Transcription Factors Drive Tet2-Mediated Enhancer Demethylation to Reprogram Cell Fate

Cell Stem Cell - Tập 23 - Trang 727-741.e9 - 2018
Jose Luis Sardina1, Samuel Collombet2, Tian V. Tian1, Antonio Gómez1, Bruno Di Stefano3,4,5,6,7, Clara Berenguer1, Justin Brumbaugh3,4,5,6,7, Ralph Stadhouders1, Carolina Segura-Morales1, Marta Gut8,9, Ivo G. Gut8,9, Simon Heath8,9, Sergi Aranda1, Luciano Di Croce1,8, Konrad Hochedlinger3,4,5,6,7, Denis Thieffry2, Thomas Graf1,8
1Gene Regulation, Stem Cells and Cancer Program, Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology (BIST), Barcelona 08003, Spain
2Institut de Biologie de l’Ecole Normale Supérieure (IBENS), Paris Sciences & Lettres Université, CNRS UMR8197, INSERM U1024, Paris 75005, France
3Department of Molecular Biology, Massachusetts General Hospital, Harvard Medical School, 185 Cambridge Street, Boston, MA 02114, USA
4Center for Regenerative Medicine, Massachusetts General Hospital, Harvard Medical School, 185 Cambridge Street, Boston, MA 02114, USA
5Cancer Center, Massachusetts General Hospital, Harvard Medical School, 185 Cambridge Street, Boston, MA 02114, USA
6Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA
7Harvard Stem Cell Institute, 1350 Massachusetts Avenue, Cambridge, MA 02138, USA
8Universitat Pompeu Fabra (UPF), Barcelona 08003, Spain
9CNAG-CRG, Centro Nacional de Análisis Genómico, Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, Barcelona 08028, Spain

Tài liệu tham khảo

Amouroux, 2016, De novo DNA methylation drives 5hmC accumulation in mouse zygotes, Nat. Cell Biol., 18, 225, 10.1038/ncb3296 Apostolou, 2013, Chromatin dynamics during cellular reprogramming, Nature, 502, 462, 10.1038/nature12749 Bar-Nur, 2014, Small molecules facilitate rapid and synchronous iPSC generation, Nat. Methods, 11, 1170, 10.1038/nmeth.3142 Bird, 2002, DNA methylation patterns and epigenetic memory, Genes Dev., 16, 6, 10.1101/gad.947102 Boiani, 2002, Oct4 distribution and level in mouse clones: consequences for pluripotency, Genes Dev., 16, 1209, 10.1101/gad.966002 Booth, 2012, Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution, Science, 336, 934, 10.1126/science.1220671 Buenrostro, 2013, Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position, Nat. Methods, 10, 1213, 10.1038/nmeth.2688 Bussmann, 2009, A robust and highly efficient immune cell reprogramming system, Cell Stem Cell, 5, 554, 10.1016/j.stem.2009.10.004 Carey, 2010, Single-gene transgenic mouse strains for reprogramming adult somatic cells, Nat. Methods, 7, 56, 10.1038/nmeth.1410 Chen, 2008, Integration of external signaling pathways with the core transcriptional network in embryonic stem cells, Cell, 133, 1106, 10.1016/j.cell.2008.04.043 Chen, 2013, H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs, Nat. Genet., 45, 34, 10.1038/ng.2491 Chronis, 2017, Cooperative binding of transcription factors orchestrates reprogramming, Cell, 168, 442, 10.1016/j.cell.2016.12.016 Collins, 1987, A stromal cell line from myeloid long-term bone marrow cultures can support myelopoiesis and B lymphopoiesis, J. Immunol., 138, 1082, 10.4049/jimmunol.138.4.1082 2012, An integrated encyclopedia of DNA elements in the human genome, Nature, 489, 57, 10.1038/nature11247 Costa, 2013, NANOG-dependent function of TET1 and TET2 in establishment of pluripotency, Nature, 495, 370, 10.1038/nature11925 Croft, 2011, Reactome: a database of reactions, pathways and biological processes, Nucleic Acids Res., 39, D691, 10.1093/nar/gkq1018 de la Rica, 2013, PU.1 target genes undergo Tet2-coupled demethylation and DNMT3b-mediated methylation in monocyte-to-osteoclast