Diverse contribution of amniogenic somatopleural cells to cardiovascular development: With special reference to thyroid vasculature

• Published in: Developmental dynamics Vol. 253; no. 1; pp. 59 - 77
• Main Authors: Haneda, Yuka, Miyagawa‐Tomita, Sachiko, Uchijima, Yasunobu, Iwase, Akiyasu, Asai, Rieko, Kohro, Takahide, Wada, Youichiro, Kurihara, Hiroki
• Format: Journal Article
• Language: English
• Published: Hoboken, USA John Wiley & Sons, Inc 01-01-2024; Wiley Subscription Services, Inc
• Subjects: amniogenic somatopleure; Amnion; angiogenesis; Cardiac muscle; Cardiomyocytes; cardiovascular development; Cell culture; Cell differentiation; Chimeras; Differentiation; Endothelial cells; FGF; Fibroblast growth factors; Gene expression; Growth factors; Heterogeneity; Interstitial cells; Pharynx; quail‐chick chimera; Quorum sensing; Smooth muscle; Thyroid; thyroid development; Thyroid gland; Transcriptomes; Vascular endothelial growth factor; VEGF; FGF; VEGF; angiogenesis; cardiovascular development; thyroid development; quail-chick chimera; amniogenic somatopleure
• DOI: 10.1002/dvdy.532
• EISSN: 1097-0177
• ISSN: 1058-8388

Background
The somatopleure serves as the primordium of the amnion, an extraembryonic membrane surrounding the embryo. Recently, we have reported that amniogenic somatopleural cells (ASCs) not only form the amnion but also migrate into the embryo and differentiate into cardiomyocytes and vascular endothelial cells. However, detailed differentiation processes and final distributions of these intra‐embryonic ASCs (hereafter referred to as iASCs) remain largely unknown.
Results
By quail‐chick chimera analysis, we here show that iASCs differentiate into various cell types including cardiomyocytes, smooth muscle cells, cardiac interstitial cells, and vascular endothelial cells. In the pharyngeal region, they distribute selectively into the thyroid gland and differentiate into vascular endothelial cells to form intra‐thyroid vasculature. Explant culture experiments indicated sequential requirement of fibroblast growth factor (FGF) and vascular endothelial growth factor (VEGF) signaling for endothelial differentiation of iASCs. Single‐cell transcriptome analysis further revealed heterogeneity and the presence of hemangioblast‐like cell population within ASCs, with a switch from FGF to VEGF receptor gene expression.
Conclusion
The present study demonstrates novel roles of ASCss especially in heart and thyroid development. It will provide a novel clue for understanding the cardiovascular development of amniotes from embryological and evolutionary perspectives.
Key Findings
Here, we show that amniogenic somatopleure cells (ASCs) differentiate into various cell types constituting the cardiovascular system, with some populations having a molecular background similar to that of hemangioblasts. Among them, those contributing to the thyroid vascular network were suggested to differentiate into vascular endothelial cells with FGF‐specification and VEGF‐induced maturation. This study will provide a novel clue for understanding the cardiovascular development of amniotes from embryological and evolutionary perspectives.