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Opposing roles of polycomb repressive complexes in hematopoietic stem and progenitor cells
Abstract
Polycomb group (PcG) proteins are transcriptional repressors with a central role in the establishment and maintenance of gene expression patterns during development. We have investigated the role of polycomb repressive complexes (PRCs) in hematopoietic stem cells (HSCs) and progenitor populations. We show that mice with loss of function mutations in PRC2 components display enhanced HSC/progenitor population activity, whereas mutations that disrupt PRC1 or pleiohomeotic repressive complex are associated with HSC/progenitor cell defects. Because the hierarchical model of PRC action would predict synergistic effects of PRC1 and PRC2 mutation, these opposing effects suggest this model does not hold true in HSC/progenitor cells. To investigate the molecular targets of each complex in HSC/progenitor cells, we measured genome-wide expression changes associated with PRC deficiency, and identified transcriptional networks that are differentially regulated by PRC1 and PRC2. These studies provide new insights into the mechanistic interplay between distinct PRCs and have important implications for approaching PcG proteins as therapeutic targets.
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“applying genas to a microarray study looking at the relationship between polycomb repressor complex (PRC) 1 and PRC2 facilitated the discovery of the opposing roles of these two complexes (51).”
From limma powers differential expression analyses for RNA-sequencing and microarray studies (2015) · cites this paper as [51]
In the citing paper
“EZH2, EED, or SUZ12 loss-of-function mutations are related to the increased activity of hematologic stem cells (HSCs) and progenitor cells [153].”
From Proteolysis targeting chimeras (PROTACs) are emerging therapeutics for hematologic malignancies (2020) · cites this paper as [153]
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limma powers differential expression analyses for RNA-sequencing and microarray studies
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“For instance, applying genas to a microarray study looking at the relationship between polycomb repressor complex (PRC) 1 and PRC2 facilitated the discovery of the opposing roles of these two complexes (51).”
MethodSiddiqui, I., Schaeuble, K., Chennupati, V., Fuertes Marraco, S. A., Calderon-Copete, S., Pais Ferreira, D., Carmona, S. J., Scarpellino, L., Gfeller, D., Pradervand, S., et al. (2019) · Immunity · doi:10.1016/j.immuni.2018.12.021 · Cited by 1,679
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“Majewski et al. (2008, 2010) studied mice with a mutation in the Suz12 gene that results in loss of function of the Suz12 protein and hence PRC2.”
BackgroundChase, A., & Cross, N. C. P. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-2156 · Cited by 563
“In HSCs, however, there is evidence for opposing roles for PRC1 and PRC2 (10–13).”
BackgroundInfluentialMcCabe, M. T., Graves, A. P., Ganji, G., Diaz, E., Halsey, W. S., Jiang, Y., Smitheman, K. N., Ott, H. M., Pappalardi, M. B., Allen, K. E., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1116418109 · Cited by 511
“In fact, multiple groups have shown that EZH2 plays an important role in the maintenance of hematopoietic stem cells (HSCs) and progenitor cells (13, 14).”
BackgroundAging of hematopoietic stem cells
de Haan, G., & Lazare, S. S. (2018) · Blood · doi:10.1182/blood-2017-06-746412 · Cited by 432
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“Similar approaches have suggested that Polycomb repressive complex-1 (PRC1 [Bmi-1 PRC1]) is antagonistic to PRC2 in HSC proliferation (Majewski et al., 2010).”
BackgroundGenome-wide remodeling of the epigenetic landscape during myogenic differentiation
Asp, P., Blum, R., Vethantham, V., Parisi, F., Micsinai, M., Cheng, J., Bowman, C., Kluger, Y., & Dynlacht, B. D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102223108 · Cited by 324
“Interestingly, recent studies suggest that PRC1 and PRC2 may also play opposing roles in hematopoietic stem cell differentiation, wherein they appear to regulate distinct sets of genes (30).”
BackgroundUnraveling the Molecular Pathophysiology of Myelodysplastic Syndromes
Bejar, R. L., Levine, R. L., & Ebert, B. L. (2011) · Journal of Clinical Oncology · doi:10.1200/jco.2010.31.1175 · Cited by 309
A key role for EZH2 and associated genes in mouse and human adult T-cell acute leukemia
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“We (Lessard et al. 1999) and others (Richie et al. 2002; Majewski et al. 2008, 2010) have shown that PRC2 restricts the activity of hemopoietic progenitor/stem cells and that heterozygosity for mutant Eed alleles accelerates lymphomagenesis (Sauvageau et al. 2008).”
