A Conserved Role for VEGF Signaling in Specification of Homologous Mesenchymal Cell Types Positioned at Spatially Distinct Developmental Addresses in Early Development of Sea Urchins

• Published in: Journal of experimental zoology. Part B, Molecular and developmental evolution Vol. 328; no. 5; pp. 423 - 432
• Main Authors: Erkenbrack, Eric M., Petsios, Elizabeth
• Format: Journal Article
• Language: English
• Published: United States 01.07.2017
• Subjects: Animals; Biological Evolution; Gastrula - metabolism; Gene Expression Regulation, Developmental; Larva - metabolism; Mesenchymal Stromal Cells - classification; Mesenchymal Stromal Cells - metabolism; RNA, Messenger - genetics; RNA, Messenger - metabolism; Signal Transduction - physiology; Strongylocentrotus - genetics; Strongylocentrotus - metabolism; Time Factors; Vascular Endothelial Growth Factor A - genetics; Vascular Endothelial Growth Factor A - metabolism
• ISSN: 1552-5007; 1552-5015; 1552-5015
• DOI: 10.1002/jez.b.22743

ABSTRACT Comparative studies of early development in echinoderms are revealing the tempo and mode of alterations to developmental gene regulatory networks and to the cell types they specify. In euechinoid sea urchins, skeletogenic mesenchyme (SM) ingresses prior to gastrulation at the vegetal pole and aligns into a ring‐like array with two bilateral pockets of cells, the sites where spiculogenesis will later occur. In cidaroid sea urchins, the anciently diverged sister clade to euechinoid sea urchins, a homologous SM cell type ingresses later in development, after gastrulation has commenced, and consequently at a distinct developmental address. Thus, a heterochronic shift of ingression of the SM cell type occurred in one of the echinoid lineages. In euechinoids, specification and migration of SM are facilitated by vascular endothelial growth factor (VEGF) signaling. We describe spatiotemporal expression of vegf and vegfr and experimental manipulations targeting VEGF signaling in the cidaroid Eucidaris tribuloides. Spatially, vegf and vegfr mRNA localizes similarly as in euechinoids, suggesting conserved deployment in echinoids despite their spatially distinct development addresses of ingression. Inhibition of VEGF signaling in E. tribuloides suggests its role in SM specification is conserved in echinoids. Temporal discrepancies between the onset of vegf expression and SM ingression likely result in previous observations of SM “random wandering” behavior. Our results indicate that, although the SM cell type in echinoids ingresses into distinct developmental landscapes, it retains a signaling mechanism that restricts their spatial localization to a conserved developmental address where spiculogenesis later occurs. GRAPHICAL ABSTRACT VEGF signaling is vital for larval spiculogenesis in anciently diverged sister subclasses of echinoids despite their skeletogenic cell lineages ingressing at distinct ontogenetic stages and is likely tightly coupled to echinoderm skeletogenesis.