Analysis of Intestinal Splanchnopleure Development

Abstract

Mesothelium is a simple squamous epithelium that forms the surface layer of all coelomic cavities and organs. Despite its widespread localization, mesothelial development has been studied almost exclusively in the heart. In this organ, mesothelial progenitors originate external to the initial heart tube and migrate across the pericardial cavity to contact and envelop the heart forming the cardiac mesothelium (epicardium). Newly formed epicardial cells then delaminate from the epithelium, invade the myocardium, and differentiate into fibroblasts, vascular smooth muscle and endothelial cells. Thus, the initial heart tube, composed of splanchnic mesoderm and endocardial cells, is devoid of both mesothelial and vascular progenitor populations and must recruit these cells from an exogenous source. Studies of the liver, lungs, and intestine demonstrated a similar capacity for mesothelial cells to invade each respective organ and contribute to the vasculature indicating mesothelial cells may have a conserved role in coelomic vasculogenesis. The aim of the research presented here was to identify the origin of mesothelial and vascular cells of the intestine to determine if the extensively studied cardiac model of mesotheliogenesis and vasculogenesis was widely applicable among coelomic organs. A comprehensive examination of mesodermal development in the avian embryo revealed a potential mesothelial progenitor population present from the onset of intestinal formation. Additionally, large blood vessels appeared to be derived via angiogenesis from the vitelline artery. A detailed lineage tracing study revealed mesothelial progenitors are indeed intrinsic to the splanchnic mesoderm of the intestinal primordium. A chick-quail chimera study demonstrated that both the vascular smooth muscle and endothelial cells at all levels of the intestine are derived from progenitors resident to the splanchnopleure through remodeling of a primordial endothelial plexus. Thus, the intestine displays a novel method of mesotheliogenesis and vascular formation compared to the heart.