The somitogenetic potential of cells in the primitive streak and the tail bud of the organogenesis-stage mouse embryo

Development ◽  
1992 ◽  
Vol 115 (3) ◽  
pp. 703-715 ◽  
Author(s):  
P.P. Tam ◽  
S.S. Tan
Keyword(s):  
Primitive Streak ◽  
Mouse Embryos ◽  
Paraxial Mesoderm ◽  
Tail Bud ◽  
Matrix Interaction ◽  
Cell Matrix ◽  
Age Related ◽  
Somite Formation ◽  
Lateral Mesoderm ◽  
Host Embryo

The developmental potency of cells isolated from the primitive streak and the tail bud of 8.5- to 13.5-day-old mouse embryos was examined by analyzing the pattern of tissue colonization after transplanting these cells to the primitive streak of 8.5-day embryos. Cells derived from these progenitor tissues contributed predominantly to tissues of the paraxial and lateral mesoderm. Cells isolated from older embryos could alter their segmental fate and participated in the formation of anterior somites after transplantation to the primitive streak of 8.5-day host embryo. There was, however, a developmental lag in the recruitment of the transplanted cells to the paraxial mesoderm and this lag increased with the extent of mismatch of developmental ages between donor and host embryos. It is postulated that certain forms of cell-cell or cell-matrix interaction are involved in the specification of segmental units and that there may be age-related variations in the interactive capability of the somitic progenitor cells during development. Tail bud mesenchyme isolated from 13.5-day embryos, in which somite formation will shortly cease, was still capable of somite formation after transplantation to 8.5-day embryos. The cessation of somite formation is therefore likely to result from a change in the tissue environment in the tail bud rather than a loss of cellular somitogenetic potency.

The control of somitogenesis in mouse embryos

Development ◽  
1981 ◽  
Vol 65 (Supplement) ◽  
pp. 103-128
Author(s):  
P. P. L. Tam
Keyword(s):  
Body Size ◽  
Primitive Streak ◽  
Mouse Embryos ◽  
The Body ◽  
Whole Body ◽  
Axis Formation ◽  
Presomitic Mesoderm ◽  
Tail Bud ◽  
Somite Formation ◽  
Somitic Mesoderm

Somitogenesis in the mouse embryo commences with the generation of presumptive somitic mesoderm at the primitive streak and in the tail-bud mesenchyme. The presumptive somitic mesoderm is then organized into somite primordia in the presomitic mesoderm. These primordia undergo morphogenesis leading to the segmentation of somites at the cranial end of the presomitic mesoderm. Somite sizes at the time of segmentation vary according to the position of the somite in the body axis: the size of lumbar and sacral somites is nearly twice that of upper trunk somites and of tail somites. The size of the presomitic mesoderm, which is governed by the balance between the addition of cells at the caudal end and the removal of somites at the cranial end, changes during embryonic development. Somitogenesis is disturbed during the compensatory growth of mouse embryos which have suffered a drastic size reduction at the primitive-streak and early-organogenesis stages. The formation of somites is retarded and the upper trunk somites are formed at a smaller size. The embryo also follows an entirely different growth profile, but a normal body size is restored by the early foetal stage. The somite number is regulated to normal and this is brought about by an altered rate of somite formation and the adjustment of somite size in proportion to the whole body size. It is proposed that axis formation and somitogenesis are related morphogenetic processes and that embryonic growth controls the kinetics of somitogenesis, namely by regulating the number of cells allocated to each somite and the rate of somite formation.

The histogenetic capacity of tissues in the caudal end of the embryonic axis of the mouse

Development ◽  
1984 ◽  
Vol 82 (1) ◽  
pp. 253-266
Author(s):  
P. P. L. Tam
Keyword(s):  
Developmental Stages ◽  
Primitive Streak ◽  
Mouse Embryos ◽  
Embryonic Axis ◽  
Tail Bud ◽  
Germ Layers ◽  
Kidney Capsule ◽  
Caudal Region ◽  
Caudal Portion ◽  
Adult Body

