The origin of the endothelial cells: an evo‐devo approach for the invertebrate/vertebrate transition of the circulatory system

Abstract

Circulatory systems of vertebrate and invertebrate metazoans are very different. Large vessels of invertebrates are constituted of spaces and lacunae located between the basement membranes of endodermal and mesodermal epithelia, and they lack an endothelial lining. Myoepithelial differentation of the coelomic cells covering hemal spaces is a frequent event, and myoepithelial cells often form microvessels in some large invertebrates. There is no phylogenetic theory about the origin of the endothelial cells in vertebrates. We herein propose that endothelial cells originated from a type of specialized blood cells, called amoebocytes, that adhere to the vascular basement membrane. The transition between amoebocytes and endothelium involved the acquisition of an epithelial phenotype. We suggest that immunological cooperation was the earliest function of these protoendothelial cells. Furthermore, their ability to transiently recover the migratory, invasive phenotype of amoebocytes (i.e., the angiogenic phenotype) allowed for vascular growth from the original visceral areas to the well-developed somatic areas of vertebrates (especially the tail, head, and neural tube). We also hypothesize that pericytes and smooth muscle cells derived from myoepithelial cells detached from the coelomic lining. As the origin of blood cells in invertebrates is probably coelomic, our hypothesis relates the origin of all the elements of the circulatory system with the coelomic wall. We have collected from the literature a number of comparative and developmental data supporting our hypothesis, for example the localization of the vascular endothelial growth factor receptor-2 ortholog in hemocytes of Drosophila or the fact that circulating progenitors can differentiate into endothelial cells even in adult vertebrates.

Building the vertebrate heart - an evolutionary approach to cardiac development

“…the same cell sheet which is able to acquire contractile abilities and give rise to the cardiac wall. Primitive blood cells probably were delaminated coelomocytes with phagocytic abilities (Muñoz-Chápuli et al, 2005). Diversification of this primitive cell type allowed for acquisition of further functions in immunological defence and oxygen transport, but the coelomic evolutionary origin of the blood cells (and thus of the vertebrate endothelium) is probably recapitulated in the embryonic origin of the endocardium from the same coelomic sheet that gives rise to the myocardium.…”

“…Thus, the question about the evolutionary origin of the endocardium is directly connected to the hypothesis about the origin of the endothelium in vertebrates. We have published elsewhere a model about the origin of the vertebrate endothelium (Muñoz-Chápuli et al, 2005). We think that the endothelium derived in the vertebrate ancestors from a type of blood cell (frequently called the amoebocyte) which is able to adhere to the vascular basal laminae and migrate onto them.…”

“…This limitation be- The vertebrate heart is characterized by a multilayered myocardium (MYO) lined internally and externally by an endocardium (EN) and an epicardium (EP). From the evolutionary point of view, we suggest that the endocardium, as well as all the vertebrate endothelium, derives from a specialized type of blood cell (Muñoz-Chápuli et al, 2005). On the other hand, the epicardium develops from the attachment to the surface of the heart of proepicardial cells (PE) which arose from an ancestral pronephric external glomerulus (Pombal et al, 2008).…”

Manganese: A New Emerging Contaminant in the Environment

“…In echinoderms, immune cells (called coelomocytes) are a heterogeneous population of free moving cells found in all coelomic spaces, including the perivisceral coelomic cavities and the water-vascular system (reviewed in Matranga, 1996;Glinski & Jarosz, 2000;Smith et al, 2010). They are also present sparsely in the connective tissue (mesodermal stromal tissue) and amongst tissues of various organs (Muñoz-Chápuli et al, 2005;Pinsino et al, 2007). Coelomocytes participate as immune cells in function similar to their vertebrate's immune system homologues.…”

Introductory Chapter: Sea Urchin - Knowledge and Perspectives

“…Echinoderm immune cells, also known as coelomocytes, are a heterogeneous population of freely moving cells found in all coelomic spaces, including the perivisceral cavities and the water vascular system. They are also present sparsely in the connective tissue and among tissues of various organs [41][42][43][44]. A rapid increase of the number of the red amoebocytes has been shown in samples taken from polluted sea water, whereas petaloid cells are actively involved in the phagocytosis and phylopodial cells trigger the clot formation [5].…”