Dynamic 3D chromatin architecture contributes to enhancer specificity and limb morphogenesis

The regulatory specificity of enhancers and their interaction with gene promoters is thought to be controlled by their sequence and the binding of transcription factors. By studying Pitx1 , a regulator of hindlimb development, we show that dynamic changes in chromatin conformation can restrict the a...

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Published inNature genetics Vol. 50; no. 10; pp. 1463 - 1473
Main Authors Kragesteen, Bjørt K., Spielmann, Malte, Paliou, Christina, Heinrich, Verena, Schöpflin, Robert, Esposito, Andrea, Annunziatella, Carlo, Bianco, Simona, Chiariello, Andrea M., Jerković, Ivana, Harabula, Izabela, Guckelberger, Philine, Pechstein, Michael, Wittler, Lars, Chan, Wing-Lee, Franke, Martin, Lupiáñez, Darío G., Kraft, Katerina, Timmermann, Bernd, Vingron, Martin, Visel, Axel, Nicodemi, Mario, Mundlos, Stefan, Andrey, Guillaume
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.10.2018
Nature Publishing Group
Subjects
38
45/41
631/136
631/208
631/337
64
64/110
64/60
692/308/2056
Agriculture
Animal Genetics and Genomics
Animals
Arm
Biomedical and Life Sciences
Biomedicine
Cancer Research
Chromatin
Chromatin - chemistry
Chromatin - genetics
Chromatin - metabolism
Chromatin Assembly and Disassembly - genetics
Conformation
CRISPR-Cas Systems
DNA - chemistry
DNA - metabolism
DNA binding proteins
Embryo, Mammalian
Enhancer Elements, Genetic - physiology
Enhancers
Evolution & development
Extremities (Anatomy)
Forelimb - embryology
Forelimb - metabolism
Gene expression
Gene Expression Regulation, Developmental - genetics
Gene Function
Genetic transformation
Genomes
Health aspects
Hindlimb - embryology
Hindlimb - metabolism
Human Genetics
Mice
Mice, Transgenic
Molecular Conformation
Morphogenesis
Morphogenesis - genetics
Nucleic Acid Conformation
Paired Box Transcription Factors - genetics
Paired Box Transcription Factors - physiology
Pituitary gland
Polymer melts
Rodents
Sensors
Stem cells
Three dimensional models
Transcription (Genetics)
Transcription factors
Online AccessGet full text

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Abstract The regulatory specificity of enhancers and their interaction with gene promoters is thought to be controlled by their sequence and the binding of transcription factors. By studying Pitx1 , a regulator of hindlimb development, we show that dynamic changes in chromatin conformation can restrict the activity of enhancers. Inconsistent with its hindlimb-restricted expression, Pitx1 is controlled by an enhancer ( Pen ) that shows activity in forelimbs and hindlimbs. By Capture Hi-C and three-dimensional modeling of the locus, we demonstrate that forelimbs and hindlimbs have fundamentally different chromatin configurations, whereby Pen and Pitx1 interact in hindlimbs and are physically separated in forelimbs. Structural variants can convert the inactive into the active conformation, thereby inducing Pitx1 misexpression in forelimbs, causing partial arm-to-leg transformation in mice and humans. Thus, tissue-specific three-dimensional chromatin conformation can contribute to enhancer activity and specificity in vivo and its disturbance can result in gene misexpression and disease. A Pitx1 enhancer shows activity in forelimbs and hindlimbs but only interacts with Pitx1 in hindlimbs because of its three-dimensional configuration. Structural variants that affect three-dimensional conformation induce Pitx1 expression in forelimbs and cause partial arm-to-leg transformation in mice and humans.
