Memory of Divisional History Directs the Continuous Process of Primitive Hematopoietic Lineage Commitment

Acar, 2015, Deep imaging of bone marrow shows non-dividing stem cells are mainly perisinusoidal, Nature, 526, 126, 10.1038/nature15250 Attwooll, 2005, A novel repressive E2F6 complex containing the polycomb group protein, EPC1, that interacts with EZH2 in a proliferation-specific manner, J. Biol. Chem., 280, 1199, 10.1074/jbc.M412509200 Beerman, 2013, Proliferation-dependent alterations of the DNA methylation landscape underlie hematopoietic stem cell aging, Cell Stem Cell, 12, 413, 10.1016/j.stem.2013.01.017 Bejar, 2011, Clinical effect of point mutations in myelodysplastic syndromes, N. Engl. J. Med., 364, 2496, 10.1056/NEJMoa1013343 Bernitz, 2017, Granulocyte-colony stimulating factor mobilizes dormant hematopoietic stem cells without proliferation in mice, Blood, 129, 1901, 10.1182/blood-2016-11-752923 Bernitz, 2016, Hematopoietic stem cells count and remember self-renewal divisions, Cell, 167, 1296, 10.1016/j.cell.2016.10.022 Bowie, 2006, Hematopoietic stem cells proliferate until after birth and show a reversible phase-specific engraftment defect, J. Clin. Invest., 116, 2808, 10.1172/JCI28310 Bracken, 2003, EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer, EMBO J., 22, 5323, 10.1093/emboj/cdg542 Bretones, 2015, Myc and cell cycle control, Biochim. Biophys. Acta, 1849, 506, 10.1016/j.bbagrm.2014.03.013 Cabezas-Wallscheid, 2017, Vitamin A-retinoic acid signaling regulates hematopoietic stem cell dormancy, Cell, 169, 807, 10.1016/j.cell.2017.04.018 Cabezas-Wallscheid, 2014, Identification of regulatory networks in HSCs and their immediate progeny via integrated proteome, transcriptome, and DNA methylome analysis, Cell Stem Cell, 15, 507, 10.1016/j.stem.2014.07.005 Cao, 2002, Role of histone H3 lysine 27 methylation in Polycomb-group silencing, Science, 298, 1039, 10.1126/science.1076997 Carrelha, 2018, Hierarchically related lineage-restricted fates of multipotent haematopoietic stem cells, Nature, 554, 106, 10.1038/nature25455 Chen, 2016, Hoxb5 marks long-term haematopoietic stem cells and reveals a homogenous perivascular niche, Nature, 530, 223, 10.1038/nature16943 Czermin, 2002, Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites, Cell, 111, 185, 10.1016/S0092-8674(02)00975-3 Danis, 2016, Ezh2 controls an early hematopoietic program and growth and survival signaling in early T cell precursor acute lymphoblastic leukemia, Cell Rep., 14, 1953, 10.1016/j.celrep.2016.01.064 Ernst, 2010, Inactivating mutations of the histone methyltransferase gene EZH2 in myeloid disorders, Nat. Genet., 42, 722, 10.1038/ng.621 Frelin, 2013, GATA-3 regulates the self-renewal of long-term hematopoietic stem cells, Nat. Immunol., 14, 1037, 10.1038/ni.2692 Gazit, 2014, Fgd5 identifies hematopoietic stem cells in the murine bone marrow, J. Exp. Med., 211, 1315, 10.1084/jem.20130428 Henriquez, 2013, Ezh1 and Ezh2 differentially regulate PSD-95 gene transcription in developing hippocampal neurons, Mol. Cell. Neurosci., 57, 130, 10.1016/j.mcn.2013.07.012 Hidalgo, 2012, Ezh1 is required for hematopoietic stem cell maintenance and prevents senescence-like cell cycle arrest, Cell Stem Cell, 11, 649, 10.1016/j.stem.2012.08.001 Howe, 2017, Is H3K4me3 instructive for transcription activation?, BioEssays, 39, 1, 10.1002/bies.201600095 Kamminga, 2006, The Polycomb group gene Ezh2 prevents hematopoietic stem cell exhaustion, Blood, 107, 2170, 10.1182/blood-2005-09-3585 