BackgroundIL-1R8 is a checkpoint in NK cells regulating anti-tumour and anti-viral activity
Molgora, M., Bonavita, E., Ponzetta, A., Riva, F., Barbagallo, M., Jaillon, S., Popović, B., Bernardini, G., Magrini, E. I., Gianni, F., et al. (2017) · Nature · doi:10.1038/nature24293 · Cited by 228
Epigenetic control of adult stem cell function
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Dependency on the polycomb gene Ezh2 distinguishes fetal from adult hematopoietic stem cells
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Role of the Polycomb Repressive Complex 2 (PRC2) in Transcriptional Regulation and CancerPreprint
Laugesen, A., Højfeldt, J. W., & Helin, K. (2016) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a026575 · Cited by 225
HematopoiesisPreprint
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“…2007; Challen et al. 2011 Bmi-1 (PRC1) Loss reduces SR, expression increases SR Lessard and Sauvageau 2003; Park et al. 2003; Iwama et al. 2004 Suz12 (PRC2) Loss increases SR Majewski et al. 2010 Ezh2 (PRC2) Expression enhances SR, loss reduces SR (mainly in fetal liver) Herrera-Merchan et al. 2012”
BackgroundRegulation of proteolysis by human deubiquitinating enzymes
Eletr, Z. M., & Wilkinson, K. D. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.06.027 · Cited by 191
“PcG proteins assemble to form three distinct complexes in Drosophila, PhoRC, PRC1 and PRC2 [149-151].”
BackgroundInfluentialDowling, J. K., Afzal, R., Gearing, L. J., Cervantes‐Silva, M. P., Annett, S., Davis, G. M., Santi, C. D., Aßmann, N., Dettmer, K., Gough, D. J., et al. (2020) · Nature Communications · doi:10.1038/s41467-021-21617-2 · Cited by 178
Epigenetics of hematopoiesis and hematological malignanciesPreprint
Hu, D., & Shilatifard, A. (2016) · Genes & Development · doi:10.1101/gad.284109.116 · Cited by 175
“Several studies have shown that PRC2 restricts HSC activity, as a partial loss of the core components such as Ezh2, Eed, or Suz12 inmice enhances HSC function (Majewski et al. 2008, 2010).”
BackgroundHoffman, G. E., Hartley, B. J., Flaherty, E. K., Ladran, I., Gochman, P., Ruderfer, D. M., Stahl, E. A., Rapoport, J. L., Sklar, P. B., & Brennand, K. (2017) · Nature Communications · doi:10.1038/s41467-017-02330-5 · Cited by 162
EMF1 and PRC2 Cooperate to Repress Key Regulators of Arabidopsis Development
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“However, there are also genomic sites bound by one, but not the other, PRC [12] and transcriptional networks differentially regulated by PRC1 and PRC2 [13].”
InfluentialMicallef, I. N., Maurer, M. J., Wiseman, G. A., Nikcevich, D. A., Kurtin, P. J., Cannon, M. W., Pérez, D. G., Soori, G. S., Link, B. K., Habermann, T. M., et al. (2011) · Blood · doi:10.1182/blood-2011-02-336990 · Cited by 138
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Proteolysis targeting chimeras (PROTACs) are emerging therapeutics for hematologic malignancies
He, Y., Khan, S., Huo, Z., Lv, D., Zhang, X., Liu, X., Yuan, Y., Hromas, R., Xu, M., Zheng, G., et al. (2020) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-00924-z · Cited by 126
“As PRC2 is highly associated with hematopoietic differentiation and proliferation [152], EZH2, EED, or SUZ12 loss-of-function mutations are related to the increased activity of hematologic stem cells (HSCs) and progenitor cells [153].”
BackgroundA complex Polycomb issue: the two faces of EZH2 in cancerPreprint
Hock, H. R. (2012) · Genes & Development · doi:10.1101/gad.191163.112 · Cited by 124
“Specifically, loss of Bmi1 (PRC1) severely compromises stem cell function, while heterozygous loss of several PRC2 components was reported to enhance stem and progenitor cell activity (Lessard et al. 1999; Lessard and Sauvageau 2003; Majewski et al. 2010).”
BackgroundEZH2 function in immune cell development
Nutt, S. L., Keenan, C. R., Chopin, M., & Allan, R. S. (2020) · Biological Chemistry · doi:10.1515/hsz-2019-0436 · Cited by 110
EZH2 in normal hematopoiesis and hematological malignancies
Herviou, L., Cavalli, G., Cartron, G., Klein, B., & Moreaux, J. (2015) · Oncotarget · doi:10.18632/oncotarget.6198 · Cited by 113
“As EZH2, EED or SUZ12 loss-of-function mutations increase the activity of hematopoietic stem cells (HSCs) and progenitor cells, PRC2 could contribute to their negative control [20].”
