{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T13:36:03Z","timestamp":1791466563752,"version":"4.3.4"},"reference-count":87,"publisher":"Springer Science and Business Media LLC","issue":"9","license":[{"start":{"date-parts":[[2023,8,14]],"date-time":"2023-08-14T00:00:00Z","timestamp":1691971200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2023,8,14]],"date-time":"2023-08-14T00:00:00Z","timestamp":1691971200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Genet"],"published-print":{"date-parts":[[2023,9]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Cellular differentiation requires extensive alterations in chromatin structure and function, which is elicited by the coordinated action of chromatin and transcription factors. By contrast with transcription factors, the roles of chromatin factors in differentiation have not been systematically characterized. Here, we combine bulk ex vivo and single-cell in vivo CRISPR screens to characterize the role of chromatin factor families in hematopoiesis. We uncover marked lineage specificities for 142 chromatin factors, revealing functional diversity among related chromatin factors (i.e. barrier-to-autointegration factor subcomplexes) as well as shared roles for unrelated repressive complexes that restrain excessive myeloid differentiation. Using epigenetic profiling, we identify functional interactions between lineage-determining transcription factors and several chromatin factors that explain their lineage dependencies. Studying chromatin factor functions in leukemia, we show that leukemia cells engage homeostatic chromatin factor functions to block differentiation, generating specific chromatin factor\u2013transcription factor interactions that might be therapeutically targeted. Together, our work elucidates the lineage-determining properties of chromatin factors across normal and malignant hematopoiesis.<\/jats:p>","DOI":"10.1038\/s41588-023-01471-2","type":"journal-article","created":{"date-parts":[[2023,8,14]],"date-time":"2023-08-14T16:03:12Z","timestamp":1692028992000},"page":"1542-1554","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":64,"title":["In vivo screening characterizes chromatin factor functions during normal and malignant hematopoiesis"],"prefix":"10.1038","volume":"55","author":[{"given":"David","family":"Lara-Astiaso","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ainhoa","family":"Go\u00f1i-Salaverri","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5834-7643","authenticated-orcid":false,"given":"Julen","family":"Mendieta-Esteban","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4106-2166","authenticated-orcid":false,"given":"Nisha","family":"Narayan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cynthia","family":"Del Valle","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Torsten","family":"Gross","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1390-6592","authenticated-orcid":false,"given":"George","family":"Giotopoulos","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tumas","family":"Beinortas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mar","family":"Navarro-Alonso","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura Pilar","family":"Aguado-Alvaro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jon","family":"Zazpe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francesco","family":"Marchese","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Natalia","family":"Torrea","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6619-4571","authenticated-orcid":false,"given":"Isabel A.","family":"Calvo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cecile K.","family":"Lopez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Diego","family":"Alignani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aitziber","family":"Lopez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Borja","family":"Saez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1025-0041","authenticated-orcid":false,"given":"Jake P.","family":"Taylor-King","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6115-8790","authenticated-orcid":false,"given":"Felipe","family":"Prosper","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4025-9968","authenticated-orcid":false,"given":"Nikolaus","family":"Fortelny","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0312-161X","authenticated-orcid":false,"given":"Brian