A phagocytic cell system of hemopoietic origin exists in the early avian embryo (Cuadros, Coltey, Nieto, and Martin: Development 115:157-168, '92). In this study we investigated the presence of cells belonging to this system in the central nervous system (CNS) of chick and quail embryos by using both histochemical staining for acid phosphatase and immunolabelling with antibodies recognizing cells of quail hemangioblastic lineage. The origin of these cells was traced in interspecific chick-quail yolk sac chimeras. Hemopoietic cells were detected within the CNS from developmental stage HH15 on, and steadily increased in number at subsequent stages. Analysis of yolk sac chimeras revealed that most of these cells were of yolk sac origin, although some hemopoietic cells of intramebryonic origin were also found in the CNS. Immunocytochemical, histochemical, and ultrastructural characterization allowed us to identify hemopoietic cells in the CNS as macrophages. These cells were consistently found in the brain vesicles and spinal cord, appearing (1) between undifferentiated neuroepithelial cells at dorsal levels of the CNS; (2) in areas of cell death; (3) in the marginal layer in close relationship with developing axons; (4) in large extracellular spaces in the subventricular layer; (5) on vascular buds growing through the marginal and subventricular layers; and (6) in the ventricular lumen. Macrophages in different locations varied in morphology and ultrastructure, suggesting that in addition to their involvement in phagocytosis, they play a role in other processes in the developing CNS, such as axonal growth and vascular development. The first macrophages migrate to the CNS independently of its vascularization, apparently traversing the pial basal lamina to reach the nervous parenchyma. Other macrophages may enter the CNS together with vascular buds at subsequent stages during CNS vascularization.
We have used two molecular markers to label blood vessel endothelial cells and their precursors in the early avian embryo. One marker, called Quek1, is the avian homologue of the mammalian VEGF receptor flk-1 and the other is the MB1/QH1 monoclonal antibody. Quek1 is expressed in a subset of mesodermal cells from the gastrulation stage. Quek1 positive cells later form blood vessel endothelial cells and express the MB1/QH1 antigen which is specific for endothelial and hemopoietic cells of the quail species. These two markers allowed us first to show that the cephalic paraxial mesoderm has angiogenic potentials which are much more extended than its trunk counterpart (the somites). Secondly, the origin of the endothelial cells lining the craniofacial and head blood vessels was mapped on the 3-somite stage cephalic mesoderm via the quail-chick chimera technique, in which well defined mesodermal territories are exchanged between stage-matched embryos of both species in a strictly isotopic manner. We found that the anterior region of the cephalic paraxial mesoderm is largely recruited to provide the forebrain and the upper face with their vasculature. This means that large volumes of tissues are vascularized by a discrete region of the cephalic mesoderm, the fate of which is otherwise to give rise to muscles. The widespread expansion of the angiogenic cells arising from the anterior paraxial mesoderm must be related to the high growth rate of the anterior region of the neural primordium, yielding the telencephalon and of the neural crest-derived facial structures which are themselves devoid of angiogenic potencies.(ABSTRACT TRUNCATED AT 250 WORDS)
We have used the quail-chick chimera technique to study the origin of the bones of the skull in the avian embryo. Although the contribution of the neural crest to the facial and visceral skeleton had been established previously, the origin of the vault of the skull (i.e. frontal and parietal bones) remained uncertain. Moreover formation of the occipito-otic region from either the somitic or the cephalic paraxial mesoderm had not been experimentally investigated. The data obtained in the present and previous works now allow us to assign a precise embryonic origin from either the mesectoderm, the paraxial cephalic mesoderm or the five first somites, to all the bones forming the avian skull. We distinguish a skull located in front of the extreme tip of the notochord which reaches the sella turcica and a skull located caudally to this boundary. The former ('prechordal skull') is derived entirely from the neural crest, the latter from the mesoderm (cephalic or somitic) in its ventromedial part ('chordal skull') and from the crest for the parietal bone and for part of the otic region. An important point enlighten in this work concerns the double origin of the corpus of the sphenoid in which basipresphenoid is of neural crest origin and the basipostsphenoid is formed by the cephalic mesoderm. Formation of the occipito-otic region of the skeleton is particularly complex and involves the cooperation of the five first somites and the paraxial mesoderm at the hind-brain level. The morphogenetic movements leading to the initial puzzle assembly could be visualized in a reproducible way by means of small grafts of quail mesodermal areas into chick embryos. The data reported here are discussed in the evolutionary context of the ‘New Head’ hypothesis of Gans and Northcutt (1983, Science, 220, 268–274).
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