Abstract
During cardiogenesis the epicardium, covering the surface of the myocardial tube, has been ascribed several functions essential for normal heart development of vertebrates from lampreys to mammals. We investigated a novel function of the epicardium in ventricular development in species with partial and complete septation. These species include reptiles, birds and mammals. Adult turtles, lizards and snakes have a complex ventricle with three cava, partially separated by the horizontal and vertical septa. The crocodilians, birds and mammals with origins some 100 million years apart, however, have a left and right ventricle that are completely separated, being a clear example of convergent evolution. In specific embryonic stages these species show similarities in development, prompting us to investigate the mechanisms underlying epicardial involvement. The primitive ventricle of early embryos becomes septated by folding and fusion of the anterior ventricular wall, trapping epicardium in its core. This folding septum develops as the horizontal septum in reptiles and the anterior part of the interventricular septum in the other taxa. The mechanism of folding is confirmed using DiI tattoos of the ventricular surface. Trapping of epicardium-derived cells is studied by transplanting embryonic quail pro-epicardial organ into chicken hosts. The effect of decreased epicardium involvement is studied in knock-out mice, and pro-epicardium ablated chicken, resulting in diminished and even absent septum formation. Proper folding followed by diminished ventricular fusion may explain the deep interventricular cleft observed in elephants. The vertical septum, although indistinct in most reptiles except in crocodilians and pythonidsis apparently homologous to the inlet septum. Eventually the various septal components merge to form the completely septated heart. In our attempt to discover homologies between the various septum components we aim to elucidate the evolution and development of this part of the vertebrate heart as well as understand the etiology of septal defects in human congenital heart malformations.
Highlights
During evolution the ventricle of the heart became divided into left and right chambers by a complete septum
Our studies show that part of the septum is critically dependent on interactions between myocardium and the epicardium including the epicardiumderived cells (EPDCs) [4,5] for its development, and will develop abnormally if the epicardium is disturbed [6,7]
We focused on the functional role of the epicardium and EPDCs using various approaches: 1. immunohistochemistry of epicardium and EPDCs in embryos of different vertebrate species, 2. quail-chicken chimeras by transplantation of early quail proepicardial organ (PEO) into the pericardial cavity of chicken to label subsets of epicardial and endothelial cells, 3. epicardiumdeficient animal models such as the podoplanin knockout mouse, and epicardial ablation experiments in chicken embryos, 4
Summary
During evolution the ventricle of the heart became divided into left and right chambers by a complete septum. Cardiac ventricular development in vertebrates, starting in an embryonic state with a primitive common ventricular tube, leading to separation into the left (LV) and right ventricle (RV), is a complex phenomenon. The mechanisms involve both the ventricular inflow and outflow compartment [8,9,10]. Other extant reptile groups including the squamates (lizards and snakes) and chelonians (turtles) show what is assumed to be a primitive pattern They show partial septation by a horizontal and a vertical septum leading to a ventricle that is divided into 3 interconnected cavities. It is not possible to reconstruct the evolutionary history of ventricular septation as fossil records of embryonic soft tissues are non-existent
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