J. P.","family":"Huntly","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,8,14]]},"reference":[{"key":"1471_CR1","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1038\/s41586-019-1182-7","volume":"569","author":"R Stadhouders","year":"2019","unstructured":"Stadhouders, R., Filion, G. J. & Graf, T. Transcription factors and 3D genome conformation in cell-fate decisions. Nature 569, 345\u2013354 (2019).","journal-title":"Nature"},{"key":"1471_CR2","doi-asserted-by":"publisher","first-page":"156","DOI":"10.1016\/j.ydbio.2021.03.003","volume":"475","author":"Y Ding","year":"2021","unstructured":"Ding, Y., Liu, Z. & Liu, F. Transcriptional and epigenetic control of hematopoietic stem cell fate decisions in vertebrates. Dev. Biol. 475, 156\u2013164 (2021).","journal-title":"Dev. Biol."},{"key":"1471_CR3","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1097\/CCO.0000000000000814","volume":"34","author":"J Al-Mousawi","year":"2022","unstructured":"Al-Mousawi, J. & Boskovic, A. Transcriptional and epigenetic control of early life cell fate decisions. Curr. Opin. Oncol. 34, 148\u2013154 (2022).","journal-title":"Curr. Opin. Oncol."},{"key":"1471_CR4","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1038\/s41556-018-0258-1","volume":"21","author":"AM Valencia","year":"2019","unstructured":"Valencia, A. M. & Kadoch, C. Chromatin regulatory mechanisms and therapeutic opportunities in cancer. Nat. Cell Biol. 21, 152\u2013161 (2019).","journal-title":"Nat. Cell Biol."},{"key":"1471_CR5","doi-asserted-by":"publisher","first-page":"418","DOI":"10.1038\/nature25022","volume":"553","author":"E Laurenti","year":"2018","unstructured":"Laurenti, E. & G\u00f6ttgens, B. From haematopoietic stem cells to complex differentiation landscapes. Nature 553, 418\u2013426 (2018).","journal-title":"Nature"},{"key":"1471_CR6","doi-asserted-by":"publisher","first-page":"631","DOI":"10.1016\/j.cell.2008.01.025","volume":"132","author":"SH Orkin","year":"2008","unstructured":"Orkin, S. H. & Zon, L. I. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132, 631\u2013644 (2008).","journal-title":"Cell"},{"key":"1471_CR7","doi-asserted-by":"publisher","first-page":"478","DOI":"10.1038\/nri2991","volume":"11","author":"H Cedar","year":"2011","unstructured":"Cedar, H. & Bergman, Y. Epigenetics of haematopoietic cell development. Nat. Rev. Immunol. 11, 478\u2013488 (2011).","journal-title":"Nat. Rev. Immunol."},{"key":"1471_CR8","doi-asserted-by":"publisher","first-page":"532","DOI":"10.1016\/j.stem.2010.07.016","volume":"7","author":"NK Wilson","year":"2010","unstructured":"Wilson, N. K. et al. Combinatorial transcriptional control in blood stem\/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 7, 532\u2013544 (2010).","journal-title":"Cell Stem Cell"},{"key":"1471_CR9","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1016\/S0959-437X(02)00018-7","volume":"13","author":"JR Downing","year":"2003","unstructured":"Downing, J. R. The core-binding factor leukemias: lessons learned from murine models. Curr. Opin. Genet. Dev. 13, 48\u201354 (2003).","journal-title":"Curr. Opin. Genet. Dev."},{"key":"1471_CR10","doi-asserted-by":"publisher","first-page":"4123","DOI":"10.1002\/j.1460-2075.1996.tb00787.x","volume":"15","author":"L Robb","year":"1996","unstructured":"Robb, L. et al. The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J. 15, 4123\u20134129 (1996).","journal-title":"EMBO J."},{"key":"1471_CR11","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1038\/nri2024","volume":"7","author":"F Rosenbauer","year":"2007","unstructured":"Rosenbauer, F. & Tenen, D. G. Transcription factors in myeloid development: balancing differentiation with transformation. Nat. Rev. Immunol. 7, 105\u2013117 (2007).","journal-title":"Nat. Rev. Immunol."},{"key":"1471_CR12","doi-asserted-by":"publisher","first-page":"2209","DOI":"10.1056\/NEJMoa1516192","volume":"374","author":"E Papaemmanuil","year":"2016","unstructured":"Papaemmanuil, E. et al. Genomic classification and prognosis in acute myeloid leukemia. N. Engl. J. Med. 374, 2209\u20132221 (2016).","journal-title":"N. Engl. J. Med."