A Single Oncogenic Enhancer Rearrangement Causes Concomitant EVI1 and GATA2 Deregulation in Leukemia

Gröschel, Stefan; Sanders, Mathijs A.; Hoogenboezem, Remco; de Wit, Elzo; Bouwman, Britta A.M.; Erpelinck, Claudia; van der Velden, Vincent H.J.; Havermans, Marije; Avellino, Roberto; van Lom, Kirsten; Rombouts, Elwin J.; van Duin, Mark; Döhner, Konstanze; Beverloo, H. Berna; Bradner, James E.; Döhner, Hartmut; Löwenberg, Bob; Valk, Peter J.M.; Bindels, Eric M.J.; de Laat, Wouter; Delwel, Ruud

doi:10.1016/j.cell.2014.02.019

Cited by 693Acute Myeloid Leukemia ResearchGenomics and Chromatin DynamicsChromatin Remodeling and Cancer

A Single Oncogenic Enhancer Rearrangement Causes Concomitant EVI1 and GATA2 Deregulation in Leukemia

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Gröschel, Stefan, Sanders, Mathijs A., Hoogenboezem, Remco, de Wit, Elzo, Bouwman, Britta A.M., Erpelinck, Claudia, van der Velden, Vincent H.J., Havermans, Marije +13 more·2014·Cell

DOI 10.1016/j.cell.2014.02.019

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Abstract

Chromosomal rearrangements without gene fusions have been implicated in leukemogenesis by causing deregulation of proto-oncogenes via relocation of cryptic regulatory DNA elements. AML with inv(3)/t(3;3) is associated with aberrant expression of the stem-cell regulator EVI1. Applying functional genomics and genome-engineering, we demonstrate that both 3q rearrangements reposition a distal GATA2 enhancer to ectopically activate EVI1 and simultaneously confer GATA2 functional haploinsufficiency, previously identified as the cause of sporadic familial AML/MDS and MonoMac/Emberger syndromes. Genomic excision of the ectopic enhancer restored EVI1 silencing and led to growth inhibition and differentiation of AML cells, which could be replicated by pharmacologic BET inhibition. Our data show that structural rearrangements involving the chromosomal repositioning of a single enhancer can cause deregulation of two unrelated distal genes, with cancer as the outcome.

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AML has recently emerged as an enhanceropathy.
“Very recently, AML has also emerged as such an “enhanceropathy”51.”
From Minimal PU.1 reduction induces a preleukemic state and promotes development of acute myeloid leukemia (2015) · cites this paper as [51]
MECOM activation due to an inversion between TADs in acute myeloid leukemia cells facilitates tumor formation.
“proto-oncogene MECOM activation due to an inversion between TADs in acute myeloid leukemia cells, which facilitates tumor formation14.”
From Disruption of chromatin folding domains by somatic genomic rearrangements in human cancer (2020) · cites this paper as [14]
Chromosomal rearrangements such as translocations or deletions which activate oncogenes also disrupt insulated neighborhoods around those genes without altering the sequence of the gene itself.
“Furthermore, chromosomal rearrangements such as translocations or deletions which activate oncogenes also disrupt insulated neighborhoods around those genes without altering the sequence of the gene itself (Groschel et al., 2014; Hnisz et al., 2016).”
From Insulated Neighborhoods: Structural and Functional Units of Mammalian Gene Control (2016) · cites this paper as Groschel et al., 2014