Kim, 2007, Sox17 dependence distinguishes the transcriptional regulation of fetal from adult hematopoietic stem cells, Cell, 130, 470, 10.1016/j.cell.2007.06.011 Klauke, 2013, Polycomb Cbx family members mediate the balance between haematopoietic stem cell self-renewal and differentiation, Nat. Cell Biol., 15, 353, 10.1038/ncb2701 Kokkaliaris, 2016, Identification of factors promoting ex vivo maintenance of mouse hematopoietic stem cells by long-term single-cell quantification, Blood, 128, 1181, 10.1182/blood-2016-03-705590 Ku, 2012, GATA-3 regulates hematopoietic stem cell maintenance and cell-cycle entry, Blood, 119, 2242, 10.1182/blood-2011-07-366070 Kuzmichev, 2002, Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein, Genes Dev., 16, 2893, 10.1101/gad.1035902 Lara-Astiaso, 2014, Immunogenetics. Chromatin state dynamics during blood formation, Science, 345, 943, 10.1126/science.1256271 Laurenti, 2018, From haematopoietic stem cells to complex differentiation landscapes, Nature, 553, 418, 10.1038/nature25022 Lee, 2015, Polycomb repressive complex 2 component Suz12 is required for hematopoietic stem cell function and lymphopoiesis, Blood, 126, 167, 10.1182/blood-2014-12-615898 Lessard, 1999, Functional antagonism of the Polycomb-Group genes eed and Bmi1 in hemopoietic cell proliferation, Genes Dev., 13, 2691, 10.1101/gad.13.20.2691 Majewski, 2008, Polycomb repressive complex 2 (PRC2) restricts hematopoietic stem cell activity, PLoS Biol., 6, e93, 10.1371/journal.pbio.0060093 Margueron, 2008, Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms, Mol. Cell, 32, 503, 10.1016/j.molcel.2008.11.004 McCabe, 2012, EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations, Nature, 492, 108, 10.1038/nature11606 Miyamoto, 2007, Foxo3a is essential for maintenance of the hematopoietic stem cell pool, Cell Stem Cell, 1, 101, 10.1016/j.stem.2007.02.001 Mochizuki-Kashio, 2015, Ezh2 loss in hematopoietic stem cells predisposes mice to develop heterogeneous malignancies in an Ezh1-dependent manner, Blood, 126, 1172, 10.1182/blood-2015-03-634428 Mochizuki-Kashio, 2011, Dependency on the polycomb gene Ezh2 distinguishes fetal from adult hematopoietic stem cells, Blood, 118, 6553, 10.1182/blood-2011-03-340554 Moore, 1997, In vitro maintenance of highly purified, transplantable hematopoietic stem cells, Blood, 89, 4337, 10.1182/blood.V89.12.4337 Mousavi, 2012, Polycomb protein Ezh1 promotes RNA polymerase II elongation, Mol. Cell, 45, 255, 10.1016/j.molcel.2011.11.019 Muller, 2002, Histone methyltransferase activity of a Drosophila Polycomb group repressor complex, Cell, 111, 197, 10.1016/S0092-8674(02)00976-5 Neff, 2012, Polycomb repressive complex 2 is required for MLL-AF9 leukemia, Proc. Natl. Acad. Sci. U S A, 109, 5028, 10.1073/pnas.1202258109 Nikoloski, 2010, Somatic mutations of the histone methyltransferase gene EZH2 in myelodysplastic syndromes, Nat. Genet., 42, 665, 10.1038/ng.620 Qiu, 2014, Divisional history and hematopoietic stem cell function during homeostasis, Stem Cell Rep., 2, 473, 10.1016/j.stemcr.2014.01.016 Riddell, 2014, Reprogramming committed murine blood cells to induced hematopoietic stem cells with defined factors, Cell, 157, 549, 10.1016/j.cell.2014.04.006 Rodriguez-Fraticelli, 2018, Clonal analysis of lineage fate in native haematopoiesis, Nature, 553, 212, 10.1038/nature25168 Rosendaal, 1976, Haemopoietic stem cells are organised for use on the basis of their generation-age, Nature, 264, 68, 10.1038/264068a0 Rosendaal, 1979, Organization of