Nr2f-dependent allocation of ventricular cardiomyocyte and pharyngeal muscle progenitors

Multiple syndromes share congenital heart and craniofacial muscle defects, indicating there is an intimate relationship between the adjacent cardiac and pharyngeal muscle (PM) progenitor fields. However, mechanisms that direct antagonistic lineage decisions of the cardiac and PM progenitors within the anterior mesoderm of vertebrates are not understood. Here, we identify that retinoic acid (RA) signaling directly promotes the expression of the transcription factor Nr2f1a within the anterior lateral plate mesoderm. Using zebrafish nr2f1a and nr2f2 mutants, we find that Nr2f1a and Nr2f2 have redundant requirements restricting ventricular cardiomyocyte (CM) number and promoting development of the posterior PMs. Cre-mediated genetic lineage tracing in nr2f1a; nr2f2 double mutants reveals that tcf21+ progenitor cells, which can give rise to ventricular CMs and PM, more frequently become ventricular CMs potentially at the expense of posterior PMs in nr2f1a; nr2f2 mutants. Our studies reveal insights into the molecular etiology that may underlie developmental syndromes that share heart, neck and facial defects as well as the phenotypic variability of congenital heart defects associated with NR2F mutations in humans.

[1]  Vincent L. Butty,et al.  Failed Progenitor Specification Underlies the Cardiopharyngeal Phenotypesin a Zebrafish Model of 22q11.2 Deletion Syndrome , 2018, Cell reports.

[2]  J Gage Crump,et al.  Essential Role of Nr2f Nuclear Receptors in Patterning the Vertebrate Upper Jaw. , 2018, Developmental cell.

[3]  Padmapriyadarshini Ravisankar,et al.  Nr2f1a balances atrial chamber and atrioventricular canal size via BMP signaling-independent and -dependent mechanisms. , 2017, Developmental biology.

[4]  Caroline E. Burns,et al.  Unique developmental trajectories and genetic regulation of ventricular and outflow tract progenitors in the zebrafish second heart field , 2017, Development.

[5]  J. Huisken,et al.  Continuous addition of progenitors forms the cardiac ventricle in zebrafish , 2017, bioRxiv.

[6]  Bin Zhou,et al.  Transcriptomic Profiling Maps Anatomically Patterned Subpopulations among Single Embryonic Cardiac Cells. , 2016, Developmental cell.

[7]  J. Hanken,et al.  Evolution of the head-trunk interface in tetrapod vertebrates , 2016, eLife.

[8]  Padmapriyadarshini Ravisankar,et al.  Rdh10a Provides a Conserved Critical Step in the Synthesis of Retinoic Acid during Zebrafish Embryogenesis , 2015, PloS one.

[9]  Padmapriyadarshini Ravisankar,et al.  Excessive feedback of Cyp26a1 promotes cell non-autonomous loss of retinoic acid signaling. , 2015, Developmental biology.

[10]  Kimara L. Targoff,et al.  Origin, Specification, and Plasticity of the Great Vessels of the Heart , 2015, Current Biology.

[11]  Lionel Christiaen,et al.  A new heart for a new head in vertebrate cardiopharyngeal evolution , 2015, Nature.

[12]  R. Diogo,et al.  Muscles of Chondrichthyan Paired Appendages: Comparison With Osteichthyans, Deconstruction of the Fore–Hindlimb Serial Homology Dogma, and New Insights on the Evolution of the Vertebrate Neck , 2015, Anatomical record.

[13]  Robert Passier,et al.  Atrial-like cardiomyocytes from human pluripotent stem cells are a robust preclinical model for assessing atrial-selective pharmacology , 2015, EMBO molecular medicine.

[14]  Wissam Hamou,et al.  Clonal analysis reveals a common origin between nonsomite-derived neck muscles and heart myocardium , 2015, Proceedings of the National Academy of Sciences.

[15]  Benjamin D. Simons,et al.  Early lineage restriction in temporally distinct populations of Mesp1 progenitors during mammalian heart development , 2014, Nature Cell Biology.

[16]  Marc Gewillig,et al.  Rare variants in NR2F2 cause congenital heart defects in humans. , 2014, American journal of human genetics.

[17]  P. Ingham,et al.  Divergence of zebrafish and mouse lymphatic cell fate specification pathways , 2014, Development.

[18]  Wei Wang,et al.  NK4 Antagonizes Tbx1/10 to Promote Cardiac versus Pharyngeal Muscle Fate in the Ascidian Second Heart Field , 2013, PLoS biology.

[19]  Joshua Bloomekatz,et al.  tal1 Regulates the formation of intercellular junctions and the maintenance of identity in the endocardium. , 2013, Developmental biology.

