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.

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.

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.

Dorsalizing and neuralizing properties of Xdsh, a maternally expressed Xenopus homolog of dishevelled

Development ◽  
1995 ◽  
Vol 121 (6) ◽  
pp. 1637-1647 ◽  
Author(s):  
S.Y. Sokol ◽  
J. Klingensmith ◽  
N. Perrimon ◽  
K. Itoh
Keyword(s):  
Signal Transduction ◽  
Signal Transduction Pathway ◽  
Neural Induction ◽  
Neural Tissue ◽  
Lineage Tracing ◽  
Axis Formation ◽  
Transduction Pathway ◽  
Vertebrate Development ◽  
Dorsal Axis ◽  
Wnt Signal

Signaling factors of the Wnt proto-oncogene family are implicated in dorsal axis formation during vertebrate development, but the molecular mechanism of this process is not known. Studies in Drosophila have indicated that the dishevelled gene product is required for wingless (Wnt1 homolog) signal transduction. We demonstrate that injection of mRNA encoding a Xenopus homolog of dishevelled (Xdsh) into prospective ventral mesodermal cells triggers a complete dorsal axis formation in Xenopus embryos. Lineage tracing experiments show that cells derived from the injected blastomere contribute to anterior and dorsal structures of the induced axis. In contrast to its effect on mesoderm, overexpression of Xdsh mRNA in prospective ectodermal cells triggers anterior neural tissue differentiation. These studies suggest that Wnt signal transduction pathway is conserved between Drosophila and vertebrates and point to a role for maternal Xdsh product in dorsal axis formation and in neural induction.

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.

Axial progenitors with extensive potency are localised to the mouse chordoneural hinge

Development ◽  
2002 ◽  
Vol 129 (20) ◽  
pp. 4855-4866 ◽  
Author(s):  
Noemí Cambray ◽  
Valerie Wilson
Keyword(s):  
Stem Cells ◽  
Cell Model ◽  
Primitive Streak ◽  
Serial Passage ◽  
Small Population ◽  
Lineage Tracing ◽  
Tail Bud ◽  
Apparent Loss ◽  
Stem Cell Model ◽  
Successive Generations

Elongation of the mouse anteroposterior axis depends on a small population of progenitors initially located in the primitive streak and later in the tail bud. Gene expression and lineage tracing have shown that there are many features common to these progenitor tissues throughout axial elongation. However, the identity and location of the progenitors is unclear. We show by lineage tracing that the descendants of 8.5 d.p.c. node and anterior primitive streak which remain in the tail bud are located in distinct territories: (1) ventral node descendants are located in the widened posterior end of the notochord; and (2) descendants of anterior streak are located in both the tail bud mesoderm, and in the posterior end of the neurectoderm. We show that cells from the posterior neurectoderm are fated to give rise to mesoderm even after posterior neuropore closure. The posterior end of the notochord, together with the ventral neurectoderm above it, is thus topologically equivalent to the chordoneural hinge region defined in Xenopus and chick. A stem cell model has been proposed for progenitors of two of the axial tissues, the myotome and spinal cord. Because it was possible that labelled cells in the tail bud represented stem cells, tail bud mesoderm and chordoneural hinge were grafted to 8.5 d.p.c. primitive streak to compare their developmental potency. This revealed that cells from the bulk of the tail bud mesoderm are disadvantaged in such heterochronic grafts from incorporating into the axis and even when they do so, they tend to contribute to short stretches of somites suggesting that tail bud mesoderm is restricted in potency. By contrast, cells from the chordoneural hinge of up to 12.5 d.p.c. embryos contribute efficiently to regions of the axis formed after grafting to 8.5 d.p.c. embryos, and also repopulate the tail bud. These cells were additionally capable of serial passage through three successive generations of embryos in culture without apparent loss of potency. This potential for self-renewal in chordoneural hinge cells strongly suggests that stem cells are located in this region.

scholarly journals Lineage tracing axial progenitors using Nkx1.2CreERT2 mice defines their trunk and tail contributions

2018 ◽  
Author(s):  
Aida Rodrigo Albors ◽  
Pamela A. Halley ◽  
Kate G. Storey
Keyword(s):  
Spinal Cord ◽  
Lineage Tracing ◽  
Paraxial Mesoderm ◽  
Mouse Line ◽  
Tail Bud ◽  
Dynamic Nature ◽  
Transgenic Mouse Line ◽  
Continuous Generation ◽  
Axis Elongation