The Sequence Alignment/Map format and SAMtools
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp352 · Cited by 62,041 · see citing works
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607 · see citing works
Model-based Analysis of ChIP-Seq (MACS)
Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W., et al. (2008) · Genome Biology · doi:10.1186/gb-2008-9-9-r137 · Cited by 18,386 · see citing works
Integrative genomics viewer
Robinson, J. T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E. S., Getz, G., & Mesirov, J. P. (2011) · Nature Biotechnology · doi:10.1038/nbt.1754 · Cited by 15,390 · see citing works
Multiplex Genome Engineering Using CRISPR/Cas Systems
Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L. A., et al. (2013) · Science · doi:10.1126/science.1231143 · Cited by 15,339 · see citing works
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions.
Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., & Salzberg, S. L. (2013) · Genome Biology · doi:10.1186/gb-2013-14-4-r36 · Cited by 12,668 · see citing works
Velvet: Algorithms for de novo short read assembly using de Bruijn graphsPreprint
Zerbino, D. R., & Birney, E. (2008) · Genome Research · doi:10.1101/gr.074492.107 · Cited by 9,387 · see citing works
RNA-Guided Human Genome Engineering via Cas9
Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., Norville, J. E., & Church, G. M. (2013) · Science · doi:10.1126/science.1232033 · Cited by 9,210 · see citing works
Topological domains in mammalian genomes identified by analysis of chromatin interactions
Dixon, J. R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J. S., & Ren, B. (2012) · Nature · doi:10.1038/nature11082 · Cited by 6,829 · see citing works
Master Transcription Factors and Mediator Establish Super-Enhancers at Key Cell Identity Genes
Whyte, W. A., Orlando, D. A., Hnisz, D., Abraham, B. J., Lin, C. Y., Kagey, M. H., Rahl, P. B., Lee, T. I., & Young, R. A. (2013) · Cell · doi:10.1016/j.cell.2013.03.035 · Cited by 4,143 · see citing works
Selective Inhibition of Tumor Oncogenes by Disruption of Super-Enhancers
Lovén, J., Hoke, H. A., Lin, C. Y., Lau, A., Orlando, D. A., Vakoc, C. R., Bradner, J. E., Lee, T. I., & Young, R. A. (2013) · Cell · doi:10.1016/j.cell.2013.03.036 · Cited by 2,961 · see citing works
Self-citation
The accessible chromatin landscape of the human genome
Thurman, R. E., Rynes, E., Humbert, R., Vierstra, J., Maurano, M. T., Haugen, E., Sheffield, N. C., Stergachis, A. B., Wang, H., Vernot, B., et al. (2012) · Nature · doi:10.1038/nature11232 · Cited by 2,679 · see citing works
RNAi screen identifies Brd4 as a therapeutic target in acute myeloid leukaemia
Zuber, J., Shi, J., Wang, E., Rappaport, A. R., Herrmann, H., Sison, E. A., Magoon, D., Qi, J., Blatt, K., Wunderlich, M., et al. (2011) · Nature · doi:10.1038/nature10334 · Cited by 1,870 · see citing works
Self-citation
Identifying ChIP-seq enrichment using MACS
Feng, J., Liu, T., Qin, B., Zhang, Y., & Liu, X. S. (2012) · Nature Protocols · doi:10.1038/nprot.2012.101 · Cited by 1,805 · see citing works
The long-range interaction landscape of gene promoters
Sanyal, A., Lajoie, B. R., Jain, G., & Dekker, J. (2012) · Nature · doi:10.1038/nature11279 · Cited by 1,489 · see citing works
BreakDancer: an algorithm for high-resolution mapping of genomic structural variation
Chen, K., Wallis, J. W., McLellan, M. D., Larson, D. E., Kalicki, J. M., Pohl, C. S., McGrath, S. D., Wendl, M. C., Zhang, Q., Locke, D. P., et al. (2009) · Nature Methods · doi:10.1038/nmeth.1363 · Cited by 1,463 · see citing works
Looping and Interaction between Hypersensitive Sites in the Active β-globin Locus
Tolhuis, B., Palstra, R.-J., Splinter, E., Grosveld, F., & de Laat, W. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00781-5 · Cited by 1,344 · see citing works
Cloning the chromosomal breakpoint of t(14;18) human lymphomas: clustering around Jh on chromosome 14 and near a transcriptional unit on 18
Bakhshi, A., Jensen, J. P., Goldman, P., Wright, J. J., McBride, O. W., Epstein, A. L., & Korsmeyer, S. J. (1985) · Cell · doi:10.1016/s0092-8674(85)80070-2 · Cited by 1,177 · see citing works
The t(14;18) Chromosome Translocations Involved in B-Cell Neoplasms Result from Mistakes in VDJ Joining
Tsujimoto, Y., Gorham, J. D., Cossman, J., Jaffe, E. S., & Croce, C. M. (1985) · Science · doi:10.1126/science.3929382 · Cited by 990 · see citing works
EuroFlow antibody panels for standardized n-dimensional flow cytometric immunophenotyping of normal, reactive and malignant leukocytes
van Dongen, J. J. M., Lhermitte, L., Böttcher, S., Almeida, J., van der Velden, V. H. J., Flores-Montero, J. A., Rawstron, A. C., Asnafi, V., Lécrevisse, Q., Lúcio, P., et al. (2012) · Leukemia · doi:10.1038/leu.2012.120 · Cited by 936 · see citing works
EuroFlow standardization of flow cytometer instrument settings and immunophenotyping protocols
Kalina, T., Flores-Montero, J. A., van der Velden, V. H. J., Martin-Ayuso, M., Böttcher, S., Ritgen, M., Almeida, J., Lhermitte, L., Asnafi, V., Mendonça, A., et al. (2012) · Leukemia · doi:10.1038/leu.2012.122 · Cited by 789 · see citing works
Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease
Stein, S., Ott, M., Schultze-Strasser, S., Jauch, A., Burwinkel, B., Kinner, A., Schmidt, M., Krämer, A., Schwable, J., Glimm, H., et al. (2010) · Nature Medicine · doi:10.1038/nm.2088 · Cited by 783 · see citing works
Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor
Deng, W., Lee, J., Wang, H., Miller, J., Reik, A., Gregory, P. D., Dean, A., & Blobel, G. A. (2012) · Cell · doi:10.1016/j.cell.2012.03.051 · Cited by 734 · see citing works
GATA2 deficiency: a protean disorder of hematopoiesis, lymphatics, and immunity
Spinner, M. A., Sanchez, L. A., Hsu, A. P., Shaw, P. A., Zerbe, C. S., Calvo, K. R., Arthur, D. C., Gu, W., Gould, C. M., Brewer, C. C., et al. (2013) · Blood · doi:10.1182/blood-2013-07-515528 · Cited by 712 · see citing works
Mutations in GATA2 are associated with the autosomal dominant and sporadic monocytopenia and mycobacterial infection (MonoMAC) syndrome
Hsu, A. P., Sampaio, E. P., Khan, J. I., Calvo, K. R., Lemieux, J. E., Patel, S. Y., Frucht, D. M., Vinh, D. C., Auth, R., Freeman, A. F., et al. (2011) · Blood · doi:10.1182/blood-2011-05-356352 · Cited by 635 · see citing works
A transcription activator-like effector toolbox for genome engineering
Sanjana, N. E., Cong, L., Zhou, Y., Cunniff, M. M., Feng, G., & Zhang, F. (2012) · Nature Protocols · doi:10.1038/nprot.2011.431 · Cited by 628 · see citing works
Heritable GATA2 mutations associated with familial myelodysplastic syndrome and acute myeloid leukemia
Hahn, C. N., Chong, C., Carmichael, C., Wilkins, E. J., Brautigan, P. J., Li, X.-C., Babic, M., Lin, M., Carmagnac, A., Lee, Y. K., et al. (2011) · Nature Genetics · doi:10.1038/ng.913 · Cited by 608 · see citing works
Transcription Factor GATA-2 Is Required for Proliferation/Survival of Early Hematopoietic Cells and Mast Cell Formation, But Not for Erythroid and Myeloid Terminal Differentiation
Tsai, F., & Orkin, S. H. (1997) · Blood · doi:10.1182/blood.v89.10.3636.3636_3636_3643 · Cited by 601 · see citing works
Mutations in GATA2 cause primary lymphedema associated with a predisposition to acute myeloid leukemia (Emberger syndrome)
Østergaard, P., Simpson, M. A., Connell, F., Steward, C. G., Brice, G. W., Woollard, W. J., Dafou, D., Kilo, T., Smithson, S., Lunt, P. W., et al. (2011) · Nature Genetics · doi:10.1038/ng.923 · Cited by 503 · see citing works
Mitelman Database (Chromosome Aberrations and Gene Fusions in Cancer)
Griffith, M., & Griffith, O. L. (2004) · Dictionary of Bioinformatics and Computational Biology · doi:10.1002/9780471650126.dob0996 · Cited by 420 · see citing works
Robust 4C-seq data analysis to screen for regulatory DNA interactions
van de Werken, H., Landan, G., Holwerda, S. J. B., Hoichman, M., Klous, P., Chachik, R., Splinter, E., Valdes-Quezada, C., Öz, Y., Bouwman, B. A., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2173 · Cited by 407 · see citing works
Self-citation
Retroviral activation of a novel gene encoding a zinc finger protein in IL-3-dependent myeloid leukemia cell lines
Morishita, K., Parker, D. S., Mucenski, M. L., Jenkins, N. A., Copeland, N. G., & Ihle, J. N. (1988) · Cell · doi:10.1016/s0092-8674(88)91175-0 · Cited by 404 · see citing works
Fusion genes and rearranged genes as a linear function of chromosome aberrations in cancer
Mitelman, F., Johansson, B., & Mertens, F. (2004) · Nature Genetics · doi:10.1038/ng1335 · Cited by 361 · see citing works
GATA-2 Plays Two Functionally Distinct Roles during the Ontogeny of Hematopoietic Stem Cells
Ling, K.-W., Ottersbach, K., van Hamburg, J. P., Oziemlak, A., Tsai, F., Orkin, S., Ploemacher, R., Hendriks, R., & Dzierzak, E. (2004) · Journal of Experimental Medicine · doi:10.1084/jem.20031556 · Cited by 355 · see citing works
Prdm3 and Prdm16 are H3K9me1 Methyltransferases Required for Mammalian Heterochromatin Integrity
Pinheiro, I., Margueron, R., Shukeir, N., Eisold, M., Fritzsch, C., Richter, F. M., Mittler, G., Genoud, C., Goyama, S., Kurokawa, M., et al. (2012) · Cell · doi:10.1016/j.cell.2012.06.048 · Cited by 328 · see citing works
Haploinsufficiency of GATA-2 perturbs adult hematopoietic stem-cell homeostasis
Rodrigues, N. P. (2005) · Blood · doi:10.1182/blood-2004-08-2989 · Cited by 292 · see citing works
Evi-1 Is a Critical Regulator for Hematopoietic Stem Cells and Transformed Leukemic Cells
Goyama, S., Yamamoto, G., Shimabe, M., Sato, T., Ichikawa, M., Ogawa, S., Chiba, S., & Kurokawa, M. (2008) · Cell stem cell · doi:10.1016/j.stem.2008.06.002 · Cited by 287 · see citing works
Gata2 is required for HSC generation and survival
de Pater, E., Kaimakis, P., Vink, C. S., Yokomizo, T., Yamada-Inagawa, T., van der Linden, R., Kartalaei, P. S., Camper, S. A., Speck, N. A., & Dzierzak, E. A. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20130751 · Cited by 257 · see citing works
High EVI1 Expression Predicts Outcome in Younger Adult Patients With Acute Myeloid Leukemia and Is Associated With Distinct Cytogenetic Abnormalities
Gröschel, S., Lugthart, S., Schlenk, R. F., Valk, P. J. M., Eiwen, K., Goudswaard, C. S., van Putten, W. J. L., Käyser, S., Verdonck, L. F., Lübbert, M., et al. (2010) · Journal of Clinical Oncology · doi:10.1200/jco.2009.26.0646 · Cited by 256 · see citing works
Self-citation
Clinical, Molecular, and Prognostic Significance of WHO Type inv(3)(q21q26.2)/t(3;3)(q21;q26.2) and Various Other 3q Abnormalities in Acute Myeloid Leukemia
Lugthart, S., Gröschel, S., Beverloo, H. B., Käyser, S., Valk, P. J. M., van Zelderen‐Bhola, S. L., Ossenkoppele, G. J., Vellenga, E., Ruiter, E. V. D. B.-D., Schanz, U., et al. (2010) · Journal of Clinical Oncology · doi:10.1200/jco.2010.29.2771 · Cited by 256 · see citing works
Self-citation
GATA2 haploinsufficiency caused by mutations in a conserved intronic element leads to MonoMAC syndrome
Hsu, A. P., Johnson, K. D., Falcone, E. L., Sanalkumar, R., Sanchez, L. A., Hickstein, D. D., Cuellar‐Rodríguez, J., Lemieux, J. E., Zerbe, C. S., Bresnick, E. H., et al. (2013) · Blood · doi:10.1182/blood-2012-08-452763 · Cited by 249 · see citing works
A Remote GATA2 Hematopoietic Enhancer Drives Leukemogenesis in inv(3)(q21;q26) by Activating EVI1 Expression
Yamazaki, H., Suzuki, M., Otsuki, A., Shimizu, R., Bresnick, E. H., Engel, J. D., & Yamamoto, M. P. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.02.008 · Cited by 237 · see citing works
Chromosomal Abnormalities in Cancer
Fröhling, S., & Döhner, H. (2008) · New England Journal of Medicine · doi:10.1056/nejmra0803109 · Cited by 229 · see citing works
Self-citation
Evi1 is essential for hematopoietic stem cell self-renewal, and its expression marks hematopoietic cells with long-term multilineage repopulating activity
Kataoka, K., Sato, T., Yoshimi, A., Goyama, S., Tsuruta-Kishino, T., Kobayashi, H., Shimabe, M., Arai, S., Nakagawa, M. M., Imai, Y., et al. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20110447 · Cited by 192 · see citing works
Identification of a breakpoint cluster region 3' of the ribophorin I gene at 3q21 associated with the transcriptional activation of the EVI1 gene in acute myelogenous leukemias with inv(3)(q21q26)
Suzukawa, K., Parganas, E., Gajjar, A. J., Abe, T., Takahashi, S., Tani, K., Asano, S., Asou, H., Kamada, N., & Yokota, J. (1994) · Blood · doi:10.1182/blood.v84.8.2681.2681 · Cited by 148 · see citing works
Pluripotent hematopoietic stem cells contain high levels of mRNA for c-kit, GATA-2, p45 NF-E2, and c-myb and low levels or no mRNA for c-fms and the receptors for granulocyte colony-stimulating factor and interleukins 5 and 7.
Orlic, D., Anderson, S. M., Biesecker, L. G., Sorrentino, B. P., & Bodine, D. M. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.10.4601 · Cited by 147 · see citing works
Distinct Functions of Dispersed GATA Factor Complexes at an Endogenous Gene Locus
Grass, J. A., Jing, H., Kim, S., Martowicz, M. L., Pal, S. K., Blobel, G. A., & Bresnick, E. H. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01033-06 · Cited by 145 · see citing works
EVI1 is critical for the pathogenesis of a subset of MLL-AF9–rearranged AMLs
Bindels, E. M., Havermans, M., Lugthart, S., Erpelinck-Verschueren, C. A. J., Wocjtowicz, E., Krivtsov, A. V., Rombouts, E. J. C., Armstrong, S. A., Taskesen, E., Haanstra, J. R., et al. (2012) · Blood · doi:10.1182/blood-2011-11-393827 · Cited by 82 · see citing works
Self-citation
Regulatory elements in the immunoglobulin kappa locus induce c‐myc activation and the promoter shift in Burkitt's lymphoma cells.
Polack, A., Feederle, R., Klobeck, G., & Hörtnagel, K. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb06069.x · Cited by 54 · see citing works
Interphase fluorescence in situ hybridization assay for the detection of rearrangements of the EVI-1 locus in chromosome band 3q26 in myeloid malignancies.
Wieser, R., Schreiner, U., Rieder, H., Pirc‐Danoewinata, H., Grüner, H., Lončarević, I., & Fonatsch, C. (2003) · PubMed · Cited by 10 · see citing works

