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The prethalamus is established during gastrulation and influences diencephalic regionalization.

Staudt N, Houart C - PLoS Biol. (2007)

Bottom Line: In this study, we draw an extended expression map of the rostral neural plate that reveals discrete domains inside the presumptive posterior forebrain.Finally, transplantation of these precursors, in the rostral-most neural epithelium, induces changes in cell identity in the surrounding host forebrain.This cell-non-autonomous property led us to propose that these committed prethalamic precursors may play an instructive role in the regionalization of the developing diencephalon.

View Article: PubMed Central - PubMed

Affiliation: Medical Research Council Centre for Developmental Neurobiology, King's College London, London, United Kingdom.

ABSTRACT
The vertebrate neural plate contains distinct domains of gene expression, prefiguring the future brain areas. In this study, we draw an extended expression map of the rostral neural plate that reveals discrete domains inside the presumptive posterior forebrain. We show, by fate mapping, that these well-defined cell populations will develop into specific diencephalic regions. To address whether these early subterritories are already committed to restricted identities, we began to analyse the consequences of ablation and transplantation of these specific cell populations. We found that precursors of the prethalamus are already specified and irreplaceable at late gastrula stage, because ablation of these cells results in loss of prethalamic markers. Moreover, when transplanted into the ectopic environment of the presumptive hindbrain, these cells still pursue their prethalamic differentiation program. Finally, transplantation of these precursors, in the rostral-most neural epithelium, induces changes in cell identity in the surrounding host forebrain. This cell-non-autonomous property led us to propose that these committed prethalamic precursors may play an instructive role in the regionalization of the developing diencephalon.

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Cell Movement in the Neural Plate(A and B) Schematic overview of the results obtained by the fate-mapping experiments. Colours at prim5 stage correspond to the territories labelled at bud stage.(C–E) Time-lapse analysis of nuclei (red) movement in the neural plate in her5pac:egfp (green): 3D rendering of a 200-μm z-series done at (C) bud stage and (D) 5-somite stage. (E) Schematic overview of the trajectories of individual nuclei over the recorded time (time-lapse movie can be seen in Video S1), with labelled nuclei in white. Wavy lines and dark to light colours of the lines represent the timeline of nuclei movement. Some lines are shorter because nuclei moved out of or into the observed area over the recorded time. We observed three types of movement: the basal cells move anteriorly (green arrow), posterior alar cells move towards the midline and then anteriorly (yellow arrow), and anterior alar cells move diagonally towards the midline (red arrow).(F–L) Transplantation of basal cells: (F) animal pole view in which labelled cells (green) are transplanted on top of the shield; (G) schematic lateral view of shield stage embryo in which transplanted cells are going to move towards the animal pole during gastrulation; (H) schematic lateral view of bud stage embryo in which transplanted cells are spread along the midline of the embryo; and (I) shhGFP is shown in green, transplanted cells in red, at 22 hpf in a live embryo. (J–L) shh is shown in red, transplanted cells in green; at 30 hpf, basally derived cells form a large proportion of the brain, showing that just the tip of the ZLI is formed by alar plate cells (white arrow), the basal ZLI is composed of basal cells (white double arrow), and the ventral part of the developing thalamus is built by basal cells (yellow arrow). The yellow line in (K) indicates the border between alar and basal plate; the arrowhead in (K) points to a single basal cell moving alar.
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pbio-0050069-g005: Cell Movement in the Neural Plate(A and B) Schematic overview of the results obtained by the fate-mapping experiments. Colours at prim5 stage correspond to the territories labelled at bud stage.(C–E) Time-lapse analysis of nuclei (red) movement in the neural plate in her5pac:egfp (green): 3D rendering of a 200-μm z-series done at (C) bud stage and (D) 5-somite stage. (E) Schematic overview of the trajectories of individual nuclei over the recorded time (time-lapse movie can be seen in Video S1), with labelled nuclei in white. Wavy lines and dark to light colours of the lines represent the timeline of nuclei movement. Some lines are shorter because nuclei moved out of or into the observed area over the recorded time. We observed three types of movement: the basal cells move anteriorly (green arrow), posterior alar cells move towards the midline and then anteriorly (yellow arrow), and anterior alar cells move diagonally towards the midline (red arrow).(F–L) Transplantation of basal cells: (F) animal pole view in which labelled cells (green) are transplanted on top of the shield; (G) schematic lateral view of shield stage embryo in which transplanted cells are going to move towards the animal pole during gastrulation; (H) schematic lateral view of bud stage embryo in which transplanted cells are spread along the midline of the embryo; and (I) shhGFP is shown in green, transplanted cells in red, at 22 hpf in a live embryo. (J–L) shh is shown in red, transplanted cells in green; at 30 hpf, basally derived cells form a large proportion of the brain, showing that just the tip of the ZLI is formed by alar plate cells (white arrow), the basal ZLI is composed of basal cells (white double arrow), and the ventral part of the developing thalamus is built by basal cells (yellow arrow). The yellow line in (K) indicates the border between alar and basal plate; the arrowhead in (K) points to a single basal cell moving alar.