AbstractThe vertebrate body forms by continuous generation of new tissue from progenitors at the posterior end of the embryo. In mice, these axial progenitors initially reside in the epiblast, from where they form the trunk; and later relocate to the chordo-neural hinge of the tail bud to form the tail. Among them, a small group of bipotent neuromesodermal progenitors (NMPs) are thought to generate the spinal cord and paraxial mesoderm to the end of axis elongation. The study of these progenitors, however, has proven challenging in vivo due to their small numbers and dynamic nature, and the lack of a unique molecular marker to identify them. Here, we report the generation of the Nkx1.2CreERT2 transgenic mouse line in which the endogenous Nkx1.2 promoter drives tamoxifen-inducible CreERT2 recombinase. We show that Nkx1.2CreERT2 targets axial progenitors, including NMPs and early neural and mesodermal progenitors. Using a YFP reporter, we demonstrate that Nkx1.2-expressing epiblast cells contribute to all three germ layers, mostly neuroectoderm and mesoderm excluding notochord; and continue contributing neural and paraxial mesoderm tissues from the tail bud. This study identifies the Nkx1.2-expressing cell population as the source of most trunk and tail tissues in the mouse; and provides a key tool to genetically label and manipulate this progenitor population in vivo.

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 Persistence, period and precision of autonomous cellular oscillators from the zebrafish segmentation clock

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Alexis B Webb ◽  
Iván M Lengyel ◽  
David J Jörg ◽  
Guillaume Valentin ◽  
Frank Jülicher ◽  
...  
Keyword(s):  
Single Cells ◽  
Expression Patterns ◽  
The Body ◽  
Transgenic Zebrafish ◽  
Correlated Noise ◽  
Vertebrate Development ◽  
Segmentation Clock ◽  
Rhythmic Gene

In vertebrate development, the sequential and rhythmic segmentation of the body axis is regulated by a “segmentation clock”. This clock is comprised of a population of coordinated oscillating cells that together produce rhythmic gene expression patterns in the embryo. Whether individual cells autonomously maintain oscillations, or whether oscillations depend on signals from neighboring cells is unknown. Using a transgenic zebrafish reporter line for the cyclic transcription factor Her1, we recorded single tailbud cells in vitro. We demonstrate that individual cells can behave as autonomous cellular oscillators. We described the observed variability in cell behavior using a theory of generic oscillators with correlated noise. Single cells have longer periods and lower precision than the tissue, highlighting the role of collective processes in the segmentation clock. Our work reveals a population of cells from the zebrafish segmentation clock that behave as self-sustained, autonomous oscillators with distinctive noisy dynamics.

Two novel chick T-box genes related to mouse Brachyury are expressed in different, non-overlapping mesodermal domains during gastrulation

Development ◽  
1997 ◽  
Vol 124 (2) ◽  
pp. 411-419 ◽  
Author(s):  
V. Knezevic ◽  
R. Santo De ◽  
S. Mackem
Keyword(s):  
Primitive Streak ◽  
The Other ◽  
Paraxial Mesoderm ◽  
Axis Formation ◽  
Potential Candidate ◽  
T Box ◽  
Evolutionarily Conserved ◽  
Prechordal Plate ◽  
Recent Demonstration ◽  
Null Mutants

The mouse Brachyury (T) gene plays critical roles in the genesis of normal mesoderm during gastrulation and in the maintenance of a functioning notochord. Abrogation of Brachyury (T) expression within the chordamesoderm of homozygous null mutants nevertheless spares anterior axis formation. An intriguing possibility to explain the preservation of anterior axis formation in these mutants would be the existence of other genes compensating for the loss of Brachyury. This compensation and the recent demonstration that Brachyury is the prototype for an evolutionarily conserved family, prompted a search for other T-box genes participating in axis formation. The chick Brachyury orthologue and two related chick T-box genes that are expressed at the onset of gastrulation have been isolated. One of these novel genes (Ch-TbxT) becomes restricted to the axial mesoderm lineage and is a potential candidate for complementing or extending Brachyury function in the anterior axis (formation of the head process, prechordal plate). The other gene (Ch-Tbx6L), together with chick T, appears to mark primitive streak progenitors before gastrulation. As cells leave the primitive streak, Ch-Tbx6L becomes restricted to the early paraxial mesoderm lineage and could play a role in regulating somitogenesis.

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