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1 of the 51 references couldn’t be matched to a known paper.

Sorted by citations

The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia
Arber, D. A., Orazi, A., Hasserjian, R., Thiele, J., Borowitz, M. J., Le Beau, M. M., Bloomfield, C. D., Cazzola, M., & Vardiman, J. W. (2016) · Blood · doi:10.1182/blood-2016-03-643544 · Cited by 10,119 · see citing works
Diagnosis and management of AML in adults: 2017 ELN recommendations from an international expert panel
Döhner, H., Estey, E. H., Grimwade, D. J., Amadori, S., Appelbaum, F. R., Büchner, T., Dombret, H., Ebert, B. L., Fenaux, P., Larson, R. A., et al. (2016) · Blood · doi:10.1182/blood-2016-08-733196 · Cited by 5,776 · see citing works
Self-citation
Acute Myeloid Leukemia
Döhner, H., Weisdorf, D. J., & Bloomfield, C. D. (2015) · New England Journal of Medicine · doi:10.1056/nejmra1406184 · Cited by 3,354 · see citing works
Self-citation
Transcriptional Addiction in Cancer
Bradner, J. E., Hnisz, D., & Young, R. A. (2017) · Cell · doi:10.1016/j.cell.2016.12.013 · Cited by 1,188 · see citing works
Self-citation
Long-range enhancer–promoter contacts in gene expression control
Schoenfelder, S., & Fraser, P. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0128-0 · Cited by 1,102 · see citing works
Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes
Dowen, J. M., Fan, Z. P., Hnisz, D., Ren, G., Abraham, B. J., Zhang, L. N., Weintraub, A. S., Schuijers, J., Lee, T. I., Zhao, K., et al. (2014) · Cell · doi:10.1016/j.cell.2014.09.030 · Cited by 884 · see citing works
BCL11A enhancer dissection by Cas9-mediated in situ saturating mutagenesis
Canver, M. C., Smith, E. C., Sher, F., Pinello, L., Sanjana, N. E., Shalem, O., Chen, D. D., Schupp, P. G., Vinjamur, D. S., Garcia, S. P., et al. (2015) · Nature · doi:10.1038/nature15521 · Cited by 886 · see citing works
The Mechanisms behind the Therapeutic Activity of BET Bromodomain Inhibition
Shi, J., & Vakoc, C. R. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.05.016 · Cited by 881 · see citing works
Chromatin Domains: The Unit of Chromosome Organization
Dixon, J. R., Gorkin, D. U., & Ren, B. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.05.018 · Cited by 811 · see citing works
What are super-enhancers?
Pott, S., & Lieb, J. D. (2014) · Nature Genetics · doi:10.1038/ng.3167 · Cited by 745 · see citing works
The role of 3D genome organization in development and cell differentiation
Zheng, H., & Xie, W. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0132-4 · Cited by 711 · see citing works
Transcription factors and 3D genome conformation in cell-fate decisions
Stadhouders, R., Filion, G. J. P., & Graf, T. (2019) · Nature · doi:10.1038/s41586-019-1182-7 · Cited by 519 · see citing works
CTCF and Cohesin in Genome Folding and Transcriptional Gene Regulation
Merkenschlager, M., & Nora, E. P. (2016) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-083115-022339 · Cited by 505 · see citing works
Convergence of Developmental and Oncogenic Signaling Pathways at Transcriptional Super-Enhancers
Hnisz, D., Schuijers, J., Lin, C. Y., Weintraub, A. S., Abraham, B. J., Lee, T. I., Bradner, J. E., & Young, R. A. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.02.014 · Cited by 476 · see citing works
Self-citation
Breaking TADs: How Alterations of Chromatin Domains Result in Disease
Lupiáñez, D. G., Spielmann, M., & Mundlos, S. (2016) · Trends in Genetics · doi:10.1016/j.tig.2016.01.003 · Cited by 439 · see citing works
Bromodomain inhibitor OTX015 in patients with acute leukaemia: a dose-escalation, phase 1 study
Berthon, C., Raffoux, E., Thomas, X., Vey, N., Gomez‐Roca, C., Yee, K. W. L., Taussig, D. C., Rezaï, K., Roumier, C., Herait, P., et al. (2016) · The Lancet Haematology · doi:10.1016/s2352-3026(15)00247-1 · Cited by 423 · see citing works
Insulated Neighborhoods: Structural and Functional Units of Mammalian Gene Control
Hnisz, D., Day, D. S., & Young, R. A. (2016) · Cell · doi:10.1016/j.cell.2016.10.024 · Cited by 420 · see citing works
Pan-cancer analysis of somatic copy-number alterations implicates IRS4 and IGF2 in enhancer hijacking
Weischenfeldt, J., Dubash, T., Drainas, A. P., Mardin, B. R., Chen, Y., Stütz, A. M., Waszak, S. M., Bosco, G., Halvorsen, A. R., Raeder, B., et al. (2017) · Nature Genetics · doi:10.1038/ng.3722 · Cited by 404 · see citing works
dbSUPER: a database of super-enhancers in mouse and human genome
Khan, A., & Zhang, X. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1002 · Cited by 399 · see citing works
The cancer epigenome: Concepts, challenges, and therapeutic opportunities
Dawson, M. A. (2017) · Science · doi:10.1126/science.aam7304 · Cited by 377 · see citing works
Active medulloblastoma enhancers reveal subgroup-specific cellular origins
Lin, C. Y., Erkek, S., Tong, Y., Yin, L., Alexander Joel Federation, Zapatka, M., Haldipur, P., Kawauchi, D., Risch, T., Warnatz, H.-J., et al. (2016) · Nature · doi:10.1038/nature16546 · Cited by 373 · see citing works
Self-citation
The second decade of 3C technologies: detailed insights into nuclear organizationPreprint
Denker, A., & de Laat, W. L. (2016) · Genes & Development · doi:10.1101/gad.281964.116 · Cited by 346 · see citing works
Super-Enhancer-Driven Transcriptional Dependencies in Cancer
Sengupta, S., & George, R. E. (2017) · Trends in cancer · doi:10.1016/j.trecan.2017.03.006 · Cited by 349 · see citing works
Identification of focally amplified lineage-specific super-enhancers in human epithelial cancers
Zhang, X., Choi, P. S., Francis, J. M., Imielinski, M. B., Watanabe, H., Cherniack, A. D., & Meyerson, M. M. (2015) · Nature Genetics · doi:10.1038/ng.3470 · Cited by 341 · see citing works
Live-cell imaging reveals enhancer-dependent Sox2 transcription in the absence of enhancer proximity
Alexander, J. M., Guan, J., Li, B., Maliskova, L., Song, M., Shen, Y., Huang, B., Lomvardas, S., & Weiner, O. D. (2019) · eLife · doi:10.7554/elife.41769 · Cited by 346 · see citing works
Functional Enhancers Shape Extrachromosomal Oncogene Amplifications
Morton, A. R., Dogan-Artun, N., Faber, Z. J., MacLeod, G. D. A. H., Bartels, C. F., Piazza, M. S., Allan, K. C., Mack, S. C., Wang, X., Gimple, R. C., et al. (2019) · Cell · doi:10.1016/j.cell.2019.10.039 · Cited by 336 · see citing works
BET Bromodomain Inhibition Suppresses the Function of Hematopoietic Transcription Factors in Acute Myeloid Leukemia
Roe, J., Mercan, F., Rivera, K. D., Pappin, D., & Vakoc, C. R. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.04.011 · Cited by 332 · see citing works