BackgroundLee, S. C.-W., Miller, S., Hyland, C. D., Kauppi, M., Lebois, M., Rago, L. D., Metcalf, D., Kinkel, S., Josefsson, E. C., Blewitt, M. E., et al. (2015) · Blood · doi:10.1182/blood-2014-12-615898 · Cited by 105
Epigenetic control of natural killer cell maturation by histone H2A deubiquitinase, MYSM1
Nandakumar, V., Chou, Y., Zang, L., Huang, X. F., & Chen, S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1308888110 · Cited by 98
“Ring1B also enhances the survival of Th2 effector cells by inhibiting apoptosis (16).”
BackgroundHematopoietic Stem Cell Development
Cullen, S. M., Mayle, A., Rossi, L., & Goodell, M. A. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416022-4.00002-0 · Cited by 98
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Jarid2 regulates mouse epidermal stem cell activation and differentiation
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“Deletion of Ezh2 causes defects in proliferation and differentiation of haematopoietic, pancreatic, and brain progenitors (Su et al, 2003; Chen et al, 2009; Majewski et al, 2010; Pereira et al, 2010).”
BackgroundPolycomb/Trithorax Antagonism: Cellular Memory in Stem Cell Fate and Function
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MicroRNA-218 inhibits EMT, migration and invasion by targeting SFMBT1 and DCUN1D1 in cervical cancer
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“SFMBT1 belongs to the malignant brain tumor (MBT) domain-containing protein family, which contributes to multiple cellular processes, including cell proliferation [29] and maintenance of the characteristics of stem cells [30].”
Epigenetic dysregulation in glioma
Kondo, Y., Katsushima, K., Ohka, F., Natsume, A., & Shinjo, K. (2014) · Cancer Science · doi:10.1111/cas.12379 · Cited by 73
Histone proteolysis: A proposal for categorization into ‘clipping’ and ‘degradation’
Dhaenens, M., Glibert, P., Meert, P., Vossaert, L., & Deforce, D. L. D. (2014) · BioEssays · doi:10.1002/bies.201400118 · Cited by 70
A microRNA Encoded by Kaposi Sarcoma-Associated Herpesvirus Promotes B-Cell Expansion In Vivo
Dahlke, C., Maul, K., Christalla, T., Walz, N., Schult, P., Stocking, C., & Grundhoff, A. T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049435 · Cited by 67
“Besides of its key role in the suppression of differentiation genes in embryonic stem cells, PRC2 has been found to restrict the activity of hematopoietic stem and precursor cells [75–77].”
BackgroundRinke, J., Chase, A., Cross, N. C. P., Hochhaus, A., & Ernst, T. (2020) · Cells · doi:10.3390/cells9071639 · Cited by 71
“This is indicated by the presence of different gene expression signatures and the induction of cell defects or enhanced population activity upon PRC1 or PRC2 abrogation, respectively [7].”
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“Gene expression enrichment for functional categories was performed on the Log2-CPM RNA-Seq data using the Romer procedure as implemented in limma with 9,999 rotations, correcting for batch effects between experiments (76, 77).”
MethodWhole Genome Expression Differences in Human Left and Right Atria Ascertained by RNA Sequencing
Hsu, J., Hanna, P., Wagoner, D. R. V., Barnard, J., Serre, D., Chung, M. K., & Smith, J. D. (2012) · Circulation Cardiovascular Genetics · doi:10.1161/circgenetics.111.961631 · Cited by 62
Notch controls the magnitude of T helper cell responses by promoting cellular longevity
Helbig, C., Gentek, R., Backer, R. A., de Souza, Y., Derks, I. A. M., Eldering, E., Wagner, K., Jankovic, D. L., Gridley, T., Moerland, P. D., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1206044109 · Cited by 62
“We made use of the rotation testing using mean ranks (ROMER) method for gene-set enrichment analysis (22), using gene sets representing biological pathways (C2) or gene ontology categories (C5) from MSigDB (http://www.”
Polycomb complexes in normal and malignant hematopoiesis
Carlo, V. D., Mocavini, I., & Croce, L. D. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201808028 · Cited by 66
Polycomb-group proteins in hematopoietic stem cell regulation and hematopoietic neoplasms
Radulović, V., de Haan, G., & Klauke, K. (2012) · Leukemia · doi:10.1038/leu.2012.368 · Cited by 62
Transcriptional Regulation of Haematopoietic Stem Cells
Wilkinson, A. C., & Göttgens, B. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-6621-1_11 · Cited by 63
“PcG proteins form two discrete complexes, polycomb repressive complex 1 and 2 (PRC1 and PRC2), which have distinct enzymatic activity (H2AK119 monoubiquitination and H3K27 trimethylation activities respectively) and discrete functions in HSCs [ 163 ] .”