haemopoietic stem cells: the generation-age hypothesis, Cell Tissue Kinet., 12, 17 Sawai, 2016, Hematopoietic stem cells are the major source of multilineage hematopoiesis in adult animals, Immunity, 45, 597, 10.1016/j.immuni.2016.08.007 Shen, 2008, EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency, Mol. Cell, 32, 491, 10.1016/j.molcel.2008.10.016 Shih, 2016, Developmental acquisition of regulomes underlies innate lymphoid cell functionality, Cell, 165, 1120, 10.1016/j.cell.2016.04.029 Signer, 2014, Haematopoietic stem cells require a highly regulated protein synthesis rate, Nature, 509, 49, 10.1038/nature13035 Stojic, 2011, Chromatin regulated interchange between polycomb repressive complex 2 (PRC2)-Ezh2 and PRC2-Ezh1 complexes controls myogenin activation in skeletal muscle cells, Epigenetics Chromatin, 4, 16, 10.1186/1756-8935-4-16 Sun, 2014, Epigenomic profiling of young and aged HSCs reveals concerted changes during aging that reinforce self-renewal, Cell Stem Cell, 14, 673, 10.1016/j.stem.2014.03.002 Trimarchi, 2002, Sibling rivalry in the E2F family, Nat. Rev. Mol. Cell Biol., 3, 11, 10.1038/nrm714 Velten, 2017, Human haematopoietic stem cell lineage commitment is a continuous process, Nat. Cell Biol., 19, 271, 10.1038/ncb3493 Vo, 2018, Regulation of embryonic haematopoietic multipotency by EZH1, Nature, 553, 506, 10.1038/nature25435 Walter, 2015, Exit from dormancy provokes DNA-damage-induced attrition in haematopoietic stem cells, Nature, 520, 549, 10.1038/nature14131 Wierstra, 2007, FOXM1, a typical proliferation-associated transcription factor, Biol. Chem., 388, 1257, 10.1515/BC.2007.159 Wilkinson, 2019, Long-term ex vivo haematopoietic-stem-cell expansion allows nonconditioned transplantation, Nature, 571, 117, 10.1038/s41586-019-1244-x Wilson, 2008, Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair, Cell, 135, 1118, 10.1016/j.cell.2008.10.048 Wilson, 2004, c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation, Genes Dev., 18, 2747, 10.1101/gad.313104 Wilson, 2015, Combined single-cell functional and gene expression analysis resolves heterogeneity within stem cell populations, Cell Stem Cell, 16, 712, 10.1016/j.stem.2015.04.004 Wu, 2001, The E2F1-3 transcription factors are essential for cellular proliferation, Nature, 414, 457, 10.1038/35106593 Xie, 2014, Polycomb repressive complex 2 regulates normal hematopoietic stem cell function in a developmental-stage-specific manner, Cell Stem Cell, 14, 68, 10.1016/j.stem.2013.10.001 Xu, 2015, Developmental control of polycomb subunit composition by GATA factors mediates a switch to non-canonical functions, Mol. Cell, 57, 304, 10.1016/j.molcel.2014.12.009 Xu, 2012, EZH2 oncogenic activity in castration-resistant prostate cancer cells is Polycomb-independent, Science, 338, 1465, 10.1126/science.1227604 Yalcin, 2008, Foxo3 is essential for the regulation of ataxia telangiectasia mutated and oxidative stress-mediated homeostasis of hematopoietic stem cells, J. Biol. Chem., 283, 25692, 10.1074/jbc.M800517200 Yamamoto, 2013, Clonal analysis unveils self-renewing lineage-restricted progenitors generated directly from hematopoietic stem cells, Cell, 154, 1112, 10.1016/j.cell.2013.08.007 Yan, 2016, EZH2 phosphorylation by JAK3 mediates a switch to noncanonical function in natural killer/T-cell lymphoma, Blood, 128, 948, 10.1182/blood-2016-01-690701 Zheng, 2015, Low-cell-number epigenome profiling aids the study of lens aging and hematopoiesis, Cell Rep., 13, 1505, 10.1016/j.celrep.2015.10.004