The organizer of the mouse gastrula is composed of a dynamic population of progenitor cells for the axial mesoderm

Development ◽  
2001 ◽  
Vol 128 (18) ◽  
pp. 3623-3634 ◽  
Author(s):  
Simon J. Kinder ◽  
Tania E. Tsang ◽  
Maki Wakamiya ◽  
Hiroshi Sasaki ◽  
Richard R. Behringer ◽  
...  

An organizer population has been identified in the anterior end of the primitive streak of the mid-streak stage embryo, by the expression of Hnf3β, GsclacZ and Chrd, and the ability of these cells to induce a second neural axis in the host embryo. This cell population can therefore be regarded as the mid-gastrula organizer and, together with the early-gastrula organizer and the node, constitute the organizer of the mouse embryo at successive stages of development. The profile of genetic activity and the tissue contribution by cells in the organizer change during gastrulation, suggesting that the organizer may be populated by a succession of cell populations with different fates. Fine mapping of the epiblast in the posterior region of the early-streak stage embryo reveals that although the early-gastrula organizer contains cells that give rise to the axial mesoderm, the bulk of the progenitors of the head process and the notochord are localized outside the early gastrula organizer. In the mid-gastrula organizer, early gastrula organizer derived cells that are fated for the prechordal mesoderm are joined by the progenitors of the head process that are recruited from the epiblast previously anterior to the early gastrula organizer. Cells that are fated for the head process move anteriorly from the mid-gastrula organizer in a tight column along the midline of the embryo. Other mid-gastrula organizer cells join the expanding mesodermal layer and colonize the cranial and heart mesoderm. Progenitors of the trunk notochord that are localized in the anterior primitive streak of the mid-streak stage embryo are later incorporated into the node. The gastrula organizer is therefore composed of a constantly changing population of cells that are allocated to different parts of the axial mesoderm.

Development ◽  
1994 ◽  
Vol 120 (3) ◽  
pp. 613-620 ◽  
Author(s):  
R.S. Beddington

The anterior aspect of the mouse primitive streak resembles the organizer of Xenopus and chick in terms of its developmental fate, ability to alter pattern in the chick limb bud and with respect to the repertoire of genes that its constituent cells express. However, until now there has been no direct evidence that the mouse node organizes pattern during gastrulation, nor that the exceptionally small mouse embryonic egg cylinder can be induced to form a second axis. Grafts of transgenically marked midgastrulation mouse node, or node labelled with DiI, to a posterolateral location in a host embryo of the same developmental stage results in the induction of a second neural axis and the formation of ectopic somites. The graft gives rise predominantly to notochord and endoderm tissue whereas the neurectoderm and somites are mainly of host origin. The ectopic notochord formed is derived solely from the donor node which suggests that the node can serve as a ‘stem cell’ source of axial mesoderm. This is corroborated by the observation that labelling in situ the population of cells on the outer surface of the mid-gastrulation node with DiI results in continuous labelling of the notochord. DiI-labelled cells are present throughout the notochord from a rostral boundary in the cranial region to its most caudal extreme and the node itself always remains labelled.


Development ◽  
1999 ◽  
Vol 126 (22) ◽  
pp. 5171-5179 ◽  
Author(s):  
P.P. Tam ◽  
K.A. Steiner

Fragments of the germ layer tissues isolated from the early-primitive-streak (early-streak) stage mouse embryos were tested for axis induction activity by transplantation to late-gastrula (late-streak to early-bud) stage host embryos. The posterior epiblast fragment that contains the early gastrula organizer was able to recruit the host tissues to form an ectopic axis. However, the most anterior neural gene that was expressed in the ectopic axis was Krox20 that marks parts of the hindbrain, but markers of the mid- and forebrain (Otx2 and En1) were not expressed. Anterior visceral endoderm or the anterior epiblast alone did not induce any ectopic neural tissue. However, when these two anterior germ layer tissues were transplanted together, they can induce the formation of ectopic host-derived neural tissues but these tissues rarely expressed anterior neural genes and did not show any organization of an ectopic axis. Therefore, although the anterior endoderm and epiblast together may display some inductive activity, they do not act like a classical organizer. Induction of the anterior neural genes in the ectopic axis was achieved only when a combination of the posterior epiblast fragment, anterior visceral endoderm and the anterior epiblast was transplanted to the host embryo. The formation of anterior neural structures therefore requires the synergistic interaction of the early gastrula organizer and anterior germ layer tissues.


