TAD boundary deletion causes PITX2-related cardiac electrical and structural defects

While 3D chromatin organization in topologically associating domains (TADs) and loops mediating regulatory element-promoter interactions is crucial for tissue-specific gene regulation, the extent of their involvement in human Mendelian disease is largely unknown. Here, we identify 7 families present...

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Published inNature communications Vol. 15; no. 1; pp. 3380 - 15
Main Authors Baudic, Manon, Murata, Hiroshige, Bosada, Fernanda M., Melo, Uirá Souto, Aizawa, Takanori, Lindenbaum, Pierre, van der Maarel, Lieve E., Guedon, Amaury, Baron, Estelle, Fremy, Enora, Foucal, Adrien, Ishikawa, Taisuke, Ushinohama, Hiroya, Jurgens, Sean J., Choi, Seung Hoan, Kyndt, Florence, Le Scouarnec, Solena, Wakker, Vincent, Thollet, Aurélie, Rajalu, Annabelle, Takaki, Tadashi, Ohno, Seiko, Shimizu, Wataru, Horie, Minoru, Kimura, Takeshi, Ellinor, Patrick T., Petit, Florence, Dulac, Yves, Bru, Paul, Boland, Anne, Deleuze, Jean-François, Redon, Richard, Le Marec, Hervé, Le Tourneau, Thierry, Gourraud, Jean-Baptiste, Yoshida, Yoshinori, Makita, Naomasa, Vieyres, Claude, Makiyama, Takeru, Mundlos, Stephan, Christoffels, Vincent M., Probst, Vincent, Schott, Jean-Jacques, Barc, Julien
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 20.04.2024
Nature Publishing Group
Nature Portfolio
SeriesNature Communications
Subjects
38/15
38/39
38/47
38/91
45/100
45/23
631/208/176
64/60
692/4019/592/2727
Binding sites
Cardiomyocytes
Chromatin remodeling
Conformation
Gene deletion
Gene regulation
Genomes
Heart
Hereditary diseases
Homeobox
Humanities and Social Sciences
Life Sciences
multidisciplinary
Phenotypes
Pluripotency
Science
Science (multidisciplinary)
Stem cells
Ventricle
Online AccessGet full text
ISSN2041-1723
2041-1723
DOI10.1038/s41467-024-47739-x

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Abstract While 3D chromatin organization in topologically associating domains (TADs) and loops mediating regulatory element-promoter interactions is crucial for tissue-specific gene regulation, the extent of their involvement in human Mendelian disease is largely unknown. Here, we identify 7 families presenting a new cardiac entity associated with a heterozygous deletion of 2 CTCF binding sites on 4q25, inducing TAD fusion and chromatin conformation remodeling. The CTCF binding sites are located in a gene desert at 1 Mb from the Paired-like homeodomain transcription factor 2 gene ( PITX2 ). By introducing the ortholog of the human deletion in the mouse genome, we recapitulate the patient phenotype and characterize an opposite dysregulation of PITX2 expression in the sinoatrial node (ectopic activation) and ventricle (reduction), respectively. Chromatin conformation assay performed in human induced pluripotent stem cell-derived cardiomyocytes harboring the minimal deletion identified in family#1 reveals a conformation remodeling and fusion of TADs. We conclude that TAD remodeling mediated by deletion of CTCF binding sites causes a new autosomal dominant Mendelian cardiac disorder. This study identifies an altered chromatin conformation associated to a cardiac disorder observed in 7 independent families. A deletion of 2 diverging CTCF binding sites on 4q25 induces TAD fusion and leads to PITX2 expression dysregulation.
AbstractList While 3D chromatin organization in topologically associating domains (TADs) and loops mediating regulatory element-promoter interactions is crucial for tissue-specific gene regulation, the extent of their involvement in human Mendelian disease is largely unknown. Here, we identify 7 families presenting a new cardiac entity associated with a heterozygous deletion of 2 CTCF binding sites on 4q25, inducing TAD fusion and chromatin conformation remodeling. The CTCF binding sites are located in a gene desert at 1 Mb from the Paired-like homeodomain transcription factor 2 gene (PITX2). By introducing the ortholog of the human deletion in the mouse genome, we recapitulate the patient phenotype and characterize an opposite dysregulation of PITX2 expression in the sinoatrial node (ectopic activation) and ventricle (reduction), respectively. Chromatin conformation assay performed in human induced pluripotent stem cell-derived cardiomyocytes harboring the minimal deletion identified in family#1 reveals a conformation remodeling and fusion of TADs. We conclude that TAD remodeling mediated by deletion of CTCF binding sites causes a new autosomal dominant Mendelian cardiac disorder.This study identifies an altered chromatin conformation associated to a cardiac disorder observed in 7 independent families. A deletion of 2 diverging CTCF binding sites on 4q25 induces TAD fusion and leads to PITX2 expression dysregulation.