BackgroundPolycomb repressive complexes in hematological malignancies
Iwama, A. (2017) · Blood · doi:10.1182/blood-2017-02-739490 · Cited by 55
Jarid2 regulates hematopoietic stem cell function by acting with polycomb repressive complex 2
Kinkel, S., Galeev, R., Flensburg, C., Keniry, A., Breslin, K. A., Gilan, O., Lee, S. C.-W., Liu, J. J., Chen, K., Gearing, L. J., et al. (2015) · Blood · doi:10.1182/blood-2014-10-603969 · Cited by 54
“5 fetal liver (FL) cell transduction and transplantation were performedasdescribed.(26,27)Lethally irradiated (11Gy) secondary transplant recipients were injected with 1 to 3 million BM cells isolated from FL primary recipients, 2 or 3 recipients per donor.”
BackgroundMethodPolycomb Group Protein YY1 Is an Essential Regulator of Hematopoietic Stem Cell Quiescence
Lu, Z., Hong, C. C., Kong, G., Assumpção, A. L. F. V., Ong, I. M., Bresnick, E. H., Zhang, J., & Pan, X. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.01.026 · Cited by 56
“Competitive bone marrow transplantation of Yy1+/− Mpl+/+ fetal liver cells suggested that Yy1+/−cells might have a compromised capacity to maintain the stem cell pool (Majewski et al., 2010).”
BackgroundGatzka, M., Tasdogan, A., Hainzl, A., Allies, G., Maity, P., Wilms, C., Wlaschek, M., & Scharffetter‐Kochanek, K. (2015) · Cell Death and Differentiation · doi:10.1038/cdd.2014.231 · Cited by 48
“inhibits the SWI/SNF–chromatin remodeling complex, are established regulators of hematopoietic stem cell (HSC) maintenance and T-cell development.(12,13) In a heterodimetric”
BackgroundPolycomb: a paradigm for genome organization from one to three dimensions
Delest, A., Sexton, T., & Cavalli, G. (2012) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2012.01.008 · Cited by 47
“However, this model does not explain the regions of H3K27me3 deposition that are devoid of PcG proteins, or the different phenotypic effects in perturbing different PcG proteins [20 ,21–23].”
BackgroundEstablishment of epigenetic patterns in development
Leeb, M., & Wutz, A. (2012) · Chromosoma · doi:10.1007/s00412-012-0365-x · Cited by 46
“associated with distinct and opposing outcomes in stem cell proliferation and differentiation (Majewski et al. 2010).”
BackgroundPolycomb complexes redundantly maintain epidermal stem cell identity during development
Cohen, I., Bar, C., Liu, H., Valdes, V. J., Zhao, D., Galbo, P. M., Silva, J. M., Koseki, H., Zheng, D., & Ezhkova, E. (2021) · Genes & Development · doi:10.1101/gad.345363.120 · Cited by 45
Boucai, L., Saqcena, M., Kuo, F., Grewal, R. K., Socci, N. D., Knauf, J. A., Krishnamoorthy, G. P., Ryder, M. M., Ho, A. L., Ghossein, R. A., et al. (2023) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-22-2882 · Cited by 40
G-CSF-activated STAT3 enhances production of the chemokine MIP-2 in bone marrow neutrophils
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“PRC2 has important roles in stem and progenitor function in the hematopoietic system [79, 80], yet little is known about its regulation or activity throughout neutrophil development.”
BackgroundPoplar Wood Rays Are Involved in Seasonal Remodeling of Tree Physiology
Larisch, C., Dittrich, M. T., Wildhagen, H., Lautner, S., Fromm, J. H., Polle, A., Hedrich, R., Rennenberg, H., Müller, T., & Ache, P. (2012) · PLANT PHYSIOLOGY · doi:10.1104/pp.112.202291 · Cited by 39
“The ROMER analysis thus served to directly extend the classical gene-wise Student’s t test to the analysis of entire pathways, and this greatly facilitated the biological interpretation of the obtained results.”
