Nuclear interacting SET domain protein 1 inactivation impairs GATA1-regulated erythroid differentiation and causes erythroleukemia.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
12 06 2020
Historique:
received: 08 08 2019
accepted: 17 04 2020
entrez: 14 6 2020
pubmed: 14 6 2020
medline: 19 8 2020
Statut: epublish

Résumé

The nuclear receptor binding SET domain protein 1 (NSD1) is recurrently mutated in human cancers including acute leukemia. We show that NSD1 knockdown alters erythroid clonogenic growth of human CD34

Identifiants

pubmed: 32533074
doi: 10.1038/s41467-020-16179-8
pii: 10.1038/s41467-020-16179-8
pmc: PMC7293310
doi:

Substances chimiques

Antigens, CD 0
Antigens, CD34 0
CD71 antigen 0
Chromatin 0
DNA-Binding Proteins 0
GATA1 Transcription Factor 0
Proto-Oncogene Proteins 0
RNA, Messenger 0
Receptors, Transferrin 0
SKI protein, human 126648-96-2
Histone-Lysine N-Methyltransferase EC 2.1.1.43
NSD1 protein, human EC 2.1.1.43
Nsd1 protein, mouse EC 2.1.1.43
Proto-Oncogene Proteins c-kit EC 2.7.10.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2807

