb-2013-14-4-r36 Kinkel, 2015, Jarid2 regulates hematopoietic stem cell function by acting with polycomb repressive complex 2, Blood, 125, 1890, 10.1182/blood-2014-10-603969 Kolpa, 2016, SAF-a requirement in anchoring XIST RNA to chromatin varies in transformed and primary cells, Dev. Cell, 39, 9, 10.1016/j.devcel.2016.09.021 Larionov, 2005, A standard curve based method for relative real time PCR data processing, BMC Bioinformatics, 6, 62, 10.1186/1471-2105-6-62 Lau, 2017, Mutation of a nucleosome compaction region disrupts Polycomb-mediated axial patterning, Science, 355, 1081, 10.1126/science.aah5403 Leong, 2013, Epigenetic regulator Smchd1 functions as a tumor suppressor, Cancer Res., 73, 1591, 10.1158/0008-5472.CAN-12-3019 Lyon, 1961, Gene action in the X-chromosome of the mouse (Mus musculus L.), Nature, 190, 372, 10.1038/190372a0 Majewski, 2008, Polycomb repressive complex 2 (PRC2) restricts hematopoietic stem cell activity, PLoS Biol., 6, e93, 10.1371/journal.pbio.0060093 McHugh, 2015, The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3, Nature, 521, 232, 10.1038/nature14443 Minajigi, 2015, Chromosomes. A comprehensive Xist interactome reveals cohesin repulsion and an RNA-directed chromosome conformation, Science, 349, 10.1126/science.aab2276 Moindrot, 2015, A pooled shRNA screen identifies Rbm15, Spen, and Wtap as factors required for Xist RNA-mediated silencing, Cell Rep., 12, 562, 10.1016/j.celrep.2015.06.053 Monfort, 2015, Identification of Spen as a crucial factor for Xist function through forward genetic screening in haploid embryonic stem cells, Cell Rep., 12, 554, 10.1016/j.celrep.2015.06.067 Mould, 2013, Smchd1 regulates a subset of autosomal genes subject to monoallelic expression in addition to being critical for X inactivation, Epigenetics Chromatin, 6, 19, 10.1186/1756-8935-6-19 Nozawa, 2013, Human inactive X chromosome is compacted through a PRC2-independent SMCHD1-HBiX1 pathway, Nat. Struct. Mol. Biol., 20, 566, 10.1038/nsmb.2532 Penny, 1996, Requirement for Xist in X chromosome inactivation, Nature, 379, 131, 10.1038/379131a0 Pintacuda, 2017, hnRNPK recruits PCGF3/5-PRC1 to the Xist RNA B-repeat to establish polycomb-mediated chromosomal silencing, Mol. Cell, 68, 955, 10.1016/j.molcel.2017.11.013 Ridings-Figueroa, 2017, The nuclear matrix protein CIZ1 facilitates localization of Xist RNA to the inactive X-chromosome territory, Genes Dev., 31, 876, 10.1101/gad.295907.117 Saldaña-Meyer, 2014, CTCF regulates the human p53 gene through direct interaction with its natural antisense transcript, Wrap53, Genes Dev., 28, 723, 10.1101/gad.236869.113 Sarma, 2010, Locked nucleic acids (LNAs) reveal sequence requirements and kinetics of Xist RNA localization to the X chromosome, Proc. Natl. Acad. Sci. USA, 107, 22196, 10.1073/pnas.1009785107 Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nat. Methods, 9, 676, 10.1038/nmeth.2019 Schoeftner, 2006, Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing, EMBO J., 25, 3110, 10.1038/sj.emboj.7601187 Seibler, 2003, Rapid generation of inducible mouse mutants, Nucleic Acids Res., 31, e12, 10.1093/nar/gng012 Sivaguru, 2018, Comparative performance of airyscan and structured illumination superresolution microscopy in the study of the surface texture and 3D shape of pollen, Microsc. Res. Tech., 81, 101, 10.1002/jemt.22732 Su, 2003, Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement, Nat. Immunol., 4, 124, 10.1038/ni876 Wang, 2018, SMCHD1 merges chromosome compartments and assists formation of super-structures on the inactive X, Cell, 174, 406, 10.1016/j.cell.2018.05.007 Wutz, 2002, Chromosomal silencing and localization are mediated by different domains of Xist RNA, Nat. Genet., 30, 167, 10.1038/ng820 Zhao, 2008, Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome, Science, 322, 750, 10.1126/science.1163045