Somite-derived cells replace ventral aortic hemangioblasts and provide aortic smooth muscle cells of the trunk

Abstract

We have previously shown that endothelial cells of the aortic floor give rise to hematopoietic cells, revealing the existence of an aortic hemangioblast. It has been proposed that the restriction of hematopoiesis to the aortic floor is based on the existence of two different and complementary endothelial lineages that form the vessel: one originating from the somite would contribute to the roof and sides, another from the splanchnopleura would contribute to the floor. Using quail/chick orthotopic transplantations of paraxial mesoderm, we have traced the distribution of somite-derived endothelial cells during aortic hematopoiesis. We show that the aortic endothelium undergoes two successive waves of remodeling by somitic cells: one when the aortae are still paired, during which the initial roof and sides of the vessels are renewed; and a second, associated to aortic hematopoiesis, in which the hemogenic floor is replaced by somite endothelial cells. This floor thus appears as a temporary structure, spent out and replaced. In addition, the somite contributes to smooth muscle cells of the aorta. In vivo lineage tracing experiments with non-replicative retroviral vectors showed that endothelial cells do not give rise to smooth muscle cells. However, in vitro, purified endothelial cells acquire smooth muscle cells characteristics. Taken together, these data point to the crucial role of the somite in shaping the aorta and also give an explanation for the short life of aortic hematopoiesis.

Myogenic progenitor cells in the mouse embryo are marked by the expression of Pax3/7 genes that regulate their survival and myogenic potential

“…Furthermore it was suggested that it may also give rise to smooth muscle cells. The somitic origin of smooth as well as endothelial cells in the dorsal aorta was recently demonstrated in the chick embryo (Pouget et al 2006). Using a retrospective clonal analysis in the mouse embryo, based on the rare intragenic recombination of a LaacZ sequence to give a functional LacZ reporter, we have shown that the smooth muscle of the dorsal aorta has a common clonal origin with the skeletal muscle of the myotome (Esner et al 2006).…”

The Avian Embryo as a Model System for Skeletal Myogenesis

“…Clonal analyses in the chick indicates that single cells in somites give rise to endothelial clones in the limb (Kardon et al 2002) while in mouse, it was shown that angioblasts leaving somites are committed to the endothelial lineage (Esner et al 2006;Pouget et al 2006;Sato et al 2008;Ohata et al 2009;Yvernogeau et al 2012). Altogether, these results strongly suggest that cells expressing VEGFR2 in somites are committed angioblasts.…”

“…The sclerotome along with mesenchymal cells from the somitocoel gives rise to the axial cartilage, tendons, and bones, while the remaining epithelial dorsal compartment of the somite is referred to as the dermomyotome. As its name indicates, the dermomyotome gives rise to the dorsal dermis and the primitive skeletal muscle, as well as smooth muscles of the aorta, lymphatic, and vascular endothelial cells (Wilting and Becker 2006;Esner et al 2006;Pouget et al 2006;Yusuf and Brand-Saberi 2006).…”

“…BMP4 is expressed in the lateral plate mesoderm and in the nascent limb bud and functional analyses showed that it represses myogenesis in the neighboring lateral somite (Pourquié et al 1996;Linker et al 2003). More recently, BMP signaling was shown to promote endothelial differentiation (Pouget et al 2006;Ben-Yair and Kalcheim 2008). However it is not known whether BMP4 acts on the level of VEGFR2 expression within each cell, on the number of cells initiating VEGFR2 expression or on other steps of their differentiation program such as proliferation and survival.…”

“…However, compelling data from lineage and genetic studies in chick and mouse strongly suggest that the differentiation of these cell types lies downstream of endothelial differentiation (Wigle and Oliver 1999;Wilting and Becker 2006;Esner et al 2006;Pouget et al 2006;Yvernogeau et al 2012). This suggests that VEGFR2-positive angioblasts that emigrate from somites are in fact pluripotent progenitors.…”