While 3D chromatin organization in topologically associating domains (TADs) and loops mediating regulatory element-promoter interactions is crucial for tissue-specific gene regulation, the extent of their involvement in human Mendelian disease is largely unknown. Here, we identify 7 families presenting a new cardiac entity associated with a heterozygous deletion of 2 CTCF binding sites on 4q25, inducing TAD fusion and chromatin conformation remodeling. The CTCF binding sites are located in a gene desert at 1 Mb from the Paired-like homeodomain transcription factor 2 gene (PITX2). By introducing the ortholog of the human deletion in the mouse genome, we recapitulate the patient phenotype and characterize an opposite dysregulation of PITX2 expression in the sinoatrial node (ectopic activation) and ventricle (reduction), respectively. Chromatin conformation assay performed in human induced pluripotent stem cell-derived cardiomyocytes harboring the minimal deletion identified in family#1 reveals a conformation remodeling and fusion of TADs. We conclude that TAD remodeling mediated by deletion of CTCF binding sites causes a new autosomal dominant Mendelian cardiac disorder.While 3D chromatin organization in topologically associating domains (TADs) and loops mediating regulatory element-promoter interactions is crucial for tissue-specific gene regulation, the extent of their involvement in human Mendelian disease is largely unknown. Here, we identify 7 families presenting a new cardiac entity associated with a heterozygous deletion of 2 CTCF binding sites on 4q25, inducing TAD fusion and chromatin conformation remodeling. The CTCF binding sites are located in a gene desert at 1 Mb from the Paired-like homeodomain transcription factor 2 gene (PITX2). By introducing the ortholog of the human deletion in the mouse genome, we recapitulate the patient phenotype and characterize an opposite dysregulation of PITX2 expression in the sinoatrial node (ectopic activation) and ventricle (reduction), respectively. Chromatin conformation assay performed in human induced pluripotent stem cell-derived cardiomyocytes harboring the minimal deletion identified in family#1 reveals a conformation remodeling and fusion of TADs. We conclude that TAD remodeling mediated by deletion of CTCF binding sites causes a new autosomal dominant Mendelian cardiac disorder.
While 3D chromatin organization in topologically associating domains (TADs) and loops mediating regulatory element-promoter interactions is crucial for tissue-specific gene regulation, the extent of their involvement in human Mendelian disease is largely unknown. Here, we identify 7 families presenting a new cardiac entity associated with a heterozygous deletion of 2 CTCF binding sites on 4q25, inducing TAD fusion and chromatin conformation remodeling. The CTCF binding sites are located in a gene desert at 1 Mb from the Paired-like homeodomain transcription factor 2 gene ( PITX2 ). By introducing the ortholog of the human deletion in the mouse genome, we recapitulate the patient phenotype and characterize an opposite dysregulation of PITX2 expression in the sinoatrial node (ectopic activation) and ventricle (reduction), respectively. Chromatin conformation assay performed in human induced pluripotent stem cell-derived cardiomyocytes harboring the minimal deletion identified in family#1 reveals a conformation remodeling and fusion of TADs. We conclude that TAD remodeling mediated by deletion of CTCF binding sites causes a new autosomal dominant Mendelian cardiac disorder. This study identifies an altered chromatin conformation associated to a cardiac disorder observed in 7 independent families. A deletion of 2 diverging CTCF binding sites on 4q25 induces TAD fusion and leads to PITX2 expression dysregulation.
While 3D chromatin organization in topologically associating domains (TADs) and loops mediating regulatory element-promoter interactions is crucial for tissue-specific gene regulation, the extent of their involvement in human Mendelian disease is largely unknown. Here, we identify 7 families presenting a new cardiac entity associated with a heterozygous deletion of 2 CTCF binding sites on 4q25, inducing TAD fusion and chromatin conformation remodeling. The CTCF binding sites are located in a gene desert at 1 Mb from the Paired-like homeodomain transcription factor 2 gene (PITX2). By introducing the ortholog of the human deletion in the mouse genome, we recapitulate the patient phenotype and characterize an opposite dysregulation of PITX2 expression in the sinoatrial node (ectopic activation) and ventricle (reduction), respectively. Chromatin conformation assay performed in human induced pluripotent stem cell-derived cardiomyocytes harboring the minimal deletion identified in family#1 reveals a conformation remodeling and fusion of TADs. We conclude that TAD remodeling mediated by deletion of CTCF binding sites causes a new autosomal dominant Mendelian cardiac disorder.