AbstractList The regulatory specificity of enhancers and their interaction with gene promoters is thought to be controlled by their sequence and the binding of transcription factors. By studying Pitx1, a regulator of hindlimb development, we show that dynamic changes in chromatin conformation can restrict the activity of enhancers. Inconsistent with its hindlimb-restricted expression, Pitx1 is controlled by an enhancer (Pen) that shows activity in forelimbs and hindlimbs. By Capture Hi-C and three-dimensional modeling of the locus, we demonstrate that forelimbs and hindlimbs have fundamentally different chromatin configurations, whereby Pen and Pitx1 interact in hindlimbs and are physically separated in forelimbs. Structural variants can convert the inactive into the active conformation, thereby inducing Pitx1 misexpression in forelimbs, causing partial arm-to-leg transformation in mice and humans. Thus, tissue-specific three-dimensional chromatin conformation can contribute to enhancer activity and specificity in vivo and its disturbance can result in gene misexpression and disease. A Pitx1 enhancer shows activity in forelimbs and hindlimbs but only interacts with Pitx1 in hindlimbs because of its three-dimensional configuration. Structural variants that affect three-dimensional conformation induce Pitx1 expression in forelimbs and cause partial arm-to-leg transformation in mice and humans.
The regulatory specificity of enhancers and their interaction with gene promoters is thought to be controlled by their sequence and the binding of transcription factors. By studying Pitx1 , a regulator of hindlimb development, we show that dynamic changes in chromatin conformation can restrict the activity of enhancers. Inconsistent with its hindlimb-restricted expression, Pitx1 is controlled by an enhancer ( Pen ) that shows activity in both fore- and hindlimb. By capture HiC and 3D-modeling of the locus, we demonstrate that fore- and hindlimbs have fundamentally different chromatin configurations, whereby Pen and Pitx1 interact in hindlimbs and are physically separated in forelimbs. Structural variants are able to convert the inactive into the active conformation, thereby inducing Pitx1 misexpression in the forelimb, causing partial arm-to-leg transformation in mice and humans. Thus, tissue-specific 3D chromatin conformation can contribute to enhancer activity and specificity in vivo and its disturbance can result in gene misexpression and disease.
The regulatory specificity of enhancers and their interaction with gene promoters is thought to be controlled by their sequence and the binding of transcription factors. By studying Pitx1, a regulator of hindlimb development, we show that dynamic changes in chromatin conformation can restrict the activity of enhancers. Inconsistent with its hindlimb-restricted expression, Pitx1 is controlled by an enhancer (Pen) that shows activity in forelimbs and hindlimbs. By Capture Hi-C and three-dimensional modeling of the locus, we demonstrate that forelimbs and hindlimbs have fundamentally different chromatin configurations, whereby Pen and Pitx1 interact in hindlimbs and are physically separated in forelimbs. Structural variants can convert the inactive into the active conformation, thereby inducing Pitx1 misexpression in forelimbs, causing partial arm-to-leg transformation in mice and humans. Thus, tissue-specific three-dimensional chromatin conformation can contribute to enhancer activity and specificity in vivo and its disturbance can result in gene misexpression and disease.
The regulatory specificity of enhancers and their interaction with gene promoters is thought to be controlled by their sequence and the binding of transcription factors. By studying Pitx1 , a regulator of hindlimb development, we show that dynamic changes in chromatin conformation can restrict the activity of enhancers. Inconsistent with its hindlimb-restricted expression, Pitx1 is controlled by an enhancer ( Pen ) that shows activity in forelimbs and hindlimbs. By Capture Hi-C and three-dimensional modeling of the locus, we demonstrate that forelimbs and hindlimbs have fundamentally different chromatin configurations, whereby Pen and Pitx1 interact in hindlimbs and are physically separated in forelimbs. Structural variants can convert the inactive into the active conformation, thereby inducing Pitx1 misexpression in forelimbs, causing partial arm-to-leg transformation in mice and humans. Thus, tissue-specific three-dimensional chromatin conformation can contribute to enhancer activity and specificity in vivo and its disturbance can result in gene misexpression and disease. A Pitx1 enhancer shows activity in forelimbs and hindlimbs but only interacts with Pitx1 in hindlimbs because of its three-dimensional configuration. Structural variants that affect three-dimensional conformation induce Pitx1 expression in forelimbs and cause partial arm-to-leg transformation in mice and humans.
Audience Academic
Author Annunziatella, Carlo
Chan, Wing-Lee
Esposito, Andrea
Jerković, Ivana
Vingron, Martin
Nicodemi, Mario
Timmermann, Bernd
Andrey, Guillaume
Chiariello, Andrea M.
Harabula, Izabela
Guckelberger, Philine
Franke, Martin
Kragesteen, Bjørt K.
