XB-ART-46561
Dev Genes Evol
2013 Mar 01;2231-2:117-29. doi: 10.1007/s00427-012-0400-1.
Show Gene links
Show Anatomy links
Islet1-expressing cardiac progenitor cells: a comparison across species.
???displayArticle.abstract???
Adult mammalian cardiac stem cells express the LIM-homeodomain transcription factor Islet1 (Isl1). They are considered remnants of Isl1-positive embryonic cardiac progenitor cells. During amniote heart development, Isl1-positive progenitor cells give rise mainly to the outflow tract, the right ventricle, and parts of the atria. This led to the hypothesis that the development of the right ventricle of the amniote heart depends on the recruitment of additional cells to the primary heart tube. The region from which these additional, Isl1-positive cells originate is called second heart field, as opposed to the first heart field whose cells form the primary heart tube. Here, we review the available data about Isl1 in different species, demonstrating that Isl1 is an important component of the core transcription factor network driving early cardiogenesis in animals of the two clades, deuterostomes, and protostomes. The data support the view of a single cardiac progenitor cell population that includes Isl1-expressing cells and which differentiates into the various cardiac lineages during embryonic development in vertebrates but not in other phyla of the animal kingdom.
???displayArticle.pubmedLink??? 22526874
???displayArticle.pmcLink??? PMC3552366
???displayArticle.link??? Dev Genes Evol
Species referenced: Xenopus
Genes referenced: atm fgf8 isl1 ltbp3 nkx2-5 shf shh tbl1x tbx2 tbx5
???attribute.lit??? ???displayArticles.show???
Fig. 1. The evolutionary relationship of the organisms discussed in this review and a schematic presentation of the gross morphology of their pumping organs. Ventricular chambers are depicted in red; atrial chambers are shown in blue. The atrium and ventricle in molluscs are colored in light blue and light red since it is not clear whether they are indeed homologous to their vertebrate counterparts. The dashed arrows indicate the appearance of Isl1-positive pharyngeal mesodermal cells in deuterostomes that contribute to the head musculature and, in craniata, to the heart. The phylogenetic tree is based on Simoes-Costa et al. (2005) | |
Fig. 2. Illustration of the evolutionary relationship of Isl1 genes in different species. a The phylogenetic tree was generated using Clustal W (http://www.ebi.ac.uk/Tools/phylogeny/clustalw2_phylogeny/) (Chenna et al. 2003). Numbers indicate the genetic distance between the nodes of the tree. Sequences used were: NP_002193.2 (Homo sapiens), NP_067434.3 (M. musculus), NP_571037.1 (D. rerio), NP_990745.1 (G. gallus), NP_001104188.1 (X. laevis), AF226616_1 (Branchiostoma floridae), NP_001027767.1 (C. intestinalis), NP_476775.1 (D. melanogaster). b Comparison of Isl1 protein sequences. The percentages depict the degree of identical and similar (in parentheses) amino acids | |
Fig. 3. A simplified schematic presentation of heart development in different species. a Mouse. Developmental stages are indicated in embryonic days (E). The cartoons show a dorsal view of a flattened embryo (E6.5), an anterior view (E7.5), and a lateral view (E8.0). Additionally, a schematic illustration of a transverse section at E8.0 is provided. The SHF is characterized by the presence of Isl1-positive cells and is indicated in red. bX. laevis. Developmental stages are according to Nieuwkoop and Faber (1975). The cartoons show an anterior view (st.13), a ventral view (st.24), and a lateral view (st.31). Additionally, a schematic illustration of a transverse section through the heart at st.31 is provided. At st.24, cells of the SHF (red) express isl1 whereas cells of the FHF (blue) are positive for tbx5. cD. rerio. Developmental stages