Identification of a Dynamic Core Transcriptional Network in t(8;21) AML that Regulates Differentiation Block and Self-Renewal
Oncogenic transcription factors such as RUNX1/ETO, which is generated by the chromosomal translocation t(8;21), subvert normal blood cell development by impairing differentiation and driving malignant self-renewal. Here, we use digital footprinting and chromatin immunoprecipitation sequencing (ChIP-...
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| Published in: | Cell reports (Cambridge) Vol. 8; no. 6; pp. 1974 - 1988 |
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| Language: | English |
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25.09.2014
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| ISSN: | 2211-1247, 2211-1247 |
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| Abstract | Oncogenic transcription factors such as RUNX1/ETO, which is generated by the chromosomal translocation t(8;21), subvert normal blood cell development by impairing differentiation and driving malignant self-renewal. Here, we use digital footprinting and chromatin immunoprecipitation sequencing (ChIP-seq) to identify the core RUNX1/ETO-responsive transcriptional network of t(8;21) cells. We show that the transcriptional program underlying leukemic propagation is regulated by a dynamic equilibrium between RUNX1/ETO and RUNX1 complexes, which bind to identical DNA sites in a mutually exclusive fashion. Perturbation of this equilibrium in t(8;21) cells by RUNX1/ETO depletion leads to a global redistribution of transcription factor complexes within preexisting open chromatin, resulting in the formation of a transcriptional network that drives myeloid differentiation. Our work demonstrates on a genome-wide level that the extent of impaired myeloid differentiation in t(8;21) is controlled by the dynamic balance between RUNX1/ETO and RUNX1 activities through the repression of transcription factors that drive differentiation.
[Display omitted]
•RUNX1/ETO drives a t(8;21)-specific transcriptional network•RUNX1/ETO and RUNX1 dynamically compete for the same genomic sites•RUNX1/ETO targets transcription factor complexes that control differentiation•RUNX1/ETO depletion activates a transcriptional network dominated by C/EBPα
Chromosomal rearrangements generate cancer-specific fusion genes that interfere with cell differentiation. Ptasinska et al. show that the most frequent fusion protein in acute myeloid leukemia (RUNX1/ETO) controls a cancer-propagating transcriptional network by binding to genomic sites in a dynamic equilibrium with wild-type RUNX1. Depletion of RUNX1/ETO installs a differentiation-promoting transcriptional network. Our findings demonstrate that the differentiation block in AML has a dynamic component as its core feature, which might provide a target for cancer-specific differentiation therapy. |
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| AbstractList | Oncogenic transcription factors such as RUNX1/ETO, which is generated by the chromosomal translocation t(8;21), subvert normal blood cell development by impairing differentiation and driving malignant self-renewal. Here, we use digital footprinting and chromatin immunoprecipitation sequencing (ChIP-seq) to identify the core RUNX1/ETO-responsive transcriptional network of t(8;21) cells. We show that the transcriptional program underlying leukemic propagation is regulated by a dynamic equilibrium between RUNX1/ETO and RUNX1 complexes, which bind to identical DNA sites in a mutually exclusive fashion. Perturbation of this equilibrium in t(8;21) cells by RUNX1/ETO depletion leads to a global redistribution of transcription factor complexes within preexisting open chromatin, resulting in the formation of a transcriptional network that drives myeloid differentiation. Our work demonstrates on a genome-wide level that the extent of impaired myeloid differentiation in t(8;21) is controlled by the dynamic balance between RUNX1/ETO and RUNX1 activities through the repression of transcription factors that drive differentiation.
•
RUNX1/ETO drives a t(8;21)-specific transcriptional network
•
RUNX1/ETO and RUNX1 dynamically compete for the same genomic sites
•
RUNX1/ETO targets transcription factor complexes that control differentiation
•
RUNX1/ETO depletion activates a transcriptional network dominated by C/EBPα
Chromosomal rearrangements generate cancer-specific fusion genes that interfere with cell differentiation. Ptasinska et al. show that the most frequent fusion protein in acute myeloid leukemia (RUNX1/ETO) controls a cancer-propagating transcriptional network by binding to genomic sites in a dynamic equilibrium with wild-type RUNX1. Depletion of RUNX1/ETO installs a differentiation-promoting transcriptional network. Our findings demonstrate that the differentiation block in AML has a dynamic component as its core feature, which might provide a target for cancer-specific differentiation therapy. Oncogenic transcription factors such as RUNX1/ETO, which is generated by the chromosomal translocation t(8;21), subvert normal blood cell development by impairing differentiation and driving malignant self-renewal. Here, we use digital footprinting and chromatin immunoprecipitation sequencing (ChIP-seq) to identify the core RUNX1/ETO-responsive transcriptional network of t(8;21) cells. We show that the transcriptional program underlying leukemic