differentiation, Genome Biol., 14, R99, 10.1186/gb-2013-14-9-r99 Di Stefano, 2014, C/EBPα poises B cells for rapid reprogramming into induced pluripotent stem cells, Nature, 506, 235, 10.1038/nature12885 Di Stefano, 2016, C/EBPα creates elite cells for iPSC reprogramming by upregulating Klf4 and increasing the levels of Lsd1 and Brd4, Nat. Cell Biol., 18, 371, 10.1038/ncb3326 Dobin, 2013, STAR: ultrafast universal RNA-seq aligner, Bioinformatics, 29, 15, 10.1093/bioinformatics/bts635 Doege, 2012, Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2, Nature, 488, 652, 10.1038/nature11333 Domcke, 2015, Competition between DNA methylation and transcription factors determines binding of NRF1, Nature, 528, 575, 10.1038/nature16462 dos Santos, 2014, MBD3/NuRD facilitates induction of pluripotency in a context-dependent manner, Cell Stem Cell, 15, 102, 10.1016/j.stem.2014.04.019 Gibson, 2009, Enzymatic assembly of DNA molecules up to several hundred kilobases, Nat. Methods, 6, 343, 10.1038/nmeth.1318 Habibi, 2013, Whole-genome bisulfite sequencing of two distinct interconvertible DNA methylomes of mouse embryonic stem cells, Cell Stem Cell, 13, 360, 10.1016/j.stem.2013.06.002 Hackett, 2014, Regulatory principles of pluripotency: from the ground state up, Cell Stem Cell, 15, 416, 10.1016/j.stem.2014.09.015 Han, 2016, A Highly Sensitive and Robust Method for Genome-wide 5hmC Profiling of Rare Cell Populations, Mol. Cell, 63, 711, 10.1016/j.molcel.2016.06.028 Hasemann, 2014, C/EBPα is required for long-term self-renewal and lineage priming of hematopoietic stem cells and for the maintenance of epigenetic configurations in multipotent progenitors, PLoS Genet., 10, e1004079, 10.1371/journal.pgen.1004079 Hu, 2014, Tet and TDG mediate DNA demethylation essential for mesenchymal-to-epithelial transition in somatic cell reprogramming, Cell Stem Cell, 14, 512, 10.1016/j.stem.2014.01.001 Huber, 2015, Orchestrating high-throughput genomic analysis with Bioconductor, Nat. Methods, 12, 115, 10.1038/nmeth.3252 Kallin, 2012, Tet2 facilitates the derepression of myeloid target genes during CEBPα-induced transdifferentiation of pre-B cells, Mol. Cell, 48, 266, 10.1016/j.molcel.2012.08.007 Ko, 2010, Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2, Nature, 468, 839, 10.1038/nature09586 Kumar, 2007, Mfuzz: a software package for soft clustering of microarray data, Bioinformation, 2, 5, 10.6026/97320630002005 Lee, 2014, An epigenomic roadmap to induced pluripotency reveals DNA methylation as a reprogramming modulator, Nat. Commun., 5, 5619, 10.1038/ncomms6619 Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol., 15, 550, 10.1186/s13059-014-0550-8 Marco-Sola, 2012, The GEM mapper: fast, accurate and versatile alignment by filtration, Nat. Methods, 9, 1185, 10.1038/nmeth.2221 Martello, 2013, Identification of the missing pluripotency mediator downstream of leukaemia inhibitory factor, EMBO J., 32, 2561, 10.1038/emboj.2013.177 Medina-Rivera, 2011, Theoretical and empirical quality assessment of transcription factor-binding motifs, Nucleic Acids Res., 39, 808, 10.1093/nar/gkq710 Medina-Rivera, 2015, RSAT 2015: Regulatory Sequence Analysis Tools, Nucleic Acids Res., 43, W50, 10.1093/nar/gkv362 Merkel, 2017, GEMBS: high through-put processing pipeline for DNA methylation data from Whole Genome Bisulfite Sequencing (WGBS), Bioinformatics Milagre, 2017, Gender differences in global but not targeted demethylation in iPSC reprogramming, Cell Rep., 18, 1079, 10.1016/j.celrep.2017.01.008 Neph, 2012, BEDOPS: High-performance genomic feature operations, Bioinformatics, 28, 1919, 