Abstract While 3D chromatin organization in topologically associating domains (TADs) and loops mediating regulatory element-promoter interactions is crucial for tissue-specific gene regulation, the extent of their involvement in human Mendelian disease is largely unknown. Here, we identify 7 families presenting a new cardiac entity associated with a heterozygous deletion of 2 CTCF binding sites on 4q25, inducing TAD fusion and chromatin conformation remodeling. The CTCF binding sites are located in a gene desert at 1 Mb from the Paired-like homeodomain transcription factor 2 gene (PITX2). By introducing the ortholog of the human deletion in the mouse genome, we recapitulate the patient phenotype and characterize an opposite dysregulation of PITX2 expression in the sinoatrial node (ectopic activation) and ventricle (reduction), respectively. Chromatin conformation assay performed in human induced pluripotent stem cell-derived cardiomyocytes harboring the minimal deletion identified in family#1 reveals a conformation remodeling and fusion of TADs. We conclude that TAD remodeling mediated by deletion of CTCF binding sites causes a new autosomal dominant Mendelian cardiac disorder.
While 3D chromatin organization in topologically associating domains (TADs) and loops mediating regulatory element-promoter interactions is crucial for tissue-specific gene regulation, the extent of their involvement in human Mendelian disease is largely unknown. Here, we identify 7 families presenting a new cardiac entity associated with a heterozygous deletion of 2 CTCF binding sites on 4q25, inducing TAD fusion and chromatin conformation remodeling. The CTCF binding sites are located in a gene desert at 1 Mb from the Paired-like homeodomain transcription factor 2 gene ( PITX2 ). By introducing the ortholog of the human deletion in the mouse genome, we recapitulate the patient phenotype and characterize an opposite dysregulation of PITX2 expression in the sinoatrial node (ectopic activation) and ventricle (reduction), respectively. Chromatin conformation assay performed in human induced pluripotent stem cell-derived cardiomyocytes harboring the minimal deletion identified in family#1 reveals a conformation remodeling and fusion of TADs. We conclude that TAD remodeling mediated by deletion of CTCF binding sites causes a new autosomal dominant Mendelian cardiac disorder.
ArticleNumber 3380
Author Aizawa, Takanori
Bru, Paul
Redon, Richard
Melo, Uirá Souto
Christoffels, Vincent M.
Thollet, Aurélie
Bosada, Fernanda M.
Le Marec, Hervé
Shimizu, Wataru
Horie, Minoru
Makita, Naomasa
Probst, Vincent
Ohno, Seiko
Le Tourneau, Thierry
Schott, Jean-Jacques
Ushinohama, Hiroya
Dulac, Yves
Barc, Julien
van der Maarel, Lieve E.
Deleuze, Jean-François
Baudic, Manon
Kyndt, Florence
Boland, Anne
Mundlos, Stephan
Petit, Florence
Fremy, Enora
Foucal, Adrien
Murata, Hiroshige
Guedon, Amaury
Le Scouarnec, Solena
Baron, Estelle
Choi, Seung Hoan
Makiyama, Takeru
Wakker, Vincent
Takaki, Tadashi
Yoshida, Yoshinori
Rajalu, Annabelle
Jurgens, Sean J.
Gourraud, Jean-Baptiste
Kimura, Takeshi
Ishikawa, Taisuke
Ellinor, Patrick T.
Lindenbaum, Pierre
Vieyres, Claude
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10.3791/52628
ContentType Journal Article
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Snippet While 3D chromatin organization in topologically associating domains (TADs) and loops mediating regulatory element-promoter interactions is crucial for...
Abstract While 3D chromatin organization in topologically associating domains (TADs) and loops mediating regulatory element-promoter interactions is crucial...
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Binding sites
Cardiomyocytes
Chromatin remodeling
Conformation
Gene deletion
Gene regulation
Genomes
Heart
Hereditary diseases
Homeobox
Humanities and Social Sciences
Life Sciences
multidisciplinary
Phenotypes
Pluripotency
Science
Science (multidisciplinary)
Stem cells
Ventricle
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Title TAD boundary deletion causes PITX2-related cardiac electrical and structural defects
URI https://link.springer.com/article/10.1038/s41467-024-47739-x
https://www.ncbi.nlm.nih.gov/pubmed/38643172
https://www.proquest.com/docview/3042251082
https://www.proquest.com/docview/3043069334
https://hal.univ-lille.fr/hal-04630944
https://pubmed.ncbi.nlm.nih.gov/PMC11032321
https://doaj.org/article/973ce46b9b9a4d84b5710238b42950a4
Volume 15
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