Abstract

Recent discoveries of at least two heart fields and dynamic nature of cardiac development as well as controversies regarding the participation of heart fields in development of different heart structures led us to investigate the dynamics of incorporation of the first and second heart fields and prospective fate of the straight heart tube by labeling chicken embryos in vivo with the fluorescent lipophilic dye DiI. The cephalic and caudal limits of the anterior and posterior segments of the straight heart tube were labeled in two groups of embryos. Labels were tracked along the “C,” “S,” and “U” loops up to the tetracavitary or mature heart (n = 30 embryos/group; torsion and looping stage). To determine whether the atria and atrioventricular canal are derived from the first heart field the straight heart tube was cultured in vitro and immunodetection of Sox-9 and troponin I was performed to identify the mesenchymal and myocardial lineages respectively. Proliferating cell nuclear antigen (PCNA) immunodetection was used to determine the involvement of cell proliferation in heart tube development during torsion and looping. Embryological constitution of the straight heart tube and heart looping (C, S, and U) were not consistent with current descriptions. In fact, right ventricle precursors were absent in the straight heart tube derived from the first heart field. During torsion and looping, the cephalic segment of the straight heart tube gradually shifted into the heart tube until it was located at the myocardial interventricular septum in the tetracavitary heart. In contrast, the caudal segment of the straight heart tube was elongated and remodeled to become the first heart field derived left ventricle and the proximal part of the ventricular inlets. The ventricular outflows, right ventricle, distal part of the ventricular inlets, and atria developed from the second heart field.

Highlights

  • The heart is the first organ to function during embryonic development

  • Based on the discovery of first heart field (FHF) and second heart fields (SHF), dynamic nature of cardiac development, and previously mentioned controversies regarding the embryological composition of the straight heart tube, this study aimed to determine the dynamics of the incorporation of FHF and SHF and prospective fate of the FHF-derived straight heart tube in chicken embryos using in vivo labeling

  • Contrary to the current data, we reported that anterior segment (AS) of the straight heart tube contributes to IVS development, while posterior segment (PS) is involved in the development of left ventricle (LV) and ventricular inlets but not the atria

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Summary

Introduction

The heart is the first organ to function during embryonic development. It is mainly formed by contribution of two spatially and temporally overlapping cardiac progenitors arising from the splanchnic layer of the anterior lateral mesoderm forming the first heart field (FHF) and the second heart fields (SHF) [1]. Both endocardial primordia coalesce along the ventral midline via “zipping” to form a myocardial primitive heart semi-tube [4,5], which is currently believed to arise from FHF [6] During their migration as a cohesive sheet, cells of the heart region become epithelial and undergo cardiac differentiation, exhibiting organized myofibrils around the time of their fusion [3,7]. Kidokoro (2018) tracked the fate of splanchnic mesodermal cell populations in chicken embryos during heart tube formation and concluded that the early heart tube is formed by joint contribution of the lateral (primary) and middle (secondary) heart fields [11] They claimed that transformation of two-dimensional planar primordia into a three-dimensional structure occurs in close coordination with transformation of the adjacent endoderm into anterior intestine [11]

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