A phase and electron microscopic study of vasculogenesis and erythropoiesis in the yolk sac of the mouse

Abstract

By seven days of gestation, the yolk sac of the mouse has a sheet of mesoderm adjacent to the basement membrane separating it from the endodermal epithelium. Localized proliferations of this mesoderm produces thickened cellular regions which transform into the angioblastic cords; all of these developmental cells are attached by tight junctions and desmosomes. By eight and onehalf days, lumina appear within the angioblastic cords; the peripheral cells become attenuated and form endothelial cells which will line the primitive vessels while the more central cells become the primitive erythroblasts of the blood island.The process of vasculogenesis and lumenization occurs between eight and onehalf and nine days of gestation and has been correlated with the reduction of cellular junctions between angioblasts and fixed primitive erythroblasts, a loss of the visceral basement membrane and the formation of wide intercellular channels between endodermal epithelial cells. The primitive erythroblasts comprising the blood islands have abundant polysomes, sparse rough endoplasmic reticulum and possess coated vesicles and ferritin aggregates in their cytoplasm and coated invaginations of their plasma membrane. By nine days of gestation, the primitive erythroblasts lose their attachments and become free in the vitelline vessels. Mitochondria of the primitive and free erythroblasts are slightly enlarged and have lighter matrices than angioblasts and mesodermal cells. By 10 to 11 days of gestation, as differentiation proceeds, coated vesicles and invaginations become more numerous and the developing erythroblasts gradually decrease in both cell and nuclear size. Concomitant with these changes is the decrease in the number and size of the mitochondria, a decrease in polysomal numbers and an increase in hemoglobin and cytoplasmic density.The inter-and intracellular events that occur during the formation of the primitive blood vessels and erythrocytic precursors of the yolk sac have not been thoroughly documented from an ultrastructural standpoint. The developmental stages in the process of hemopoiesis occur rapidly with the undifferentiated cells undergoing irreversible specialization along distinct pathways. Submicroscopic analysis has the dual potential of determining the earliest morphological features which signal the initial steps of differentiation and illuminating the changes in structural and functional relationships that occur during subsequent maturation and specialization. Previous studies have dealt with such features as the cellular versus syncytial nature of the primitive angioblastic cords, how ANAT. REC., 170: 199-224. vascular lumen form and the developmental pathway and structural features of erythrocyte differentiation and maturation (Bloom, '38; Danchakoff, '16a,b; Haar, '70; Jones, '64; Kovach et al., '67; Maximow, '09, '24; Sorenson, '61). It is the purpose of this correlated phase and electron microscopic study to expand and clarify the early developmental processes involved in erythropoiesis and vas...

Vasculogenesis of the embryonic heart: Origin of blood island‐like structures

“…They enter the heart at the stage of development corresponding to the established erythroid lineage, not at the stage of hematopoietic progenitor cells. This was confirmed by their more mature morphology (ultrastructure) as compared to the erythroblasts of yolk sac blood islands (Haar and Ackerman 1971;Tavassoli, 1991) and their Ter/119 antigen expression, the latter being specific to cells of erythroid/erythrocyte stage (Ikuta et al, 1990). A similar observation, namely, that commitment to hematopoietic lineage precedes the formation of blood island-like structures in the embryonic heart, has been suggested in a previous study by Kattan et al (2004).…”

“…We were unable, however, to demonstrate the presence of hematopoietic stem cells in the embryonic heart neither by the use of TEM or by immunohistochemical staining with antibodies to HSC antigens. We also could not find any blood island exhibiting a pattern of cellular assembly similar to a yolk sac blood island (Haar and Ackerman, 1971). Our study indicates that the embryonic heart supplies only new erythroblasts owing to their proliferative capacity within the primitive vascular vesicles at the time before coronary vessels are connected to the aorta (Fig.…”

“…The current evidence for this opinion comes from common molecular markers in cells of endothelial/angioblastic and hematopoietic potential (Millauer et al, 1993;Lin et al, 1995;Shalaby et al, 1995;Young et al, 1995;Eichmann et al, 1997). In addition, the areas of embryos where hematoblasts appear are strictly related to hematopoietic and vasculogenic events (yolk sac) (Haar and Ackerman, 1971;Tavassoli, 1991). The issue of the relationship between hematopoietic cells and vasculogenesis in embryonic heart development has been raised in a current study by Kattan et al (2004).…”

Coordinate expression of vascular endothelial growth factor receptor‐1 (fit‐1) and its ligand suggests a paracrine regulation of murine vascular development

“…At these developmental stages, the segregation of the hemangioblastic lineage takes place in the yolk sac mesoderm (Haar and Ackermann, 1971). These events are accompanied by the induction of VEGFRl/flt-1 expression and of VEGFR2If lk-1 expression, which was first detected at E7-7.25 (Yamaguchi et al, 1993).…”

“…(Haar and Ackermann, 1971). To investigate whether VEGFRlKlt-1 is expressed during these early steps of vascular development, we performed in situ hybridization analyses of mouse embryos at E7.5.…”