Axis-inducing activities and cell fates of the zebrafish organizer

Development ◽  
2000 ◽  
Vol 127 (16) ◽  
pp. 3407-3417 ◽  
Author(s):  
L. Saude ◽  
K. Woolley ◽  
P. Martin ◽  
W. Driever ◽  
D.L. Stemple
Keyword(s):  
Organizer Region ◽  
Complete Removal ◽  
Floor Plate ◽  
Significant Loss ◽  
Cell Fates ◽  
Deep Tissue ◽  
Head Formation ◽  
Prechordal Plate ◽  
Embryonic Shield ◽  
Organizer Activity

We have investigated axis-inducing activities and cellular fates of the zebrafish organizer using a new method of transplantation that allows the transfer of both deep and superficial organizer tissues. Previous studies have demonstrated that the zebrafish embryonic shield possesses classically defined dorsal organizer activity. When we remove the morphologically defined embryonic shield, embryos recover and are completely normal by 24 hours post-fertilization. We find that removal of the morphological shield does not remove all goosecoid- and floating head-expressing cells, suggesting that the morphological shield does not comprise the entire organizer region. Complete removal of the embryonic shield and adjacent marginal tissue, however, leads to a loss of both prechordal plate and notochord. In addition, these embryos are cyclopean, show a significant loss of floor plate and primary motorneurons and display disrupted somite patterning. Motivated by apparent discrepancies in the literature we sought to test the axis-inducing activity of the embryonic shield. A previous study suggested that the shield is capable of only partial axis induction, specifically being unable to induce the most anterior neural tissues. Contrary to this study, we find shields can induce complete secondary axes when transplanted into host ventral germ-ring. In induced secondary axes donor tissue contributes to notochord, prechordal plate and floor plate. When explanted shields are divided into deep and superficial fragments and separately transplanted we find that deep tissue is able to induce the formation of ectopic axes with heads but lacking posterior tissues. We conclude that the deep tissue included in our transplants is important for proper head formation.

scholarly journals The one-eyed pinhead gene functions in mesoderm and endoderm formation in zebrafish and interacts with no tail

Development ◽  
1997 ◽  
Vol 124 (2) ◽  
pp. 327-342 ◽  
Author(s):  
A.F. Schier ◽  
S.C. Neuhauss ◽  
K.A. Helde ◽  
W.S. Talbot ◽  
W. Driever
Keyword(s):  
Lithium Treatment ◽  
Floor Plate ◽  
Wild Type ◽  
Cell Fates ◽  
No Tail ◽  
Mesoderm Formation ◽  
Prechordal Plate ◽  
The One ◽  
Brain Patterning ◽  
Anterior Posterior

The zebrafish locus one-eyed pinhead (oep) is essential for the formation of anterior axial mesoderm, endoderm and ventral neuroectoderm. At the beginning of gastrulation anterior axial mesoderm cells form the prechordal plate and express goosecoid (gsc) in wild-type embryos. In oep mutants the prechordal plate does not form and gsc expression is not maintained. Exposure to lithium, a dorsalizing agent, leads to the ectopic induction and maintenance of gsc expression in wild-type embryos. Lithium treatment of oep mutants still leads to ectopic gsc induction but not maintenance, suggesting that oep acts downstream of inducers of dorsal mesoderm. In genetic mosaics, wild-type cells are capable of forming anterior axial mesoderm in oep embryos, suggesting that oep is required in prospective anterior axial mesoderm cells before gastrulation. The oep gene is also essential for endoderm formation and the early development of ventral neuroectoderm, including the floor plate. The loss of endoderm is already manifest during gastrulation by the absence of axial-expressing cells in the hypoblast of oep mutants. These findings suggest that oep is also required in lateral and ventral regions of the gastrula margin. The sonic hedgehog (shh).gene is expressed in the notochord of oep animals. Therefore, the impaired floor plate development in oep mutants is not caused by the absence of the floor plate inducer shh. This suggests that oep is required downstream or in parallel to shh signaling. The ventral region of the forebrain is also absent in oep mutants, leading to severe cyclopia. In contrast, anterior-posterior brain patterning appears largely unaffected, suggesting that underlying prechordal plate is not required for anterior-posterior pattern formation but might be involved in dorsoventral brain patterning. To test if oep has a wider, partially redundant role, we constructed double mutants with two other zebrafish loci essential for patterning during gastrulation. Double mutants with floating head, the zebrafish Xnot homologue, display enhanced floor plate and adaxial muscle phenotypes. Double mutants with no tail (ntl), the zebrafish homologue of the mouse Brachyury locus, display severe defects in midline and mesoderm formation including absence of most of the somitic mesoderm. These results reveal a redundant function of oep and ntl in mesoderm formation. Our data suggest that both oep and ntl act in the blastoderm margin to specify mesendodermal cell fates.

