C/EBPα Activates Pre-existing and De Novo Macrophage Enhancers during Induced Pre-B Cell Transdifferentiation and Myelopoiesis

Transcription-factor-induced somatic cell conversions are highly relevant for both basic and clinical research yet their mechanism is not fully understood and it is unclear whether they reflect normal differentiation processes. Here we show that during pre-B-cell-to-macrophage transdifferentiation,...

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Published in:Stem cell reports Vol. 5; no. 2; pp. 232 - 247
Main Authors: van Oevelen, Chris, Collombet, Samuel, Vicent, Guillermo, Hoogenkamp, Maarten, Lepoivre, Cyrille, Badeaux, Aimee, Bussmann, Lars, Sardina, Jose Luis, Thieffry, Denis, Beato, Miguel, Shi, Yang, Bonifer, Constanze, Graf, Thomas
Format: Journal Article
Language:English
Published: United States Elsevier Inc 11.08.2015
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ISSN:2213-6711, 2213-6711
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Abstract Transcription-factor-induced somatic cell conversions are highly relevant for both basic and clinical research yet their mechanism is not fully understood and it is unclear whether they reflect normal differentiation processes. Here we show that during pre-B-cell-to-macrophage transdifferentiation, C/EBPα binds to two types of myeloid enhancers in B cells: pre-existing enhancers that are bound by PU.1, providing a platform for incoming C/EBPα; and de novo enhancers that are targeted by C/EBPα, acting as a pioneer factor for subsequent binding by PU.1. The order of factor binding dictates the upregulation kinetics of nearby genes. Pre-existing enhancers are broadly active throughout the hematopoietic lineage tree, including B cells. In contrast, de novo enhancers are silent in most cell types except in myeloid cells where they become activated by C/EBP factors. Our data suggest that C/EBPα recapitulates physiological developmental processes by short-circuiting two macrophage enhancer pathways in pre-B cells. [Display omitted] •C/EBPα activates two classes of prospective myeloid enhancers in B cells•Pre-existing enhancers are bound by PU.1 and become hyper-activated by C/EBPα•C/EBPα acts as a pioneer factor with delayed kinetics on de novo enhancers•The two types of enhancers direct myeloid cell fate in B cells and hematopoiesis In this study, Graf and colleagues show that, during B-cell-to-macrophage transdifferentiation, C/EBPα activates two types of myeloid enhancers in B cells. The two enhancer types are differentially activated, dictating gene expression levels of macrophage genes during the conversion of B cells into macrophages and normal hematopoiesis.
AbstractList Transcription-factor-induced somatic cell conversions are highly relevant for both basic and clinical research yet their mechanism is not fully understood and it is unclear whether they reflect normal differentiation processes. Here we show that during pre-B-cell-to-macrophage transdifferentiation, C/EBPα binds to two types of myeloid enhancers in B cells: pre-existing enhancers that are bound by PU.1, providing a platform for incoming C/EBPα; and de novo enhancers that are targeted by C/EBPα, acting as a pioneer factor for subsequent binding by PU.1. The order of factor binding dictates the upregulation kinetics of nearby genes. Pre-existing enhancers are broadly active throughout the hematopoietic lineage tree, including B cells. In contrast, de novo enhancers are silent in most cell types except in myeloid cells where they become activated by C/EBP factors. Our data suggest that C/EBPα recapitulates physiological developmental processes by short-circuiting two macrophage enhancer pathways in pre-B cells. • C/EBPα activates two classes of prospective myeloid enhancers in B cells • Pre-existing enhancers are bound by PU.1 and become hyper-activated by C/EBPα • C/EBPα acts as a pioneer factor with delayed kinetics on de novo enhancers • The two types of enhancers direct myeloid cell fate in B cells and hematopoiesis In this study, Graf and colleagues show that, during B-cell-to-macrophage transdifferentiation, C/EBPα activates two types of myeloid enhancers in B cells. The two enhancer types are differentially activated, dictating gene expression levels of macrophage genes during the conversion of B cells into macrophages and normal hematopoiesis.
Transcription-factor-induced somatic cell conversions are highly relevant for both basic and clinical research yet their mechanism is not fully understood and it is unclear whether they reflect normal differentiation processes. Here we show that during pre-B-cell-to-macrophage transdifferentiation, C/EBPα binds to two types of myeloid enhancers in B cells: pre-existing enhancers that are bound by PU.1, providing a platform for incoming C/EBPα; and de novo enhancers that are targeted by C/EBPα, acting as a pioneer factor for subsequent binding by PU.1. The order of factor binding dictates the upregulation kinetics of nearby genes. Pre-existing enhancers are broadly active throughout the hematopoietic lineage tree, including B cells. In contrast, de novo enhancers are silent in most cell types except in myeloid cells where they become activated by C/EBP factors. Our data suggest that C/EBPα recapitulates physiological developmental processes by short-circuiting two macrophage enhancer pathways in pre-B cells.Transcription-factor-induced somatic cell conversions are highly relevant for both basic and clinical research yet their mechanism is not fully understood and it is unclear whether they reflect normal differentiation processes. Here we show that during pre-B-cell-to-macrophage transdifferentiation, C/EBPα binds to two types of myeloid enhancers in B cells: pre-existing enhancers that are bound by PU.1, providing a platform for incoming C/EBPα; and de novo enhancers that are targeted by C/EBPα, acting as a pioneer factor for subsequent binding by PU.1. The order of factor binding dictates the upregulation kinetics of nearby genes. Pre-existing enhancers are broadly active throughout the hematopoietic lineage tree, including B cells. In contrast, de novo enhancers are silent in most cell types except in myeloid cells where they become activated by C/EBP factors. Our data suggest that C/EBPα recapitulates physiological developmental processes by short-circuiting two macrophage enhancer pathways in pre-B cells.