Regulation of disease-associated gene expression in the 3D genome
Krijger, P. H. L., & de Laat, W. L. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.138 · Cited by 316 · see citing works
Structural and functional diversity of Topologically Associating Domains
Dekker, J., & Heard, É. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.08.044 · Cited by 313 · see citing works
TCGA Workflow: Analyze cancer genomics and epigenomics data using Bioconductor packages
Silva, T. C., Colaprico, A., Olsen, C., D’Angelo, F., Bontempi, G., Ceccarelli, M., & Noushmehr, H. (2016) · F1000Research · doi:10.12688/f1000research.8923.1 · Cited by 295 · see citing works
Epigenetics and approaches to targeted epigenetic therapy in acute myeloid leukemia
Wouters, B. J., & Delwel, R. (2015) · Blood · doi:10.1182/blood-2015-07-604512 · Cited by 293 · see citing works
Self-citation
An oncogenic MYB feedback loop drives alternate cell fates in adenoid cystic carcinoma
Drier, Y., Cotton, M. J., Williamson, K. E., Gillespie, S. M., Ryan, R. J. H., Kluk, M., Carey, C. D., Rodig, S. J., Sholl, L. M., Afrogheh, A., et al. (2016) · Nature Genetics · doi:10.1038/ng.3502 · Cited by 294 · see citing works
Self-citation
From profiles to function in epigenomics
Stricker, S. H., Köferle, A., & Beck, S. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.138 · Cited by 290 · see citing works
Disruption of chromatin folding domains by somatic genomic rearrangements in human cancer
Akdemir, K. C., Le, V. T., Chandran, S., Li, Y., Verhaak, R. G., Beroukhim, R., Campbell, P. J., Chin, L., Dixon, J. R., Futreal, P. A., et al. (2020) · Nature Genetics · doi:10.1038/s41588-019-0564-y · Cited by 283 · see citing works
BET inhibitor OTX015 targets BRD2 and BRD4 and decreases c-MYC in acute leukemia cells
Coudé, M.-M., Braun, T., Berrou, J., Dupont, M., Bertrand, S., Massé, A., Raffoux, E., Itzykson, R., Delord, M., Riveiro, M. E., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.4131 · Cited by 279 · see citing works
Cancer transcriptome profiling at the juncture of clinical translation
Cieslik, M. P., & Chinnaiyan, A. M. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.96 · Cited by 261 · see citing works
Dynamic Control of Enhancer Repertoires Drives Lineage and Stage-Specific Transcription during Hematopoiesis
Huang, J., Liu, X., Li, D., Shao, Z., Cao, H., Zhang, Y., Trompouki, E., Bowman, T. V., Zon, L. I., Yuan, G., et al. (2016) · Developmental Cell · doi:10.1016/j.devcel.2015.12.014 · Cited by 239 · see citing works
A Remote GATA2 Hematopoietic Enhancer Drives Leukemogenesis in inv(3)(q21;q26) by Activating EVI1 Expression
Yamazaki, H., Suzuki, M., Otsuki, A., Shimizu, R., Bresnick, E. H., Engel, J. D., & Yamamoto, M. P. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.02.008 · Cited by 237 · see citing works
Mutational Cooperativity Linked to Combinatorial Epigenetic Gain of Function in Acute Myeloid Leukemia
Shih, A. H., Jiang, Y., Meydan, C., Shank, K., Pandey, S., Barreyro, L., Antony-Debre, I., Viale, A., Socci, N., Sun, Y., et al. (2015) · Cancer Cell · doi:10.1016/j.ccell.2015.03.009 · Cited by 236 · see citing works
TAD disruption as oncogenic driver
Valton, A.-L., & Dekker, J. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.03.008 · Cited by 226 · see citing works
Haematopoietic and immune defects associated with GATA2 mutation
Collin, M. P., Dickinson, R. E., & Bigley, V. (2015) · British Journal of Haematology · doi:10.1111/bjh.13317 · Cited by 237 · see citing works
Transcriptional Dysregulation of MYC Reveals Common Enhancer-Docking Mechanism
Schuijers, J., Manteiga, J. C., Weintraub, A. S., Day, D. S., Zamudio, A. V., Hnisz, D., Lee, T. I., & Young, R. A. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.056 · Cited by 232 · see citing works
MYC Drives a Subset of High-Risk Pediatric Neuroblastomas and Is Activated through Mechanisms Including Enhancer Hijacking and Focal Enhancer Amplification
Zimmerman, M. W., Liu, Y., He, S., Durbin, A. D., Abraham, B. J., Easton, J. B., Shao, Y., Xu, B., Zhu, S., Zhang, X., et al. (2017) · Cancer Discovery · doi:10.1158/2159-8290.cd-17-0993 · Cited by 229 · see citing works
Regulatory Enhancer–Core-Promoter Communication via Transcription Factors and Cofactors
Zabidi, M. A., & Stark, A. (2016) · Trends in Genetics · doi:10.1016/j.tig.2016.10.003 · Cited by 228 · see citing works
Aging Human Hematopoietic Stem Cells Manifest Profound Epigenetic Reprogramming of Enhancers That May Predispose to Leukemia
Adelman, E. R., Huang, H.-T., Roisman, A., Olsson, A., Colaprico, A., Qin, T., Lindsley, R. C., Bejar, R. L., Salomonis, N., Grimes, H. L., et al. (2019) · Cancer Discovery · doi:10.1158/2159-8290.cd-18-1474 · Cited by 222 · see citing works
Chromatin signatures of cancerPreprint
Morgan, M. A., & Shilatifard, A. (2015) · Genes & Development · doi:10.1101/gad.255182.114 · Cited by 214 · see citing works
4C-seq from beginning to end: A detailed protocol for sample preparation and data analysis
Krijger, P. H. L., Geeven, G., Bianchi, V., Hilvering, C. R. E., & de Laat, W. L. (2019) · Methods · doi:10.1016/j.ymeth.2019.07.014 · Cited by 201 · see citing works
Subtype-specific 3D genome alteration in acute myeloid leukaemia
Xu, J., Song, F., Lyu, H., Kobayashi, M., Zhang, B., Zhao, Z., Hou, Y., Wang, X., Luan, Y., Jia, B., et al. (2022) · Nature · doi:10.1038/s41586-022-05365-x · Cited by 208 · see citing works
Topologically associating domain boundaries that are stable across diverse cell types are evolutionarily constrained and enriched for heritability
McArthur, E., & Capra, J. A. (2021) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2021.01.001 · Cited by 200 · see citing works
CRISPR Reveals a Distal Super-Enhancer Required for Sox2 Expression in Mouse Embryonic Stem Cells
Li, Y., Rivera, C. M., Ishii, H., Jin, F., Selvaraj, S., Lee, A. Y., Dixon, J. R., & Ren, B. (2014) · PLoS ONE · doi:10.1371/journal.pone.0114485 · Cited by 212 · see citing works
HOTTIP lncRNA Promotes Hematopoietic Stem Cell Self-Renewal Leading to AML-like Disease in Mice
Luo, H., Zhu, G., Xu, J., Lai, Q., Yan, B., Guo, Y., Fung, T. K., Zeisig, B. B., Cui, Y., Zha, J., et al. (2019) · Cancer Cell · doi:10.1016/j.ccell.2019.10.011 · Cited by 192 · see citing works
Sequence-based modeling of three-dimensional genome architecture from kilobase to chromosome scale
Zhou, J. (2022) · Nature Genetics · doi:10.1038/s41588-022-01065-4 · Cited by 177 · see citing works