are indicated in hours post-fertilization (hpf). The cartoons show a lateral view for stage 5 hpf and dorsal views for stages 12.5, 20, and 30 hpf with the anterior side up. The localization of early cardiac progenitor cells at 40 % epiboly, as well as the distinction between an atrial and a ventricular fate was analyzed by fate-mapping experiments. An Isl1-positive cell population that contributes to the arterial pole is located posterior and dorsal to the ventricle and is indicated in red. It only partially contributes to the heart. The zebrafish SHF is characterized by the expression of ltbp3. Of note, the arrangement of the atrium and ventricle along the anteriorâposterior axis is inverted at later stages (not shown here). As a result, the atrium will come to lie posterior to the ventricle. CPC: common cardiac progenitor cell population, A: anterior, D: dorsal, P: posterior, V: ventral, FHF: first heart field; SHF: second heart field, PHT: primary heart tube. Partly adopted from Gessert and Kühl (2009) | |
Fig. 4. Early heart development in C. intestinalis. The heart derives from the bilateral B7.5 blastomeres indicated in red. TVC: trunk ventral cells, ATM: anterior tail muscles. Adopted from Stolfi et al. (2010) | |
Fig. 5. Gene regulatory networks in cardiac cells including Isl1. a Interaction of key cardiac transcription factors in the early cardiac mesoderm in Drosophila. doc: dorsocross, tup: tailup, pnr: pannier, tin: Tinman. b Interaction of signaling molecules and transcription factors including Isl1 in the pharyngeal mesoderm/SHF in the mouse. Shh: sonic hedgehog, RA: retinoic acid, Fgf8: fibroblast growth factor 8 |
References [+] :
Abu-Issa,
Heart field: from mesoderm to heart tube.
2007, Pubmed
Abu-Issa, Heart field: from mesoderm to heart tube. 2007, Pubmed
Abu-Issa, Patterning of the heart field in the chick. 2008, Pubmed
Blair, Evolutionary sequence analysis of complete eukaryote genomes. 2005, Pubmed
Bodmer, The gene tinman is required for specification of the heart and visceral muscles in Drosophila. 1993, Pubmed
Bondue, Mesp1 acts as a master regulator of multipotent cardiovascular progenitor specification. 2008, Pubmed
Bondue, Defining the earliest step of cardiovascular progenitor specification during embryonic stem cell differentiation. 2011, Pubmed
Bourlat, Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. 2006, Pubmed
Brade, The amphibian second heart field: Xenopus islet-1 is required for cardiovascular development. 2007, Pubmed , Xenbase
Bu, Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. 2009, Pubmed
Cai, Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. 2003, Pubmed
Chenna, Multiple sequence alignment with the Clustal series of programs. 2003, Pubmed
Cohen, Wnt/beta-catenin signaling promotes expansion of Isl-1-positive cardiac progenitor cells through regulation of FGF signaling. 2007, Pubmed
Davidson, Ciona intestinalis as a model for cardiac development. 2007, Pubmed
Delsuc, Tunicates and not cephalochordates are the closest living relatives of vertebrates. 2006, Pubmed
de Pater, Distinct phases of cardiomyocyte differentiation regulate growth of the zebrafish heart. 2009, Pubmed
Dodou, Mef2c is a direct transcriptional target of ISL1 and GATA factors in the anterior heart field during mouse embryonic development. 2004, Pubmed
Gajewski, Pannier is a transcriptional target and partner of Tinman during Drosophila cardiogenesis. 2001, Pubmed
Garcia-Martinez, Primitive-streak origin of the cardiovascular system in avian embryos. 1993, Pubmed
Genead, Islet-1 cells are cardiac progenitors present during the entire lifespan: from the embryonic stage to adulthood. 2010, Pubmed
Gessert, The multiple phases and faces of wnt signaling during cardiac differentiation and development. 2010, Pubmed