},{"key":"1471_CR13","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1038\/s41580-019-0143-1","volume":"29","author":"EM Michalak","year":"2019","unstructured":"Michalak, E. M. et al. The roles of DNA, RNA and histone methylation in ageing and cancer. Nat. Rev. Mol. Cell Biol. 29, 573\u2013589 (2019).","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"1471_CR14","doi-asserted-by":"publisher","first-page":"932","DOI":"10.1038\/s41590-018-0184-1","volume":"19","author":"S Cuartero","year":"2018","unstructured":"Cuartero, S. et al. Control of inducible gene expression links cohesin to hematopoietic progenitor self-renewal and differentiation. Nat. Immunol. 19, 932\u2013941 (2018).","journal-title":"Nat. Immunol."},{"key":"1471_CR15","doi-asserted-by":"publisher","first-page":"2195","DOI":"10.1182\/blood.2019001553","volume":"134","author":"D Sasca","year":"2019","unstructured":"Sasca, D. et al. Cohesin-dependent regulation of gene expression during differentiation is lost in cohesin-mutated myeloid malignancies. Blood 134, 2195\u20132208 (2019).","journal-title":"Blood"},{"key":"1471_CR16","doi-asserted-by":"publisher","first-page":"936","DOI":"10.1016\/j.tig.2020.07.011","volume":"36","author":"RC Centore","year":"2020","unstructured":"Centore, R. C., Sandoval, G. J., Soares, L. M. M., Kadoch, C. & Chan, H. M. Mammalian SWI\/SNF chromatin remodeling complexes: emerging mechanisms and therapeutic strategies. Trends Genet. 36, 936\u2013950 (2020).","journal-title":"Trends Genet."},{"key":"1471_CR17","doi-asserted-by":"publisher","first-page":"735","DOI":"10.1016\/j.stem.2014.05.006","volume":"14","author":"A Laugesen","year":"2014","unstructured":"Laugesen, A. & Helin, K. Chromatin repressive complexes in stem cells, development, and cancer. Cell Stem Cell 14, 735\u2013751 (2014).","journal-title":"Cell Stem Cell"},{"key":"1471_CR18","doi-asserted-by":"publisher","first-page":"588","DOI":"10.1038\/nrc3091","volume":"11","author":"A Lai","year":"2011","unstructured":"Lai, A. & Wade, P. Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat. Rev. Cancer 11, 588\u2013596 (2011).","journal-title":"Nat. Rev. Cancer"},{"key":"1471_CR19","doi-asserted-by":"publisher","first-page":"13670","DOI":"10.3390\/ijms232213670","volume":"23","author":"I Vaicekauskait\u0117","year":"2022","unstructured":"Vaicekauskait\u0117, I., Sabaliauskait\u0117, R., Lazutka, J. R. & Jarmalait\u0117, S. The emerging role of chromatin remodeling complexes in ovarian cancer. Int. J. Mol. Sci. 23, 13670 (2022).","journal-title":"Int. J. Mol. Sci."},{"key":"1471_CR20","doi-asserted-by":"publisher","first-page":"1691","DOI":"10.1182\/blood.2021011682","volume":"138","author":"L Yu","year":"2021","unstructured":"Yu, L. et al. An erythroid-to-myeloid cell fate conversion is elicited by LSD1 inactivation. Blood 138, 1691\u20131704 (2021).","journal-title":"Blood"},{"key":"1471_CR21","doi-asserted-by":"publisher","first-page":"960","DOI":"10.1016\/j.molcel.2020.03.031","volume":"78","author":"MA Gillespie","year":"2020","unstructured":"Gillespie, M. A. et al. Absolute quantification of transcription factors reveals principles of gene regulation in erythropoiesis. Mol. Cell 78, 960\u2013974 (2020).","journal-title":"Mol. Cell"},{"key":"1471_CR22","doi-asserted-by":"publisher","first-page":"538","DOI":"10.1016\/j.celrep.2017.06.072","volume":"20","author":"C Kerimoglu","year":"2017","unstructured":"Kerimoglu, C. et al. KMT2A and KMT2B mediate memory function by affecting distinct genomic regions. Cell Rep. 20, 538\u2013548 (2017).","journal-title":"Cell Rep."},{"key":"1471_CR23","first-page":"7173","volume":"44","author":"Y Li","year":"2016","unstructured":"Li, Y. Setd1a and NURF mediate chromatin dynamics and gene regulation during erythroid lineage commitment and differentiation. Nucleic Acids Res. 44, 7173\u20137188 (2016).","journal-title":"Nucleic Acids Res."},{"key":"1471_CR24","doi-asserted-by":"publisher","first-page":"753","DOI":"10.1038\/ng.3812","volume":"49","author":"P Priam","year":"2017","unstructured":"Priam, P. et al. SMARCD2 subunit of SWI\/SNF chromatin-remodeling complexes mediates granulopoiesis through a CEBP\u025b dependent mechanism. Nat. Genet. 49, 753\u2013764 (2017).","journal-title":"Nat. Genet."