Transcription-factor-induced somatic cell conversions are highly relevant for both basic and clinical research yet their mechanism is not fully understood and it is unclear whether they reflect normal differentiation processes. Here we show that during pre-B-cell-to-macrophage transdifferentiation, C/EBPα binds to two types of myeloid enhancers in B cells: pre-existing enhancers that are bound by PU.1, providing a platform for incoming C/EBPα; and de novo enhancers that are targeted by C/EBPα, acting as a pioneer factor for subsequent binding by PU.1. The order of factor binding dictates the upregulation kinetics of nearby genes. Pre-existing enhancers are broadly active throughout the hematopoietic lineage tree, including B cells. In contrast, de novo enhancers are silent in most cell types except in myeloid cells where they become activated by C/EBP factors. Our data suggest that C/EBPα recapitulates physiological developmental processes by short-circuiting two macrophage enhancer pathways in pre-B cells.
Transcription-factor-induced somatic cell conversions are highly relevant for both basic and clinical research yet their mechanism is not fully understood and it is unclear whether they reflect normal differentiation processes. Here we show that during pre-B-cell-to-macrophage transdifferentiation, C/EBPα binds to two types of myeloid enhancers in B cells: pre-existing enhancers that are bound by PU.1, providing a platform for incoming C/EBPα; and de novo enhancers that are targeted by C/EBPα, acting as a pioneer factor for subsequent binding by PU.1. The order of factor binding dictates the upregulation kinetics of nearby genes. Pre-existing enhancers are broadly active throughout the hematopoietic lineage tree, including B cells. In contrast, de novo enhancers are silent in most cell types except in myeloid cells where they become activated by C/EBP factors. Our data suggest that C/EBPα recapitulates physiological developmental processes by short-circuiting two macrophage enhancer pathways in pre-B cells. [Display omitted] •C/EBPα activates two classes of prospective myeloid enhancers in B cells•Pre-existing enhancers are bound by PU.1 and become hyper-activated by C/EBPα•C/EBPα acts as a pioneer factor with delayed kinetics on de novo enhancers•The two types of enhancers direct myeloid cell fate in B cells and hematopoiesis In this study, Graf and colleagues show that, during B-cell-to-macrophage transdifferentiation, C/EBPα activates two types of myeloid enhancers in B cells. The two enhancer types are differentially activated, dictating gene expression levels of macrophage genes during the conversion of B cells into macrophages and normal hematopoiesis.
Author Collombet, Samuel
Badeaux, Aimee
Bonifer, Constanze
Sardina, Jose Luis
van Oevelen, Chris
Bussmann, Lars
Beato, Miguel
Hoogenkamp, Maarten
Shi, Yang
Vicent, Guillermo
Lepoivre, Cyrille
Graf, Thomas
Thieffry, Denis
AuthorAffiliation 2 Ecole Normale Supérieure, Institut de Biologie de l’ENS, INSERM, U1024, Centre National de la Recherche Scientifique (CNRS) 8197, 75005 Paris, France
1 Center for Genomic Regulation and Pompeu Fabra University, 08003 Barcelona, Spain
4 CNRS, Aix-Marseille Université, IGS UMR7256, 13288 Marseille, France
3 School of Cancer Sciences, Institute of Biomedical Research, University of Birmingham, Birmingham B15 2TT, UK
5 Harvard Medical School, Children’s Hospital, Boston, MA 02115, USA
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– name: 1 Center for Genomic Regulation and Pompeu Fabra University, 08003 Barcelona, Spain
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Snippet Transcription-factor-induced somatic cell conversions are highly relevant for both basic and clinical research yet their mechanism is not fully understood and...
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SubjectTerms B-Lymphocytes - cytology
B-Lymphocytes - metabolism
CCAAT-Enhancer-Binding Protein-alpha - genetics
CCAAT-Enhancer-Binding Protein-alpha - metabolism
Cell Line
Cell Transdifferentiation
Humans
Myeloid Cells - cytology
Myeloid Cells - metabolism
Myelopoiesis
Proto-Oncogene Proteins c-ets - genetics
Proto-Oncogene Proteins c-ets - metabolism
Title C/EBPα Activates Pre-existing and De Novo Macrophage Enhancers during Induced Pre-B Cell Transdifferentiation and Myelopoiesis
URI https://dx.doi.org/10.1016/j.stemcr.2015.06.007
https://www.ncbi.nlm.nih.gov/pubmed/26235892
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