Gessert, Comparative gene expression analysis and fate mapping studies suggest an early segregation of cardiogenic lineages in Xenopus laevis. 2009, Pubmed , Xenbase
Goddeeris, Independent requirements for Hedgehog signaling by both the anterior heart field and neural crest cells for outflow tract development. 2007, Pubmed
Hami, Zebrafish cardiac development requires a conserved secondary heart field. 2011, Pubmed
Hartenstein, The blood/vascular system in a phylogenetic perspective. 2006, Pubmed
Higashijima, Visualization of cranial motor neurons in live transgenic zebrafish expressing green fluorescent protein under the control of the islet-1 promoter/enhancer. 2000, Pubmed
Hoofnagle, Myocardin is differentially required for the development of smooth muscle cells and cardiomyocytes. 2011, Pubmed
Ilagan, Fgf8 is required for anterior heart field development. 2006, Pubmed
Jackman, islet reveals segmentation in the Amphioxus hindbrain homolog. 2000, Pubmed
Kappen, Identification of regulatory elements in the Isl1 gene locus. 2009, Pubmed
Khattar, Distinction between two populations of islet-1-positive cells in hearts of different murine strains. 2011, Pubmed
Kokubo, Mechanisms of heart development in the Japanese lamprey, Lethenteron japonicum. 2010, Pubmed
Korzh, Zebrafish primary neurons initiate expression of the LIM homeodomain protein Isl-1 at the end of gastrulation. 1993, Pubmed
Koshiba-Takeuchi, Reptilian heart development and the molecular basis of cardiac chamber evolution. 2009, Pubmed
Kühl, Improving cardiac regeneration after injury: are we a step closer? 2011, Pubmed
Kwon, A regulatory pathway involving Notch1/beta-catenin/Isl1 determines cardiac progenitor cell fate. 2009, Pubmed
Laugwitz, Islet1 cardiovascular progenitors: a single source for heart lineages? 2008, Pubmed
Laugwitz, Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. 2005, Pubmed
Lee, Cardiac neural crest is dispensable for outflow tract septation in Xenopus. 2011, Pubmed , Xenbase
Lee, Cardiovascular development in the zebrafish. II. Endocardial progenitors are sequestered within the heart field. 1994, Pubmed
Lescroart, Clonal analysis reveals common lineage relationships between head muscles and second heart field derivatives in the mouse embryo. 2010, Pubmed
Li, The serum response factor coactivator myocardin is required for vascular smooth muscle development. 2003, Pubmed
Lin, Beta-catenin directly regulates Islet1 expression in cardiovascular progenitors and is required for multiple aspects of cardiogenesis. 2007, Pubmed
Lin, Isl1 is upstream of sonic hedgehog in a pathway required for cardiac morphogenesis. 2006, Pubmed
Lindsley, Mesp1 coordinately regulates cardiovascular fate restriction and epithelial-mesenchymal transition in differentiating ESCs. 2008, Pubmed
Liu, Bmp4 signaling is required for outflow-tract septation and branchial-arch artery remodeling. 2004, Pubmed
Long, Myocardin is a bifunctional switch for smooth versus skeletal muscle differentiation. 2007, Pubmed
Ma, Reassessment of Isl1 and Nkx2-5 cardiac fate maps using a Gata4-based reporter of Cre activity. 2008, Pubmed
Mann, The Drosophila homolog of vertebrate Islet1 is a key component in early cardiogenesis. 2009, Pubmed
Mjaatvedt, The outflow tract of the heart is recruited from a novel heart-forming field. 2001, Pubmed
Moore, A genomewide survey of basic helix-loop-helix factors in Drosophila. 2000, Pubmed
Moretti, Biology of Isl1+ cardiac progenitor cells in development and disease. 2007, Pubmed
Moretti, Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. 2006, Pubmed
Moretti, Mouse and human induced pluripotent stem cells as a source for multipotent Isl1+ cardiovascular progenitors. 2010, Pubmed
Nathan, The contribution of Islet1-expressing splanchnic mesoderm cells to distinct branchiomeric muscles reveals significant heterogeneity in head muscle development. 2008, Pubmed