Bianco, Simona
Wittler, Lars
Paliou, Christina
Spielmann, Malte
Pechstein, Michael
Lupiáñez, Darío G.
Visel, Axel
Mundlos, Stefan
Schöpflin, Robert
Heinrich, Verena
Kraft, Katerina
AuthorAffiliation 4 Berlin-Brandenburg School for Regenerative Therapies (BSRT), Charité Universitätsmedizin Berlin, 13353 Berlin, Germany
5 Department of Computational Molecular Biology, Max Planck Institute for Molecular Genetics, 14195 Berlin, Germany
9 Present address: Epigenetics and Sex Development Group, Berlin Institute for Medical Systems Biology, Max-Delbrück Center for Molecular Medicine, Berlin-Buch, Germany
6 Dipartimento di Fisica, Università di Napoli Federico II, and INFN Napoli, Complesso Universitario di Monte Sant’Angelo, 80126 Naples, Italy
8 Department of Developmental Genetics, Max Planck Institute for Molecular Genetics, 14195 Berlin, Germany
1 RG Development & Disease, Max Planck Institute for Molecular Genetics, 14195 Berlin, Germany
12 U.S. Department of Energy Joint Genome Institute, Walnut Creek, CA 94598, USA
7 Berlin Institute of Health (BIH), MDC-Berlin, 13125 Berlin, Germany
10 Max Planck Institute for Molecular Genetics, Sequencing Core Facility, 14195 Berlin, Germany
2 Institute
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30262816$$D View this record in MEDLINE/PubMed
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content type line 23
G.A., S.M., B.K. and M.S., conceived the project. G.A., B.K. and M.F. performed cHiC. V.H, R.S and M.V. performed the computational analysis. M.S., B.K., I.H., I.J., P.G., K.K. and D.G.L produced transgenic reporter and carried out transgenic validation. G.A., B.K., M.S., C.P, M.P. and P.G. performed the knockout and knockin studies. B.T. sequenced the cHiC samples. L.W. performed morula aggregation. W.L.C performed the micro-CT analyses. M.N. conceived the polymer modelling study. A.E., C.A., S.B. and A.M.C. run the related computer simulations and analyses. G.A., S.M., M.S., B.K. and A.V. wrote the manuscript with input from the remaining authors.
These authors contributed equally to this work
Author Contributions
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0000-0002-4626-3290
0000-0001-9707-8303
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Snippet The regulatory specificity of enhancers and their interaction with gene promoters is thought to be controlled by their sequence and the binding of...
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SubjectTerms 38
45/41
631/136
631/208
631/337
64
64/110
64/60
692/308/2056
Agriculture
Animal Genetics and Genomics
Animals
Arm
Biomedical and Life Sciences
Biomedicine
Cancer Research
Chromatin
Chromatin - chemistry
Chromatin - genetics
Chromatin - metabolism
Chromatin Assembly and Disassembly - genetics
Conformation
CRISPR-Cas Systems
DNA - chemistry
DNA - metabolism
DNA binding proteins
Embryo, Mammalian
Enhancer Elements, Genetic - physiology
Enhancers
Evolution & development
Extremities (Anatomy)
Forelimb - embryology
Forelimb - metabolism
Gene expression
Gene Expression Regulation, Developmental - genetics
Gene Function
Genetic transformation
Genomes
Health aspects
Hindlimb - embryology
Hindlimb - metabolism
Human Genetics
Mice
Mice, Transgenic
Molecular Conformation
Morphogenesis
Morphogenesis - genetics
Nucleic Acid Conformation
Paired Box Transcription Factors - genetics
Paired Box Transcription Factors - physiology
Pituitary gland
Polymer melts
Rodents
Sensors
Stem cells
Three dimensional models
Transcription (Genetics)
Transcription factors
Title Dynamic 3D chromatin architecture contributes to enhancer specificity and limb morphogenesis
URI https://link.springer.com/article/10.1038/s41588-018-0221-x
https://www.ncbi.nlm.nih.gov/pubmed/30262816
https://www.proquest.com/docview/2124705338
https://search.proquest.com/docview/2114696100
https://pubmed.ncbi.nlm.nih.gov/PMC10154999
Volume 50
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