Chapter Twenty-Six - Organizers in Development

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Abstract

An “organizer” is formally defined as a region, or group of cells in an embryo that can both induce (change the fate) and pattern (generate an organized set of structures) adjacent embryonic cells. To date, about four such regions have been demonstrated: the primary or Spemann organizer (Hensen's node in amniotes), the notochord, the zone of polarizing activity of the limb bud, and the mid-hindbrain boundary. Here we review the evidence for these and compare them with a few other regions which have been proposed to represent other organizers and we speculate on why so few such regions have been discovered.

Section snippets

The “Spemann Organizer”

Initially, there was some debate concerning whether one particular structure in the early amphibian embryo (the dorsal lip of the blastopore, the site of ingression of cells during gastrulation) itself gives rise to the embryonic axis or whether it also acts by influencing neighboring cells (Hamburger, 1988, Lewis, 1907, Oppenheimer, 1991, Sander and Faessler, 2001). The critical experiments that finally resolved the controversy were performed by Hilde Mangold and Hans Spemann in 1921–1924 (

The Notochord and Floor Plate

Following gastrulation, the dorsal blastopore (or shield in fish, Hensen's node in amniotes) gradually gives rise to a rod of axial mesoderm underling the neural plate: the notochord. A graft of notochord adjacent to the lateral neural tube of the trunk changes the fate of the latter and transforms them into ventral cell types: a floor plate and motor neurons, arranged in their normal relation to each other, recapitulating the pattern of the ventral neural tube (Placzek, Tessier-Lavigne, et

Organizers and Brain Patterning

The notochord and floor plate end anteriorly in the prospective pituitary/Rathke's pouch area, underlying the confluence between midbrain and forebrain. A floor plate-like region, expressing several common markers including Sonic hedgehog (Shh), extends rostrally in the ventral brain: the hypothalamus and basal plate. From the middle of its trajectory, a dorsally projecting extension of the Shh-expressing region, the zona limitans intrathalamica (ZLI) marks the border between the first two

Patterning the Limb

Two major signaling regions have been implicated in limb patterning: the zone of polarizing activity (ZPA) situated in the posterior limb bud mesenchyme, and the apical ectodermal ridge (AER), running along the edge of the ectodermal covering of the bud. A ZPA graft into the anterior limb mesenchyme generates anteroposterior mirror-image duplication of limb skeletal structures and associated soft tissues; the earlier this is done, the more complete the duplication (Saunders and Gasseling, 1968,

Spemann's Experiments on the Lens

Spemann had approached the famous organizer experiment after having studied the cell interactions that lead to formation of the lens of the eye, two decades earlier. There he had already thought of the ideas of inductive and patterning influences between tissues. The lens develops from the non-neural ectoderm overlying the neural optic vesicle in the forebrain. Spemann suggested that the optic vesicle induces the lens and showed that injury to eye rudiment in the frog (Rana fusca) results in

Common Features Between Organizers?

When it was discovered as a marker for the dorsal lip/shield/Hensen's node of vertebrate embryos at the time when this structure has organizing ability, the homeobox gene Goosecoid (GSC) was hailed as a universal marker of the organizer (Blum et al., 1992, Cho et al., 1991, Izpisua-Belmonte et al., 1993, Zhu et al., 1999). Although it is not expressed in most of the “secondary” organizers listed above, it does seem to play a role in regulating signaling in the limb (Heanue et al., 1997).

GSC

Conclusions

We have briefly presented evidence (see Table 1) that suggests that at least four regions of the vertebrate embryo can act as true organizers in that they possess both inducing and patterning functions: the classical Spemann organizer (the shield in fish, Hensen's node in amniotes), the notochord, the midbrain–hindbrain boundary, and the ZPA (perhaps together with the AER) of the limb bud. There are other regions that have been, or could be, considered to possess organizing properties (for

Acknowledgment

Our research on this topic was funded by the BBSRC.

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