Development ◽  
1989 ◽  
Vol 105 (1) ◽  
pp. 175-182 ◽  
Author(s):  
L. Niswander ◽  
D. Yee ◽  
E.M. Rinchik ◽  
L.B. Russell ◽  
T. Magnuson

A detailed embryological analysis has been undertaken on embryos carrying the c4FR60Hd-, c5FR60Hg- or c2YPSj-albino deletions of mouse chromosome 7. Embryos homozygous for the c4FR60Hd deletion are abnormal at day 7.5 of gestation. The extraembryonic ectoderm does not develop, and primitive-streak formation and mesoderm production do not occur. In contrast, extensive development of the extraembryonic ectoderm, as well as mesoderm production, are observed in the c5FR60Hg- and c2YPSj-homozygous embryos. The mesoderm does not, however, organize into somites and the neural axis does not form. The embryos are grossly abnormal by day 8.5 of development. There are two other albino deletions (c6H and c11DSD) that are known to affect the embryo around the time of gastrulation (Niswander et al. 1988), and the lethal phenotype observed for the c4FR60Hd-homozygous embryos is similar to that described for c6H-homozygous embryos, whereas the c5FR60Hg- and c2YPSj-homozygous embryos display a phenotype that is similar to c11DSD-homozygous embryos. A detailed complementation analysis using these five deletions revealed that the c5FR60Hg, c2YPSj and c11DSD deletions could partially complement the phenotype produced by the c4FR60Hd and c6H deletions in any combination. Extensive development of the extraembryonic structures and production of mesoderm occurs in the compound heterozygotes. These results suggest that the distal breakpoints of the c5FR60Hg, c2YPSj and c11DSD deletions lie more proximal than the distal breakpoints of the c4FR60Hd and c6H deletions.(ABSTRACT TRUNCATED AT 250 WORDS)


In chick blastoderms at primitive streak stage, lengths of the primitive streak were cut out and replaced with their antero-posterior orientation reversed. In some experiments the region immediately in front of the primitive streak (presumptive prechordal head) was also included in the excisedpiece. Control operations involving excision and replacement without reversal were also performed. The embryos were subsequently grown in vitro by Waddington’s technique. After reversal of a variety of different parts of the streak at various developmental stages, many cases of regulative development were obtained. In these, the original orientation of the blastoderm was maintained, and while there were abnormalities of various kinds in the embryos, they were no different from the abnormalities found in the controls. Very occasionally the regulated axis was partially doubled after a reversal, though not after a control operation. A few specimens which had undergone reversal of long pieces of the primitive streak and had completely healed showed a failure of regulation in that there was some tendency for the reversed-piece to develop according to its own orientation. But at best this reversed differentiation was very distorted and incomplete. Evidently the orientation of the primitive streak does not at any stage control the orientation of the embryo; and the primitive streak, when it is fully developed and contains most of the presumptive axial material, is highly labile in its powers of differentiation. In spite of its well-known ‘organizer' activity, the primitive streak is subject to control by the surrounding blastoderm.


2019 ◽  
Author(s):  
Juan A. Sanchez ◽  
Duarte Mesquita ◽  
María C. Ingaramo ◽  
Federico Ariel ◽  
Marco Milán ◽  
...  