The caudal end of the embryonic axis consists of the primitive streak and the tail bud. Small fragments of this caudal tissue were transplanted from mouse embryos of various developmental stages to the kidney capsule in order to test their histogenetic capacity. The variety of mature tissues obtained from these small fragments was similar to that obtained by grafting a larger caudal portion of the embryo. Initially, the grafted tissue broke up into loose masses of embryonic mesenchyme and this was later re-organized into more compact tissues and into cysts that were lined with various types of epithelia. After 14 days in the ectopic site, grafted tissues coming from embryos of the primitive-streak, the early-somite and the forelimb-bud stages differentiated into structures that has presumably originated from the three embryonic germ layers. Many of these structures were related to the caudal region of the adult body, such as the mid- and hindgut segments and urogenital derivatives. The histogenetic capacity for endodermal tissues and urogenital organs was lost when the grafted tissue consisted entirely of the tail bud of the hindlimb-bud-stage embryos. The behaviour of the caudal tissues suggested that (1) the primordia for the various parts of embryonic body were derived from a small progenitor population in the primitive streak and the tail bud, and (2) the histogenetic capacity of this population changed during development.

The formation of mesodermal tissues in the mouse embryo during gastrulation and early organogenesis

Development ◽  
1987 ◽  
Vol 99 (1) ◽  
pp. 109-126 ◽  
Author(s):  
P.P. Tam ◽  
R.S. Beddington
Keyword(s):  
Anterior Part ◽  
Primitive Streak ◽  
Paraxial Mesoderm ◽  
Substantial Contribution ◽  
Fate Map ◽  
Extraembryonic Mesoderm ◽  
Lateral Mesoderm ◽  
Embryonic Ectoderm ◽  
Specific Labelling

Orthotopic grafts of [3H]thymidine-labelled cells have been used to demonstrate differences in the normal fate of tissue located adjacent to and in different regions of the primitive streak of 8th day mouse embryos developing in vitro. The posterior streak produces predominantly extraembryonic mesoderm, while the middle portion gives rise to lateral mesoderm and the anterior region generates mostly paraxial mesoderm, gut and notochord. Embryonic ectoderm adjacent to the anterior part of the streak contributes mainly to paraxial mesoderm and neurectoderm. This pattern of colonization is similar to the fate map constructed in primitive-streak-stage chick embryos. Similar grafts between early-somite-stage (9th day) embryos have established that the older primitive streak continues to generate embryonic mesoderm and endoderm, but ceases to make a substantial contribution to extraembryonic mesoderm. Orthotopic grafts and specific labelling of ectodermal cells with wheat germ agglutinin conjugated to colloidal gold (WGA-Au) have been used to analyse the recruitment of cells into the paraxial mesoderm of 8th and 9th day embryos. The continuous addition of primitive-streak-derived cells to the paraxial mesoderm is confirmed and the distribution of labelled cells along the craniocaudal sequence of somites is consistent with some cell mixing occurring within the presomitic mesoderm.

Defining subregions of Hensen's node essential for caudalward movement, midline development and cell survival

Development ◽  
1999 ◽  
Vol 126 (21) ◽  
pp. 4771-4783 ◽  
Author(s):  
J.B. Charrier ◽  
M.A. Teillet ◽  
F. Lapointe ◽  
N.M. Le Douarin
Keyword(s):  
Primitive Streak ◽  
Floor Plate ◽  
Paraxial Mesoderm ◽  
Avian Embryo ◽  
Tail Bud ◽  
Anterior Portion ◽  
T Box ◽  
Endodermal Cells ◽  
Further Development ◽  
Midline Development

Hensen's node, also called the chordoneural hinge in the tail bud, is a group of cells that constitutes the organizer of the avian embryo and that expresses the gene HNF-3(β). During gastrulation and neurulation, it undergoes a rostral-to-caudal movement as the embryo elongates. Labeling of Hensen's node by the quail-chick chimera system has shown that, while moving caudally, Hensen's node leaves in its wake not only the notochord but also the floor plate and a longitudinal strand of dorsal endodermal cells. In this work, we demonstrate that the node can be divided into functionally distinct subregions. Caudalward migration of the node depends on the presence of the most posterior region, which is closely apposed to the anterior portion of the primitive streak as defined by expression of the T-box gene Ch-Tbx6L. We call this region the axial-paraxial hinge because it corresponds to the junction of the presumptive midline axial structures (notochord and floor plate) and the paraxial mesoderm. We propose that the axial-paraxial hinge is the equivalent of the neuroenteric canal of other vertebrates such as Xenopus. Blocking the caudal movement of Hensen's node at the 5- to 6-somite stage by removing the axial-paraxial hinge deprives the embryo of midline structures caudal to the brachial level, but does not prevent formation of the neural tube and mesoderm located posteriorly. However, the whole embryonic region generated posterior to the level of Hensen's node arrest undergoes widespread apoptosis within the next 24 hours. Hensen's node-derived structures (notochord and floor plate) thus appear to produce maintenance factor(s) that ensures the survival and further development of adjacent tissues.

