Transdifferentiation of Fast Skeletal Muscle Into Functional Endothelium in Vivo by Transcription Factor Etv2

Veldman, Matthew B.; Zhao, Chengjian; Gomez, Gustavo A.; Lindgren, Anne; Huang, Haigen; Yang, Huiling; Yao, Su; Martin, Benjamin L.; Kimelman, David; Lin, Shuo

doi:10.1371/journal.pbio.1001590

Cited by 51 publications

(59 citation statements)

References 52 publications

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“…To determine whether Wnt signaling also induces new mesoderm formation within the tailbud MPCs, we used heat shockinducible transgenic lines to temporally inhibit (hsp70l:TCFΔC-GFP) or activate (hsp70l:β-Catenin-TFP) Wnt signaling (Martin and Kimelman, 2012;Veldman et al, 2013). The T-box gene ntla (also known as T, brachyury homolog a) is expressed in differentiated notochord cells, notochord progenitors located just posterior to the differentiated notochord, and in posterior wall mesoderm progenitors (Martin and Kimelman, 2008;SchulteMerker et al, 1994).…”

Section: Resultsmentioning

confidence: 99%

“…Initial experiments used donor embryos from stable transgenic lines (Martin and Kimelman, 2012;Veldman et al, 2013). To quantify tissue contribution an alternate transient transgenic approach was employed, using donors injected with plasmid DNA and integrated genomically with the tol2 transposase system, which creates a mosaic scatter labeled embryo (Kikuta Table 1).…”

Section: Resultsmentioning

confidence: 99%

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The zebrafish tailbud contains two independent populations of midline progenitor cells that maintain long-term germ layer plasticity and differentiate based on local signaling cues

et al. 2015

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Vertebrate body axis formation depends on a population of bipotential neuromesodermal cells along the posterior wall of the tailbud that make a germ layer decision after gastrulation to form spinal cord and mesoderm. Despite exhibiting germ layer plasticity, these cells never give rise to midline tissues of the notochord, floor plate and dorsal endoderm, raising the question of whether midline tissues also arise from basal posterior progenitors after gastrulation. We show in zebrafish that local posterior signals specify germ layer fate in two basal tailbud midline progenitor populations. Wnt signaling induces notochord within a population of notochord/floor plate bipotential cells through negative transcriptional regulation of sox2. Notch signaling, required for hypochord induction during gastrulation, continues to act in the tailbud to specify hypochord from a notochord/hypochord bipotential cell population. Our results lend strong support to a continuous allocation model of midline tissue formation in zebrafish, and provide an embryological basis for zebrafish and mouse bifurcated notochord phenotypes as well as the rare human congenital split notochord syndrome. We demonstrate developmental equivalency between the tailbud progenitor cell populations. Midline progenitors can be transfated from notochord to somite fate after gastrulation by ectopic expression of msgn1, a master regulator of paraxial mesoderm fate, or if transplanted into the bipotential progenitors that normally give rise to somites. Our results indicate that the entire non-epidermal posterior body is derived from discrete, basal tailbud cell populations. These cells remain receptive to extracellular cues after gastrulation and continue to make basic germ layer decisions.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

The zebrafish tailbud contains two independent populations of midline progenitor cells that maintain long-term germ layer plasticity and differentiate based on local signaling cues

et al. 2015

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“…Their model fits well with our current results in zebrafish. It is well known that Etv2 overexpression also results in endothelialization in zebrafish (35,37,42,59) and Xenopus (57). All of these observations suggest that Etv2 may play a conserved role in maintaining the endothelial characteristics of hemangioblasts in the early developmental periods.…”

Section: Discussionmentioning

confidence: 99%

LSD1/KDM1A promotes hematopoietic commitment of hemangioblasts through downregulation of Etv2

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Watanabe

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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The hemangioblast is a progenitor cell with the capacity to give rise to both hematopoietic and endothelial progenitors. Currently, the regulatory mechanisms underlying hemangioblast formation are being elucidated, whereas those controllers for the selection of hematopoietic or endothelial fates still remain a mystery. To answer these questions, we screened for zebrafish mutants that have defects in the hemangioblast expression of Gata1, which is never expressed in endothelial progenitors. One of the isolated mutants, it627, showed not only down-regulation of hematopoietic genes but also up-regulation of endothelial genes. We identified the gene responsible for the it627 mutant as the zebrafish homolog of Lys-specific demethylase 1 (LSD1/KDM1A). Surprisingly, the hematopoietic defects in lsd1it627 embryos were rescued by the gene knockdown of the Ets variant 2 gene (etv2), an essential regulator for vasculogenesis. Our results suggest that the LSD1-dependent shutdown of Etv2 gene expression may be a significant event required for hemangioblasts to initiate hematopoietic differentiation.

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“…HS:dnfgfr1-GFP (Lee et al, 2005), HS:caβ-catenin (Veldman et al, 2013), HS:cafgfr1 (Marques et al, 2008), HS:msgn1-p2a-NLS-kikume (Row et al, 2016), HS:TCFΔC-GFP , HS:tbx16-p2a-NLS-kikume (this study) and HS:CAAXmCherry-p2a-NLS-kikume (this study) fish provided embryos that were heat shocked at the previously described temperatures for 30 min. Transgenic embryos were sorted from their wild-type siblings based on fluorescence or unique phenotypes.…”

Section: Fish Lines and Heat Shocksmentioning

confidence: 99%

FGF and canonical Wnt signaling cooperate to induce paraxial mesoderm from tailbud neuromesodermal progenitors through regulation of a two-step epithelial to mesenchymal transition

et al. 2017

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Mesoderm induction begins during gastrulation. Recent evidence from several vertebrate species indicates that mesoderm induction continues after gastrulation in neuromesodermal progenitors (NMPs) within the posteriormost embryonic structure, the tailbud. It is unclear to what extent the molecular mechanisms of mesoderm induction are conserved between gastrula and post-gastrula stages of development. Fibroblast growth factor (FGF) signaling is required for mesoderm induction during gastrulation through positive transcriptional regulation of the T-box transcription factor brachyury. We find in zebrafish that FGF is continuously required for paraxial mesoderm (PM) induction in post-gastrula NMPs. FGF signaling represses the NMP markers brachyury (ntla) and sox2 through regulation of tbx16 and msgn1, thereby committing cells to a PM fate. FGF-mediated PM induction in NMPs functions in tight coordination with canonical Wnt signaling during the epithelial to mesenchymal transition (EMT) from NMP to mesodermal progenitor. Wnt signaling initiates EMT, whereas FGF signaling terminates this event. Our results indicate that germ layer induction in the zebrafish tailbud is not a simple continuation of gastrulation events.

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Transdifferentiation of Fast Skeletal Muscle Into Functional Endothelium in Vivo by Transcription Factor Etv2

Abstract: Etv2, a master regulator of endothelial cell fate, can induce fast skeletal muscle cells to transdifferentiate into endothelial cells in the zebrafish embryo.

Cited by 51 publications

References 52 publications

The zebrafish tailbud contains two independent populations of midline progenitor cells that maintain long-term germ layer plasticity and differentiate based on local signaling cues

The zebrafish tailbud contains two independent populations of midline progenitor cells that maintain long-term germ layer plasticity and differentiate based on local signaling cues

LSD1/KDM1A promotes hematopoietic commitment of hemangioblasts through downregulation of Etv2

FGF and canonical Wnt signaling cooperate to induce paraxial mesoderm from tailbud neuromesodermal progenitors through regulation of a two-step epithelial to mesenchymal transition

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