InfluentialNew developments in the management of diffuse large B-cell lymphoma
Habermann, T. M. (2012) · Hematology · doi:10.1179/102453312x13336169156014 · Cited by 37
Epigenetic regulation of adult stem cell function
Rinaldi, L., & Benitah, S. A. (2014) · FEBS Journal · doi:10.1111/febs.12946 · Cited by 38
Early Lineage Priming by Trisomy of Erg Leads to Myeloproliferation in a Down Syndrome Model
Ng, A. P., Hu, Y., Metcalf, D., Hyland, C. D., Ierino, H., Phipson, B., Wu, D., Baldwin, T. M., Kauppi, M., Kiu, H., et al. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005211 · Cited by 33
“Genuine Association analysis [37] used the genas function of the limma package.”
BackgroundMethodKaramitros, D., Patmanidi, A. L., Kotantaki, P., Potocnik, A. J., Bähr-Ivacevic, T., Beneš, V., Lygerou, Z., Kioussis, D., & Taraviras, S. L. (2014) · Development · doi:10.1242/dev.109454 · Cited by 34
“A plausible hypothesis is that geminin participates in a specific composition of the PcG complex (Majewski et al., 2010) and could modify signals mediated by Polycomb and Trithorax for some of their targets genes (Schwartz et al., 2010), leading to aberrant or untimely expression in the absence of…”
Eschbaumer, M., Stenfeldt, C., Smoliga, G. R., Pacheco, J. M., Rodrı́guez, L. L., Li, R. W., Zhu, J. J., & Arzt, J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0162750 · Cited by 32
“In addition, the biological correlation between the differential gene expression in non-vaccinated and vaccinated animals was calculated by separating the biological from the technical components of the correlation [120] .”
Polycomb repressive complex 2 (PRC2) suppresses Eμ-myc lymphoma
Lee, S. C.-W., Phipson, B., Hyland, C. D., Leong, H. S., Allan, R. S., Lun, A. T. L., Hilton, D. J., Nutt, S. L., Blewitt, M. E., Smyth, G. K., et al. (2013) · Blood · doi:10.1182/blood-2013-02-484055 · Cited by 29
“Cells were stained with monoclonal antibodies to B220 [RA3-6B2], CD19 [1D3], CD25 [PC61], c-Kit [2B8], IgM [II/41], IgD [11-26], Mac-1 [M1- 5 70], Gr-1 [RB6-8C5], Ter119 [Ter119], CD4 [GK1.”
MethodPolycomb Directed Cell Fate Decisions in Development and Cancer
German, B., & Ellis, L. (2022) · Epigenomes · doi:10.3390/epigenomes6030028 · Cited by 34
“In adult stem cells, PRC complexes maintain their HSC identity, suppressing lineage-specific gene expression [166,167], but the heterozygous depletion of EZH2, SUZ12, or EED increases hematopoietic stem progenitor cell (HSPC) activity [143,168].”
BackgroundYong, A. S. M., Stephens, N., Weber, G., Yixin, L. I., Savani, B. N., Eniafe, R. B., Keyvanfar, K., Kurlander, R. J., Rezvani, K., & Barrett, A. J. (2011) · Leukemia · doi:10.1038/leu.2010.325 · Cited by 31
“Recent transgenic mouse studies dissecting the function of individual members of polycomb repressive complexes (PRC) found that the relationship between BMI-1 and EZH2 (components of PRC1 and PRC2 respectively) is not necessarily hierarchical in hematopoietic stem cells (38).”
Saputra, E., Kowalczyk, A., Cusick, L., Clark, N., & Chikina, M. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab068 · Cited by 41
Clonal Hematopoiesis and Mutations of Myeloproliferative Neoplasms
Kjær, L. (2020) · Cancers · doi:10.3390/cancers12082100 · Cited by 30
“During healthy hematopoiesis, HSCs give rise to highly polyclonal cell populations.”
BackgroundInfluentialEpigenetic regulation of hematopoietic stem cell homeostasis
Jiang, P., Wang, H., Zheng, J., Han, Y., Huang, H., & Qian, P. (2019) · Blood Science · doi:10.1097/bs9.0000000000000018 · Cited by 29
“Majewski et al reported that heterozygous mutation in PRC2 components, Ezh2, Eed, or Suz12, promoted HSPC differentiation, and enhanced reconstitution ability in transplantation assay, implying that PRC2 functions as negative regulator of HSC activity and keeps them in quiescent state.(37) However, overexpression of E…”
BackgroundDetection of Simultaneous Group Effects in MicroRNA Expression and Related Target Gene Sets
Artmann, S., Jung, K., Bleckmann, A., & Beißbarth, T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038365 · Cited by 25
“In addition, we employ a rotation test, that is the competitive ‘Romer’ test [24].”