},{"key":"1471_CR25","doi-asserted-by":"publisher","first-page":"638","DOI":"10.1182\/blood-2016-01-694810","volume":"128","author":"S Koide","year":"2016","unstructured":"Koide, S. et al. Setdb1 maintains hematopoietic stem and progenitor cells by restricting the ectopic activation of nonhematopoietic genes. Blood 128, 638\u2013649 (2016).","journal-title":"Blood"},{"key":"1471_CR26","doi-asserted-by":"publisher","first-page":"3112","DOI":"10.1172\/JCI60806","volume":"123","author":"AR Summers","year":"2013","unstructured":"Summers, A. R. et al. HDAC3 is essential for DNA replication in hematopoietic progenitor cells. J. Clin. Invest. 123, 3112\u20133123 (2013).","journal-title":"J. Clin. Invest."},{"key":"1471_CR27","doi-asserted-by":"publisher","first-page":"961601","DOI":"10.3389\/fimmu.2022.961601","volume":"13","author":"S Paudel","year":"2022","unstructured":"Paudel, S. et al. Regulation of emergency granulopoiesis during infection. Front. Immunol. 13, 961601 (2022).","journal-title":"Front. Immunol."},{"key":"1471_CR28","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-18035-1","volume":"11","author":"M Bentsen","year":"2020","unstructured":"Bentsen, M. et al. ATAC-seq footprinting unravels kinetics of transcription factor binding during zygotic genome activation. Nat. Commun. 11, 4267 (2020).","journal-title":"Nat. Commun."},{"key":"1471_CR29","doi-asserted-by":"publisher","first-page":"1535","DOI":"10.1189\/jlb.0806516","volume":"81","author":"AF Gombart","year":"2007","unstructured":"Gombart, A. F., Grewal, J. & Koeffler, H. P. ATF4 differentially regulates transcriptional activation of myeloid-specific genes by C\/EBP\u03b5 and C\/EBP\u03b1. J. Leukoc. Biol. 81, 1535\u20131547 (2007).","journal-title":"J. Leukoc. Biol."},{"key":"1471_CR30","doi-asserted-by":"publisher","first-page":"2251","DOI":"10.1016\/j.celrep.2017.10.112","volume":"21","author":"M Wahlestedt","year":"2017","unstructured":"Wahlestedt, M. et al. Critical modulation of hematopoietic lineage fate by hepatic leukemia factor. Cell Rep. 21, 2251\u20132263 (2017).","journal-title":"Cell Rep."},{"key":"1471_CR31","doi-asserted-by":"publisher","first-page":"1443","DOI":"10.1038\/s41588-021-00925-9","volume":"53","author":"H Yun","year":"2021","unstructured":"Yun, H. et al. Mutational synergy during leukemia induction remodels chromatin accessibility, histone modifications and three-dimensional DNA topology to alter gene expression. Nat. Genet. 53, 1443\u20131455 (2021).","journal-title":"Nat. Genet."},{"key":"1471_CR32","doi-asserted-by":"publisher","first-page":"3364","DOI":"10.21037\/tcr-21-42","volume":"10","author":"L Zhou","year":"2021","unstructured":"Zhou, L., Yao, Q., Li, H. & Chen, J. Targeting BRD9 by I-BRD9 efficiently inhibits growth of acute myeloid leukemia cells. Transl. Cancer Res. 10, 3364\u20133372 (2021).","journal-title":"Transl. Cancer Res."},{"key":"1471_CR33","doi-asserted-by":"publisher","first-page":"672","DOI":"10.1038\/nchembio.2115","volume":"12","author":"AF Hohmann","year":"2016","unstructured":"Hohmann, A. F. et al. Sensitivity and engineered resistance of myeloid leukemia cells to BRD9 inhibition. Nat. Chem. Biol. 12, 672\u2013679 (2016).","journal-title":"Nat. Chem. Biol."},{"key":"1471_CR34","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1182\/blood-2020-134942","volume":"136","author":"ES Wang","year":"2020","unstructured":"Wang, E. S. et al. Preliminary data on a phase 1\/2A first in human study of the menin-KMT2A (MLL) inhibitor KO-539 in patients with relapsed or refractory acute myeloid leukemia. Blood 136, 7\u20138 (2020).","journal-title":"Blood"},{"key":"1471_CR35","doi-asserted-by":"publisher","first-page":"2885","DOI":"10.1007\/s00018-019-03143-z","volume":"76","author":"NT Crump","year":"2019","unstructured":"Crump, N. T. & Milne, T. A. Why are so many MLL lysine methyltransferases required for normal mammalian development? Cell. Mol. Life Sci. 76, 2885\u20132898 (2019).","journal-title":"Cell. Mol. Life Sci."},{"key":"1471_CR36","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1038\/s41588-020-0618-1","volume":"52","author":"D Douillet","year":"2020","unstructured":"Douillet, D. Uncoupling histone H3K4 trimethylation from developmental gene expression via an equilibrium of COMPASS, Polycomb and DNA methylation. Nat. Genet. 52, 615\u2013625 (2020).","journal-title":"Nat. Genet."