Références

Hattangadi, S. M., Wong, P., Zhang, L., Flygare, J. & Lodish, H. F. From stem cell to red cell: regulation of erythropoiesis at multiple levels by multiple proteins, RNAs, and chromatin modifications. Blood 118, 6258–6268 (2011).
pubmed: 21998215 pmcid: 3236116 doi: 10.1182/blood-2011-07-356006
Kerenyi, M. A. & Orkin, S. H. Networking erythropoiesis. J. Exp. Med. 207, 2537–2541 (2010).
pubmed: 21098097 pmcid: 2989762 doi: 10.1084/jem.20102260
Yu, M. et al. Insights into GATA-1-mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol. Cell 36, 682–695 (2009).
pubmed: 19941827 pmcid: 2800995 doi: 10.1016/j.molcel.2009.11.002
Fujiwara, Y., Browne, C. P., Cunniff, K., Goff, S. C. & Orkin, S. H. Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc. Natl. Acad. Sci. USA 93, 12355–12358 (1996).
pubmed: 8901585 doi: 10.1073/pnas.93.22.12355
Shimizu, R. et al. Leukemogenesis caused by incapacitated GATA-1 function. Mol. Cell Biol. 24, 10814–10825 (2004).
pubmed: 15572684 pmcid: 533998 doi: 10.1128/MCB.24.24.10814-10825.2004
Boddu, P. et al. Erythroleukemia-historical perspectives and recent advances in diagnosis and management. Blood Rev. 32, 96–105 (2018).
pubmed: 28965757 doi: 10.1016/j.blre.2017.09.002
Iacobucci, I. et al. Genomic subtyping and therapeutic targeting of acute erythroleukemia. Nat. Genet. 51, 694–704 (2019).
pubmed: 30926971 pmcid: 6828160 doi: 10.1038/s41588-019-0375-1
Huang, N. et al. Two distinct nuclear receptor interaction domains in NSD1, a novel SET protein that exhibits characteristics of both corepressors and coactivators. EMBO J. 17, 3398–3412 (1998).
pubmed: 9628876 pmcid: 1170677 doi: 10.1093/emboj/17.12.3398
Wang, X. et al. Identification and characterization of a novel androgen receptor coregulator ARA267-alpha in prostate cancer cells. J. Biol. Chem. 276, 40417–40423 (2001).
pubmed: 11509567 doi: 10.1074/jbc.M104765200
Wagner, E. J. & Carpenter, P. B. Understanding the language of Lys36 methylation at histone H3. Nat. Rev. Mol. Cell Biol. 13, 115–126 (2012).
pubmed: 22266761 pmcid: 3969746 doi: 10.1038/nrm3274
Kudithipudi, S., Lungu, C., Rathert, P., Happel, N. & Jeltsch, A. Substrate specificity analysis and novel substrates of the protein lysine methyltransferase NSD1. Chem. Biol. 21, 226–237 (2014).
pubmed: 24412544 doi: 10.1016/j.chembiol.2013.10.016
Dolnik, A. et al. Commonly altered genomic regions in acute myeloid leukemia are enriched for somatic mutations involved in chromatin remodeling and splicing. Blood 120, e83–e92 (2012).
pubmed: 22976956 doi: 10.1182/blood-2011-12-401471
Garg, M. et al. Profiling of somatic mutations in acute myeloid leukemia with FLT3-ITD at diagnosis and relapse. Blood 126, 2491–2501 (2015).
pubmed: 26438511 pmcid: 4661172 doi: 10.1182/blood-2015-05-646240
Papillon-Cavanagh, S. et al. Impaired H3K36 methylation defines a subset of head and neck squamous cell carcinomas. Nat. Genet. 49, 180–185 (2017).
pubmed: 28067913 pmcid: 5549104 doi: 10.1038/ng.3757
Su, X. et al. NSD1 inactivation and SETD2 mutation drive a convergence toward loss-of-function of H3K36 writers in clear-cell renal cell carcinomas. Cancer Res. 77, 4835–4845 (2017).
pubmed: 28754676 pmcid: 6211291 doi: 10.1158/0008-5472.CAN-17-0143
Peri, S. et al. NSD1- and NSD2-damaging mutations define a subset of laryngeal tumors with favorable prognosis. Nat. Commun. 8, 1772 (2017).
pubmed: 29176703 pmcid: 5701248 doi: 10.1038/s41467-017-01877-7
Berdasco, M. et al. Epigenetic inactivation of the Sotos overgrowth syndrome gene histone methyltransferase NSD1 in human neuroblastoma and glioma. Proc. Natl. Acad. Sci. USA 106, 21830–21835 (2009).
pubmed: 20018718 doi: 10.1073/pnas.0906831106
Lee, S. T. & Wiemels, J. L. Genome-wide CpG island methylation and intergenic demethylation propensities vary among different tumor sites. Nucleic Acids Res. 44, 1105–1117 (2016).
pubmed: 26464434 doi: 10.1093/nar/gkv1038
Kurotaki, N. et al. Haploinsufficiency of NSD1 causes Sotos syndrome. Nat. Genet. 30, 365–366 (2002).
pubmed: 11896389 doi: 10.1038/ng863
Baujat, G. & Cormier-Daire, V. Sotos syndrome. Orphanet J. Rare Dis. 2, 36 (2007).
pubmed: 17825104 pmcid: 2018686 doi: 10.1186/1750-1172-2-36
Park, S., Supek, F. & Lehner, B. Systematic discovery of germline cancer predisposition genes through the identification of somatic second hits. Nat. Commun. 9, 2601 (2018).
pubmed: 29973584 pmcid: 6031629 doi: 10.1038/s41467-018-04900-7