The GATA factor revolution in hematology
Katsumura, K. R., Bresnick, E. H., & the GATA Factor Mechanisms Group (2017) · Blood · doi:10.1182/blood-2016-09-687871 · Cited by 174 · see citing works
A selective HDAC8 inhibitor potentiates antitumor immunity and efficacy of immune checkpoint blockade in hepatocellular carcinoma
Yang, W., Feng, Y., Zhou, J., Cheung, O. K.-W., Cao, J., Wang, J., Tang, W., Tu, Y., Xu, L., Wu, F., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.aaz6804 · Cited by 172 · see citing works
GATA2 deficiency and related myeloid neoplasms
Włodarski, M. W., Collin, M. P., & Horwitz, M. S. (2017) · Seminars in Hematology · doi:10.1053/j.seminhematol.2017.05.002 · Cited by 171 · see citing works
Risk stratification of chromosomal abnormalities in chronic myelogenous leukemia in the era of tyrosine kinase inhibitor therapy
Wang, W., Cortes, J. E., Tang, G., Khoury, J. D., Wang, S., Bueso-Ramos, C. E., DiGiuseppe, J. A., Chen, Z., Kantarjian, H. M., Medeiros, L. J., et al. (2016) · Blood · doi:10.1182/blood-2016-01-690230 · Cited by 198 · see citing works
Genetic variation at MECOM, TERT, JAK2 and HBS1L-MYB predisposes to myeloproliferative neoplasms
Tapper, W., Jones, A. V., Královics, R., Harutyunyan, A. S., Zoi, K., Leung, W. C. Y., Godfrey, A. L., Guglielmelli, P., Callaway, A., Ward, D., et al. (2015) · Nature Communications · doi:10.1038/ncomms7691 · Cited by 168 · see citing works
Self-citation
Epigenetics of hematopoiesis and hematological malignanciesPreprint
Hu, D., & Shilatifard, A. (2016) · Genes & Development · doi:10.1101/gad.284109.116 · Cited by 167 · see citing works
A Highly Sensitive and Robust Method for Genome-wide 5hmC Profiling of Rare Cell Populations
Han, D., Lu, X., Shih, A. H., Nie, J., You, Q., Xu, M. M., Melnick, A. M., Levine, R. L., & He, C. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.06.028 · Cited by 167 · see citing works
Genome-scale high-resolution mapping of activating and repressive nucleotides in regulatory regions
Ernst, J., Melnikov, A., Zhang, X., Wang, L., Rogov, P., Mikkelsen, T. S., & Kellis, M. (2016) · Nature Biotechnology · doi:10.1038/nbt.3678 · Cited by 162 · see citing works
Super-enhancers in cancer
Thandapani, P. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.02.014 · Cited by 163 · see citing works
CRISPR-based functional genomics for neurological disease
Kampmann, M. (2020) · Nature Reviews Neurology · doi:10.1038/s41582-020-0373-z · Cited by 163 · see citing works
UTX-mediated enhancer and chromatin remodeling suppresses myeloid leukemogenesis through noncatalytic inverse regulation of ETS and GATA programs
Gozdecka, M., Meduri, E., Mazan, M. M., Tzelepis, K., Dudek, M., Knights, A. J., Pardo, M., Yu, L., Choudhary, J. S., Metzakopian, E., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0114-z · Cited by 157 · see citing works
GATA2 deficiency-associated bone marrow disorder differs from idiopathic aplastic anemia.
Ganapathi, K. A., Townsley, D., Hsu, A. P., Arthur, D., Zerbe, C. S., Cuellar-Rodríguez, J., Hickstein, D., Rosenzweig, S., Braylan, R., Young, N., et al. (2015) · Blood · doi:10.1182/blood-2014-06-580340 · Cited by 153 · see citing works
BET Family Protein BRD4: An Emerging Actor in NFκB Signaling in Inflammation and Cancer
Hajmirza, A., Emadali, A., Gauthier, A., Casasnovas, O., Gressin, R., & Callanan, M. B. (2018) · Biomedicines · doi:10.3390/biomedicines6010016 · Cited by 159 · see citing works
Genome-wide detection of enhancer-hijacking events from chromatin interaction data in rearranged genomes
Wang, X., Xu, J., Zhang, B., Hou, Y., Song, F., Lyu, H., & Yue, F. (2021) · Nature Methods · doi:10.1038/s41592-021-01164-w · Cited by 152 · see citing works
Enhancer Architecture and Essential Core Regulatory Circuitry of Chronic Lymphocytic Leukemia
Ott, C. J., Alexander Joel Federation, Schwartz, L. S., Kasar, S. N., Klitgaard, J. L., Lenci, R., Li, Q., Lawlor, M. A., Fernandes, S. M., Souza, A., et al. (2018) · Cancer Cell · doi:10.1016/j.ccell.2018.11.001 · Cited by 148 · see citing works
Self-citation
Aberrant Super‐Enhancer Landscape in Human Hepatocellular Carcinoma
Tsang, F. H., Law, C., Tang, T. C. C., Cheng, C. L., Chin, D. W., Tam, V., Wei, L., Wong, C. C., Ng, I. O., & Wong, C. (2019) · Hepatology · doi:10.1002/hep.30544 · Cited by 153 · see citing works
Looking beyond the genes: the role of non-coding variants in human disease
Spielmann, M., & Mundlos, S. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw205 · Cited by 143 · see citing works
How best to identify chromosomal interactions: a comparison of approaches
Davies, J. O. J., Oudelaar, A. M., Higgs, D. R., & Hughes, J. R. (2017) · Nature Methods · doi:10.1038/nmeth.4146 · Cited by 148 · see citing works
GATA2 deficiency
Hsu, A. P., McReynolds, L. J., & Holland, S. M. (2014) · Current Opinion in Allergy and Clinical Immunology · doi:10.1097/aci.0000000000000126 · Cited by 145 · see citing works
Super-enhancer function and its application in cancer targeted therapy
Tang, F., Yang, Z., Tan, Y., & Li, Y. (2020) · npj Precision Oncology · doi:10.1038/s41698-020-0108-z · Cited by 143 · see citing works
Epigenetic Identity in AML Depends on Disruption of Nonpromoter Regulatory Elements and Is Affected by Antagonistic Effects of Mutations in Epigenetic Modifiers
Glass, J. L., Hassane, D., Wouters, B. J., Kunimoto, H., Avellino, R., Garrett-Bakelman, F. E., Guryanova, O. A., Bowman, R., Redlich, S., Intlekofer, A. M., et al. (2017) · Cancer Discovery · doi:10.1158/2159-8290.cd-16-1032 · Cited by 142 · see citing works
Self-citation
GenomeDISCO: a concordance score for chromosome conformation capture experiments using random walks on contact map graphs
Ursu, O., Boley, N. P., Taranova, M., Wang, Y. X. R., Yardımcı, G. G., Noble, W. S., & Kundaje, A. B. (2018) · Bioinformatics · doi:10.1093/bioinformatics/bty164 · Cited by 137 · see citing works
Endogenous retroviruses are a source of enhancers with oncogenic potential in acute myeloid leukaemia
Deniz, Ö., Ahmed, M., Todd, C. D., Rio‐Machín, A., Dawson, M. A., & Branco, M. R. (2020) · Nature Communications · doi:10.1038/s41467-020-17206-4 · Cited by 135 · see citing works
Mechanisms of erythrocyte development and regeneration: implications for regenerative medicine and beyond
Bresnick, E. H., Hewitt, K. J., Mehta, C., Keleş, S., Paulson, R. F., & Johnson, K. D. (2018) · Development · doi:10.1242/dev.151423 · Cited by 133 · see citing works
Minimal PU.1 reduction induces a preleukemic state and promotes development of acute myeloid leukemia
