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Planar cell polarity signaling regulates polarized second heart field morphogenesis to promote both arterial and venous pole septation.

ABSTRACT: The second heart field (SHF) harbors progenitors that are important for heart formation, but little is known about its morphogenesis. We show that SHF population in the mouse splanchnic mesoderm (SpM-SHF) undergoes polarized morphogenesis to preferentially elongate anteroposteriorly. Loss of Wnt5, a putative ligand of the planar cell polarity (PCP) pathway, causes the SpM-SHF to expand isotropically. Temporal tracking reveals that the Wnt5a lineage is a unique subpopulation specified as early as E7.5, and undergoes bi-directional deployment to form specifically the pulmonary trunk and the dorsal mesenchymal protrusion (DMP). In Wnt5a-/- mutants, Wnt5a lineage fails to extend into the arterial and venous poles, leading to both outflow tract and atrial septation defects that can be rescued by an activated form of PCP effector Daam1. We identify oriented actomyosin cables in the medial SpM-SHF as a potential Wnt5a-mediated mechanism that promotes SpM-SHF lengthening and restricts its widening. Finally, the Wnt5a lineage also contributes to the pulmonary mesenchyme, suggesting that Wnt5a/PCP is a molecular circuit recruited by the recently identified cardiopulmonary progenitors to coordinate morphogenesis of the pulmonary airways and the cardiac septations necessary for pulmonary circulation.This article has an associated 'The people behind the papers' interview.

SUBMITTER: Li D

PROVIDER: S-EPMC6826042 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Planar cell polarity signaling regulates polarized second heart field morphogenesis to promote both arterial and venous pole septation.

Li Ding D Angermeier Allyson A Wang Jianbo J

Development (Cambridge, England) 20191009 20

The second heart field (SHF) harbors progenitors that are important for heart formation, but little is known about its morphogenesis. We show that SHF population in the mouse splanchnic mesoderm (SpM-SHF) undergoes polarized morphogenesis to preferentially elongate anteroposteriorly. Loss of Wnt5, a putative ligand of the planar cell polarity (PCP) pathway, causes the SpM-SHF to expand isotropically. Temporal tracking reveals that the <i>Wnt5a</i> lineage is a unique subpopulation specified as e ...[more]

PMID: 31488563

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Project description:Quantitative analysis of the vascular network anatomy is critical for the understanding of the vasculature structure and function. In this study, we have combined microcomputed tomography (microCT) and computational analysis to provide quantitative three-dimensional geometrical and topological characterization of the normal kidney vasculature, and to investigate how 2 core genes of the Wnt/planar cell polarity, Frizzled4 and Frizzled6, affect vascular network morphogenesis. Experiments were performed on frizzled4 (Fzd4-/-) and frizzled6 (Fzd6-/-) deleted mice and littermate controls (WT) perfused with a contrast medium after euthanasia and exsanguination. The kidneys were scanned with a high-resolution (16 μm) microCT imaging system, followed by 3D reconstruction of the arterial vasculature. Computational treatment includes decomposition of 3D networks based on Diameter-Defined Strahler Order (DDSO). We have calculated quantitative (i) Global scale parameters, such as the volume of the vasculature and its fractal dimension (ii) Structural parameters depending on the DDSO hierarchical levels such as hierarchical ordering, diameter, length and branching angles of the vessel segments, and (iii) Functional parameters such as estimated resistance to blood flow alongside the vascular tree and average density of terminal arterioles. In normal kidneys, fractal dimension was 2.07±0.11 (n = 7), and was significantly lower in Fzd4-/- (1.71±0.04; n = 4), and Fzd6-/- (1.54±0.09; n = 3) kidneys. The DDSO number was 5 in WT and Fzd4-/-, and only 4 in Fzd6-/-. Scaling characteristics such as diameter and length of vessel segments were altered in mutants, whereas bifurcation angles were not different from WT. Fzd4 and Fzd6 deletion increased vessel resistance, calculated using the Hagen-Poiseuille equation, for each DDSO, and decreased the density and the homogeneity of the distal vessel segments. Our results show that our methodology is suitable for 3D quantitative characterization of vascular networks, and that Fzd4 and Fzd6 genes have a deep patterning effect on arterial vessel morphogenesis that may determine its functional efficiency.

Dataset Information

Planar cell polarity signaling regulates polarized second heart field morphogenesis to promote both arterial and venous pole septation.

Publications

Planar cell polarity signaling regulates polarized second heart field morphogenesis to promote both arterial and venous pole septation.

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