scholarly journals Dynamics of primitive streak regression controls the fate of neuro-mesodermal progenitors in the chicken embryo

2020 ◽  
Author(s):  
Charlene Guillot ◽  
Arthur Michaut ◽  
Brian Rabe ◽  
Olivier Pourquié
Keyword(s):  
Chicken Embryo ◽  
Single Cells ◽  
Primitive Streak ◽  
Clonal Analysis ◽  
Lineage Tracing ◽  
The Body ◽  
Paraxial Mesoderm ◽  
Axis Formation ◽  
Vertebrate Development ◽  
Tail Bud

AbstractIn classical descriptions of vertebrate development, the segregation of the three embryonic germ layers is completed by the end of gastrulation. Body formation then proceeds in a head to tail fashion by progressive deposition of lineage committed progenitors during regression of the Primitive Streak (PS) and tail bud (Pasteels, 1937b; Stern, 2004). Identification of Neuro-Mesodermal Progenitors (NMPs) contributing to both musculo-skeletal precursors (paraxial mesoderm) and spinal cord during axis formation by retrospective clonal analysis challenged these notions (Henrique et al., 2015; Tzouanacou et al., 2009). However, in amniotes such as mouse and chicken, the precise identity and localization of these cells has remained unclear despite a wealth of fate mapping analyses of the PS region. Here, we use lineage tracing in the chicken embryo to show that single cells located in the SOX2/T positive anterior PS region contribute to both neural and mesodermal lineages in the trunk and tail, but only express this bipotential fate with some delay. We demonstrate that posterior to anterior gradients of convergence speed and ingression along the PS gradually lead to exhaustion of all mesodermal precursor territories except for NMPs where limited ingression and increased proliferation maintain and amplify this pool of axial progenitors. As a result, most of the remaining mesodermal precursors from the PS in the tail bud are bipotential NMPs. Together, our results provide a novel understanding of the contribution of the PS and tail bud to the formation of the body of amniote embryos.

scholarly journals Dynamics of primitive streak regression controls the fate of neuromesodermal progenitors in the chicken embryo

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Charlene Guillot ◽  
Yannis Djeffal ◽  
Arthur Michaut ◽  
Brian Rabe ◽  
Olivier Pourquié
Keyword(s):  
Single Cell ◽  
Cell Population ◽  
Chicken Embryo ◽  
Primitive Streak ◽  
Lineage Tracing ◽  
The Body ◽  
Paraxial Mesoderm ◽  
Axis Formation ◽  
Tail Bud ◽  
Transcriptomic Signature

In classical descriptions of vertebrate development, the segregation of the three embryonic germ layers completes by the end of gastrulation. Body formation then proceeds in a head to tail fashion by progressive deposition of lineage-committed progenitors during regression of the primitive streak (PS) and tail bud (TB). The identification by retrospective clonal analysis of a population of neuromesodermal progenitors (NMPs) contributing to both musculoskeletal precursors (paraxial mesoderm) and spinal cord during axis formation challenged these notions. However, classical fate mapping studies of the PS region in amniotes have so far failed to provide direct evidence for such bipotential cells at the single-cell level. Here, using lineage tracing and single-cell RNA sequencing in the chicken embryo, we identify a resident cell population of the anterior PS epiblast, which contributes to neural and mesodermal lineages in trunk and tail. These cells initially behave as monopotent progenitors as classically described and only acquire a bipotential fate later, in more posterior regions. We show that NMPs exhibit a conserved transcriptomic signature during axis elongation but lose their epithelial characteristicsin the TB. Posterior to anterior gradients of convergence speed and ingression along the PS lead to asymmetric exhaustion of PS mesodermal precursor territories. Through limited ingression and increased proliferation, NMPs are maintained and amplified as a cell population which constitute the main progenitors in the TB. Together, our studies provide a novel understanding of the PS and TB contribution through the NMPs to the formation of the body of amniote embryos.

