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Article ; Online: Tropomyosin-troponin complex in inherited cardiomyopathies.

Juárez, Christian Krijger / Sequeira, Vasco / van den Boogaard, Malou / Veerman, Christiaan C / Hoetjes, Nicola J / Poel, Edwin / Tanck, Michael W T / Lekanne Deprez, Ronald H / Vermeer, Alexa M C / van der Velden, Jolanda / Amin, Ahmad S

Heart rhythm

2024

Language	English
Publishing date	2024-02-19
Publishing country	United States
Document type	Journal Article
ZDB-ID	2229357-7
ISSN	1556-3871 ; 1547-5271
ISSN (online)	1556-3871
ISSN	1547-5271
DOI	10.1016/j.hrthm.2024.02.034
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Article ; Online: Twisting of the zebrafish heart tube during cardiac looping is a

Tessadori, Federico / Tsingos, Erika / Colizzi, Enrico Sandro / Kruse, Fabian / van den Brink, Susanne C / van den Boogaard, Malou / Christoffels, Vincent M / Merks, Roeland Mh / Bakkers, Jeroen

eLife

2021 Volume 10

Abstract: Organ laterality refers to the left-right asymmetry in disposition and conformation of internal organs and is established during embryogenesis. The heart is the first organ to display visible left-right asymmetries through its left-sided positioning and ... ...

Abstract	Organ laterality refers to the left-right asymmetry in disposition and conformation of internal organs and is established during embryogenesis. The heart is the first organ to display visible left-right asymmetries through its left-sided positioning and rightward looping. Here, we present a new zebrafish loss-of-function allele for
MeSH term(s)	Animals ; Body Patterning ; Embryo, Nonmammalian/embryology ; Heart/embryology ; Organogenesis/genetics ; Transcription Factors/genetics ; Transcription Factors/metabolism ; Zebrafish/embryology ; Zebrafish Proteins/genetics ; Zebrafish Proteins/metabolism
Chemical Substances	Transcription Factors ; Zebrafish Proteins ; tbx5a protein, zebrafish
Language	English
Publishing date	2021-08-10
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.61733
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Article ; Online: Localized and temporal gene regulation in heart development.

Barnett, Phil / van den Boogaard, Malou / Christoffels, Vincent

Current topics in developmental biology

2012 Volume 100, Page(s) 171–201

Abstract: The heart is a structurally complex and functionally heterogeneous organ. The repertoire of genes active in a given cardiac cell defines its shapes and function. This process of localized or heterogeneous gene expression is regulated to a large extent at ...

Abstract	The heart is a structurally complex and functionally heterogeneous organ. The repertoire of genes active in a given cardiac cell defines its shapes and function. This process of localized or heterogeneous gene expression is regulated to a large extent at the level of transcription, dictating the degree particular genes in a cell are active. Therefore, errors in the regulation of localized gene expression are at the basis of misregulation of the delicate process of heart development and function. In this review, we provide an overview of the origin of the different components of the vertebrate heart, and discuss our current understanding of the regulation of localized gene expression in the developing heart. We will also discuss where future research may lead to gain more insight into this process, which should provide much needed insight into the dysregulation of heart development and function, and the etiology of congenital defects.
MeSH term(s)	Animals ; Chromatin/genetics ; Gene Expression Regulation, Developmental ; Heart/embryology ; Heart/growth & development ; Humans ; Myocardium/cytology ; Myocardium/metabolism ; Transcription Factors/metabolism
Chemical Substances	Chromatin ; Transcription Factors
Language	English
Publishing date	2012
Publishing country	United States
Document type	Journal Article ; Review
ISSN	1557-8933 ; 0070-2153
ISSN (online)	1557-8933
ISSN	0070-2153
DOI	10.1016/B978-0-12-387786-4.00004-X
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Article ; Online: From GWAS to function: genetic variation in sodium channel gene enhancer influences electrical patterning.

van den Boogaard, Malou / Barnett, Phil / Christoffels, Vincent M

Trends in cardiovascular medicine

2014 Volume 24, Issue 3, Page(s) 99–104

Abstract: The electrical activity of the heart depends on the correct interplay between key transcription factors and cis-regulatory elements, which together regulate the proper heterogeneous expression of genes encoding for ion channels and other proteins. Genome- ...