10.1093/bioinformatics/bts277 Pastor, 2013, TETonic shift: Biological roles of TET proteins in DNA demethylation and transcription, Nat. Rev. Mol. Cell Biol., 14, 341, 10.1038/nrm3589 Polo, 2012, A molecular roadmap of reprogramming somatic cells into iPS cells, Cell, 151, 1617, 10.1016/j.cell.2012.11.039 Rais, 2013, Deterministic direct reprogramming of somatic cells to pluripotency, Nature, 502, 65, 10.1038/nature12587 Ramírez, 2016, deepTools2: a next generation web server for deep-sequencing data analysis, Nucleic Acids Res., 44, 10.1093/nar/gkw257 Sardina, 2010, p22phox-dependent NADPH oxidase activity is required for megakaryocytic differentiation, Cell Death Differ., 17, 1842, 10.1038/cdd.2010.67 Schmidl, 2015, ChIPmentation: Fast, robust, low-input ChIP-seq for histones and transcription factors, Nat. Methods, 12, 963, 10.1038/nmeth.3542 Smith, 2013, DNA methylation: roles in mammalian development, Nat. Rev. Genet., 14, 204, 10.1038/nrg3354 Soufi, 2015, Pioneer transcription factors target partial DNA motifs on nucleosomes to initiate reprogramming, Cell, 161, 555, 10.1016/j.cell.2015.03.017 Stadhouders, 2018, Transcription factors orchestrate dynamic interplay between genome topology and gene regulation during cell reprogramming, Nat. Genet., 50, 238, 10.1038/s41588-017-0030-7 Stadtfeld, 2010, A reprogrammable mouse strain from gene-targeted embryonic stem cells, Nat. Methods, 7, 53, 10.1038/nmeth.1409 Takahashi, 2006, Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors, Cell, 126, 663, 10.1016/j.cell.2006.07.024 Thomas-Chollier, 2011, Transcription factor binding predictions using TRAP for the analysis of ChIP-seq data and regulatory SNPs, Nat. Protoc., 6, 1860, 10.1038/nprot.2011.409 van Oevelen, 2015, C/EBPα activates pre-existing and de novo macrophage enhancers during induced pre-B cell transdifferentiation and myelopoiesis, Stem Cell Reports, 5, 232, 10.1016/j.stemcr.2015.06.007 Vidal, 2014, Combinatorial modulation of signaling pathways reveals cell-type-specific requirements for highly efficient and synchronous iPSC reprogramming, Stem Cell Reports, 3, 574, 10.1016/j.stemcr.2014.08.003 Wang, 2015, WT1 recruits TET2 to regulate its target gene expression and suppress leukemia cell proliferation, Mol. Cell, 57, 662, 10.1016/j.molcel.2014.12.023 Wu, 2017, TET-mediated active DNA demethylation: mechanism, function and beyond, Nat. Rev. Genet., 18, 517, 10.1038/nrg.2017.33 Wu, 2014, Single-base resolution analysis of active DNA demethylation using methylase-assisted bisulfite sequencing, Nat. Biotechnol., 32, 1231, 10.1038/nbt.3073 Xiong, 2016, Cooperative action between SALL4A and TET proteins in stepwise oxidation of 5-methylcytosine, Mol. Cell, 64, 913, 10.1016/j.molcel.2016.10.013 Yildirim, 2011, Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells, Cell, 147, 1498, 10.1016/j.cell.2011.11.054 Yin, 2017, Impact of cytosine methylation on DNA binding specificities of human transcription factors, Science, 10.1126/science.aaj2239 Ying, 2008, The ground state of embryonic stem cell self-renewal, Nature, 453, 519, 10.1038/nature06968 Yu, 2012, Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome, Cell, 149, 1368, 10.1016/j.cell.2012.04.027 Zhang, 1997, Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer binding protein alpha-deficient mice, Proc. Natl. Acad. Sci. USA, 94, 569, 10.1073/pnas.94.2.569 Zhang, 2015, Tet2 is required to resolve inflammation by recruiting Hdac2 to specifically repress IL-6, Nature, 525, 389, 10.1038/nature15252 Zhang, 2008, Model-based analysis of ChIP-Seq (MACS), Genome Biol., 9, R137, 10.1186/gb-2008-9-9-r137