Pattern of the insulin-like growth factor II gene expression during early mouse embryogenesis

Development ◽  
1990 ◽  
Vol 110 (1) ◽  
pp. 151-159 ◽  
Author(s):  
J.E. Lee ◽  
J. Pintar ◽  
A. Efstratiadis
Keyword(s):  
Growth Factor ◽  
Immunohistochemical Analysis ◽  
Primitive Streak ◽  
Insulin Like Growth Factor ◽  
Surface Ectoderm ◽  
Factor Ii ◽  
Extraembryonic Mesoderm ◽  
Early Mouse ◽  
Lateral Mesoderm

The mouse insulin-like growth factor II (IGF-II) gene encodes a polypeptide that plays a role in embryonic growth. We have examined the temporal and spatial pattern of expression of this gene in sections of the mouse conceptus between embryonic days 4.0 and 8.5 by in situ hybridization. Abundant IGF-II transcripts were detected in all the trophectodermal derivatives, after implantation. Labeling was then observed in primitive endoderm, but was transient and disappeared after formation of the yolk sac. Expression was next detected in extraembryonic mesoderm at the early primitive streak stage. Labeling in the embryo proper appeared first at the late primitive streak/neural plate stage in lateral mesoderm and in anterior-proximal cells located between the visceral endoderm and the most cranial region of the embryonic ectoderm. The position of the latter cells suggests that their descendants are likely to participate in the formation of the heart and the epithelium of the ventral and lateral walls of the foregut, where intense labeling was observed at the neural fold stage. Hybridization was also detected in cranial mesenchyme, including neural crest cells. The intensity of hybridization signal increased progressively in paraxial (presomitic and somitic) mesoderm, while declining in the ectoplacental cone. The neuroectoderm and surface ectoderm did not exhibit hybridization at any stage. Immunohistochemical analysis indicated co-localization of IGF-II transcripts, translated pre-pro-IGF-II, and the cognate IGF-II/mannose-6-phosphate receptor. These correlations are consistent with the hypothesis that IGF-II has an autocrine function.

A developmental pathway controlling outgrowth of the Xenopus tail bud

Development ◽  
1999 ◽  
Vol 126 (8) ◽  
pp. 1611-1620 ◽  
Author(s):  
C.W. Beck ◽  
J.M. Slack
Keyword(s):  
Normal Development ◽  
Posterior Part ◽  
Neural Plate ◽  
General Mechanism ◽  
Developmental Pathway ◽  
Tail Bud ◽  
Neural Tubes ◽  
Tailbud Stage ◽  
Tail Tip ◽  
Host Embryo

We have developed a new assay to identify factors promoting formation and outgrowth of the tail bud. A piece of animal cap filled with the test mRNAs is grafted into the posterior region of the neural plate of a host embryo. With this assay we show that expression of a constitutively active Notch (Notch ICD) in the posterior neural plate is sufficient to produce an ectopic tail consisting of neural tube and fin. The ectopic tails express the evenskipped homologue Xhox3, a marker for the distal tail tip. Xhox3 will also induce formation of an ectopic tail in our assay. We show that an antimorphic version of Xhox3, Xhox3VP16, will prevent tail formation by Notch ICD, showing that Xhox3 is downstream of Notch signalling. An inducible version of this reagent, Xhox3VP16GR, specifically blocks tail formation when induced in tailbud stage embryos, comfirming the importance of Xhox3 for tail bud outgrowth in normal development. Grafts containing Notch ICD will only form tails if placed in the posterior part of the neural plate. However, if Xwnt3a is also present in the grafts they can form tails at any anteroposterior level. Since Xwnt3a expression is localised appropriately in the posterior at the time of tail bud formation it is likely to be responsible for restricting tail forming competence to the posterior neural plate in our assay. Combined expression of Xwnt3a and active Notch in animal cap explants is sufficient to induce Xhox3, provoke elongation and form neural tubes. Conservation of gene expression in the tail bud of other vertebrates suggests that this pathway may describe a general mechanism controlling tail outgrowth and secondary neurulation.