propagation is regulated by a dynamic equilibrium between RUNX1/ETO and RUNX1 complexes, which bind to identical DNA sites in a mutually exclusive fashion. Perturbation of this equilibrium in t(8;21) cells by RUNX1/ETO depletion leads to a global redistribution of transcription factor complexes within preexisting open chromatin, resulting in the formation of a transcriptional network that drives myeloid differentiation. Our work demonstrates on a genome-wide level that the extent of impaired myeloid differentiation in t(8;21) is controlled by the dynamic balance between RUNX1/ETO and RUNX1 activities through the repression of transcription factors that drive differentiation. Oncogenic transcription factors such as RUNX1/ETO, which is generated by the chromosomal translocation t(8;21), subvert normal blood cell development by impairing differentiation and driving malignant self-renewal. Here, we use digital footprinting and chromatin immunoprecipitation sequencing (ChIP-seq) to identify the core RUNX1/ETO-responsive transcriptional network of t(8;21) cells. We show that the transcriptional program underlying leukemic propagation is regulated by a dynamic equilibrium between RUNX1/ETO and RUNX1 complexes, which bind to identical DNA sites in a mutually exclusive fashion. Perturbation of this equilibrium in t(8;21) cells by RUNX1/ETO depletion leads to a global redistribution of transcription factor complexes within preexisting open chromatin, resulting in the formation of a transcriptional network that drives myeloid differentiation. Our work demonstrates on a genome-wide level that the extent of impaired myeloid differentiation in t(8;21) is controlled by the dynamic balance between RUNX1/ETO and RUNX1 activities through the repression of transcription factors that drive differentiation.Oncogenic transcription factors such as RUNX1/ETO, which is generated by the chromosomal translocation t(8;21), subvert normal blood cell development by impairing differentiation and driving malignant self-renewal. Here, we use digital footprinting and chromatin immunoprecipitation sequencing (ChIP-seq) to identify the core RUNX1/ETO-responsive transcriptional network of t(8;21) cells. We show that the transcriptional program underlying leukemic propagation is regulated by a dynamic equilibrium between RUNX1/ETO and RUNX1 complexes, which bind to identical DNA sites in a mutually exclusive fashion. Perturbation of this equilibrium in t(8;21) cells by RUNX1/ETO depletion leads to a global redistribution of transcription factor complexes within preexisting open chromatin, resulting in the formation of a transcriptional network that drives myeloid differentiation. Our work demonstrates on a genome-wide level that the extent of impaired myeloid differentiation in t(8;21) is controlled by the dynamic balance between RUNX1/ETO and RUNX1 activities through the repression of transcription factors that drive differentiation. Oncogenic transcription factors such as RUNX1/ETO, which is generated by the chromosomal translocation t(8;21), subvert normal blood cell development by impairing differentiation and driving malignant self-renewal. Here, we use digital footprinting and chromatin immunoprecipitation sequencing (ChIP-seq) to identify the core RUNX1/ETO-responsive transcriptional network of t(8;21) cells. We show that the transcriptional program underlying leukemic propagation is regulated by a dynamic equilibrium between RUNX1/ETO and RUNX1 complexes, which bind to identical DNA sites in a mutually exclusive fashion. Perturbation of this equilibrium in t(8;21) cells by RUNX1/ETO depletion leads to a global redistribution of transcription factor complexes within preexisting open chromatin, resulting in the formation of a transcriptional network that drives myeloid differentiation. Our work demonstrates on a genome-wide level that the extent of impaired myeloid differentiation in t(8;21) is controlled by the dynamic balance between RUNX1/ETO and RUNX1 activities through the repression of transcription factors that drive differentiation. [Display omitted] •RUNX1/ETO drives a t(8;21)-specific transcriptional network•RUNX1/ETO and RUNX1 dynamically compete for the same genomic sites•RUNX1/ETO targets transcription factor complexes that control differentiation•RUNX1/ETO depletion activates a transcriptional network dominated by C/EBPα Chromosomal rearrangements generate cancer-specific fusion genes that interfere with cell differentiation. Ptasinska et al. show that the most frequent fusion protein in acute myeloid leukemia (RUNX1/ETO) controls a cancer-propagating transcriptional network by binding to genomic sites in a dynamic equilibrium with wild-type RUNX1. Depletion of RUNX1/ETO installs a differentiation-promoting transcriptional network. Our findings demonstrate that the differentiation block in AML has a dynamic component as its core feature, which might provide a target for cancer-specific differentiation therapy. |
| Author | Westhead, David R. Bonifer, Constanze Wu, Mengchu Piper, Jason Heidenreich, Olaf Pickin, Anna Cockerill, Peter N. Ptasinska, Anetta Martinez-Soria, Natalia Imperato, Maria Rosaria Hoogenkamp, Maarten Tenen, Daniel G. Assi, Salam A. Ott, Sascha Cauchy, Pierre James, Sally R. Williamson, Dan |