},{"key":"1471_CR37","doi-asserted-by":"publisher","first-page":"568","DOI":"10.1016\/j.molcel.2017.04.018","volume":"66","author":"KM Dorighi","year":"2017","unstructured":"Dorighi, K. M. et al. Mll3 and Mll4 facilitate enhancer RNA synthesis and transcription from promoters independently of H3K4 monomethylation. Mol. Cell 66, 568\u2013576 (2017).","journal-title":"Mol. Cell"},{"key":"1471_CR38","doi-asserted-by":"publisher","first-page":"1135","DOI":"10.1016\/j.cell.2018.04.013","volume":"173","author":"Z Wei","year":"2018","unstructured":"Wei, Z. Vitamin D switches BAF complexes to protect \u03b2 cells. Cell 173, 1135\u20131149 (2018).","journal-title":"Cell"},{"key":"1471_CR39","doi-asserted-by":"publisher","first-page":"432","DOI":"10.1038\/s41586-019-1646-9","volume":"574","author":"D Inoue","year":"2019","unstructured":"Inoue, D. et al. Spliceosomal disruption of the non-canonical BAF complex in cancer. Nature 574, 432\u2013436 (2019).","journal-title":"Nature"},{"key":"1471_CR40","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1038\/s41586-019-1115-5","volume":"569","author":"D Barisic","year":"2019","unstructured":"Barisic, D., Stadler, M. B., Iurlaro, M. & Sch\u00fcbeler, D. Mammalian ISWI and SWI\/SNF selectively mediate binding of distinct transcription factors. Nature 569, 136\u2013140 (2019).","journal-title":"Nature"},{"key":"1471_CR41","doi-asserted-by":"publisher","first-page":"4710","DOI":"10.1172\/JCI136155","volume":"130","author":"L Liu","year":"2020","unstructured":"Liu, L. et al. Histone methyltransferase MLL4 controls myofiber identity and muscle performance through MEF2 interaction. J. Clin. Invest. 130, 4710\u20134725 (2020).","journal-title":"J. Clin. Invest."},{"key":"1471_CR42","doi-asserted-by":"publisher","first-page":"554","DOI":"10.1016\/j.molcel.2018.06.040","volume":"71","author":"GJ Sandoval","year":"2018","unstructured":"Sandoval, G. J. et al. Binding of TMPRSS2-ERG to BAF chromatin remodeling complexes mediates prostate oncogenesis. Mol. Cell 71, 554\u2013566 (2018).","journal-title":"Mol. Cell"},{"key":"1471_CR43","doi-asserted-by":"publisher","first-page":"1067","DOI":"10.1016\/j.molcel.2017.11.026","volume":"68","author":"T Vierbuchen","year":"2017","unstructured":"Vierbuchen, T. et al. AP-1 transcription factors and the BAF complex mediate signal-dependent enhancer selection. Mol. Cell 68, 1067\u20131082 (2017).","journal-title":"Mol. Cell"},{"key":"1471_CR44","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-021-25107-3","volume":"12","author":"X Huang","year":"2021","unstructured":"Huang, X. et al. OCT4 cooperates with distinct ATP-dependent chromatin remodelers in na\u00efve and primed pluripotent states in human. Nat. Commun. 12, 5123 (2021).","journal-title":"Nat. Commun."},{"key":"1471_CR45","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1016\/j.stem.2013.07.002","volume":"13","author":"J Ninkovic","year":"2013","unstructured":"Ninkovic, J. et al. The BAF complex interacts with Pax6 in adult neural progenitors to establish a neurogenic cross-regulatory transcriptional network. Cell Stem Cell 13, 403\u2013418 (2013).","journal-title":"Cell Stem Cell"},{"key":"1471_CR46","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1038\/s41588-021-00777-3","volume":"53","author":"S Schick","year":"2021","unstructured":"Schick, S. et al. Acute BAF perturbation causes immediate changes in chromatin accessibility. Nat. Genet. 53, 269\u2013278 (2021).","journal-title":"Nat. Genet."},{"key":"1471_CR47","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-021-21893-y","volume":"12","author":"Y-K Park","year":"2021","unstructured":"Park, Y.-K. et al. Interplay of BAF and MLL4 promotes cell type-specific enhancer activation. Nat. Commun. 12, 1630 (2021).","journal-title":"Nat. Commun."},{"key":"1471_CR48","doi-asserted-by":"publisher","first-page":"2370","DOI":"10.1101\/gad.471408","volume":"22","author":"M Lange","year":"2008","unstructured":"Lange, M. et al. Regulation of muscle development by DPF3, a novel histone acetylation and methylation reader of the BAF chromatin remodeling complex. Genes Dev. 22, 2370\u20132384 (2008).","journal-title":"Genes Dev."},{"key":"1471_CR49","doi-asserted-by":"publisher","first-page":"eabh3635","DOI":"10.1126\/sciadv.abh3635","volume":"8","author":"AG Holmes","year":"2022","unstructured":"Holmes, A. G. et al. A MYC inhibitor selectively alters the MYC and MAX cistromes and modulates the epigenomic landscape to regulate target gene expression. Sci. Adv. 8, eabh3635 (2022).","journal-title":"Sci. Adv."