her1, a zebrafish pair-rule like gene, acts downstream of notch signalling to control somite development

Development ◽  
1999 ◽  
Vol 126 (13) ◽  
pp. 3005-3014 ◽  
Author(s):  
C. Takke ◽  
J.A. Campos-Ortega
Keyword(s):  
Active Form ◽  
Notch Signalling ◽  
Paraxial Mesoderm ◽  
Presomitic Mesoderm ◽  
Essentially Normal ◽  
Early Embryos ◽  
Somite Formation ◽  
Genes Encoding ◽  
Ectopic Activation ◽  
Pair Rule

During vertebrate embryonic development, the paraxial mesoderm becomes subdivided into metameric units known as somites. In the zebrafish embryo, genes encoding homologues of the proteins of the Drosophila Notch signalling pathway are expressed in the presomitic mesoderm and expression is maintained in a segmental pattern during somitogenesis. This expression pattern suggests a role for these genes during somite development. We misexpressed various zebrafish genes of this group by injecting mRNA into early embryos. RNA encoding a constitutively active form of notch1a (notch1a-intra) and a truncated variant of deltaD [deltaD(Pst)], as well as transcripts of deltaC and deltaD, the hairy-E(spl) homologues her1 and her4, and groucho2 were tested for their effects on somite formation, myogenesis and on the pattern of transcription of putative downstream genes. In embryos injected with any of these RNAs, with the exception of groucho2 RNA, the paraxial mesoderm differentiated normally into somitic tissue, but failed to segment correctly. Activation of notch results in ectopic activation of her1 and her4. This misregulation of the expression of her genes might be causally related to the observed mesodermal defects, as her1 and her4 mRNA injections led to effects similar to those seen with notch1a-intra. deltaC and deltaD seem to function after subdivision of the presomitic mesoderm, since the her gene transcription pattern in the presomitic mesoderm remains essentially normal after misexpression of delta genes. Whereas notch signalling alone apparently does not affect myogenesis, zebrafish groucho2 is involved in differentiation of mesodermal derivatives.

Onset of the segmentation clock in the chick embryo: evidence for oscillations in the somite precursors in the primitive streak

Development ◽  
2002 ◽  
Vol 129 (5) ◽  
pp. 1107-1117 ◽  
Author(s):  
Caroline Jouve ◽  
Tadahiro Iimura ◽  
Olivier Pourquie
Keyword(s):  
Continuous Process ◽  
Notch Pathway ◽  
Primitive Streak ◽  
The Body ◽  
Paraxial Mesoderm ◽  
Segmentation Clock ◽  
Head Mesoderm ◽  
Dynamic Expression ◽  
Mesoderm Formation ◽  
Cyclic Gene

Vertebrate somitogenesis is associated with a molecular oscillator, the segmentation clock, which is defined by the periodic expression of genes related to the Notch pathway such as hairy1 and hairy2 or lunatic fringe (referred to as the cyclic genes) in the presomitic mesoderm (PSM). Whereas earlier studies describing the periodic expression of these genes have essentially focussed on later stages of somitogenesis, we have analysed the onset of the dynamic expression of these genes during chick gastrulation until formation of the first somite. We observed that the onset of the dynamic expression of the cyclic genes in chick correlated with ingression of the paraxial mesoderm territory from the epiblast into the primitive streak. Production of the paraxial mesoderm from the primitive streak is a continuous process starting with head mesoderm formation, while the streak is still extending rostrally, followed by somitic mesoderm production when the streak begins its regression. We show that head mesoderm formation is associated with only two pulses of cyclic gene expression. Because such pulses are associated with segment production at the body level, it suggests the existence of, at most, two segments in the head mesoderm. This is in marked contrast to classical models of head segmentation that propose the existence of more than five segments. Furthermore, oscillations of the cyclic genes are seen in the rostral primitive streak, which contains stem cells from which the entire paraxial mesoderm originates. This indicates that the number of oscillations experienced by somitic cells is correlated with their position along the AP axis.

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