MethodSantis, C. D., Crampton, V. O., Bicskei, B., & Tocher, D. R. (2015) · Comparative Biochemistry and Physiology Part D Genomics and Proteomics · doi:10.1016/j.cbd.2015.07.005 · Cited by 24
“The algorithm also allowed discriminating true biological correlation (ρbiol) from technical correlation (ρtech) (Majewski et al., 2010).”
BackgroundBerisha, S. Z., Hsu, J., Robinet, P., & Smith, J. D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065003 · Cited by 24
“The romer function in the limma package was used to test for gene set enrichment analysis [24,25] with the Molecular Signature Database from the Broad Institute as gene sets [26].”
MethodThe role of histone methyltransferase EZH2 in myelodysplastic syndromes
Xu, F., & Li, X. (2012) · Expert Review of Hematology · doi:10.1586/ehm.12.5 · Cited by 22
MOZ and BMI1 act synergistically to maintain hematopoietic stem cells
Sheikh, B. N., Metcalf, D., Voss, A. K., & Thomas, T. (2016) · Experimental Hematology · doi:10.1016/j.exphem.2016.10.006 · Cited by 24
Li, R., Qiao, M., Zhao, X., Yan, J., Wang, X., & Sun, Q. (2018) · Cellular Signalling · doi:10.1016/j.cellsig.2018.06.003 · Cited by 21
“SFMBT1 belongs to the malignant brain tumor (MBT) domain-containing protein family, which contributes to multiple cellular processes, including cell proliferation and maintenance of the characteristics of stem cells [28-30].”
BackgroundLi, Z., Cheng, D., Mon, H., Tatsuke, T., Zhu, L., Xu, J. C., Lee, J. M., Xia, Q., & Kusakabe, T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034330 · Cited by 19
“For instance, a study in mouse hematopoietic stem cells has revealed an opposite role mediated by PRC1 and PRC2 complexes based on the expression microarray analyses after mutating of different Polycomb components [17].”
BackgroundAmbivalent role of pFAK-Y397 in serous ovarian cancer-a study of the OVCAD consortium
Aust, S., Auer, K., Bachmayr-Heyda, A., Denkert, C., Sehouli, J., Braicu, I., Mahner, S., Lambrechts, S., Vergote, I., Grimm, C., et al. (2014) · Molecular Cancer · doi:10.1186/1476-4598-13-67 · Cited by 17
“org/gsea/) was performed with the romer function [27] from the R-package limma v3.”
MethodMcAdams, R. M., McPherson, R. J., Beyer, R. P., Bammler, T. K., Farin, F. M., & Juul, S. E. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123047 · Cited by 18
Odenike, O. M., Anastasi, J., & Beau, M. M. L. (2011) · Clinics in Laboratory Medicine · doi:10.1016/j.cll.2011.08.005 · Cited by 20
Stem cells: A view from the roots
Somorjai, I., Lohmann, J. U., Holstein, T. W., & Zhao, Z. (2012) · Biotechnology Journal · doi:10.1002/biot.201100349 · Cited by 16
BAF complex-mediated chromatin relaxation is required for establishment of X chromosome inactivation
Keniry, A., Jansz, N., Gearing, L. J., Wanigasuriya, I., Chen, J., Nefzger, C. M., Hickey, P. F., Gouil, Q. A., Liu, J. J., Breslin, K. A., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29333-1 · Cited by 18
Emerging role of EZH2 in rheumatic diseases: A comprehensive review
Xu, W., Huang, Q., & Huang, A. (2022) · International Journal of Rheumatic Diseases · doi:10.1111/1756-185x.14416 · Cited by 16
Dual role of EZH2 in megakaryocyte differentiation
Mazzi, S., Dessen, P., Vieira, M., Dufour, V., Cambot, M., El-Khoury, M., Antony‐Debré, I., Arkoun, B., Basso‐Valentina, F., BenAbdoulahab, S., et al. (2021) · Blood · doi:10.1182/blood.2019004638 · Cited by 16
Dianhydrogalactitol Overcomes Multiple Temozolomide Resistance Mechanisms in Glioblastoma
Jiménez-Alcázar, M., Curiel‐García, Á., Nogales, P., Perales-Patón, J., Schuhmacher, A. J., Galán-Ganga, M., Zhu, L., Lowe, S. W., Al‐Shahrour, F., & Squatrito, M. (2021) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-20-0319 · Cited by 15
“The sScore and RiScore were obtained using the ROMER and ROAST methods (22, 23), respectively.”
