NK4 Antagonizes Tbx1/10 to Promote Cardiac versus Pharyngeal Muscle Fate in the Ascidian Second Heart Field

Cross inhibition between NK4 and TBX1 transcription factors specifies heart versus pharyngeal muscle fates by promoting the activation of tissue-specific regulators in distinct precursors within the cardiopharyngeal lineage of the ascidian, Ciona intestinalis.

[1]  Ken Dewar,et al.  Improved genome assembly and evidence-based global gene model set for the chordate Ciona intestinalis: new insight into intron and operon populations , 2008, Genome Biology.

[2]  Kimara L. Targoff,et al.  Nkx genes regulate heart tube extension and exert differential effects on ventricular and atrial cell number. , 2008, Developmental biology.

[3]  M. Levine,et al.  Evolutionary origins of the vertebrate heart: Specification of the cardiac lineage in Ciona intestinalis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[4]  M. Levine,et al.  Isolation of sea squirt (Ciona) gametes, fertilization, dechorionation, and development. , 2009, Cold Spring Harbor protocols.

[5]  V. Papaioannou,et al.  DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1 , 2001, Nature Genetics.

[6]  P. Francis-West,et al.  The differentiation and morphogenesis of craniofacial muscles , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[7]  E. Mancini,et al.  Structure of the DNA‐bound T‐box domain of human TBX1, a transcription factor associated with the DiGeorge syndrome , 2011, Proteins.

[8]  N. Satoh,et al.  Retinoic acid-driven Hox1 is required in the epidermis for forming the otic/atrial placodes during ascidian metamorphosis , 2012, Development.

[9]  Susan Tang,et al.  Tbx1 Regulates Proliferation and Differentiation of Multipotent Heart Progenitors , 2009, Circulation research.

[10]  Kazuho Ikeo,et al.  A web‐based interactive developmental table for the ascidian Ciona intestinalis, including 3D real‐image embryo reconstructions: I. From fertilized egg to hatching larva , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[11]  B. Bruneau,et al.  Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract , 2004, Development.

[12]  R. Kelly,et al.  Properties of branchiomeric and somite‐derived muscle development in Tbx1 mutant embryos , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[13]  J. Seidman,et al.  Mutations in the cardiac transcription factor NKX2.5 affect diverse cardiac developmental pathways. , 1999, The Journal of clinical investigation.

[14]  B. Davidson Ciona intestinalis as a model for cardiac development. , 2007, Seminars in cell & developmental biology.

[15]  I. Komuro,et al.  Csx: a murine homeobox-containing gene specifically expressed in the developing heart. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[16]  A. Baldini,et al.  Mesodermal expression of Tbx1 is necessary and sufficient for pharyngeal arch and cardiac outflow tract development , 2006, Development.

[17]  I. Harel,et al.  The contribution of Islet1-expressing splanchnic mesoderm cells to distinct branchiomeric muscles reveals significant heterogeneity in head muscle development , 2008, Development.

[18]  F. Delsuc,et al.  Tunicates and not cephalochordates are the closest living relatives of vertebrates , 2006, Nature.

[19]  M. Levine,et al.  miRTRAP, a computational method for the systematic identification of miRNAs from high throughput sequencing data , 2010, Genome Biology.

[20]  S. B. Wechsler,et al.  Molecular Cloning, Chromosomal Mapping, and Characterization of the Human Cardiac-Specific Homeobox Gene hCsx , 1996, Molecular medicine.

[21]  Milena B. Furtado,et al.  A tyrosine-rich domain within homeodomain transcription factor Nkx2-5 is an essential element in the early cardiac transcriptional regulatory machinery , 2006, Development.

[22]  M. Levine,et al.  Characterization of a notochord-specific enhancer from the Brachyury promoter region of the ascidian, Ciona intestinalis. , 1997, Development.

[23]  Thomas Werner,et al.  MatInspector and beyond: promoter analysis based on transcription factor binding sites , 2005, Bioinform..

[24]  David J. Miller,et al.  Gene Regulatory Networks in the Evolution and Development of the Heart , 2006 .

[25]  L. Jerome-Majewska,et al.  The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. , 2004, Human molecular genetics.

[26]  H. Saiga,et al.  Dynamic change in the expression of developmental genes in the ascidian central nervous system: revisit to the tripartite model and the origin of the midbrain-hindbrain boundary region. , 2007, Developmental biology.