Rayasam, G. V. et al. NSD1 is essential for early post-implantation development and has a catalytically active SET domain. EMBO J. 22, 3153–3163 (2003).
pubmed: 12805229 pmcid: 162140 doi: 10.1093/emboj/cdg288
Koulnis, M. et al. Identification and analysis of mouse erythroid progenitors using the CD71/TER119 flow-cytometric assay. J. Visualized Exp. 54, 2809 (2011).
Ogilvy, S. et al. Promoter elements of vav drive transgene expression in vivo throughout the hematopoietic compartment. Blood 94, 1855–1863 (1999).
pubmed: 10477714 doi: 10.1182/blood.V94.6.1855
Kingsley, P. D. et al. Ontogeny of erythroid gene expression. Blood 121, e5–e13 (2013).
pubmed: 23243273 pmcid: 3567347 doi: 10.1182/blood-2012-04-422394
Kogan, S. C. et al. Bethesda proposals for classification of nonlymphoid hematopoietic neoplasms in mice. Blood 100, 238–245 (2002).
pubmed: 12070033 doi: 10.1182/blood.V100.1.238
England, S. J., McGrath, K. E., Frame, J. M. & Palis, J. Immature erythroblasts with extensive ex vivo self-renewal capacity emerge from the early mammalian fetus. Blood 117, 2708–2717 (2011).
pubmed: 21127173 pmcid: 3062358 doi: 10.1182/blood-2010-07-299743
Ferreira, R., Ohneda, K., Yamamoto, M. & Philipsen, S. GATA1 function, a paradigm for transcription factors in hematopoiesis. Mol. Cell Biol. 25, 1215–1227 (2005).
pubmed: 15684376 pmcid: 548021 doi: 10.1128/MCB.25.4.1215-1227.2005
Welch, J. J. et al. Global regulation of erythroid gene expression by transcription factor GATA-1. Blood 104, 3136–3147 (2004).
pubmed: 15297311 doi: 10.1182/blood-2004-04-1603
Wang, G. G., Cai, L., Pasillas, M. P. & Kamps, M. P. NUP98-NSD1 links H3K36 methylation to Hox-A gene activation and leukaemogenesis. Nat. Cell Biol. 9, 804–812 (2007).
pubmed: 17589499 doi: 10.1038/ncb1608
Dai, M. S., Mantel, C. R., Xia, Z. B., Broxmeyer, H. E. & Lu, L. An expansion phase precedes terminal erythroid differentiation of hematopoietic progenitor cells from cord blood in vitro and is associated with up-regulation of cyclin E and cyclin-dependent kinase 2. Blood 96, 3985–3987 (2000).
pubmed: 11090089 doi: 10.1182/blood.V96.12.3985
DeVilbiss, A. W., Boyer, M. E. & Bresnick, E. H. Establishing a hematopoietic genetic network through locus-specific integration of chromatin regulators. Proc. Natl. Acad. Sci. USA 110, E3398–E3407 (2013).
pubmed: 23959865 doi: 10.1073/pnas.1302771110
DeVilbiss, A. W. et al. Epigenetic determinants of erythropoiesis: role of the histone methyltransferase SetD8 in promoting erythroid cell maturation and survival. Mol. Cell Biol. 35, 2073–2087 (2015).
pubmed: 25855754 pmcid: 4438249 doi: 10.1128/MCB.01422-14
Malik, J., Getman, M. & Steiner, L. A. Histone methyltransferase Setd8 represses Gata2 expression and regulates erythroid maturation. Mol. Cell Biol. 35, 2059–2072 (2015).
pubmed: 25848090 pmcid: 4438238 doi: 10.1128/MCB.01413-14
Zhang, L. et al. ZFP36L2 is required for self-renewal of early burst-forming unit erythroid progenitors. Nature 499, 92–96 (2013).
pubmed: 23748442 pmcid: 3702661 doi: 10.1038/nature12215
Wu, W. et al. Dynamics of the epigenetic landscape during erythroid differentiation after GATA1 restoration. Genome Res. 21, 1659–1671 (2011).
pubmed: 21795386 pmcid: 3202283 doi: 10.1101/gr.125088.111
Hattangadi, S. M. et al. Histones to the cytosol: exportin 7 is essential for normal terminal erythroid nuclear maturation. Blood 124, 1931–1940 (2014).
pubmed: 25092175 pmcid: 4168348 doi: 10.1182/blood-2013-11-537761
Shaw, G. C. et al. Mitoferrin is essential for erythroid iron assimilation. Nature 440, 96–100 (2006).
pubmed: 16511496 doi: 10.1038/nature04512
Aizawa, S. et al. Ineffective erythropoiesis in mutant mice with deficient pyruvate kinase activity. Exp. Hematol. 33, 1292–1298 (2005).
pubmed: 16263413 doi: 10.1016/j.exphem.2005.07.008
Gubin, A. N. et al. Identification of the dombrock blood group glycoprotein as a polymorphic member of the ADP-ribosyltransferase gene family. Blood 96, 2621–2627 (2000).
pubmed: 11001920 doi: 10.1182/blood.V96.7.2621
Bartunek, P. et al. bFGF signaling and v-Myb cooperate in sustained growth of primitive erythroid progenitors. Oncogene 21, 400–410 (2002).
pubmed: 11821952 doi: 10.1038/sj/onc/1205103
Rodriguez, P. et al. GATA-1 forms distinct activating and repressive complexes in erythroid cells. EMBO J. 24, 2354–2366 (2005).
pubmed: 15920471 pmcid: 1173143 doi: 10.1038/sj.emboj.7600702
Ueki, N., Zhang, L. & Hayman, M. J. Ski negatively regulates erythroid differentiation through its interaction with GATA1. Mol. Cell Biol. 24, 10118–10125 (2004).