MethodBleckmann, A., Leha, A., Artmann, S., Menck, K., Salinas, G., Binder, C. R., Pukrop, T., Beißbarth, T., & Klemm, F. (2014) · Molecular Oncology · doi:10.1016/j.molonc.2014.07.023 · Cited by 15
Whole genome RNAi screens reveal a critical role of REV3 in coping with replication stress
Kotov, I. N., Olst, E. S., Knobel, P. A., van der Meulen‐Muileman, I. H., Felley‐Bosco, E., van Beusechem, V. W., Smit, E. F., Stahel, R. A., & Marti, T. M. (2014) · Molecular Oncology · doi:10.1016/j.molonc.2014.07.008 · Cited by 15
Becker, M., Potapenko, T., Niklaus, A. L., Bieback, K., Ho, A. D., & Müller, A. M. (2016) · Stem Cells and Development · doi:10.1089/scd.2015.0277 · Cited by 14
“Opposing roles for PRC1 and PRC2 have also been reported in hematopoietic stem and progenitor cells [58].”
EZH2 identifies the precursors of human natural killer cells with trained immunity
Zhang, C., Yin, J., Zheng, J., Xiao, J. H., Hu, J., Su, Y., Zhou, K., Zhang, Y., Zhang, X., Zhang, H., et al. (2021) · Cancer Biology and Medicine · doi:10.20892/j.issn.2095-3941.2020.0791 · Cited by 15
“EZH2 plays a major role in hematopoiesis by promoting pluripotency maintenance and self-renewal of adult stem cells 20-22 .”
Li, Z., Cheng, D., Mon, H., Zhu, L., Xu, J. C., Tatsuke, T., Lee, J. M., Xia, Q., & Kusakabe, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0052320 · Cited by 14
“This case of the BmASNS gene in Bombyx is in agreement with the negative correlation of PcG proteins and C/ebp on target gene expression in mouse [21], and therefore suggests a common model in which most target genes orchestrated by PcG complexes tend to be cooperatively regulated by the C/ebp protein.”
BackgroundInfluentialFlinders, C., Lam, L., Rubbi, L., Ferrari, R., Fitz‐Gibbon, S. T., Chen, P., Thompson, M. J., Christofk, H. R., Agus, D. B., Ruderman, D., et al. (2016) · Genome Medicine · doi:10.1186/s13073-016-0305-0 · Cited by 14
“hematopoietic stem cells to differentiation [30, 31, 39].”
Yin Yang 1 regulates cohesin complex protein SMC3 in mouse hematopoietic stem cells
Lu, Z., Wang, Y., Assumpção, A. L. F. V., Liu, P., Kopp, A., Saka, S., McIlwain, S. J., Viny, A. D., Brand, M., & Pan, X. (2024) · Blood Advances · doi:10.1182/bloodadvances.2023011411 · Cited by 15
Oberin, R., Petautschnig, S., Jarred, E. G., Qu, Z., Tsai, T., Youngson, N. A., Pulsoni, G., Truong, T. T., Fernando, D., Bildsoe, H., et al. (2024) · eLife · doi:10.7554/elife.81875 · Cited by 13
“…of Eed, Ezh2, or Suz12 result in altered patterning and organ function in a range of tissues ( Pasini et al., 2004 ; Prokopuk et al., 2018 ; Boyer et al., 2006 ; Hemming et al., 2014 ; Dudakovic et al., 2015 ; Majewski et al., 2010 ; Liu et al., 2019 ; Sun et al., 2018 ; Miao et al., 2020 ).”
BackgroundThe Mutational Landscape of Myeloid Leukaemia in Down Syndrome
de Castro, C. P. M., Cadefau-Fabregat, M., & Cuartero, S. (2021) · Cancers · doi:10.3390/cancers13164144 · Cited by 16
Bret, C., Viziteu, E., Kassambara, A., & Moreaux, J. (2016) · Expert Review of Hematology · doi:10.1586/17474086.2016.1141673 · Cited by 13
“(HSC) and progenitors self-renewal activity [107].”
Insights into high-risk multiple myeloma from an analysis of the role of PHF19 in cancer
Ghamlouch, H., Boyle, E. M., Blaney, P., Wang, Y., Choi, J., Williams, L. S., Bauer, M., Auclair, D., Bruno, B., Walker, B. A., et al. (2021) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-02185-1 · Cited by 12
“Although it is difficult to compare data on hematopoiesis between different transgenic mice models of PRC2component loss (i.e. the developmental stage at which the KO is induced using Cre), the impact of Phf19-loss on HSCs shows some differences by comparison with published results for other PRC2 subunits [9, 57–60].”