Will, B., Vogler, T. O., Narayanagari, S., Bartholdy, B., Todorova, T. I., da Silva Ferreira, M., Chen, J., Yu, Y., Mayer, J., Barreyro, L., et al. (2015) · Nature Medicine · doi:10.1038/nm.3936 · Cited by 127 · see citing works
The nuclear matrix protein HNRNPU maintains 3D genome architecture globally in mouse hepatocytesPreprint
Fan, H., Lv, P., Huo, X., Wu, J., Wang, Q., Cheng, L., Liu, Y., Tang, Q., Zhang, L., Zhang, F., et al. (2017) · Genome Research · doi:10.1101/gr.224576.117 · Cited by 113 · see citing works
A new genomic framework to categorize pediatric acute myeloid leukemia
Umeda, M., Ma, J., Westover, T., Ni, Y., Song, G., Maciaszek, J. L., Rusch, M., Rahbarinia, D., Foy, S. G., Huang, B. J., et al. (2024) · Nature Genetics · doi:10.1038/s41588-023-01640-3 · Cited by 121 · see citing works
Conformation of sister chromatids in the replicated human genome
Mitter, M., Gasser, C., Takács, Z., Langer, C. C. H., Tang, W., Jessberger, G., Beales, C. T., Neuner, E., Ameres, S. L., Peters, J., et al. (2020) · Nature · doi:10.1038/s41586-020-2744-4 · Cited by 107 · see citing works
Modeling the Pathological Long-Range Regulatory Effects of Human Structural Variation with Patient-Specific hiPSCs
Laugsch, M., Bartusel, M., Rehimi, R., Alirzayeva, H., Karaolidou, A., Crispatzu, G., Zentis, P., Nikolić, M., Bleckwehl, T., Kolovos, P., et al. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.03.004 · Cited by 106 · see citing works
Super-enhancers: critical roles and therapeutic targets in hematologic malignancies
Jia, Y., Chng, W. J., & Zhou, J. (2019) · Journal of Hematology & Oncology · doi:10.1186/s13045-019-0757-y · Cited by 112 · see citing works
Structural variations in cancer and the 3D genome
Dubois, F. P. B., Sidiropoulos, N., Weischenfeldt, J., & Beroukhim, R. (2022) · Nature reviews. Cancer · doi:10.1038/s41568-022-00488-9 · Cited by 110 · see citing works
Enhancer deregulation in cancer and other diseases
Herz, H. (2016) · BioEssays · doi:10.1002/bies.201600106 · Cited by 107 · see citing works
Promoter Capture Hi-C: High-resolution, Genome-wide Profiling of Promoter Interactions
Schoenfelder, S., Javierre, B. M., Furlan-Magaril, M., Wingett, S., & Fraser, P. (2018) · Journal of Visualized Experiments · doi:10.3791/57320 · Cited by 114 · see citing works
Epigenetic maintenance of topological domains in the highly rearranged gibbon genome
Lazar, N. H., Nevonen, K. A., O'Connell, B., McCann, C., O'Neill, R. J., Green, R. E., Meyer, T. J., Okhovat, M., & Carbone, L. (2018) · Genome Research · doi:10.1101/gr.233874.117 · Cited by 107 · see citing works
A clinical transcriptome approach to patient stratification and therapy selection in acute myeloid leukemia
Docking, R., Parker, J., Jädersten, M., Duns, G., Chang, L., Jiang, J., Pilsworth, J. A., Swanson, L., Chan, S. K., Chiu, R., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22625-y · Cited by 106 · see citing works
Mutational spectrum of myeloid malignancies with inv(3)/t(3;3) reveals a predominant involvement of RAS/RTK signaling pathways
Gröschel, S., Sanders, M. A., Hoogenboezem, R. M., Zeilemaker, A., Havermans, M., Erpelinck-Verschueren, C. A. J., Bindels, E. M., Beverloo, H. B., Döhner, H., Löwenberg, B., et al. (2014) · Blood · doi:10.1182/blood-2014-07-591461 · Cited by 105 · see citing works
Self-citation
Mutant NPM1 Hijacks Transcriptional Hubs to Maintain Pathogenic Gene Programs in Acute Myeloid Leukemia
Wang, X. Q. D., Fan, D., Han, Q., Liu, Y., Miao, H. Z., Wang, X., Li, Q., Chen, D., Gore, H., Himadewi, P., et al. (2022) · Cancer Discovery · doi:10.1158/2159-8290.cd-22-0424 · Cited by 105 · see citing works
Candidate Cancer Driver Mutations in Distal Regulatory Elements and Long-Range Chromatin Interaction Networks.
Zhu, H., Uusküla-Reimand, L., Isaev, K., Wadi, L., Alizada, A., Shuai, S.-M., Huang, V., Aduluso-Nwaobasi, D., Paczkowska, M., Abd-Rabbo, D., et al. (2020) · Molecules and Cells · doi:10.1016/j.molcel.2019.12.027 · Cited by 86 · see citing works
Structural variants drive context-dependent oncogene activation in cancer
Xu, Z., Lee, D.-S., Chandran, S., Le, V. T., Bump, R., Yasis, J., Dallarda, S., Marcotte, S., Clock, B., Haghani, N. K., et al. (2022) · Nature · doi:10.1038/s41586-022-05504-4 · Cited by 97 · see citing works
STARR-seq — Principles and applications
Muerdter, F., Boryń, Ł. M., & Arnold, C. D. (2015) · Genomics · doi:10.1016/j.ygeno.2015.06.001 · Cited by 101 · see citing works
Integrated Genomic Analysis Identifies UBTF Tandem Duplications as a Recurrent Lesion in Pediatric Acute Myeloid Leukemia
Umeda, M., Ma, J., Huang, B. J., Hagiwara, K., Westover, T., Abdelhamed, S., Barajas, J. M., Thomas, M. E., Walsh, M. P., Song, G., et al. (2022) · Blood Cancer Discovery · doi:10.1158/2643-3230.bcd-21-0160 · Cited by 101 · see citing works
3C and 3C-based techniques: the powerful tools for spatial genome organization deciphering
Han, J., Zhang, Z., & Wang, K. (2018) · Molecular Cytogenetics · doi:10.1186/s13039-018-0368-2 · Cited by 97 · see citing works
Targeting Super-Enhancers for Disease Treatment and Diagnosis.
Shin, H. Y. (2018) · Europe PMC (PubMed Central) · doi:10.14348/molcells.2018.2297 · Cited by 97 · see citing works
Cross-species chromatin interactions drive transcriptional rewiring in Epstein–Barr virus–positive gastric adenocarcinoma
Okabe, A., Huang, K. K., Matsusaka, K., Fukuyo, M., Xing, M., Ong, X., Hoshii, T., Usui, G., Seki, M., Mano, Y., et al. (2020) · Nature Genetics · doi:10.1038/s41588-020-0665-7 · Cited by 97 · see citing works
Cytogenetics of Pediatric Acute Myeloid Leukemia: A Review of the Current Knowledge
Quessada, J., Cuccuini, W., Saultier, P., Loosveld, M., Harrison, C. J., & Lafage‐Pochitaloff, M. (2021) · Genes · doi:10.3390/genes12060924 · Cited by 96 · see citing works
Structural Variation in Cancer: Role, Prevalence, and Mechanisms
Cosenza, M. R., Rodríguez–Martín, B., & Korbel, J. O. (2022) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-120121-101149 · Cited by 92 · see citing works
Identification of copy number variations and translocations in cancer cells from Hi-C data
Chakraborty, A., & Ay, F. (2018) · Bioinformatics · doi:10.1093/bioinformatics/btx664 · Cited by 94 · see citing works
Demystifying the secret mission of enhancers: linking distal regulatory elements to target genes
Yao, L., Berman, B. P., & Farnham, P. (2015) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2015.1087961 · Cited by 91 · see citing works