[20]  Caroline E. Burns,et al.  Heart field origin of great vessel precursors relies on nkx2.5-mediated vasculogenesis , 2013, Nature Cell Biology.

[21]  J. Waxman,et al.  Depletion of Retinoic Acid Receptors Initiates a Novel Positive Feedback Mechanism that Promotes Teratogenic Increases in Retinoic Acid , 2013, PLoS genetics.

[22]  R. Lanz,et al.  Atrial identity is determined by a COUP-TFII regulatory network. , 2013, Developmental cell.

[23]  N. Mongan,et al.  Polycomb recruitment attenuates retinoic acid–induced transcription of the bivalent NR2F1 gene , 2013, Nucleic acids research.

[24]  Caroline E. Burns,et al.  Tbx1 is required for second heart field proliferation in zebrafish , 2013, Developmental dynamics : an official publication of the American Association of Anatomists.

[25]  Caroline E. Burns,et al.  Zebrafish second heart field development relies on progenitor specification in anterior lateral plate mesoderm and nkx2.5 function , 2013, Development.

[26]  J. Hegesh,et al.  Pharyngeal mesoderm regulatory network controls cardiac and head muscle morphogenesis , 2012, Proceedings of the National Academy of Sciences.

[27]  V. Prince,et al.  Expression and retinoic acid regulation of the zebrafish nr2f orphan nuclear receptor genes , 2012, Developmental dynamics : an official publication of the American Association of Anatomists.

[28]  D. Moras,et al.  Retinoic Acid Receptors Recognize the Mouse Genome through Binding Elements with Diverse Spacing and Topology* , 2012, The Journal of Biological Chemistry.

[29]  P. Hu,et al.  Identification and Characterization of a Novel Retinoic Acid Response Element in Zebrafish cyp26a1 Promoter , 2012, Anatomical record.

[30]  A. Werdich,et al.  The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion , 2011, Development.

[31]  J. Holdway,et al.  Development and Stem Cells Research Article , 2022 .

[32]  Huai-Jen Tsai,et al.  Zebrafish cardiac development requires a conserved secondary heart field , 2011, Development.

[33]  Caroline E. Burns,et al.  Latent TGFβ binding protein 3 identifies a second heart field in zebrafish , 2011, Nature.

[34]  Y. Makita,et al.  5.78 Mb terminal deletion of chromosome 15q in a girl, evaluation of NR2F2 as candidate gene for congenital heart defects. , 2011, European journal of medical genetics.

[35]  D. Yelon,et al.  Zebrafish retinoic acid receptors function as context-dependent transcriptional activators. , 2011, Developmental biology.

[36]  B. Morrow,et al.  A Tbx1-Six1/Eya1-Fgf8 genetic pathway controls mammalian cardiovascular and craniofacial morphogenesis. , 2011, The Journal of clinical investigation.

[37]  J. Qin,et al.  Coup d'Etat: an orphan takes control. , 2011, Endocrine reviews.

[38]  V. Abdala,et al.  Comparative anatomy, homologies and evolution of the pectoral and forelimb musculature of tetrapods with special attention to extant limbed amphibians and reptiles , 2010, Journal of anatomy.

[39]  F. Lescroart,et al.  Clonal analysis reveals common lineage relationships between head muscles and second heart field derivatives in the mouse embryo , 2010, Development.

[40]  K. Patel,et al.  The occipital lateral plate mesoderm is a novel source for vertebrate neck musculature , 2010, Development.

[41]  Lionel Christiaen,et al.  Early Chordate Origins of the Vertebrate Second Heart Field , 2010, Science.

[42]  D. Yelon,et al.  Dhrs3a regulates retinoic acid biosynthesis through a feedback inhibition mechanism. , 2010, Developmental biology.

[43]  M. Kirby,et al.  The role of secondary heart field in cardiac development. , 2009, Developmental biology.

[44]  O. Poch,et al.  Cell-Specific Interaction of Retinoic Acid Receptors with Target Genes in Mouse Embryonic Fibroblasts and Embryonic Stem Cells , 2009, Molecular and Cellular Biology.

[45]  Richard L Robertson,et al.  NR2F1 deletion in a patient with a de novo paracentric inversion, inv(5)(q15q33.2), and syndromic deafness , 2009, American journal of medical genetics. Part A.

[46]  E. Tzahor,et al.  Heart and craniofacial muscle development: a new developmental theme of distinct myogenic fields. , 2009, Developmental biology.

[47]  D. Yelon,et al.  Hoxb5b acts downstream of retinoic acid signaling in the forelimb field to restrict heart field potential in zebrafish. , 2008, Developmental cell.