BackgroundInfluentialDC immunotherapy in HIV-1 infection induces a major blood transcriptome shift
de Goede, A. L., Andeweg, A. C., van den Ham, H., Bijl, M., Zaaraoui‐Boutahar, F., van IJcken, W. F. J., Wilgenhof, S., Aerts, J. L., Gruters, R. A., Osterhaus, A. D. M. E., et al. (2015) · Vaccine · doi:10.1016/j.vaccine.2015.04.047 · Cited by 12
Huang, L., Li, F., Ye, L., Yu, F., & Wang, C. (2023) · Cell Proliferation · doi:10.1111/cpr.13413 · Cited by 11
Zhan, Y., Zhang, Y., Zhang, S., Coughlan, H. D., Baldoni, P. L., Jacquelot, N., Cao, W. H. J., Preston, S., Louis, C., Rautela, J., et al. (2021) · Science Immunology · doi:10.1126/sciimmunol.abf7268 · Cited by 12
“However, it should be noted that the partial reduction of PRC2 activity can lead to very different outcomes, such as the increased self-renewal activity observed in HSCs (59, 60) and myeloid malignancies (27, 61).”
BackgroundConducting gene set tests in meta‐analyses of transcriptome expression data
Kosch, R., & Jung, K. (2018) · Research Synthesis Methods · doi:10.1002/jrsm.1337 · Cited by 9
Empirical Bayes in the presence of exceptional cases, with application to microarray dataPreprint
Phipson, B., Lee, S., Majewski, I. J., Alex, W. S., & Smyth, G. K. (2013) · Cited by 9
A Decision‐Theory Approach to Interpretable Set Analysis for High‐Dimensional Data
Boca, S. M., Bravo, H. C., Caffo, B. S., Leek, J. T., & Parmigiani, G. (2013) · Biometrics · doi:10.1111/biom.12060 · Cited by 8
“We carried out simulations which compared our method to two representative testing methods which are in the limma package in R (Smyth, 2004): roast (Wu et al., 2010) and romer (Majewski et al., 2010).”
Heterochromatin and Polycomb as regulators of haematopoiesis
Keenan, C. R. (2021) · Biochemical Society Transactions · doi:10.1042/bst20200737 · Cited by 9
Varagnolo, L., Lin, Q., Obier, N., Plass, C., Dietl, J., Zenke, M., Claus, R., & Müller, A. M. (2015) · Scientific Reports · doi:10.1038/srep12319 · Cited by 7
Polycomb group proteins in hematopoietic stem cell aging and malignancies
Klauke, K., & de Haan, G. (2011) · International Journal of Hematology · doi:10.1007/s12185-011-0857-0 · Cited by 8
“Hox genes such as HoxB4 and HoxA9, cell cycle-related genes such as p21, p27, cyclin D2, Geminin, and cdc6, C/EBPa target genes, and lineage developmental regulator genes (Pax5 and Ebf1) have all been suggested as being direct PcG targets in HSCs [66, 75, 78, 95, 96].”
Background
Metadata
- Authors
- Majewski, I. J., Ritchie, M. E., Phipson, B., Corbin, J., Pakusch, M., Ebert, A., Busslinger, M., Koseki, H., Hu, Y., Smyth, G. K., Alexander, W. S., Hilton, D. J., & Blewitt, M. E.
- Affiliations
- Molecular Medicine Division,
- Walter and Eliza Hall Institute of Medical Research (AU)
- Research Institute of Molecular Pathology (AT)
- RIKEN (JP)
- The University of Melbourne (AU)
- ORCID
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 2010-08-05
- Volume
- 116
- Issue
- 5
- Pages
- 731-739
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- OpenAlex
- W2046417042
- Cited by
- 135
- References
- 54
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 3 · 2023: 8 · 2022: 4 · 2021: 12 · 2020: 4 · 2019: 4 · 2018: 7 · 2017: 4 · 2016: 13 · 2015: 12 · 2014: 11 · 2013: 13 · 2012: 22
- FWCI
- 9.21
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Blood (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- polycomb repressive complex, hematopoietic stem cells, hematopoietic progenitor cells, PRC1, polycomb repressive complex 2, transcriptional repression, gene expression profiling, transcriptional regulatory networks, loss-of-function mutations
- MeSH terms
- Enhancer of Zeste Homolog 2 Protein, Animals, Hematopoietic Stem Cells, Mice, Inbred C57BL, Mutation, Phenotype, Histone-Lysine N-Methyltransferase, Radiation Chimera, Repressor Proteins, Stem Cells, Transcription, Genetic, Bone Marrow Transplantation, Gene Expression Regulation, Developmental, Gene Expression Profiling, RNA Interference, Multiprotein Complexes, YY1 Transcription Factor, Mice, Gene Knockdown Techniques, Polycomb-Group Proteins, Polycomb Repressive Complex 2
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