pubmed: 15542823 pmcid: 529047 doi: 10.1128/MCB.24.23.10118-10125.2004
Ueki, N. & Hayman, M. J. Signal-dependent N-CoR requirement for repression by the Ski oncoprotein. J. Biol. Chem. 278, 24858–24864 (2003).
pubmed: 12716897 doi: 10.1074/jbc.M303447200
Mukai, H. Y. et al. Establishment of erythroleukemic GAK14 cells and characterization of GATA1 N-terminal domain. Genes Cells 18, 886–898 (2013).
pubmed: 23890289
Moreau-Gachelin, F. Lessons from models of murine erythroleukemia to acute myeloid leukemia (AML): proof-of-principle of co-operativity in AML. Haematologica 91, 1644–1652 (2006).
pubmed: 17145601
Moreau-Gachelin, F. et al. Spi-1/PU.1 transgenic mice develop multistep erythroleukemias. Mol. Cell Biol. 16, 2453–2463 (1996).
pubmed: 8628313 pmcid: 231234 doi: 10.1128/MCB.16.5.2453
Kosmider, O. et al. Kit-activating mutations cooperate with Spi-1/PU.1 overexpression to promote tumorigenic progression during erythroleukemia in mice. Cancer cell 8, 467–478 (2005).
pubmed: 16338660 doi: 10.1016/j.ccr.2005.11.009
Rekhtman, N., Radparvar, F., Evans, T. & Skoultchi, A. I. Direct interaction of hematopoietic transcription factors PU.1 and GATA-1: functional antagonism in erythroid cells. Genes Development 13, 1398–1411 (1999).
pubmed: 10364157 pmcid: 316770 doi: 10.1101/gad.13.11.1398
Choe, K. S. et al. Reversal of tumorigenicity and the block to differentiation in erythroleukemia cells by GATA-1. Cancer Res. 63, 6363–6369 (2003).
pubmed: 14559825
Tecalco-Cruz, A. C., Rios-Lopez, D. G., Vazquez-Victorio, G., Rosales-Alvarez, R. E. & Macias-Silva, M. Transcriptional cofactors Ski and SnoN are major regulators of the TGF-beta/Smad signaling pathway in health and disease. Signal Transduct. Target Ther. 3, 15 (2018).
pubmed: 29892481 pmcid: 5992185 doi: 10.1038/s41392-018-0015-8
Bonnon, C. & Atanasoski, S. c-Ski in health and disease. Cell Tissue Res. 347, 51–64 (2012).
pubmed: 21647564 doi: 10.1007/s00441-011-1180-z
Ritter, M. et al. Inhibition of retinoic acid receptor signaling by Ski in acute myeloid leukemia. Leukemia 20, 437–443 (2006).
pubmed: 16424870 doi: 10.1038/sj.leu.2404093
Teichler, S. et al. MicroRNA29a regulates the expression of the nuclear oncogene Ski. Blood 118, 1899–1902 (2011).
pubmed: 21685371 doi: 10.1182/blood-2010-09-306258
Feld, C. et al. Combined cistrome and transcriptome analysis of SKI in AML cells identifies SKI as a co-repressor for RUNX1. Nucleic Acids Res. 46, 3412–3428 (2018).
pubmed: 29471413 pmcid: 5909421 doi: 10.1093/nar/gky119
Muench, D. E. et al. SKI controls MDS-associated chronic TGF-beta signaling, aberrant splicing, and stem cell fitness. Blood 132, e24–e34 (2018).
pubmed: 30249787 pmcid: 6251005 doi: 10.1182/blood-2018-06-860890
Gillespie, M. A. et al. Absolute quantification of transcription factors reveals principles of gene regulation in erythropoiesis. Mol Cell, https://doi.org/10.1016/j.molcel.2020.03.031 (2020).
Brumbaugh, J. et al. Inducible histone K-to-M mutations are dynamic tools to probe the physiological role of site-specific histone methylation in vitro and in vivo. Nat. Cell Biol, https://doi.org/10.1038/s41556-019-0403-5 (2019).
Weinberg, D. N. et al. The histone mark H3K36me2 recruits DNMT3A and shapes the intergenic DNA methylation landscape. Nature 573, 281–286 (2019).
pubmed: 31485078 pmcid: 31485078 doi: 10.1038/s41586-019-1534-3
Schulz, V. P. et al. A unique epigenomic landscape defines human erythropoiesis. Cell Rep. 28, 2996–3009 e2997 (2019).
Chiba, S. et al. Establishment and erythroid differentiation of a cytokine-dependent human leukemic cell line F-36: a parental line requiring granulocyte-macrophage colony-stimulating factor or interleukin-3, and a subline requiring erythropoietin. Blood 78, 2261–2268 (1991).
pubmed: 1834251 doi: 10.1182/blood.V78.9.2261.2261
Fagnan, A. et al. Human erythroleukemia genetics and transcriptomes identify master transcription factors as functional disease drivers. Blood 003062, https://doi.org/10.1182/blood.2019003062 (2020).
Georgiades, P. et al. VavCre transgenic mice: a tool for mutagenesis in hematopoietic and endothelial lineages. Genesis 34, 251–256 (2002).
pubmed: 12434335 doi: 10.1002/gene.10161
Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408 (2001).
pubmed: 11846609 pmcid: 11846609 doi: 10.1006/meth.2001.1262
Perez-Riverol, Y. et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 47, D442–D450 (2019).
pubmed: 30395289 doi: 10.1093/nar/gky1106