[27]  T. Holak,et al.  Lifeact: a versatile marker to visualize F-actin , 2008, Nature Methods.

[28]  Mauro W. Costa,et al.  Conformational stability and DNA binding specificity of the cardiac T-box transcription factor Tbx20. , 2009, Journal of molecular biology.

[29]  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.

[30]  Lior Pachter,et al.  VISTA: computational tools for comparative genomics , 2004, Nucleic Acids Res..

[31]  A. Moorman,et al.  Cooperative action of Tbx2 and Nkx2.5 inhibits ANF expression in the atrioventricular canal: implications for cardiac chamber formation. , 2002, Genes & development.

[32]  L. Christiaen,et al.  Development and evolution of the ascidian cardiogenic mesoderm. , 2012, Current topics in developmental biology.

[33]  M. Levine,et al.  The sea squirt Ciona intestinalis. , 2009, Cold Spring Harbor protocols.

[34]  S. Fujiwara,et al.  RNA interference by expressing short hairpin RNA in the Ciona intestinalis embryo , 2008, Development, growth & differentiation.

[35]  Jean-Philippe Vert,et al.  An accurate and interpretable model for siRNA efficacy prediction , 2006, BMC Bioinformatics.

[36]  Y. S. Green,et al.  EBF proteins participate in transcriptional regulation of Xenopus muscle development. , 2011, Developmental biology.

[37]  Stephen M. Mount,et al.  The genome sequence of Drosophila melanogaster. , 2000, Science.

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

[39]  B. Morrow,et al.  Mesodermal Tbx1 is required for patterning the proximal mandible in mice. , 2010, Developmental biology.

[40]  N. Satoh,et al.  The ascidian Mesp gene specifies heart precursor cells , 2004, Development.

[41]  M. Levine,et al.  FoxF is essential for FGF-induced migration of heart progenitor cells in the ascidian Ciona intestinalis , 2007, Development.

[42]  A. Baldini,et al.  In vivo response to high-resolution variation of Tbx1 mRNA dosage. , 2007, Human molecular genetics.

[43]  N. Satoh,et al.  A genomewide survey of developmentally relevant genes in Ciona intestinalis , 2003, Development Genes and Evolution.

[44]  Gergana Dobreva,et al.  The LIM protein Ajuba restricts the second heart field progenitor pool by regulating Isl1 activity. , 2012, Developmental cell.

[45]  P. Scambler,et al.  Tbx1 haploinsufficiency in the DiGeorge syndrome region causes aortic arch defects in mice , 2001, Nature.

[46]  S. Sweeney,et al.  A single GATA factor plays discrete, lineage specific roles in ascidian heart development. , 2011, Developmental biology.

[47]  M. Levine,et al.  Electroporation of transgenic DNAs in the sea squirt Ciona. , 2009, Cold Spring Harbor protocols.

[48]  Michael Kyba,et al.  Mesp1 acts as a master regulator of multipotent cardiovascular progenitor specification. , 2008, Cell stem cell.

[49]  Takeshi Kawashima,et al.  The Transcription/Migration Interface in Heart Precursors of Ciona intestinalis , 2008, Science.

[50]  Lionel Christiaen,et al.  FGF signaling delineates the cardiac progenitor field in the simple chordate, Ciona intestinalis. , 2006, Genes & development.

[51]  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.

[52]  R. Kelly,et al.  Organogenesis of the vertebrate heart , 2013, Wiley interdisciplinary reviews. Developmental biology.

[53]  F. Lescroart,et al.  Lineage Tree for the Venous Pole of the Heart: Clonal Analysis Clarifies Controversial Genealogy Based on Genetic Tracing , 2012, Circulation research.

[54]  M. Levine,et al.  Whole-mount in situ hybridization on sea squirt (Ciona intestinalis) embryos. , 2009, Cold Spring Harbor protocols.

[55]  N. Satoh,et al.  A bHLH transcription factor gene, Twist-like 1, is essential for the formation of mesodermal tissues of Ciona juveniles. , 2005, Developmental biology.

[56]  E. Davidson,et al.  Response to Comment on "Gene Regulatory Networks and the Evolution of Animal Body Plans" , 2006, Science.

[57]  B. Morrow,et al.  Identification of downstream genetic pathways of Tbx1 in the second heart field. , 2008, Developmental biology.

