Head induction in the chick

The formation of the head is a multistep process beginning early in embryogenesis. Transplantation, gene knock-out and gene-transfer experiments indicate the existence of a head organizer as a separate entity, which is distinct from the trunk organizer (for reviews see Bouwmeester and Leyns, 1997; Harland and Gerhart, 1997). A common vertebrate characteristic is the successive appearance and the structural continuity of the definitive endoderm (prospective foregut, liver), the mesendoderm (prechordal plate) and the notochord. In the development of the amniota (reptiles, birds, mammalia), these three tissue types are preceded by the primitive endoderm, the visceral endoderm in mice and the hypoblast in the chick, which gives rise to the extraembryonic yolk sac. Classically, the prechordal mesendoderm cells were considered to be the cell population inducing and patterning the head. They populate the early dorsal blastopore lip in amphibia, or the tip of the fully extended primitive streak in amniota, from where they ingress to underlie the prospective forebrain region (for review see Ruiz i Altaba, 1993). The importance of the endoderm for head development has become evident in Xenopus laevis. It expresses a secreted factor, Cerberus, which can induce a secondary head upon injection into the D4-blastomere of 32-cell embryos (Bouwmeester et al., 1996). However, on its own, the endoderm is not capable of head induction in transplantation experiments, which is in contrast to the prechordal mesendoderm (Bouwmeester et al., 1996). More recently, a murine gene related to Cerberus, the Cerberus-like gene, has been isolated (Belo et al., 1997; Thomas et al., 1997; Biben et al., 1998; Shawlot et al., 1998). After mid-streak stages, it is expressed in the definitive endoderm as it emerges from the node. This endoderm has the same fate, foregut and liver, as the non-involuting endoderm of Xenopus, in which Cerberus is expressed. However, in contrast to the frog gene, there is another expression domain of Cerberus-like in the anterior visceral endoderm (AVE) prior to the onset of gastrulation. A specific role of the AVE in the mammalian head organizer is suggested by a number of recent findings (for review see Beddington and Robertson, 1998). Several genes are expressed in an independent domain in the AVE of the prospective head region before or at the onset of primitive streak formation, prior to their expression in the axial mesendoderm or the node during gastrulation. These include the homeobox genes Hesx1 (Rpx), Gsc, Lim1, Hex and Otx2, the forkhead gene HNF3β, the 815 Development 126, 815-825 (1999) Printed in Great Britain © The Company of Biologists Limited 1999 DEV2358