},{"key":"1471_CR50","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1038\/s41587-022-01504-x","volume":"41","author":"TE Speltz","year":"2023","unstructured":"Speltz, T. E. et al. Targeting MYC with modular synthetic transcriptional repressors derived from bHLH DNA-binding domains. Nat. Biotechnol. 41, 541\u2013551 (2023).","journal-title":"Nat. Biotechnol."},{"key":"1471_CR51","doi-asserted-by":"publisher","first-page":"eaay1018","DOI":"10.1126\/scitranslmed.aay1018","volume":"11","author":"C Kadoch","year":"2019","unstructured":"Kadoch, C. Diverse compositions and functions of chromatin remodeling machines in cancer. Sci. Transl. Med. 11, eaay1018 (2019).","journal-title":"Sci. Transl. Med."},{"key":"1471_CR52","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-021-25245-8","volume":"12","author":"AC Trotman-Grant","year":"2021","unstructured":"Trotman-Grant, A. C. et al. DL4-\u03bcbeads induce T cell lineage differentiation from stem cells in a stromal cell-free system. Nat. Commun. 12, 5023 (2021).","journal-title":"Nat. Commun."},{"key":"1471_CR53","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-18548-9","volume":"11","author":"A Lundin","year":"2020","unstructured":"Lundin, A. et al. Development of an ObLiGaRe doxycycline inducible Cas9 system for pre-clinical cancer drug discovery. Nat. Commun. 11, 4903 (2020).","journal-title":"Nat. Commun."},{"key":"1471_CR54","doi-asserted-by":"publisher","first-page":"1410","DOI":"10.1016\/j.cell.2020.04.048","volume":"181","author":"S Bowling","year":"2020","unstructured":"Bowling, S. et al. An engineered CRISPR\u2013Cas9 mouse line for simultaneous readout of lineage histories and gene expression profiles in single cells. Cell 181, 1410\u20131422 (2020).","journal-title":"Cell"},{"key":"1471_CR55","doi-asserted-by":"publisher","first-page":"571","DOI":"10.1016\/j.immuni.2021.01.001","volume":"54","author":"J Dubrot","year":"2021","unstructured":"Dubrot, J. et al. In vivo screens using a selective CRISPR antigen removal lentiviral vector system reveal immune dependencies in renal cell carcinoma. Immunity 54, 571\u2013585 (2021).","journal-title":"Immunity"},{"key":"1471_CR56","doi-asserted-by":"publisher","first-page":"378","DOI":"10.1038\/s41588-020-0595-4","volume":"52","author":"F Izzo","year":"2020","unstructured":"Izzo, F. et al. DNA methylation disruption reshapes the hematopoietic differentiation landscape. Nat. Genet. 52, 378\u2013387 (2020).","journal-title":"Nat. Genet."},{"key":"1471_CR57","doi-asserted-by":"publisher","first-page":"1917","DOI":"10.1038\/leu.2013.77","volume":"27","author":"A Mupo","year":"2013","unstructured":"Mupo, A. et al. A powerful molecular synergy between mutant nucleophosmin and Flt3-ITD drives acute myeloid leukemia in mice. Leukemia 27, 1917\u20131920 (2013).","journal-title":"Leukemia"},{"key":"1471_CR58","doi-asserted-by":"publisher","first-page":"470","DOI":"10.1038\/ng.796","volume":"43","author":"GS Vassiliou","year":"2011","unstructured":"Vassiliou, G. S. et al. Mutant nucleophosmin and cooperating pathways drive leukemia initiation and progression in mice. Nat. Genet. 43, 470\u2013475 (2011).","journal-title":"Nat. Genet."},{"key":"1471_CR59","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1038\/s41586-019-1244-x","volume":"571","author":"AC Wilkinson","year":"2019","unstructured":"Wilkinson, A. C. et al. Long-term ex vivo haematopoietic-stem-cell expansion allows nonconditioned transplantation. Nature 571, 117\u2013121 (2019).","journal-title":"Nature"},{"key":"1471_CR60","doi-asserted-by":"publisher","unstructured":"csbg\/tfcf: published code. Zenodo https:\/\/doi.org\/10.5281\/zenodo.7891703 (2023).","DOI":"10.5281\/zenodo.7891703"},{"key":"1471_CR61","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","volume":"26","author":"MD Robinson","year":"2010","unstructured":"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\u2013140 (2010).","journal-title":"Bioinformatics"},{"key":"1471_CR62","doi-asserted-by":"publisher","first-page":"e47","DOI":"10.1093\/nar\/gkv007","volume":"43","author":"ME Ritchie","year":"2015","unstructured":"Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).","journal-title":"Nucleic Acids Res."