| AuthorAffiliation | 4 Northern Institute for Cancer Research, University of Newcastle, Newcastle upon Tyne NE2 4HH, UK 6 Section of Experimental Haematology, Leeds Institute for Molecular Medicine, University of Leeds, Leeds LS2 9JT, UK 3 School of Molecular and Cellular Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK 2 Warwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, UK 1 School of Cancer Sciences, College of Medicine and Dentistry, University of Birmingham, Birmingham B15 2TT, UK 5 Cancer Science Institute, National University of Singapore, Republic of Singapore, Singapore 117456, Singapore |
| AuthorAffiliation_xml | – name: 6 Section of Experimental Haematology, Leeds Institute for Molecular Medicine, University of Leeds, Leeds LS2 9JT, UK – name: 3 School of Molecular and Cellular Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK – name: 2 Warwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, UK – name: 4 Northern Institute for Cancer Research, University of Newcastle, Newcastle upon Tyne NE2 4HH, UK – name: 5 Cancer Science Institute, National University of Singapore, Republic of Singapore, Singapore 117456, Singapore – name: 1 School of Cancer Sciences, College of Medicine and Dentistry, University of Birmingham, Birmingham B15 2TT, UK |
| Author_xml | – sequence: 1 givenname: Anetta surname: Ptasinska fullname: Ptasinska, Anetta organization: School of Cancer Sciences, College of Medicine and Dentistry, University of Birmingham, Birmingham B15 2TT, UK – sequence: 2 givenname: Salam A. surname: Assi fullname: Assi, Salam A. organization: School of Cancer Sciences, College of Medicine and Dentistry, University of Birmingham, Birmingham B15 2TT, UK – sequence: 3 givenname: Natalia surname: Martinez-Soria fullname: Martinez-Soria, Natalia organization: Northern Institute for Cancer Research, University of Newcastle, Newcastle upon Tyne NE2 4HH, UK – sequence: 4 givenname: Maria Rosaria surname: Imperato fullname: Imperato, Maria Rosaria organization: School of Cancer Sciences, College of Medicine and Dentistry, University of Birmingham, Birmingham B15 2TT, UK – sequence: 5 givenname: Jason surname: Piper fullname: Piper, Jason organization: Warwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, UK – sequence: 6 givenname: Pierre surname: Cauchy fullname: Cauchy, Pierre organization: School of Cancer Sciences, College of Medicine and Dentistry, University of Birmingham, Birmingham B15 2TT, UK – sequence: 7 givenname: Anna surname: Pickin fullname: Pickin, Anna organization: School of Cancer Sciences, College of Medicine and Dentistry, University of Birmingham, Birmingham B15 2TT, UK – sequence: 8 givenname: Sally R. surname: James fullname: James, Sally R. organization: Section of Experimental Haematology, Leeds Institute for Molecular Medicine, University of Leeds, Leeds LS2 9JT, UK – sequence: 9 givenname: Maarten surname: Hoogenkamp fullname: Hoogenkamp, Maarten organization: School of Cancer Sciences, College of Medicine and Dentistry, University of Birmingham, Birmingham B15 2TT, UK – sequence: 10 givenname: Dan surname: Williamson fullname: Williamson, Dan organization: Northern Institute for Cancer Research, University of Newcastle, Newcastle upon Tyne NE2 4HH, UK – sequence: 11 givenname: Mengchu surname: Wu fullname: Wu, Mengchu organization: Cancer Science Institute, National University of Singapore, Republic of Singapore, Singapore 117456, Singapore – sequence: 12 givenname: Daniel G. surname: Tenen fullname: Tenen, Daniel G. organization: Cancer Science Institute, National University of Singapore, Republic of Singapore, Singapore 117456, Singapore – sequence: 13 givenname: Sascha surname: Ott fullname: Ott, Sascha organization: Warwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, UK – sequence: 14 givenname: David R. surname: Westhead fullname: Westhead, David R. organization: School of Molecular and Cellular Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK – sequence: 15 givenname: Peter N. surname: Cockerill fullname: Cockerill, Peter N. organization: School of Cancer Sciences, College of Medicine and Dentistry, University of Birmingham, Birmingham B15 2TT, UK – sequence: 16 givenname: Olaf surname: Heidenreich fullname: Heidenreich, Olaf email: olaf.heidenreich@ncl.ac.uk organization: Northern Institute for Cancer Research, University of Newcastle, Newcastle upon Tyne NE2 4HH, UK – sequence: 17 givenname: Constanze surname: Bonifer fullname: Bonifer, Constanze email: c.bonifer@bham.ac.uk organization: School of Cancer Sciences, College of Medicine and Dentistry, University of Birmingham, Birmingham B15 2TT, UK |
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| SubjectTerms | Adaptor Proteins, Signal Transducing - metabolism CCAAT-Enhancer-Binding Protein-alpha - genetics CCAAT-Enhancer-Binding Protein-alpha - metabolism Cell Line, Tumor Chromatin Immunoprecipitation Chromosome Mapping Chromosomes, Human, Pair 21 Chromosomes, Human, Pair 8 Core Binding Factor Alpha 2 Subunit - metabolism Gene Regulatory Networks Humans Leukemia, Myeloid, Acute - metabolism Leukemia, Myeloid, Acute - pathology LIM Domain Proteins - metabolism Protein Binding Proto-Oncogene Proteins - metabolism RNA Interference RNA, Messenger - metabolism RNA, Small Interfering Sequence Analysis, RNA Trans-Activators - metabolism Translocation, Genetic |
| Title | Identification of a Dynamic Core Transcriptional Network in t(8;21) AML that Regulates Differentiation Block and Self-Renewal |
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