Two effects of GATA2 enhancer repositioning by 3q chromosomal rearrangements
Suzuki, M., Katayama, S., & Yamamoto, M. P. (2019) · IUBMB Life · doi:10.1002/iub.2191 · Cited by 7 · see citing works
Chromosomal rearrangements between 3q21 and 3q26 induce leukemogenesis by misdirecting both EVI1 and GATA2 genes.
Suzuki, M. (2017) · PubMed · doi:10.11406/rinketsu.58.806
Defects in the RAS/RTK Signaling Pathways Predominate the Mutational Spectrum of EVI1/GATA2 Rearranged Myeloid Malignancies with Inv(3)/t(3;3)
Sanders, M. A., Gröschel, S., Hoogenboezem, R. M., Zeilemaker, A., Havermans, M., Erpelinck-Verschueren, C. A. J., Bindels, E. M., Beverloo, B. H. B., Döhner, H., Löwenberg, B., et al. (2014) · Blood · doi:10.1182/blood.v124.21.701.701
Self-citation
A Remote GATA2 Hematopoietic Enhancer Drives Leukemogenesis in inv(3)(q21;q26) by Activating EVI1 Expression
Yamazaki, H., Suzuki, M., Otsuki, A., Shimizu, R., Bresnick, E. H., Engel, J. D., & Yamamoto, M. P. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.02.008 · Cited by 237 · see citing works
EVI1 and GATA2 misexpression induced by inv(3)(q21q26) contribute to megakaryocyte-lineage skewing and leukemogenesis
Yamaoka, A., Suzuki, M., Katayama, S., Orihara, D., Engel, J. D., & Yamamoto, M. P. (2020) · Blood Advances · doi:10.1182/bloodadvances.2019000978 · Cited by 25 · see citing works