Properties of the primary organization field in the embryo of Xenopus laevis

Development ◽  
1972 ◽  
Vol 28 (1) ◽  
pp. 13-26
Author(s):  
J. Cooke
Keyword(s):  
Marginal Zone ◽  
Organizer Region ◽  
Angular Distance ◽  
Cell Polarization ◽  
Subsequent Paper ◽  
Basic Operation ◽  
Primary Organization ◽  
Organizer Activity ◽  
Set Up ◽  
Cell Immigration

The work presented, in this and the subsequent papers of a series, was begun in order to re-examine the properties of the amphibian primary embryonic field, in the light of current theories concerning the nature of individuation fields in developing animal systems. A detailed description is given of the basic operation whose results are described in this and the subsequent paper. This involves the transplantation, into a late blastula or stage-10 gastrula host, of a supernumerary stage-10 organizer region. The consequences of such operations during the following 4–6 h, up to the late gastrula stage, are also described. Evidence is presented that, from a time some 2·5 h before the organizer site first becomes externally visible, its presumptive region is immune from interference by the proximity of another, implanted organizer, even one which is itself 2·5 h older. That is to say, the final site of development of host organizer activity is not altered by the presence of such an implant. Pairs of early organizers at comparable stages of activity appear to set up competing fields of cellular orientation and immigration, which show a fairly sharp boundary at their interface. This is most obvious for pairs of organizers fairly close together, since the cell polarization and stretching is most pronounced in the region near to the apex of the field, i.e. the initial site of cell immigration. Independent initial fields of immigration due to two organizers can reliably be distinguished in cases where they are as little as 30° of angular distance apart in the marginal zone of the host. These results are to be considered in relation to those of Paper II, for the same series of operations, where the final patterns of cell differentiation are studied, and to those of Paper III, where evidence is given for the development of autonomous polarity in the region of the organizer.

scholarly journals An evolutionary-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra

2018 ◽  
Author(s):  
Matthias C. Vogg ◽  
Leonardo Beccari ◽  
Laura Iglesias Ollé ◽  
Christine Rampon ◽  
Sophie Vriz ◽  
...  
Keyword(s):  
Mammalian Cells ◽  
Feedback Loop ◽  
Rna Seq ◽  
Temporal Gene Expression ◽  
Basal Expression ◽  
Head Formation ◽  
Organizer Activity ◽  
Head Regeneration ◽  
Expression In Mammalian Cells ◽  
Head Inhibitor

AbstractThe Hydra polyp regenerates its head by transforming the gastric tissue below the wound into a head organizer made of two antagonistic cross-reacting components. The activator, previously characterized as Wnt3, drives apical differentiation by acting locally and auto-catalytically. The uncharacterized inhibitor, produced under the control of the activator, prevents ectopic head formation. By crossing RNA-seq data obtained in a β-catenin(RNAi) screen performed in planarians and a quantitative analysis of positional and temporal gene expression in Hydra, we identified Sp5 as a transcription factor that fulfills the head inhibitor properties: a Wnt/β-catenin inducible expression, a graded apical-to-basal expression, a sustained up-regulation during head regeneration, a multi-headed phenotype when knocked-down, a repressing activity on Wnt3 expression. In mammalian cells, Hydra and zebrafish Sp5 repress Wnt3 promoter activity while Hydra Sp5 also auto-activates its expression, possibly via β-catenin and/or Tcf/Lef1 interaction. This work identifies Sp5 as a novel potent feedback loop inhibitor of Wnt/β-catenin signaling across eumetazoans.

Properties of the primary organization field in the embryo of Xenopus laevis

Development ◽  
1973 ◽  
Vol 30 (2) ◽  
pp. 283-300
Author(s):  
J. Cooke
Keyword(s):  
Organizer Region ◽  
Positional Information ◽  
Host Cells ◽  
Normal Embryo ◽  
Tail Bud ◽  
Essentially Normal ◽  
Head Formation ◽  
Source Data ◽  
Primary Organization ◽  
Host Embryo