[48]  G. Duester,et al.  Retinoic acid controls heart anteroposterior patterning by down‐regulating Isl1 through the Fgf8 pathway , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[49]  Markus Affolter,et al.  Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. , 2008, Developmental biology.

[50]  R. Schwartz,et al.  Retinoic acid deficiency alters second heart field formation , 2008, Proceedings of the National Academy of Sciences.

[51]  S. Hughes,et al.  Development of mandibular, hyoid and hypobranchial muscles in the zebrafish: homologies and evolution of these muscles within bony fishes and tetrapods , 2008, BMC Developmental Biology.

[52]  R. Hochstenbach,et al.  Proportional growth failure and oculocutaneous albinism in a girl with a 6.87 Mb deletion of region 15q26.2-->qter. , 2007, European journal of medical genetics.

[53]  M. Kirby,et al.  Heart field: from mesoderm to heart tube. , 2007, Annual review of cell and developmental biology.

[54]  B. Thisse,et al.  High-resolution in situ hybridization to whole-mount zebrafish embryos , 2007, Nature Protocols.

[55]  R. Blomhoff,et al.  A robust characterization of retinoic acid response elements based on a comparison of sites in three species , 2005, The Journal of Steroid Biochemistry and Molecular Biology.

[56]  N. Satoh,et al.  Oligonucleotide‐based microarray analysis of retinoic acid target genes in the protochordate, Ciona intestinalis , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[57]  P. Ingham,et al.  Retinoic Acid Signaling Restricts the Cardiac Progenitor Pool , 2005, Science.

[58]  M. Tsai,et al.  The Nuclear Orphan Receptor COUP-TFII Is Required for Limb and Skeletal Muscle Development , 2004, Molecular and Cellular Biology.

[59]  D. Meyer,et al.  Organization of cardiac chamber progenitors in the zebrafish blastula , 2004, Development.

[60]  J. Bastien,et al.  Nuclear retinoid receptors and the transcription of retinoid-target genes. , 2004, Gene.

[61]  R. Ho,et al.  The zebrafish van gogh mutation disrupts tbx1, which is involved in the DiGeorge deletion syndrome in humans , 2003, Development.

[62]  K. Hashimoto,et al.  Regulation of constitutive expression of mouse PTEN by the 5′-untranslated region , 2003, Oncogene.

[63]  E. Olson,et al.  Control of Facial Muscle Development by MyoR and Capsulin , 2002, Science.

[64]  R. Blomhoff,et al.  Gene expression regulation by retinoic acid Published, JLR Papers in Press, August 16, 2002. DOI 10.1194/jlr.R100015-JLR200 , 2002, Journal of Lipid Research.

[65]  Antonio Baldini,et al.  DiGeorge syndrome: the use of model organisms to dissect complex genetics. , 2002, Human molecular genetics.

[66]  P. Ingham,et al.  The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. , 2001, Development.

[67]  M. Tsai,et al.  COUP-TF orphan nuclear receptors in development and differentiation , 2000, Cellular and Molecular Life Sciences CMLS.

[68]  Michael C Crair,et al.  The Nuclear Orphan Receptor COUP-TFI Is Required for Differentiation of Subplate Neurons and Guidance of Thalamocortical Axons , 1999, Neuron.

[69]  M. Tsai,et al.  The orphan nuclear receptor COUP-TFII is required for angiogenesis and heart development. , 1999, Genes & development.

[70]  P. Chambon,et al.  Embryonic retinoic acid synthesis is essential for early mouse post-implantation development , 1999, Nature Genetics.

[71]  G. Muscat,et al.  The orphan nuclear receptor, COUP-TF II, inhibits myogenesis by post-transcriptional regulation of MyoD function: COUP-TF II directly interacts with p300 and myoD. , 1998, Nucleic acids research.

[72]  H Okamoto,et al.  High-frequency generation of transgenic zebrafish which reliably express GFP in whole muscles or the whole body by using promoters of zebrafish origin. , 1997, Developmental biology.

[73]  C. Kimmel,et al.  Musculoskeletal patterning in the pharyngeal segments of the zebrafish embryo. , 1997, Development.

[74]  J. Hixson,et al.  Identification of promoter sequences in the 5' untranslated region of the baboon apolipoprotein[a] gene. , 1996, Journal of lipid research.

[75]  C. Pals,et al.  Cloning and expression during development of three murine members of the COUP family of nuclear orphan receptors , 1994, Mechanisms of Development.

[76]  A. Sater,et al.  Features of embryonic induction. , 1988, Development.