},{"key":"1471_CR63","doi-asserted-by":"publisher","first-page":"954","DOI":"10.1038\/s41587-020-0470-y","volume":"38","author":"JM Replogle","year":"2020","unstructured":"Replogle, J. M. et al. Combinatorial single-cell CRISPR screens by direct guide RNA capture and targeted sequencing. Nat. Biotechnol. 38, 954\u2013961 (2020).","journal-title":"Nat. Biotechnol."},{"key":"1471_CR64","doi-asserted-by":"publisher","first-page":"3573","DOI":"10.1016\/j.cell.2021.04.048","volume":"184","author":"Y Hao","year":"2021","unstructured":"Hao, Y. et al. Integrated analysis of multimodal single-cell data. Cell 184, 3573\u20133587 (2021).","journal-title":"Cell"},{"key":"1471_CR65","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1038\/nbt.2859","volume":"32","author":"C Trapnell","year":"2014","unstructured":"Trapnell, C. et al. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat. Biotechnol. 32, 381\u2013386 (2014).","journal-title":"Nat. Biotechnol."},{"key":"1471_CR66","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1126\/science.aax0249","volume":"367","author":"GS Gulati","year":"2020","unstructured":"Gulati, G. S. et al. Single-cell transcriptional diversity is a hallmark of developmental potential. Science 367, 405\u2013411 (2020).","journal-title":"Science"},{"key":"1471_CR67","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1038\/s41590-018-0276-y","volume":"20","author":"D Aran","year":"2019","unstructured":"Aran, D. et al. Reference-based analysis of lung single-cell sequencing reveals a transitional profibrotic macrophage. Nat. Immunol. 20, 163\u2013172 (2019).","journal-title":"Nat. Immunol."},{"key":"1471_CR68","doi-asserted-by":"publisher","first-page":"943","DOI":"10.1126\/science.1256271","volume":"345","author":"D Lara-Astiaso","year":"2014","unstructured":"Lara-Astiaso, D. et al. Immunogenetics. Chromatin state dynamics during blood formation. Science 345, 943\u2013949 (2014).","journal-title":"Science"},{"key":"1471_CR69","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-021-23324-4","volume":"12","author":"M Andreatta","year":"2021","unstructured":"Andreatta, M. et al. Interpretation of T cell states from single-cell transcriptomics data using reference atlases. Nat. Commun. 12, 2965 (2021).","journal-title":"Nat. Commun."},{"key":"1471_CR70","doi-asserted-by":"publisher","first-page":"629","DOI":"10.1038\/s42003-021-02146-6","volume":"4","author":"L He","year":"2021","unstructured":"He, L. et al. NEBULA is a fast negative binomial mixed model for differential or co-expression analysis of large-scale multi-subject single-cell data. Commun. Biol. 4, 629 (2021).","journal-title":"Commun. Biol."},{"key":"1471_CR71","doi-asserted-by":"publisher","unstructured":"Korotkevich, G. et al. Fast gene set enrichment analysis. Preprint at bioRxiv https:\/\/doi.org\/10.1101\/060012 (2021).","DOI":"10.1101\/060012"},{"key":"1471_CR72","doi-asserted-by":"publisher","first-page":"845","DOI":"10.1038\/nmeth.3971","volume":"13","author":"L Haghverdi","year":"2016","unstructured":"Haghverdi, L., B\u00fcttner, M., Wolf, F. A., Buettner, F. A. & Theis, F. J. Diffusion pseudotime robustly reconstructs lineage branching. Nat. Methods 13, 845\u2013848 (2016).","journal-title":"Nat. Methods"},{"key":"1471_CR73","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-017-1382-0","volume":"19","author":"FA Wolf","year":"2018","unstructured":"Wolf, F. A., Angerer, P. & Theis, F. J. SCANPY: large-scale single-cell gene expression data analysis. Genome Biol. 19, 15 (2018).","journal-title":"Genome Biol."},{"key":"1471_CR74","doi-asserted-by":"publisher","first-page":"1193","DOI":"10.1038\/ng.3646","volume":"48","author":"MR Corces","year":"2016","unstructured":"Corces, M. R. et al. Lineage-specific and single-cell chromatin accessibility charts human hematopoiesis and leukemia evolution. Nat. Genet. 48, 1193\u20131203 (2016).","journal-title":"Nat. Genet."},{"key":"1471_CR75","doi-asserted-by":"publisher","unstructured":"Krueger, F., James, F., Ewels, P., Afyounian, E. & Schuster-Boeckler, B. Zenodo FelixKrueger\/TrimGalore: v0.6.7 https:\/\/doi.org\/10.5281\/zenodo.5127899 (2021).","DOI":"10.5281\/zenodo.5127899"},{"key":"1471_CR76","doi-asserted-by":"publisher","first-page":"10","DOI":"10.14806\/ej.17.1.200","volume":"17","author":"M Martin","year":"2011","unstructured":"Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10\u201312 (2011).","journal-title":"EMBnet J."