Abstract
The cardiovascular system of bilaterians developed from a common ancestor. However, no endothelial cells exist in invertebrates demonstrating that primitive cardiovascular tubes do not require this vertebrate-specific cell type in order to form. This raises the question of how cardiovascular tubes form in invertebrates? Here we discovered that in the invertebrate cephalochordate amphioxus, the basement membranes of endoderm and mesoderm line the lumen of the major vessels, namely aorta and heart. During amphioxus development a laminin-containing extracellular matrix (ECM) was found to fill the space between the basal cell surfaces of endoderm and mesoderm along their anterior-posterior (A-P) axes. Blood cells appear in this ECM-filled tubular space, coincident with the development of a vascular lumen. To get insight into the underlying cellular mechanism, we induced vessels in vitro with a cell polarity similar to the vessels of amphioxus. We show that basal cell surfaces can form a vascular lumen filled with ECM, and that phagocytotic blood cells can clear this luminal ECM to generate a patent vascular lumen. Therefore, our experiments suggest a mechanism of blood vessel formation via basal cell surfaces in amphioxus and possibly in other invertebrates that do not have any endothelial cells. In addition, a comparison between amphioxus and mouse shows that endothelial cells physically separate the basement membranes from the vascular lumen, suggesting that endothelial cells create cardiovascular tubes with a cell polarity of epithelial tubes in vertebrates and mammals.
Highlights
It has been suggested that the cardiovascular system of bilaterians evolved from a common ancestor [1,2,3]
Based on previous morphological studies, an electron dense layer, morphologically similar to a basement membrane, has been observed on the luminal side of invertebrate blood vessels [3,10,11,12]. It remained to be shown whether invertebrate vessels were lined by a real basement membrane or, alternatively, by an apical extracellular matrix (ECM) that is morphologically similar, but molecularly different from a basement membrane [13,14,15,16]
Our study provides the first model of vessel formation in amphioxus and possibly in other invertebrates (Fig. 5A and 5B)
Summary
It has been suggested that the cardiovascular system of bilaterians evolved from a common ancestor [1,2,3]. This is because the heart and major blood vessels develop as tubes along the anterior-posterior (AP) axes in both vertebrates and invertebrates [4,5]. Despite conservation of several genes involved in cardiovascular development, new features evolved in the vertebrates. In order to understand the ancestral and conserved part of cardiovascular tube formation, we investigated developing vessels in the invertebrate amphioxus and compared these vessels with the homologous ones in mouse. We used the cephalochordate amphioxus, Branchiostoma lanceolatum, because its body plan is similar to the one of vertebrates [7,8], and because it forms a monophyletic clade with vertebrates and urochordates [9]
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