Patterns of individuation occurring in the primary embryonic axis of Xenopus following excision of the organizer region of the early gastrula are described. In some 70% of cases the information for induction of the complete head is qualitatively restored by the time of cell determination, giving rise to an essentially normal embryo. In some 40% of cases a second posterior axis of bilaterality is formed, causing development of a secondary anus, tail-fin and spinal cord, and often somites. The probabilities of twinning in the tailfield and of failure to complete apical regulation (= head formation) are largely independent. After such excision of the head organizer region, a delay of some 3 h in the schedule of visible differentiation in the neurula/tail-bud embryo is commonly incurred, whether or not apical regulation is successful. When the apex is excised from a host embryo which has already contained for some hours a second apex (= head organizer) as described in an earlier paper, that grafted apex then captures a considerably increased territory in the host material, as seen from the size of the individuation field finally caused by it. Such a shift across host cells, of the boundary between fields of positional information due to two organizers, is not seen under any conditions where these are left intact, or where host excision is carried out soon after implanting the donor organizer. In discussing the results and reconciling them with earlier observations, it is shown that they strongly suggest the presence of local polar (i.e. vectorial) properties in the presumptive mesoderm, due to signals from restricted regions which have achieved a special apical state. Repolarization of cells by a new organizer is not very rapid, and may spread decrementally from the source. Data on further delays in development, caused by the presence of the second organizer during regulation in the host apex, suggest that one organizer may act directly on cells elsewhere to delay or prevent the restoration of the apical state there.

Cngsc, a homologue of goosecoid, participates in the patterning of the head, and is expressed in the organizer region of Hydra

Development ◽  
1999 ◽  
Vol 126 (23) ◽  
pp. 5245-5254 ◽  
Author(s):  
M. Broun ◽  
S. Sokol ◽  
H.R. Bode
Keyword(s):  
Sensory Neurons ◽  
Organizer Region ◽  
Ventral Side ◽  
Evolutionary Conservation ◽  
The Body ◽  
Secondary Axis ◽  
Head Formation ◽  
Per Se ◽  
Endodermal Cells ◽  
Body Column

We have isolated Cngsc, a hydra homologue of goosecoid gene. The homeodomain of Cngsc is identical to the vertebrate (65-72%) and Drosophila (70%) orthologues. When injected into the ventral side of an early Xenopus embryo, Cngsc induces a partial secondary axis. During head formation, Cngsc expression appears prior to, and directly above, the zone where the tentacles will emerge, but is not observed nearby when the single apical tentacle is formed. This observation indicates that the expression of the gene is not necessary for the formation of a tentacle per se. Rather, it may be involved in defining the border between the hypostome and the tentacle zone. When Cngsc(+) tip of an early bud is grafted into the body column, it induces a secondary axis, while the adjacent Cngsc(−) region has much weaker inductive capacities. Thus, Cngsc is expressed in a tissue that acts as an organizer. Cngsc is also expressed in the sensory neurons of the tip of the hypostome and in the epithelial endodermal cells of the upper part of the body column. The plausible roles of Cngsc in organizer function, head formation and anterior neuron differentiation are similar to roles goosecoid plays in vertebrates and Drosophila. It suggests widespread evolutionary conservation of the function of the gene.

Goosecoid promotes head organizer activity by direct repression of Xwnt8 in Spemann’s organizer

Development ◽  
2001 ◽  
Vol 128 (15) ◽  
pp. 2975-2987 ◽  
Author(s):  
Jie Yao ◽  
Daniel S. Kessler
Keyword(s):  
Marginal Zone ◽  
The Body ◽  
Treated Animal ◽  
Homeodomain Protein ◽  
Regulatory Domains ◽  
Spemann's Organizer ◽  
Transcriptional Regulatory ◽  
Head Formation ◽  
Wnt Inhibitor ◽  
Organizer Activity

Formation of the vertebrate body plan is controlled by discrete head and trunk organizers that establish the anteroposterior pattern of the body axis. The Goosecoid (Gsc) homeodomain protein is expressed in all vertebrate organizers and has been implicated in the activity of Spemann’s organizer in Xenopus. The role of Gsc in organizer function was examined by fusing defined transcriptional regulatory domains to the Gsc homeodomain. Like native Gsc, ventral injection of an Engrailed repressor fusion (Eng-Gsc) induced a partial axis, while a VP16 activator fusion (VP16-Gsc) did not, indicating that Gsc functions as a transcriptional repressor in axis induction. Dorsal injection of VP16-Gsc resulted in loss of head structures anterior to the hindbrain, while axial structures were unaffected, suggesting a requirement for Gsc function in head formation. The anterior truncation caused by VP16-Gsc was fully rescued by Frzb, a secreted Wnt inhibitor, indicating that activation of ectopic Wnt signaling was responsible, at least in part, for the anterior defects. Supporting this idea, Xwnt8 expression was activated by VP16-Gsc in animal explants and the dorsal marginal zone, and repressed by Gsc in Activin-treated animal explants and the ventral marginal zone. Furthermore, expression of Gsc throughout the marginal zone inhibited trunk formation, identical to the effects of Frzb and other Xwnt8 inhibitors. A region of the Xwnt8 promoter containing four consensus homeodomain-binding sites was identified and this region mediated repression by Gsc and activation by VP16-Gsc, consistent with direct transcriptional regulation of Xwnt8 by Gsc. Therefore, Gsc promotes head organizer activity by direct repression of Xwnt8 in Spemann’s organizer and this activity is essential for anterior development.