Abstract	The electrical activity of the heart depends on the correct interplay between key transcription factors and cis-regulatory elements, which together regulate the proper heterogeneous expression of genes encoding for ion channels and other proteins. Genome-wide association studies of ECG parameters implicated genetic variants in the genes for these factors and ion channels modulating conduction and depolarization. Here, we review recent insights into the regulation of localized expression of ion channel genes and the mechanism by which a single-nucleotide polymorphism (SNP) associated with alterations in cardiac conduction patterns in humans affects the transcriptional regulation of the sodium channel genes, SCN5A and SCN10A. The identification of regulatory elements of electrical activity genes helps to explain the impact of genetic variants in non-coding regulatory DNA sequences on regulation of cardiac conduction and the predisposition for cardiac arrhythmias.
MeSH term(s)	Arrhythmias, Cardiac/genetics ; Humans ; NAV1.5 Voltage-Gated Sodium Channel/genetics ; NAV1.8 Voltage-Gated Sodium Channel/genetics ; Polymorphism, Single Nucleotide/genetics
Chemical Substances	NAV1.5 Voltage-Gated Sodium Channel ; NAV1.8 Voltage-Gated Sodium Channel ; SCN10A protein, human ; SCN5A protein, human
Language	English
Publishing date	2014-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1097434-9
ISSN	1873-2615 ; 1050-1738
ISSN (online)	1873-2615
ISSN	1050-1738
DOI	10.1016/j.tcm.2013.09.001
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Article ; Online: Deep phenotyping of two preclinical mouse models and a cohort of RBM20 mutation carriers reveals no sex-dependent disease severity in

Lennermann, David C / Pepin, Mark E / Grosch, Markus / Konrad, Laura / Kemmling, Elena / Hartmann, Joshua / Nolte, Janica L / Clauder-Münster, Sandra / Kayvanpour, Elham / Sedaghat-Hamedani, Farbod / Haas, Jan / Meder, Benjamin / van den Boogaard, Malou / Amin, Ahmad S / Dewenter, Matthias / Krüger, Marcus / Steinmetz, Lars M / Backs, Johannes / van den Hoogenhof, Maarten M G

American journal of physiology. Heart and circulatory physiology

2022 Volume 323, Issue 6, Page(s) H1296–H1310

Abstract: ... ...

Abstract	RBM20
Language	English
Publishing date	2022-11-11
Publishing country	United States
Document type	Journal Article
ZDB-ID	603838-4
ISSN	1522-1539 ; 0363-6135
ISSN (online)	1522-1539
ISSN	0363-6135
DOI	10.1152/ajpheart.00328.2022
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Article ; Online: Identification and Characterization of a Transcribed Distal Enhancer Involved in Cardiac Kcnh2 Regulation.

van den Boogaard, Malou / van Weerd, Jan Hendrik / Bawazeer, Amira C / Hooijkaas, Ingeborg B / van de Werken, Harmen J G / Tessadori, Federico / de Laat, Wouter / Barnett, Phil / Bakkers, Jeroen / Christoffels, Vincent M

Cell reports

2019 Volume 28, Issue 10, Page(s) 2704–2714.e5

Abstract: The human ether-a-go-go-related gene KCNH2 encodes the voltage-gated potassium channel underlying ... ...

Abstract	The human ether-a-go-go-related gene KCNH2 encodes the voltage-gated potassium channel underlying I
MeSH term(s)	Animals ; CRISPR-Cas Systems/genetics ; Cell Line ; ERG1 Potassium Channel/genetics ; ERG1 Potassium Channel/metabolism ; Enhancer Elements, Genetic/genetics ; Female ; Gene Expression Regulation ; Genetic Loci ; Heart Ventricles/metabolism ; Humans ; Myocardium/metabolism ; Promoter Regions, Genetic/genetics ; Protein Isoforms/genetics ; Protein Isoforms/metabolism ; RNA, Untranslated/genetics ; RNA, Untranslated/metabolism ; Sequence Deletion ; Transcription, Genetic ; Zebrafish
Chemical Substances	ERG1 Potassium Channel ; KCNH2 protein, human ; Kcnh2 protein, mouse ; Protein Isoforms ; RNA, Untranslated
Language	English
Publishing date	2019-09-01
Publishing country	United States
Document type	Journal Article
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2019.08.007
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Article ; Online: OccuPeak: ChIP-Seq peak calling based on internal background modelling.

de Boer, Bouke A / van Duijvenboden, Karel / van den Boogaard, Malou / Christoffels, Vincent M / Barnett, Phil / Ruijter, Jan M

PloS one

2014 Volume 9, Issue 6, Page(s) e99844

Abstract: Unlabelled: ChIP-seq has become a major tool for the genome-wide identification of transcription factor binding or histone modification sites. Most peak-calling algorithms require input control datasets to model the occurrence of background reads to ... ...