ABSTRACTCoordinated intra- and inter-organ growth is essential during animal development to generate individuals of proper size and shape. TheDrosophilawing has been a valuable model system to reveal the existence of a stress response mechanism mediated by Drosophila p53 (Dmp53) and involved in the coordination of tissue growth between adjacent cell populations upon targeted reduction of growth rates. Here we present evidence that a two-step molecular mechanism is being used by Dmp53 to reduce in a non-autonomous manner growth and proliferation in adjacent cell populations. First, Dmp53-mediated transcriptional induction ofDrosophilaTNFα ligand Eiger leads to cell autonomous activation of JNK. Second, two different signaling events downstream of the Eiger/JNK axis are induced in the growth depleted territory in order to independently regulate tissue size and cell number in adjacent cell populations. Whereas expression of the systemic hormone dILP8 coordinates intra-organ growth and final tissue size, induction of Reactive Oxygen Species downstream of Eiger/JNK and, as a consequence of apoptosis induction, acts non-cell-autonomously to regulate proliferation rates of adjacent epithelial cells. Our results unravel how local and systemic signals can act concertedly to coordinate growth and proliferation within an organ in order to generate well-proportioned organs and functionally integrated adults.Author SummaryCoordination of growth between the different parts of a given developing organ is an absolute requirement for the generation of functionally integrated structures during animal development. Although this question has fascinated biologists for centuries, the responsible molecular mechanisms have remained so far unknown. In this work, we have used the developing wing primordium of Drosophila to identify the molecular mechanisms and signaling molecules mediating communication between adjacent cell populations upon targeted reduction in growth rates. We first present evidence that activation of Drosophila p53 in the growth-depleted territory induces expression of the fly TNF ligand Eiger which cell autonomously activates the JNK stress signaling pathway. While JNK-dependent expression of the systemic hormone dILP8 reduces growth and final size of the adjacent territories, production of Reactive Oxygen Species downstream of JNK and the apoptotic machinery act locally to regulate proliferation rates in adjacent epithelial cells. Our data reveal how signals acting locally or systemically can regulate cell proliferation and growth independently to accomplish coordination in tissue size and cell number among different parts of an organ in order to give rise to well-proportioned adult structures.HIGHLIGHTS✓ Dmp53-dependent Eiger expression is required to coordinate intra-organ growth✓ Eiger acts through its receptor Grindelwald and JNK signaling to reduce growth and proliferation rates in a non-cell-autonomous manner✓ Eiger/JNK-dependent Dilp8 expression coordinates intra-organ growth but not proliferation✓ Eiger/JNK activation triggers ROS production✓ ROS act non-cell-autonomously to regulate proliferation of adjacent epithelial cells.


Development ◽  
1991 ◽  
Vol 112 (4) ◽  
pp. 959-970 ◽  
Author(s):  
C. Roberts ◽  
N. Platt ◽  
A. Streit ◽  
M. Schachner ◽  
C.D. Stern

The pattern of expression of the carbohydrate epitope L5 was studied during early development of the chick neuroepithelium. Immunoreactivity first appears during gastrulation, at mid-primitive streak stage, and persists until at least 3.5 days of development. The epitope is expressed on all the components of the developing nervous system, both central and peripheral. In immunoblots, the antibody recognises a major component of about Mr 500,000 and several more minor components of lower molecular mass. If a Hensen's node from a donor embryo is transplanted into the area opaca of a host embryo, L5 immunoreactivity appears in the epiblast surrounding the graft. If hybridoma cells secreting the antibody are grafted together with Hensen's node into a host chick embryo, the induction of a supernumerary nervous system is inhibited. We suggest that the L5 epitope is an early and general marker for neural induction and that it may be involved directly in inductive interactions.


Development ◽  
1980 ◽  
Vol 58 (1) ◽  
pp. 209-216
Author(s):  
Nikolas Zagris

Morphologically distinct erythroid cell types characteristic of the primitive and the definitiveerythroid cell lines, and embryonic and adult haemoglobins are produced when the unin-cubated chick blastoderm is cultured ventral side down on a filter raft to inhibit morphogeneticmovements and subsequent primitive-streak formation mechanically in serum-free minimalessential medium. The primitive and definitive erythroid cell populations appear consecutivelyin culture even though there is no axis formation nor apparent morphogenesis. The informa-tion to produce both the early and late haemoglobins and erythroid cell types is independentof axis formation and of specific extra-embryonic influences, such as progressive inductionexerted by the yolk mass.