Characterization of the head organizer in hydra

Development ◽  
2002 ◽  
Vol 129 (4) ◽  
pp. 875-884 ◽  
Author(s):  
Mariya Broun ◽  
Hans R. Bode
Keyword(s):  
Organizer Region ◽  
Apical Part ◽  
The Body ◽  
Central Process ◽  
Axial Patterning ◽  
Secondary Axis ◽  
Head Formation ◽  
Body Column ◽  
Self Organizing

A central process in the maintenance of axial patterning in the adult hydra is the head activation gradient, i.e. the potential to form a secondary axis, which is maximal in the head and is graded down the body column. Earlier evidence suggested that this gradient was based on a single parameter. Using transplantation experiments, we provide evidence that the hypostome, the apical part of the head, has the characteristics of an organizer in that it has the capacity to induce host tissue to form most of the second axis. By contrast, tissue of the body column has a self-organizing capacity, but not an inductive capacity. That the inductive capacity is confined to the hypostome is supported by experiments involving a hypostome-contact graft. The hypostome, but not the body column, transmits a signal(s) leading to the formation of a second axis. In addition, variations of the transplantation grafts and hypostome-contact grafts provide evidence for several characteristics of the organizer. The inductive capacity of the head and the self-organizing capacity of the body column are based on different pathways. Head inhibition, yya signal produced in the head and transmitted to the body column to prevent head formation, represses the effect of the inducing signal by interfering with formation of the hypostome/organizer. These results indicate that the organizer characteristics of the hypostome of an adult hydra are similar to those of the organizer region of vertebrate embryos. They also indicate that the Gierer-Meinhardt model provides a reasonable framework for the mechanisms that underlie the organizer and its activities. In addition, the results suggest that a region of an embryo or adult with the characteristics of an organizer arose early in metazoan evolution.

scholarly journals Floor plate-derived sonic hedgehog regulates glial and ependymal cell fates in the developing spinal cord

Development ◽  
2013 ◽  
Vol 140 (7) ◽  
pp. 1594-1604 ◽  
Author(s):  
K. Yu ◽  
S. McGlynn ◽  
M. P. Matise
Keyword(s):  
Spinal Cord ◽  
Sonic Hedgehog ◽  
Ependymal Cell ◽  
Floor Plate ◽  
Cell Fates ◽  
Developing Spinal Cord

Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system

Development ◽  
1998 ◽  
Vol 125 (15) ◽  
pp. 2759-2770 ◽  
Author(s):  
M.P. Matise ◽  
D.J. Epstein ◽  
H.L. Park ◽  
K.A. Platt ◽  
A.L. Joyner
Keyword(s):  
Spinal Cord ◽  
Central Nervous System ◽  
Nervous System ◽  
Floor Plate ◽  
Cell Fates ◽  
Ventral Midline ◽  
Mouse Mutants ◽  
Necessary And Sufficient ◽  
Vertebrate Central Nervous System ◽  
Mouse Central Nervous System

Induction of the floor plate at the ventral midline of the neural tube is one of the earliest events in the establishment of dorsoventral (d/v) polarity in the vertebrate central nervous system (CNS). The secreted molecule, Sonic hedgehog, has been shown to be both necessary and sufficient for this induction. In vertebrates, several downstream components of this signalling pathway have been identified, including members of the Gli transcription factor family. In this study, we have examined d/v patterning of the CNS in Gli2 mouse mutants. We have found that the floor plate throughout the midbrain, hindbrain and spinal cord does not form in Gli2 homozygotes. Despite this, motoneurons and ventral interneurons form in their normal d/v positions at 9.5 to 12.5 days postcoitum (dpc). However, cells that are generated in the region flanking the floor plate, including dopaminergic and serotonergic neurons, were greatly reduced in number or absent in Gli2 homozygous embryos. These results suggest that early signals derived from the notochord can be sufficient for establishing the basic d/v domains of cell differentiation in the ventral spinal cord and hindbrain. Interestingly, the notochord in Gli2 mutants does not regress ventrally after 10.5 dpc, as in normal embryos. Finally, the spinal cord of Gli1/Gli2 zinc-finger-deletion double homozygous mutants appeared similar to Gli2 homozygotes, indicating that neither gene is required downstream of Shh for the early development of ventral cell fates outside the ventral midline.

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