Origin of hemopoietic stem cells in embryonic bursa of Fabricius and bone marrow studied through interspecific chimeras.

The histogenesis of the bursa of Fabricius and of bone marrow was studied by a biological cell marking technique based on differences in the nuclear structure of two species of birds, Japanese quail (Coturnix coturnix japonica) and chick (Gallus gallus). In quail cells the nucleus contains a large amount of heterochromatin associated with the nucleolus. That makes it possible to distinguish them from chick cells after Feulgen-Rossenbeck staining and by electron microscopy. By grafting bursal rudiments and limb buds of quail into chick and inversely it was possible to demonstrate that the whole hemopoietic population of the bursa of Fabricius and of bone marrow is derived from bloodborne extrinsic stem cells. Neither endoderm nor mesoderm of the bursal rudiments is capable of differentiating into lymphoid cells. Combinations of quail bursal endoderm with chick homologous mesenchyme showed that the reticular cells of the follicles are the only endodermal derivatives of the bursa. The mesenchymal bursal component gives rise to the interfollicular connective cells. The contribution to bone marrow histogenesis of cells of vascular and blood origin, on one hand, and of the elements of the cartilaginous model, on the other hand, was analyzed. It appeared that osteoblasts, osteocytes, and stromal cells of marrow are derived from the perichondrium. In contrast, the endothelium of the vascular buds and the hemopoietic cells which invade the diaphysal cartilage during the endochondral ossification process do not belong to the mesenchymal bone primordium but have a fully extrinsic origin.