Abstract	Unlabelled: ChIP-seq has become a major tool for the genome-wide identification of transcription factor binding or histone modification sites. Most peak-calling algorithms require input control datasets to model the occurrence of background reads to account for local sequencing and GC bias. However, the GC-content of reads in Input-seq datasets deviates significantly from that in ChIP-seq datasets. Moreover, we observed that a commonly used peak calling program performed equally well when the use of a simulated uniform background set was compared to an Input-seq dataset. This contradicts the assumption that input control datasets are necessary to fatefully reflect the background read distribution. Because the GC-content of the abundant single reads in ChIP-seq datasets is similar to those of randomly sampled regions we designed a peak-calling algorithm with a background model based on overlapping single reads. The application, OccuPeak, uses the abundant low frequency tags present in each ChIP-seq dataset to model the background, thereby avoiding the need for additional datasets. Analysis of the performance of OccuPeak showed robust model parameters. Its measure of peak significance, the excess ratio, is only dependent on the tag density of a peak and the global noise levels. Compared to the commonly used peak-calling applications MACS and CisGenome, OccuPeak had the highest sensitivity in an enhancer identification benchmark test, and performed similar in an overlap tests of transcription factor occupation with DNase I hypersensitive sites and H3K27ac sites. Moreover, peaks called by OccuPeak were significantly enriched with cardiac disease-associated SNPs. OccuPeak runs as a standalone application and does not require extensive tweaking of parameters, making its use straightforward and user friendly. Availability: http://occupeak.hfrc.nl.
MeSH term(s)	Animals ; Base Composition ; Base Sequence ; Chromatin Immunoprecipitation ; Genome-Wide Association Study ; Humans ; Models, Genetic ; Polymorphism, Single Nucleotide ; Sequence Analysis, DNA ; Software
Language	English
Publishing date	2014-06-17
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0099844
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Article ; Online: Genetic determinants of P wave duration and PR segment.

Verweij, Niek / Mateo Leach, Irene / van den Boogaard, Malou / van Veldhuisen, Dirk J / Christoffels, Vincent M / Hillege, Hans L / van Gilst, Wiek H / Barnett, Phil / de Boer, Rudolf A / van der Harst, Pim

Circulation. Cardiovascular genetics

2014 Volume 7, Issue 4, Page(s) 475–481

Abstract: Background: The PR interval on the ECG reflects atrial depolarization and atrioventricular nodal delay which can be partially differentiated by P wave duration and PR segment, respectively. Genome-wide association studies have identified several genetic ...

Abstract	Background: The PR interval on the ECG reflects atrial depolarization and atrioventricular nodal delay which can be partially differentiated by P wave duration and PR segment, respectively. Genome-wide association studies have identified several genetic loci for PR interval, but it remains to be determined whether this is driven by P wave duration, PR segment, or both. Methods and results: We replicated 7 of the 9 known PR interval loci in 16 468 individuals of European ancestry. Four loci were unambiguously associated with PR segment, while the others were shared for P wave duration and PR segment. Next, we performed a genome-wide analysis on P wave duration and PR segment separately and identified 5 novel loci. Single-nucleotide polymorphisms in KCND3 (P=8.3×10(-11)) and FADS2 (P=2.7×10(-8)) were associated with P wave duration, whereas single-nucleotide polymorphisms near IL17D (P=2.3×10(-8)), in EFHA1 (P=3.3×10(-10)), and in LRCH1 (P=2.1×10(-8)) were associated with PR segment. Analysis on DNA elements indicated that genome-wide significant single-nucleotide polymorphisms were enriched at genomic regions suggesting active gene transcription in the human right atrium. Quantitative polymerase chain reaction showed that genes were significantly higher expressed in the right atrium and atrioventricular node compared with left ventricle (P=5.6×10(-6)). Conclusions: Genetic associations of PR interval seem to be mainly driven by genetic determinants of the PR segment. Some of the PR interval associations are strengthened by a directional consistent effect of genetic determinants of P wave duration. Through genome-wide association we also identified genetic variants specifically associated with P wave duration which might be relevant for cardiac biology.
MeSH term(s)	Atrioventricular Node/metabolism ; Calcium-Binding Proteins/genetics ; Cohort Studies ; Electrocardiography ; Fatty Acid Desaturases/genetics ; Gene Expression Regulation ; Genetic Loci ; Genome-Wide Association Study ; Genotype ; Heart Atria/metabolism ; Heart Ventricles/metabolism ; Humans ; Interleukin-17/genetics ; Kidney Failure, Chronic/genetics ; Kidney Failure, Chronic/pathology ; Microfilament Proteins/genetics ; Polymorphism, Single Nucleotide ; Shal Potassium Channels/genetics
Chemical Substances	Calcium-Binding Proteins ; IL17D protein, human ; Interleukin-17 ; KCND3 protein, human ; LRCH1 protein, human ; Microfilament Proteins ; Shal Potassium Channels ; Fatty Acid Desaturases (EC 1.14.19.-) ; FADS2 protein, human (EC 1.14.19.3)
Language	English
Publishing date	2014-05-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2477394-3
ISSN	1942-3268 ; 1942-325X
ISSN (online)	1942-3268
ISSN	1942-325X
DOI	10.1161/CIRCGENETICS.113.000373
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Article ; Online: A large permissive regulatory domain exclusively controls Tbx3 expression in the cardiac conduction system.

van Weerd, Jan Hendrik / Badi, Ileana / van den Boogaard, Malou / Stefanovic, Sonia / van de Werken, Harmen J G / Gomez-Velazquez, Melisa / Badia-Careaga, Claudio / Manzanares, Miguel / de Laat, Wouter / Barnett, Phil / Christoffels, Vincent M

Circulation research

2014 Volume 115, Issue 4, Page(s) 432–441

Abstract: Rationale: The evolutionary conserved Tbx3/Tbx5 gene cluster encodes T-box transcription factors that play crucial roles in the development and homeostasis of the cardiac conduction system in human and mouse. Both genes are expressed in overlapping ... ...

Abstract	Rationale: The evolutionary conserved Tbx3/Tbx5 gene cluster encodes T-box transcription factors that play crucial roles in the development and homeostasis of the cardiac conduction system in human and mouse. Both genes are expressed in overlapping patterns and function in strictly tissue-specific and dose-dependent manners, yet, their regulation is poorly understood. Objective: To analyze the mechanism underlying the complex regulation of the Tbx3/Tbx5 cluster. Methods and results: By probing the 3-dimensional architecture of the Tbx3/Tbx5 cluster using high-resolution circular chromosome conformation capture sequencing in vivo, we found that its regulatory landscape is in a preformed conformation similar in embryonic heart, limbs, and brain. Tbx3 and its flanking gene desert form a 1 Mbp loop between CCCTC-binding factor (CTCF)-binding sites that is separated from the neighboring Tbx5 loop. However, Ctcf inactivation did not result in transcriptional regulatory interaction between Tbx3 and Tbx5. Multiple sites within the Tbx3 locus contact the promoter, including sites corresponding to regions known to contain variations in the human genome influencing conduction. We identified an atrioventricular-specific enhancer and a pan-cardiac enhancer that contact the promoter and each other and synergize to activate transcription in the atrioventricular conduction system. Conclusions: We provide a high-resolution model of the 3-dimensional structure and function of the Tbx3/Tbx5 locus and show that the locus is organized in a preformed, permissive structure. The Tbx3 locus forms a CTCF-independent autonomous regulatory domain with multiple combinatorial regulatory elements that control the precise pattern of Tbx3 in the cardiac conduction system.
MeSH term(s)	3' Flanking Region ; Animals ; Binding Sites ; Bone Morphogenetic Proteins/genetics ; Bone Morphogenetic Proteins/metabolism ; CCCTC-Binding Factor ; Chromosomes, Artificial, Bacterial ; DNA, Circular/genetics ; Gene Expression Regulation, Developmental ; Genes, Reporter ; Green Fluorescent Proteins/genetics ; Green Fluorescent Proteins/metabolism ; Heart Conduction System/embryology ; Heart Conduction System/metabolism ; Mice, Inbred C57BL ; Mice, Knockout ; Mice, Transgenic ; Morphogenesis ; Multigene Family ; Repressor Proteins/deficiency ; Repressor Proteins/genetics ; Signal Transduction ; T-Box Domain Proteins/genetics ; T-Box Domain Proteins/metabolism ; Transcription, Genetic ; Transcriptional Activation
Chemical Substances	Bone Morphogenetic Proteins ; CCCTC-Binding Factor ; CTCF protein, human ; Ctcf protein, mouse ; DNA, Circular ; Repressor Proteins ; T-Box Domain Proteins ; T-box transcription factor 5 ; Tbx3 protein, mouse ; Green Fluorescent Proteins (147336-22-9)
Language	English
Publishing date	2014-08-01
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80100-8
ISSN	1524-4571 ; 0009-7330 ; 0931-6876
ISSN (online)	1524-4571
ISSN	0009-7330 ; 0931-6876
DOI	10.1161/CIRCRESAHA.115.303591
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Article ; Online: Genetic variation in T-box binding element functionally affects SCN5A/SCN10A enhancer.