Ogasawara, Gene expression profiles in young adult Ciona intestinalis. 2002, Pubmed
Park, Required, tissue-specific roles for Fgf8 in outflow tract formation and remodeling. 2006, Pubmed
Prall, An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. 2007, Pubmed
Qyang, The renewal and differentiation of Isl1+ cardiovascular progenitors are controlled by a Wnt/beta-catenin pathway. 2007, Pubmed
Reim, The T-box-encoding Dorsocross genes function in amnioserosa development and the patterning of the dorsolateral germ band downstream of Dpp. 2003, Pubmed
Rochais, Signaling pathways controlling second heart field development. 2009, Pubmed
Ryckebusch, Retinoic acid deficiency alters second heart field formation. 2008, Pubmed
Saga, MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. 1999, Pubmed
Satou, The ascidian Mesp gene specifies heart precursor cells. 2004, Pubmed
Saudemont, Complementary striped expression patterns of NK homeobox genes during segment formation in the annelid Platynereis. 2008, Pubmed
Schoenebeck, Illuminating cardiac development: Advances in imaging add new dimensions to the utility of zebrafish genetics. 2007, Pubmed
Schultheiss, Induction of avian cardiac myogenesis by anterior endoderm. 1995, Pubmed , Xenbase
Simões-Costa, The evolutionary origin of cardiac chambers. 2005, Pubmed
Sirbu, Retinoic acid controls heart anteroposterior patterning by down-regulating Isl1 through the Fgf8 pathway. 2008, Pubmed
Sirbu, Saving hearts through basic research. 2009, Pubmed
Solloway, Molecular pathways in myocardial development: a stem cell perspective. 2003, Pubmed
Stennard, T-box transcription factors and their roles in regulatory hierarchies in the developing heart. 2005, Pubmed
Stolfi, Early chordate origins of the vertebrate second heart field. 2010, Pubmed , Xenbase
Sun, Islet 1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. 2007, Pubmed
Tao, Requirement of the LIM homeodomain transcription factor tailup for normal heart and hematopoietic organ formation in Drosophila melanogaster. 2007, Pubmed
Tirosh-Finkel, Mesoderm progenitor cells of common origin contribute to the head musculature and the cardiac outflow tract. 2006, Pubmed
Tsuchihashi, Hand2 function in second heart field progenitors is essential for cardiogenesis. 2011, Pubmed
Tzahor, Pharyngeal mesoderm development during embryogenesis: implications for both heart and head myogenesis. 2011, Pubmed
van den Berg, Concepts of cardiac development in retrospect. 2009, Pubmed
von Both, Foxh1 is essential for development of the anterior heart field. 2004, Pubmed
Wada, A genomewide survey of developmentally relevant genes in Ciona intestinalis. II. Genes for homeobox transcription factors. 2003, Pubmed
Waldo, Conotruncal myocardium arises from a secondary heart field. 2001, Pubmed , Xenbase
Wang, Bmp signaling regulates myocardial differentiation from cardiac progenitors through a MicroRNA-mediated mechanism. 2010, Pubmed
Wang, Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. 2001, Pubmed , Xenbase
Washington Smoak, Sonic hedgehog is required for cardiac outflow tract and neural crest cell development. 2005, Pubmed
Watanabe, The formation of the embryonic mouse heart: heart fields and myocardial cell lineages. 2010, Pubmed
Witman, Recapitulation of developmental cardiogenesis governs the morphological and functional regeneration of adult newt hearts following injury. 2011, Pubmed
Xu, Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. 2004, Pubmed
Yang, Isl1Cre reveals a common Bmp pathway in heart and limb development. 2006, Pubmed
Yuan, Islet-1 marks the early heart rudiments and is asymmetrically expressed during early rotation of the foregut in the chick embryo. 2000, Pubmed
Zhou, Latent TGF-β binding protein 3 identifies a second heart field in zebrafish. 2011, Pubmed