Abstract
Integration of blood vessels and organ primordia determines organ shape and function. The head kidney in the zebrafish interacts with the dorsal aorta (DA) and the posterior cardinal vein (PCV) to achieve glomerular filtration and definitive hematopoiesis, respectively. How the head kidney co-develops with both the axial artery and vein remains unclear. We found that in endodermless sox32-deficient embryos, the head kidney associated with the PCV but not the DA. Disrupted convergent migration of the PCV and the head kidney in sox32-deficient embryos was rescued in a highly coordinated fashion through the restoration of endodermal cells. Moreover, grafted endodermal cells abutted the host PCV endothelium in the transplantation assay. Interestingly, the severely-disrupted head kidney convergence in the sox32-deficient embryo was suppressed by both the cloche mutation and the knockdown of endothelial genes, indicating that an interaction between the endoderm and the PCV restricts the migration of the head kidney. Furthermore, knockdown of either vegfC or its receptor vegfr3 suppressed the head kidney convergence defect in endodermless embryos and perturbed the head kidney-PCV association in wild-type embryos. Our findings thus underscore a role for PCV and VegfC in patterning the head kidney prior to organ assembly and function.
Highlights
The hematopoietic precursors from the caudal hematopoietic tissue through the PCV renders the pronephros one of the definitive sites of hematopoiesis
To examine whether and how head kidney morphogenesis is disrupted in the endodermless embryo, we first assessed the functional differentiation of the interrenal tissue (IR), the last-differentiated segment of the kidney field, in the cas embryo and its wild-type sibling
Whole-mount 3β-hydroxysteroid dehydrogenase (3β-Hsd) enzymatic staining that detects steroidogenic cells indicated that morphogenesis but not differentiation of the IR was disrupted in the cas mutant, where the bilateral IRs failed to migrate toward the midline (Fig. 1A–F)
Summary
The hematopoietic precursors from the caudal hematopoietic tissue through the PCV renders the pronephros one of the definitive sites of hematopoiesis It remains unclear how the PCV endothelium integrates with the developing head kidney during embryogenesis. In the one-eye pinhead (oep) and squint (sqt) mutants in which the Nodal signalling is defective, the midline convergence of the head kidney and the formation of the PCV are both severely defective[4,18,19]. In the endodermless sox[32] (casanova, cas) mutant, mesodermal organs including the heart, vasculature, blood and kidney demonstrate convergence defects[22]. While the endothelium-free cloche (clo) mutant demonstrated a fusion defect of the bilateral PG and IR, this mutation significantly suppressed the severe convergence phenotype in endodermless embryos. We underscored a novel role for VegfC in embryonic kidney development
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