Chapter Twenty-Six - Organizers in Development
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.
References (107)
- et al.
BMPs as mediators of roof plate repulsion of commissural neurons
Neuron
(1999) - et al.
Lens specification is the ground state of all sensory placodes, from which FGF promotes olfactory identity
Developmental Cell
(2006) - et al.
Gastrulation in the mouse: The role of the homeobox gene goosecoid
Cell
(1992) - et al.
Molecular nature of Spemann's organizer: The role of the Xenopus homeobox gene goosecoid
Cell
(1991) - et al.
Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity
Cell
(1993) - et al.
Goosecoid misexpression alters the morphology and Hox gene expression of the developing chick limb bud
Mechanisms of Development
(1997) - et al.
Inductive interactions in the spatial and temporal restriction of lens-forming potential in embryonic ectoderm of Xenopus laevis
Developmental Biology
(1987) - et al.
Establishment of the telencephalon during gastrulation by local antagonism of Wnt signaling
Neuron
(2002) - et al.
The homeobox gene goosecoid and the origin of organizer cells in the early chick blastoderm
Cell
(1993) - et al.
A role for the roof plate and its resident TGFbeta-related proteins in neuronal patterning in the dorsal spinal cord
Cell
(1997)
In vivo regulation of somite differentiation and proliferation by Sonic Hedgehog
Developmental Biology
Patterning of the embryonic avian midbrain after experimental inversions: A polarizing activity from the isthmus
Developmental Biology
Expression of the homeobox Chick-en gene in chick/quail chimeras with inverted mes-metencephalic grafts
Developmental Biology
Induction of ectopic engrailed expression and fate change in avian rhombomeres: Intersegmental boundaries as barriers
Mechanisms of Development
Induction of a mesencephalic phenotype in the 2-day-old chick prosencephalon is preceded by the early expression of the homeobox gene en
Neuron
The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain
Cell
The midbrain-hindbrain phenotype of Wnt-1-/Wnt-1-mice results from stepwise deletion of engrailed-expressing cells by 9.5 days postcoitum
Cell
FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb
Cell
Lateral and axial signals involved in avian somite patterning: A role for BMP4
Cell
Sonic hedgehog mediates the polarizing activity of the ZPA
Cell
Fgf signaling controls the number of phalanges and tip formation in developing digits
Current Biology
SWiP-1: Novel SOCS box containing WD-protein regulated by signalling centres and by Shh during development
Mechanisms of Development
Sonic hedgehog from the basal plate and the zona limitans intrathalamica exhibits differential activity on diencephalic molecular regionalization and nuclear structure
Neuroscience
Notochord induction of zebrafish slow muscle mediated by Sonic hedgehog
Genes and Development
The ventralizing effect of the notochord on somite differentiation in chick embryos
Anatomy and Embryology (Berlin)
The roof plate boundary is a bi-directional organiser of dorsal neural tube and choroid plexus development
Development
Cngsc, a homologue of goosecoid, participates in the patterning of the head, and is expressed in the organizer region of Hydra
Development
The production of new hydranths in hydra by the insertion of small grafts
Journal of Experimental Zoology
The roof plate regulates cerebellar cell-type specification and proliferation
Development
A model for anteroposterior patterning of the vertebrate limb based on sequential long- and short-range Shh signalling and Bmp signalling
Development
Polarising zone activity in limb buds of amniotes
FGF-2: Apical ectodermal ridge growth signal for chick limb development
Science
Lens induction and determination
Neocortex patterning by the secreted signaling molecule FGF8
Science
The cellular environment controls the expression of engrailed-like protein in the cranial neuroepithelium of quail-chick chimeric embryos
Development
A functional homologue of goosecoid in Drosophila
Development
Embryonic induction—Molecular prospects
Development
The heritage of experimental embryology: Hans Spemann and the organizer
Secondary axis induction by heterospecific organizers in zebrafish
Developmental Dynamics
Notochord repression of endodermal Sonic hedgehog permits pancreas development
Genes and Development
Differenzierungspotenzen isolierter Teile der Urodelengastrula
Wilhelm Roux' Archiv für Entwicklungsmechanik der Organismen
Reminiscences on the life and work of Johannes Holtfreter
Positional signalling by Hensen's node when grafted to the chick limb bud
Journal of Embryology and Experimental Morphology
A small population of anterior cells patterns the forebrain during zebrafish gastrulation
Nature
Regeneration of isthmic tissue is the result of a specific and direct interaction between rhombomere 1 and midbrain
Development
Hedgehog signaling from the ZLI regulates diencephalic regional identity
Nature Neuroscience
Notochord to endoderm signaling is required for pancreas development
Development
Experimental studies on the eye of the frog embryo
Archiv für Entwicklungsmechanik der Organismen
Hensen's node induces neural tissue in Xenopus ectoderm. Implications for the action of the organizer in neural induction
Development
Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification
Nature
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2022, Developmental BiologyCitation Excerpt :A sequential order emanates from the interplay of intrinsic & extrinsic controls, where: first, local extrinsic parameters modulate primary organ positioning; second, neuromast migration dictates the innervation and therefore neuronal network (Haas and Gilmour, 2006); and third, the final position of the organ induces in situ the formation of a life-long niche for neuromast stem cells during organ maturation (Seleit et al., 2017b). The same hierarchical organisation is well reported in different induction paradigms, like the induction of the lens by the neural retina in vertebrates (Cvekl and Ashery-Padan, 2014) or the generation of a new neural plate by the Henses’ node in chicken (Storey et al., 1992) (Anderson and Stern, 2016). While both siml and Da mutants result in a majority of organs retained at the midline, the phenotypes and their aetiology are distinct.