Auteurs

Katharina Leonards (K)

University Children's Hospital Basel, Basel, Switzerland.
Department of Biomedicine, University of Basel, 4031, Basel, Switzerland.

Marwa Almosailleakh (M)

University Children's Hospital Basel, Basel, Switzerland.
Department of Biomedicine, University of Basel, 4031, Basel, Switzerland.

Samantha Tauchmann (S)

University Children's Hospital Basel, Basel, Switzerland.
Department of Biomedicine, University of Basel, 4031, Basel, Switzerland.

Frederik Otzen Bagger (FO)

University Children's Hospital Basel, Basel, Switzerland.
Department of Biomedicine, University of Basel, 4031, Basel, Switzerland.
Swiss Institute of Bioinfomatics, 4031, Basel, Switzerland.
Genomic Medicine, Righospitalet, University of Copenhagen, 2100, Copenhagen, Denmark.

Cécile Thirant (C)

INSERM U1170, Equipe Labellisée Ligue Contre le Cancer, Gustave Roussy Institute, Université Paris Diderot, Université Paris-Sud, Villejuif, 94800, France.

Sabine Juge (S)

University Children's Hospital Basel, Basel, Switzerland.
Department of Biomedicine, University of Basel, 4031, Basel, Switzerland.

Thomas Bock (T)

Proteomics Core Facility, Biozentrum University of Basel, Basel, Switzerland.

Hélène Méreau (H)

Department of Biomedicine, University of Basel, 4031, Basel, Switzerland.

Matheus F Bezerra (MF)

University Children's Hospital Basel, Basel, Switzerland.
Department of Biomedicine, University of Basel, 4031, Basel, Switzerland.
Aggeu Magalhães Institute, Oswaldo Cruz Foundation, Recife, Brazil.

Alexandar Tzankov (A)

Institute for Pathology, University Hospital Basel, 4031, Basel, Switzerland.

Robert Ivanek (R)

Department of Biomedicine, University of Basel, 4031, Basel, Switzerland.
Swiss Institute of Bioinfomatics, 4031, Basel, Switzerland.

Régine Losson (R)

Institute de Génétique et de Biologie Moléculaire et Cellulaire (I.G.B.M.C.), CNRS/INSERM Université de Strasbourg, BP10142, 67404, Illkirch Cedex, France.

Antoine H F M Peters (AHFM)

Friedrich Miescher Institute for Biomedical Research, 4058, Basel, Switzerland.
Faculty of Sciences, University of Basel, 4056, Basel, Switzerland.

Thomas Mercher (T)

INSERM U1170, Equipe Labellisée Ligue Contre le Cancer, Gustave Roussy Institute, Université Paris Diderot, Université Paris-Sud, Villejuif, 94800, France.

Juerg Schwaller (J)

University Children's Hospital Basel, Basel, Switzerland. J.Schwaller@unibas.ch.
Department of Biomedicine, University of Basel, 4031, Basel, Switzerland. J.Schwaller@unibas.ch.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH