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TETs Regulate Proepicardial Cell Migration Through Extracellular Matrix Organization During Zebrafish Cardiogenesis

Yahui Lan, H. Pan, Cheng Li, Kelly M. Banks, J. Sam, Bo Ding, O. Elemento, M. Goll, T. Evans
Published 2019 · Biology, Medicine

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SUMMARY Ten-eleven translocation (Tet) enzymes (Tet1/2/3) mediate 5-methylcytosine (5mC) hydroxylation, which can facilitate DNA demethylation and thereby impact gene expression. Studied mostly for how mutant isoforms impact cancer, the normal roles for Tet enzymes during organogenesis are largely unknown. By analyzing compound mutant zebrafish, we discovered a requirement for Tet2/3 activity in the embryonic heart for recruitment of epicardial progenitors, associated with development of the atrial-ventricular canal (AVC). Through a combination of methylation, hydroxymethylation, and transcript profiling, the genes encoding the activin A subunit Inhbaa (in endocardium) and Sox9b (in myocardium) were implicated as demethylation targets of Tet2/3 and critical for organization of AVC-localized extracellular matrix (ECM), facilitating migration of epicardial progenitors onto the developing heart tube. This study elucidates essential DNA demethylation modifications that govern gene expression changes during cardiac development with striking temporal and lineage specificities, highlighting complex interactions in multiple cell populations during development of the vertebrate heart.
This paper references
10.1161/01.RES.73.3.559
Development of the cardiac coronary vascular endothelium, studied with antiendothelial antibodies, in chicken-quail chimeras.
R. Poelmann (1993)
Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development.
J. Yang (1995)
10.1002/AJA.1002030302
Stages of embryonic development of the zebrafish
C. Kimmel (1995)
10.1006/DBIO.1997.8801
Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart.
R. Dettman (1998)
10.1016/S0091-679X(08)61821-X
Analysis of protein and gene expression.
T. Jowett (1999)
10.1101/GAD.13.22.2983
Gata5 is required for the development of the heart and endoderm in zebrafish.
J. Reiter (1999)
10.1038/nm742
Heart-valve mesenchyme formation is dependent on hyaluronan-augmented activation of ErbB2–ErbB3 receptors
T. Camenisch (2002)
10.1016/S1359-6101(03)00044-3
Transforming growth factor beta in cardiovascular development and function.
M. Azhar (2003)
10.1016/S0092-8674(03)00432-X
Mechanisms of TGF-β Signaling from Cell Membrane to the Nucleus
Yigong Shi (2003)
10.1002/dvdy.10335
Evidence for an extracellular matrix bridge guiding proepicardial cell migration to the myocardium of chick embryos
P. Nahirney (2003)
10.1002/dvdy.10356
Germ‐line transmission of a myocardium‐specific GFP transgene reveals critical regulatory elements in the cardiac myosin light chain 2 promoter of zebrafish
Chiu-Ju Huang (2003)
10.1152/PHYSIOLGENOMICS.00060.2004
A role for Tbx5 in proepicardial cell migration during cardiogenesis.
C. J. Hatcher (2004)
10.1016/J.YDBIO.2003.09.042
T-box binding sites are required for activity of a cardiac GATA-4 enhancer.
Alice Heicklen-Klein (2004)
10.1016/S1534-5807(04)00133-9
The clonal origin of myocardial cells in different regions of the embryonic mouse heart.
S. Meilhac (2004)
10.1242/dev.01674
A pair of Sox: distinct and overlapping functions of zebrafish sox9 co-orthologs in craniofacial and pectoral fin development
Yi-Lin Yan (2005)
10.1146/ANNUREV.BIOCHEM.74.010904.153721
Eukaryotic cytosine methyltransferases.
M. G. Goll (2005)
10.1038/nrg1655
DNA methylation and human disease
K. Robertson (2005)
10.1016/S0074-7696(05)43005-3
Cell biology of cardiac cushion development.
Anthony D. Person (2005)
10.1016/J.YGCEN.2005.04.003
Cloning of a second form of activin-betaA cDNA and regulation of activin-betaA subunits and activin type II receptor mRNA expression by gonadotropin in the zebrafish ovary.
Tamara DiMuccio (2005)
10.2144/000112135
Purification of hearts from zebrafish embryos.
C. G. Burns (2006)
10.1016/J.BBRC.2006.04.148
Activation and roles of ALK4/ALK7-mediated maternal TGFbeta signals in zebrafish embryo.
Zhihui Sun (2006)
10.1161/01.RES.0000197782.21444.8F
Control of cardiac growth by histone acetylation/deacetylation.
J. Backs (2006)
Activin-betaA signaling is required for zebrafish fin regeneration.
Anna Jaźwińska (2007)
10.1016/j.cub.2007.07.019
Activin-βA Signaling Is Required for Zebrafish Fin Regeneration
Anna Jaźwińska (2007)
10.1016/J.YDBIO.2007.02.002
Sox9 is required for precursor cell expansion and extracellular matrix organization during mouse heart valve development.
J. Lincoln (2007)
10.1038/nature05987
DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA
Steen K T Ooi (2007)
10.1007/s12199-007-0007-8
Epigenetic abnormalities in cardiac hypertrophy and heart failure
H. Mano (2008)
10.1101/gad.1629408
Foxn4 directly regulates tbx2b expression and atrioventricular canal formation.
N. Chi (2008)
10.1002/dvdy.21725
Origin and fate of cardiac mesenchyme
Brian S Snarr (2008)
10.1186/gb-2008-9-9-r137
Model-based Analysis of ChIP-Seq (MACS)
Yong Zhang (2008)
10.1016/j.ydbio.2007.10.007
Development of the proepicardial organ in the zebrafish.
F. Serluca (2008)
10.1387/ijdb.072340ar
Embryonic development of the proepicardium and coronary vessels.
A. Ratajska (2008)
10.1073/pnas.0900635106
T-box 2, a mediator of Bmp-Smad signaling, induced hyaluronan synthase 2 and Tgfβ2 expression and endocardial cushion formation
Manabu Shirai (2009)
10.1016/j.mod.2009.07.002
Notch-responsive cells initiate the secondary transition in larval zebrafish pancreas
Michael J. Parsons (2009)
10.1172/JCI39104
The basics of epithelial-mesenchymal transition.
R. Kalluri (2009)
10.1093/bioinformatics/btp324
Fast and accurate short read alignment with Burrows–Wheeler transform
Heng Li (2009)
10.1016/j.bbrc.2010.08.064
Epigenetic regulation of neonatal cardiomyocytes differentiation.
Cecy Ying-Chuck Kou (2010)
10.1161/CIRCRESAHA.110.217950
Tbx5 and Bmp Signaling Are Essential for Proepicardium Specification in Zebrafish
Jiandong Liu (2010)
10.1126/science.1190614
Epigenetic Reprogramming in Plant and Animal Development
S. Feng (2010)
10.1038/nature08873
Coronary arteries form by developmental reprogramming of venous cells
K. Red-Horse (2010)
10.1016/j.yexcr.2010.07.006
TGFβ2-mediated production of hyaluronan is important for the induction of epicardial cell differentiation and invasion.
Evisabel A Craig (2010)
10.1016/j.ydbio.2009.10.003
Gata4 directs development of cardiac-inducing endoderm from ES cells.
Audrey Holtzinger (2010)
10.1016/j.devcel.2010.07.017
BMP signals promote proepicardial protrusion necessary for recruitment of coronary vessel and epicardial progenitors to the heart.
Y. Ishii (2010)
10.1038/nature08683
DNMT1 Maintains Progenitor Function in Self-Renewing Somatic Tissue
George L Sen (2010)
10.1242/dev.067454
Nephronectin regulates atrioventricular canal differentiation via Bmp4-Has2 signaling in zebrafish
Chinmoy Patra (2011)
10.1126/science.1210944
Tet-Mediated Formation of 5-Carboxylcytosine and Its Excision by TDG in Mammalian DNA
Y. He (2011)
10.1007/s12265-011-9313-z
Patterning and Development of the Atrioventricular Canal in Zebrafish
David S. Peal (2011)
10.1007/s00018-011-0884-2
Tbx2 and Tbx3 induce atrioventricular myocardial development and endocardial cushion formation
Reena Singh (2011)
10.1016/j.devcel.2011.06.033
Semaphorin-PlexinD1 signaling limits angiogenic potential via the VEGF decoy receptor sFlt1.
T. Zygmunt (2011)
10.1002/dvdy.22521
Long form of latent TGF‐β binding protein 1 (Ltbp1L) regulates cardiac valve development
V. Todorovic (2011)
10.1242/dev.067041
tcf21+ epicardial cells adopt non-myocardial fates during zebrafish heart development and regeneration
K. Kikuchi (2011)
10.1016/j.devcel.2011.06.022
Notch initiates the endothelial-to-mesenchymal transition in the atrioventricular canal through autocrine activation of soluble guanylyl cyclase.
A. Chang (2011)
10.1161/CIRCULATIONAHA.110.956839
Epigenetic modifications: basic mechanisms and role in cardiovascular disease.
D. Handy (2011)
10.1038/nature10222
Chromatin regulation by Brg1 underlies heart muscle development and disease
Calvin T. Hang (2011)
10.1101/gad.179184.111
Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation.
H. Wu (2011)
10.1002/bdra.20804
Wnt signaling regulates atrioventricular canal formation upstream of BMP and Tbx2.
M. Verhoeven (2011)
10.1371/journal.pgen.1002781
Base-Pair Resolution DNA Methylation Sequencing Reveals Profoundly Divergent Epigenetic Landscapes in Acute Myeloid Leukemia
A. Akalin (2012)
10.1101/gad.198747.112
DNA methyltransferase3A as a molecular switch mediating the neural tube-to-neural crest fate transition.
Naiying Hu (2012)
10.1016/j.ydbio.2012.03.023
In vivo Wnt signaling tracing through a transgenic biosensor fish reveals novel activity domains.
E. Moro (2012)
10.1016/j.diff.2012.04.001
Atrioventricular valve development: new perspectives on an old theme.
Annemarieke de Vlaming (2012)
10.1093/glycob/cws095
Versican/PG-M is essential for ventricular septal formation subsequent to cardiac atrioventricular cushion development.
S. Hatano (2012)
10.1101/gr.134833.111
Dynamics of enhancer chromatin signatures mark the transition from pluripotency to cell specification during embryogenesis.
O. Bogdanović (2012)
10.1242/dev.081869
SUMO1-activating enzyme subunit 1 is essential for the survival of hematopoietic stem/progenitor cells in zebrafish
X. Li (2012)
10.1161/CIRCULATIONAHA.111.040352
Epithelial-to-Mesenchymal and Endothelial-to-Mesenchymal Transition: From Cardiovascular Development to Disease
J. Kovacic (2012)
10.1093/abbs/gmr090
Epigenetic mechanisms in cardiac development and disease.
Marcus Vallaster (2012)
10.1124/mol.113.086413
Sox9b Is Required for Epicardium Formation and Plays a Role in TCDD-Induced Heart Malformation in Zebrafish
Peter Hofsteen (2013)
10.1038/nature12750
TET enzymes, TDG and the dynamics of DNA demethylation
R. M. Kohli (2013)
10.1038/nrm3589
TETonic shift: biological roles of TET proteins in DNA demethylation and transcription
William A Pastor (2013)
10.1016/j.devcel.2012.12.015
Combined deficiency of Tet1 and Tet2 causes epigenetic abnormalities but is compatible with postnatal development.
M. Dawlaty (2013)
10.1371/journal.pone.0060244
Endocardial to Myocardial Notch-Wnt-Bmp Axis Regulates Early Heart Valve Development
Y. Wang (2013)
10.1186/1471-213X-14-18
Multiple modes of proepicardial cell migration require heartbeat
Jessica S Plavicki (2013)
10.1242/dev.113639
The sinus venosus contributes to coronary vasculature through VEGFC-stimulated angiogenesis
H. Chen (2014)
10.1086/675979
Epigenetic Modifications: Basic Mechanisms and Role in Cardiovascular Disease (2013 Grover Conference Series)
J. Loscalzo (2014)
10.3390/jdb2020101
The Epicardium in the Embryonic and Adult Zebrafish
M. Peralta (2014)
10.1038/leu.2013.337
The Ten-Eleven Translocation-2 (TET2) gene in hematopoiesis and hematopoietic diseases
E. Solary (2014)
10.3389/fphys.2014.00318
Mechanical regulation of cardiac development
Stephanie E. Lindsey (2014)
10.1016/j.molcel.2014.08.026
5mC oxidation by Tet2 modulates enhancer activity and timing of transcriptome reprogramming during differentiation.
G. Hon (2014)
10.1128/MCB.01061-13
TET2 Plays an Essential Role in Erythropoiesis by Regulating Lineage-Specific Genes via DNA Oxidative Demethylation in a Zebrafish Model
L. Ge (2014)
10.1016/j.devcel.2014.03.003
Loss of Tet enzymes compromises proper differentiation of embryonic stem cells.
M. Dawlaty (2014)
10.1159/000360766
Epigenetics of Cardiovascular Disease: A New ‘Beat' in Coronary Artery Disease
P. Turgeon (2014)
10.1016/j.celrep.2013.11.044
Hydroxymethylation at gene regulatory regions directs stem/early progenitor cell commitment during erythropoiesis.
J. Madzo (2014)
10.1387/ijdb.140288jp
Construction and characterization of a sox9b transgenic reporter line.
Jessica S Plavicki (2014)
10.1073/pnas.1322921111
Distinct roles of the methylcytosine oxidases Tet1 and Tet2 in mouse embryonic stem cells
Y. Huang (2014)
10.1038/ncomms7921
Epigenomic evolution in diffuse large B-cell lymphomas
H. Pan (2015)
10.1038/ng.3272
FBXL10 protects Polycomb-bound genes from hypermethylation
M. Boulard (2015)
10.1242/dev.125252
SOX9 modulates the expression of key transcription factors required for heart valve development
Victoria Garside (2015)
10.1111/imr.12239
TET proteins and 5‐methylcytosine oxidation in hematological cancers
M. Ko (2015)
10.1016/j.molcel.2015.05.017
Engineering of a Histone-Recognition Domain in Dnmt3a Alters the Epigenetic Landscape and Phenotypic Features of Mouse ESCs.
K. Noh (2015)
10.1016/j.celrep.2015.07.025
Overlapping Requirements for Tet2 and Tet3 in Normal Development and Hematopoietic Stem Cell Emergence.
Cheng Li (2015)
10.1038/ncomms7315
Developmental enhancers revealed by extensive DNA methylome maps of zebrafish early embryos
H. J. Lee (2015)
Engineering of ahistone-recognition domain in Dnmt3a alters the epigenetic landscape and phenotypic features of mouse
K-M Noh (2015)
10.1073/pnas.1617802113
Tet proteins influence the balance between neuroectodermal and mesodermal fate choice by inhibiting Wnt signaling
Xia Li (2016)
10.1038/ncomms12418
DNA hydroxymethylation controls cardiomyocyte gene expression in development and hypertrophy
C. Greco (2016)
10.3390/jcm5020027
Epicardial Epithelial-to-Mesenchymal Transition in Heart Development and Disease
Michael Krainock (2016)
10.1371/journal.pone.0166575
5'-Hydroxymethylcytosine Precedes Loss of CpG Methylation in Enhancers and Genes Undergoing Activation in Cardiomyocyte Maturation
David K. Kranzhöfer (2016)
10.1038/ng.3522
Active DNA demethylation at enhancers during the vertebrate phylotypic period
O. Bogdanović (2016)
10.1038/nature20095
TET-mediated DNA demethylation controls gastrulation by regulating Lefty–Nodal signalling
Hai-Qiang Dai (2016)
10.1101/gad.276568.115
Role of TET enzymes in DNA methylation, development, and cancer.
K. D. Rasmussen (2016)
10.1016/j.ydbio.2016.02.003
Id4 functions downstream of Bmp signaling to restrict TCF function in endocardial cells during atrioventricular valve development.
Suchit Ahuja (2016)
10.1371/journal.pgen.1006987
Tet-mediated DNA hydroxymethylation regulates retinal neurogenesis by modulating cell-extrinsic signaling pathways
Pawat Seritrakul (2017)
10.1177/1535370217732737
The canonical way to make a heart: β-catenin and plakoglobin in heart development and remodeling
O. Piven (2017)
10.1038/s41588-017-0002-y
TET proteins safeguard bivalent promoters from de novo methylation in human embryonic stem cells
N. Verma (2017)
10.7554/eLife.20728
Oncogenic BRAF disrupts thyroid morphogenesis and function via twist expression
Viviana Anelli (2017)
10.1038/nrg.2017.33
TET-mediated active DNA demethylation: mechanism, function and beyond
Xiaoji Wu (2017)
WISH for AVC marker bmp4 in 48 hpf and confocal imaging for GFP-labeled PE and epicardium in 72-hpf control and IWR-1-treated larvae



This paper is referenced by
10.1093/bfgp/elab001
New tools for 'ZEBRA-FISHING'.
V. Bergo (2021)
10.1016/j.celrep.2020.108632
Tet Proteins Regulate Neutrophil Granulation in Zebrafish through Demethylation of socs3b mRNA
Kelly M. Banks (2021)
10.1007/978-1-0716-0876-0_16
Immunohistochemical Detection of 5-Hydroxymethylcytosine and 5-Carboxylcytosine in Sections of Zebrafish Embryos.
P. Jessop (2021)
10.1242/dev.191320
The ECM as a driver of heart development and repair
Christopher J. Derrick (2021)
10.1093/bfgp/elab022
DNA methylation and histone modifications are essential for regulation of stem cell formation and differentiation in zebrafish development.
Alissa D Marchione (2021)
10.1097/FJC.0000000000000926
Agrin-YAP promotes the proliferation of epicardial cells.
X. Jing (2020)
10.14814/phy2.14396
Sexual dimorphism in cardiac transcriptome associated with a troponin C murine model of hypertrophic cardiomyopathy
Karissa M. Dieseldorff Jones (2020)
10.3390/ijms21228610
Cardiac ECM: Its Epigenetic Regulation and Role in Heart Development and Repair
Rui Song (2020)
10.1016/j.omtn.2020.05.033
LINC-PINT Suppresses the Aggressiveness of Thyroid Cancer by Downregulating miR-767-5p to Induce TET2 Expression
Meng Jia (2020)
10.1007/s11033-020-05602-4
The role of molecular mechanism of Ten-Eleven Translocation2 (TET2) family proteins in pathogenesis of cardiovascular diseases (CVDs)
F. J. Zadeh (2020)
10.36069/jols/20190901
Epigenetic Regulation of Cardiac Development and Disease through DNA Methylation.
Yahui Lan (2019)
10.1016/j.gene.2019.144049
Role of epigenetics in zebrafish development.
Satheeswaran Balasubramanian (2019)
10.3389/fcell.2019.00310
Activation of Galectin-3 (LGALS3) Transcription by Injurious Stimuli in the Liver Is Commonly Mediated by BRG1
Zilong Li (2019)
10.1016/j.semcdb.2019.10.011
Cardiac progenitors and paracrine mediators in cardiogenesis and heart regeneration.
Nevin Witman (2019)
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