},{"key":"1471_CR77","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.1923","volume":"4","author":"B Langmead","year":"2012","unstructured":"Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 4, 357\u2013359 (2012).","journal-title":"Nat. Methods"},{"key":"1471_CR78","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-019-45839-z","volume":"9","author":"HM Amemiya","year":"2019","unstructured":"Amemiya, H. M., Kundaje, A. & Boyle, A. P. The ENCODE blacklist: identification of problematic regions of the genome. Sci. Rep. 9, 9354 (2019).","journal-title":"Sci. Rep."},{"key":"1471_CR79","doi-asserted-by":"publisher","first-page":"W160","DOI":"10.1093\/nar\/gkw257","volume":"44","author":"F Ram\u00edrez","year":"2016","unstructured":"Ram\u00edrez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160\u2013W165 (2016).","journal-title":"Nucleic Acids Res."},{"key":"1471_CR80","doi-asserted-by":"publisher","first-page":"giab008","DOI":"10.1093\/gigascience\/giab008","volume":"10","author":"P Danecek","year":"2021","unstructured":"Danecek, P. et al. Twelve years of SAMtools and BCFtools. Gigascience 10, giab008 (2021).","journal-title":"Gigascience"},{"key":"1471_CR81","doi-asserted-by":"publisher","first-page":"841","DOI":"10.1093\/bioinformatics\/btq033","volume":"26","author":"AR Quinlan","year":"2010","unstructured":"Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841\u2013842 (2010).","journal-title":"Bioinformatics"},{"key":"1471_CR82","doi-asserted-by":"publisher","first-page":"R137","DOI":"10.1186\/gb-2008-9-9-r137","volume":"9","author":"Y Zhang","year":"2008","unstructured":"Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).","journal-title":"Genome Biol."},{"key":"1471_CR83","doi-asserted-by":"publisher","first-page":"576","DOI":"10.1016\/j.molcel.2010.05.004","volume":"38","author":"S Heinz","year":"2010","unstructured":"Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576\u2013589 (2010).","journal-title":"Mol. Cell"},{"key":"1471_CR84","doi-asserted-by":"publisher","first-page":"923","DOI":"10.1093\/bioinformatics\/btt656","volume":"30","author":"Y Liao","year":"2014","unstructured":"Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923\u2013930 (2014).","journal-title":"Bioinformatics"},{"key":"1471_CR85","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","volume":"15","author":"MI Love","year":"2014","unstructured":"Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).","journal-title":"Genome Biol."},{"key":"1471_CR86","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms3535","volume":"4","author":"E Wolf","year":"2013","unstructured":"Wolf, E. et al. Miz1 is required to maintain autophagic flux. Nat. Commun. 4, 2535 (2013).","journal-title":"Nat. Commun."},{"key":"1471_CR87","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-09234-6","volume":"10","author":"Y Zhou","year":"2019","unstructured":"Zhou, Y. et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat. Commun. 10, 1523 (2019).","journal-title":"Nat. Commun."}],"container-title":["Nature Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41588-023-01471-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41588-023-01471-2","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41588-023-01471-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,7]],"date-time":"2023-09-07T23:05:23Z","timestamp":1694127923000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41588-023-01471-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,14]]},"references-count":87,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2023,9]]}},"alternative-id":["1471"],"URL":"https:\/\/doi.org\/10.1038\/s41588-023-01471-2","relation":{},"ISSN":["1061-4036","1546-1718"],"issn-type":[{"value":"1061-4036","type":"print"},{"value":"1546-1718","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,14]]},"assertion":[{"value":"29 September 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 July 2023","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 August 2023","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"T.G. and J.P.T.-K. are employees receiving compensation from Relation Therapeutics. J.P.T.-K. is a founder of Relation Therapeutics. D.L.-A. is a consultant of Relation Therapeutics. The other authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}