[58]  M. Levine,et al.  Uncoupling heart cell specification and migration in the simple chordate Ciona intestinalis , 2005, Development.

[59]  M. Levine,et al.  A genomewide survey of developmentally relevant genes in Ciona intestinalis , 2003, Development Genes and Evolution.

[60]  N. Satoh,et al.  Genomewide surveys of developmentally relevant genes in Ciona intestinalis , 2003, Development Genes and Evolution.

[61]  Birgit Funke,et al.  TBX1 Is Responsible for Cardiovascular Defects in Velo-Cardio-Facial/DiGeorge Syndrome , 2001, Cell.

[62]  T. Lints,et al.  XNkx-2.5, a Xenopus gene related to Nkx-2.5 and tinman: evidence for a conserved role in cardiac development. , 1994, Developmental biology.

[63]  Yutaka Satou,et al.  Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: towards a comprehensive understanding of gene networks , 2004, Development.

[64]  M. Fishman,et al.  Zebrafish tinman homolog demarcates the heart field and initiates myocardial differentiation. , 1996, Development.

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

[66]  E. Tzahor,et al.  Mesoderm progenitor cells of common origin contribute to the head musculature and the cardiac outflow tract , 2006, Development.

[67]  A. Kuroiwa,et al.  Fibroblast growth factor 10 gene regulation in the second heart field by Tbx1, Nkx2-5, and Islet1 reveals a genetic switch for down-regulation in the myocardium , 2012, Proceedings of the National Academy of Sciences.

[68]  A. Vincent,et al.  Tup/Islet1 integrates time and position to specify muscle identity in Drosophila , 2012, Development.

[69]  Milena B. Furtado,et al.  An Nkx2-5/Bmp2/Smad1 Negative Feedback Loop Controls Heart Progenitor Specification and Proliferation , 2007, Cell.

[70]  Delphine Dauga,et al.  The ANISEED database: digital representation, formalization, and elucidation of a chordate developmental program. , 2010, Genome research.

[71]  M. Buckingham,et al.  The clonal origin of myocardial cells in different regions of the embryonic mouse heart. , 2004, Developmental cell.

[72]  Joe C. Adams,et al.  Full spectrum of malformations in velo-cardio-facial syndrome/DiGeorge syndrome mouse models by altering Tbx1 dosage. , 2004, Human molecular genetics.

[73]  P. Scambler,et al.  Tbx1 regulation of myogenic differentiation in the limb and cranial mesoderm , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[74]  R. Gronostajski,et al.  Differential DNA binding and transcription modulation by three T-box proteins, T, TBX1 and TBX2. , 2000, Gene.

[75]  M. Levine,et al.  A distinct class of small RNAs arises from pre-miRNA–proximal regions in a simple chordate , 2009, Nature Structural &Molecular Biology.

[76]  M. Vitale,et al.  Transcription Factor Nkx-2.5 Induces Sodium/Iodide Symporter Gene Expression and Participates in Retinoic Acid- and Lactation-Induced Transcription in Mammary Cells , 2004, Molecular and Cellular Biology.

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

[78]  B. Morrow,et al.  Tbx1 affects asymmetric cardiac morphogenesis by regulating Pitx2 in the secondary heart field , 2006, Development.

[79]  M. Frasch,et al.  Org-1 is required for the diversification of circular visceral muscle founder cells and normal midgut morphogenesis. , 2013, Developmental biology.

[80]  A. Lassar,et al.  Induction of avian cardiac myogenesis by anterior endoderm. , 1995, Development.

[81]  R J Schwartz,et al.  Identification of Novel DNA Binding Targets and Regulatory Domains of a Murine Tinman Homeodomain Factor, nkx-2.5(*) , 1995, The Journal of Biological Chemistry.

[82]  M. Frasch,et al.  Org-1, the Drosophila ortholog of Tbx1, is a direct activator of known identity genes during muscle specification , 2012, Development.

[83]  L. Silver,et al.  Expression of the T‐box family genes, Tbx1–Tbx5, during early mouse development , 1996, Developmental dynamics : an official publication of the American Association of Anatomists.

[84]  E. Lander,et al.  Dorsoventral Patterning in Hemichordates: Insights into Early Chordate Evolution , 2006, PLoS biology.

[85]  M. Levine,et al.  BMP signaling coordinates gene expression and cell migration during precardiac mesoderm development. , 2010, Developmental biology.