Development ◽  
1994 ◽  
Vol 120 (10) ◽  
pp. 2879-2889 ◽  
Author(s):  
Y. Hatada ◽  
C.D. Stern

We have used carbocyanine dyes (DiI and DiO) to generate fate maps for the epiblast layer of the chick embryo between stage X and the early primitive streak stage (stages 2–3). The overall distribution of presumptive cell types in these maps is similar to that described for other laboratory species (zebrafish, frog, mouse). Our maps also reveal certain patterns of movement for these presumptive areas. Most areas converge towards the midline and then move anteriorly along it. Interestingly, however, some presumptive tissue types do not take part in these predominant movements, but behave in a different way, even if enclosed within an area that does undergo medial convergence and anterior movement. The apparently independent behaviour of certain cell populations suggests that at least some presumptive cell types within the epiblast are already specified at preprimitive streak stages.


Development ◽  
2000 ◽  
Vol 127 (15) ◽  
pp. 3283-3293 ◽  
Author(s):  
L. Gunhaga ◽  
T.M. Jessell ◽  
T. Edlund

A secreted signaling factor, Sonic hedgehog (Shh), has a crucial role in the generation of ventral cell types along the entire rostrocaudal axis of the neural tube. At caudal levels of the neuraxis, Shh is secreted by the notochord and floor plate during the period that ventral cell fates are specified. At anterior prosencephalic levels that give rise to the telencephalon, however, neither the prechordal mesoderm nor the ventral neural tube expresses Shh at the time that the overt ventral character of the telencephalon becomes evident. Thus, the precise role and timing of Shh signaling relevant to the specification of ventral telencephalic identity remains unclear. By analysing neural cell differentiation in chick neural plate explants we provide evidence that neural cells acquire molecular properties characteristic of the ventral telencephalon in response to Shh signals derived from the anterior primitive streak/Hensen's node region at gastrula stages. Exposure of prospective anterior prosencephalic cells to Shh at this early stage is sufficient to initiate a temporal program of differentiation that parallels that of neurons generated normally in the medial ganglionic eminence subdivision of the ventral telencephalon.


Development ◽  
1992 ◽  
Vol 114 (4) ◽  
pp. 841-852 ◽  
Author(s):  
O. Sundin ◽  
G. Eichele

Chick Ghox 2.9 protein, a homeodomain-containing polypeptide, is first detected in the mid-gastrula stage embryo and its levels increase rapidly in the late gastrula. At this time, the initially narrow band of expression along the primitive streak expands laterally to form a shield-like domain that encompasses almost the entire posterior region of the embryo and extends anteriorly as far as Hensen's node. We have found that this expression domain co-localizes with a morphological feature that consists of a stratum of refractile, thickened mesoderm. Antibody-staining indicates that Ghox 2.9 protein is present in all cells of this mesodermal region. In contrast, expression within the ectoderm overlying the region of refractile mesoderm varies considerably. The highest levels of expression are found in ectoderm near the streak and surrounding Hensen's node, regions that recent fate mapping studies suggest that primarily destined to give rise to neurectoderm. At the definitive streak stage (Hamburger and Hamilton stage 4) the chick embryo is especially sensitive to the induction of axial malformations by retinoic acid. Four hours after the treatment of definitive streak embryos with a pulse of retinoic acid the expression of Ghox 2.9 protein is greatly elevated. This ectopic expression occurs in tissues anterior to Hensen's node, including floor plate, notochord, presumptive neural plate and lateral plate mesoderm, but does not occur in the anteriormost region of the embryo. The ectopic induction of Ghox 2.9 is strongest in ectoderm, and weaker in the underlying mesoderm. Endoderm throughout the embryo is unresponsive. At stage 11, Ghox 2.9 is normally expressed at high levels within rhombomere 4 of the developing hindbrain. In retinoic-acid-treated embryos which have developed to this stage, typical rhombomere boundaries are largely absent. Nevertheless, Ghox 2.9 is still expressed as a discrete band, but one that is widened and displaced to a more anterior position.


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