Authors: Gröschel, S., Sanders, M. A., Hoogenboezem, R., de Wit, E., Bouwman, B. A. M., Erpelinck, C., van der Velden, V. H. J., Havermans, M., Avellino, R., van Lom, K., Rombouts, E. J., van Duin, M., Döhner, K., Beverloo, H. B., Bradner, J. E., Döhner, H., Löwenberg, B., Valk, P. J. M., Bindels, E. M. J., de Laat, W., & Delwel, R.
Affiliations: Erasmus MC (NL)
University Medical Center Utrecht (NL)
University Hospital Ulm (DE)
Harvard University (US)
Corresponding author: Delwel, Ruud
ORCID: Gröschel, Stefan
Sanders, Mathijs A.
Hoogenboezem, Remco
Bouwman, Britta A.M.
Havermans, Marije
Avellino, Roberto
Döhner, Konstanze
Beverloo, H. Berna
Bradner, James E.
Döhner, Hartmut
Löwenberg, Bob
Valk, Peter J.M.
Bindels, Eric M.J.
Delwel, Ruud
Venue: Cell
Publisher: Elsevier BV
Published: 2014-04
Volume: 157
Issue: 2
Pages: 369-381
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2014.02.019
OpenAlex: W1978902427
Cited by: 687
References: 51
Citations by year: 2026: 29 · 2025: 45 · 2024: 42 · 2023: 72 · 2022: 55 · 2021: 69 · 2020: 66 · 2019: 62 · 2018: 59 · 2017: 65 · 2016: 59 · 2015: 45 · 2014: 15 · 2012: 3
FWCI: 43.09
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 444 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Funders: Association for International Cancer Research
Deutsche Forschungsgemeinschaft (GR 3955/1-1)
Lady Tata Memorial Trust
European Hematology Association
Center for Translational Molecular Medicine (GR03O-102)
Topics: Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Keywords: EVI1, GATA2, acute myeloid leukemia, haploinsufficiency, BET inhibition, leukemia cell differentiation, leukemogenesis
MeSH terms: MDS1 and EVI1 Complex Locus Protein, Chromosomes, Human, Pair 3, DNA-Binding Proteins, Enhancer Elements, Genetic, Humans, Chromosome Inversion, Myelodysplastic Syndromes, Promoter Regions, Genetic, Proto-Oncogenes, Transcription Factors, Translocation, Genetic, Leukemia, Myeloid, Acute, Transcriptional Activation, Gene Expression Regulation, Neoplastic, Cell Line, Tumor, GATA2 Transcription Factor

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A Single Oncogenic Enhancer Rearrangement Causes Concomitant EVI1 and GATA2 Deregulation in Leukemia

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