van den Boogaard, Malou / Wong, L Y Elaine / Tessadori, Federico / Bakker, Martijn L / Dreizehnter, Lisa K / Wakker, Vincent / Bezzina, Connie R / 't Hoen, Peter A C / Bakkers, Jeroen / Barnett, Phil / Christoffels, Vincent M

The Journal of clinical investigation

2012 Volume 122, Issue 7, Page(s) 2519–2530

Abstract: The contraction pattern of the heart relies on the activation and conduction of the electrical impulse. Perturbations of cardiac conduction have been associated with congenital and acquired arrhythmias as well as cardiac arrest. The pattern of conduction ...

Abstract	The contraction pattern of the heart relies on the activation and conduction of the electrical impulse. Perturbations of cardiac conduction have been associated with congenital and acquired arrhythmias as well as cardiac arrest. The pattern of conduction depends on the regulation of heterogeneous gene expression by key transcription factors and transcriptional enhancers. Here, we assessed the genome-wide occupation of conduction system-regulating transcription factors TBX3, NKX2-5, and GATA4 and of enhancer-associated coactivator p300 in the mouse heart, uncovering cardiac enhancers throughout the genome. Many of the enhancers colocalized with ion channel genes repressed by TBX3, including the clustered sodium channel genes Scn5a, essential for cardiac function, and Scn10a. We identified 2 enhancers in the Scn5a/Scn10a locus, which were regulated by TBX3 and its family member and activator, TBX5, and are functionally conserved in humans. We also provided evidence that a SNP in the SCN10A enhancer associated with alterations in cardiac conduction patterns in humans disrupts TBX3/TBX5 binding and reduces the cardiac activity of the enhancer in vivo. Thus, the identification of key regulatory elements for cardiac conduction helps to explain how genetic variants in noncoding regulatory DNA sequences influence the regulation of cardiac conduction and the predisposition for cardiac arrhythmias.
MeSH term(s)	Animals ; Base Sequence ; Binding Sites ; Cell Line ; Chromatin Immunoprecipitation ; Consensus Sequence ; Enhancer Elements, Genetic ; Gene Expression Profiling ; Gene Expression Regulation, Developmental ; Genetic Loci ; Genetic Variation ; Heart Conduction System/metabolism ; Humans ; Male ; Mice ; Mice, Transgenic ; Myocardium/metabolism ; NAV1.5 Voltage-Gated Sodium Channel ; NAV1.8 Voltage-Gated Sodium Channel ; Oligonucleotide Array Sequence Analysis ; Polymorphism, Single Nucleotide ; Protein Binding ; Sequence Analysis, DNA ; Sodium Channels/genetics ; T-Box Domain Proteins/metabolism ; Zebrafish
Chemical Substances	NAV1.5 Voltage-Gated Sodium Channel ; NAV1.8 Voltage-Gated Sodium Channel ; SCN10A protein, human ; SCN5A protein, human ; Scn10a protein, mouse ; Scn5a protein, mouse ; Sodium Channels ; T-Box Domain Proteins ; T-box transcription factor 5 ; Tbx3 protein, mouse
Language	English
Publishing date	2012-06-18
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	3067-3
ISSN	1558-8238 ; 0021-9738
ISSN (online)	1558-8238
ISSN	0021-9738
DOI	10.1172/JCI62613
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