Mentions: If one compares the relative distribution of the subdomains at bud stage and at prim5 (Figure 5A and 5B), one can predict that a simple rostral shift of the midline accompanying the closure of the plate into a keel may be sufficient to create most of the embryonic brain pattern observed at prim5. To investigate whether such a shift takes place and if so, at which stage of development this movement happens, we used confocal microscopy to create time-lapse movies allowing to monitor the movement of neural plate cells from bud stage to mid-somitogenesis. We recorded her5pac:egfp transgenic embryos in which a proportion of the nuclei were labelled with red fluorescent protein (RFP; see Materials and Methods). With this technique, we were able to follow cells of the diencephalic territory during the course of development (Video S1). After three-dimensional (3D) reconstruction (Figure 5C and 5D), the movement of specific nuclei could be tracked over the course of the recorded time (Figure 5E). We found that between bud and 5-somite stage (when the rostral neural plate is just completing closure), substantial movement can be observed in the ectoderm. Looking at the trajectories of the nuclei (Figure 5E), one sees that cells of the medial neural populations (basal plate) move anteriorly (green arrow), while lateral cells (alar plate) move either first towards the midline and then anterior (posterior alar forebrain, yellow arrow) or diagonally towards the anterior if they belong to the anterior alar forebrain (red arrow). These results therefore strongly suggest that the final location of the different diencephalic areas found in prim5 brains is taken during the beginning of somitogenesis, as the neural plate is “keeling.”


The prethalamus is established during gastrulation and influences diencephalic regionalization.

Staudt N, Houart C - PLoS Biol. (2007)

Cell Movement in the Neural Plate(A and B) Schematic overview of the results obtained by the fate-mapping experiments. Colours at prim5 stage correspond to the territories labelled at bud stage.(C–E) Time-lapse analysis of nuclei (red) movement in the neural plate in her5pac:egfp (green): 3D rendering of a 200-μm z-series done at (C) bud stage and (D) 5-somite stage. (E) Schematic overview of the trajectories of individual nuclei over the recorded time (time-lapse movie can be seen in Video S1), with labelled nuclei in white. Wavy lines and dark to light colours of the lines represent the timeline of nuclei movement. Some lines are shorter because nuclei moved out of or into the observed area over the recorded time. We observed three types of movement: the basal cells move anteriorly (green arrow), posterior alar cells move towards the midline and then anteriorly (yellow arrow), and anterior alar cells move diagonally towards the midline (red arrow).(F–L) Transplantation of basal cells: (F) animal pole view in which labelled cells (green) are transplanted on top of the shield; (G) schematic lateral view of shield stage embryo in which transplanted cells are going to move towards the animal pole during gastrulation; (H) schematic lateral view of bud stage embryo in which transplanted cells are spread along the midline of the embryo; and (I) shhGFP is shown in green, transplanted cells in red, at 22 hpf in a live embryo. (J–L) shh is shown in red, transplanted cells in green; at 30 hpf, basally derived cells form a large proportion of the brain, showing that just the tip of the ZLI is formed by alar plate cells (white arrow), the basal ZLI is composed of basal cells (white double arrow), and the ventral part of the developing thalamus is built by basal cells (yellow arrow). The yellow line in (K) indicates the border between alar and basal plate; the arrowhead in (K) points to a single basal cell moving alar.
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Related In: Results  -  Collection

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pbio-0050069-g005: Cell Movement in the Neural Plate(A and B) Schematic overview of the results obtained by the fate-mapping experiments. Colours at prim5 stage correspond to the territories labelled at bud stage.(C–E) Time-lapse analysis of nuclei (red) movement in the neural plate in her5pac:egfp (green): 3D rendering of a 200-μm z-series done at (C) bud stage and (D) 5-somite stage. (E) Schematic overview of the trajectories of individual nuclei over the recorded time (time-lapse movie can be seen in Video S1), with labelled nuclei in white. Wavy lines and dark to light colours of the lines represent the timeline of nuclei movement. Some lines are shorter because nuclei moved out of or into the observed area over the recorded time. We observed three types of movement: the basal cells move anteriorly (green arrow), posterior alar cells move towards the midline and then anteriorly (yellow arrow), and anterior alar cells move diagonally towards the midline (red arrow).(F–L) Transplantation of basal cells: (F) animal pole view in which labelled cells (green) are transplanted on top of the shield; (G) schematic lateral view of shield stage embryo in which transplanted cells are going to move towards the animal pole during gastrulation; (H) schematic lateral view of bud stage embryo in which transplanted cells are spread along the midline of the embryo; and (I) shhGFP is shown in green, transplanted cells in red, at 22 hpf in a live embryo. (J–L) shh is shown in red, transplanted cells in green; at 30 hpf, basally derived cells form a large proportion of the brain, showing that just the tip of the ZLI is formed by alar plate cells (white arrow), the basal ZLI is composed of basal cells (white double arrow), and the ventral part of the developing thalamus is built by basal cells (yellow arrow). The yellow line in (K) indicates the border between alar and basal plate; the arrowhead in (K) points to a single basal cell moving alar.
Mentions: If one compares the relative distribution of the subdomains at bud stage and at prim5 (Figure 5A and 5B), one can predict that a simple rostral shift of the midline accompanying the closure of the plate into a keel may be sufficient to create most of the embryonic brain pattern observed at prim5. To investigate whether such a shift takes place and if so, at which stage of development this movement happens, we used confocal microscopy to create time-lapse movies allowing to monitor the movement of neural plate cells from bud stage to mid-somitogenesis. We recorded her5pac:egfp transgenic embryos in which a proportion of the nuclei were labelled with red fluorescent protein (RFP; see Materials and Methods). With this technique, we were able to follow cells of the diencephalic territory during the course of development (Video S1). After three-dimensional (3D) reconstruction (Figure 5C and 5D), the movement of specific nuclei could be tracked over the course of the recorded time (Figure 5E). We found that between bud and 5-somite stage (when the rostral neural plate is just completing closure), substantial movement can be observed in the ectoderm. Looking at the trajectories of the nuclei (Figure 5E), one sees that cells of the medial neural populations (basal plate) move anteriorly (green arrow), while lateral cells (alar plate) move either first towards the midline and then anterior (posterior alar forebrain, yellow arrow) or diagonally towards the anterior if they belong to the anterior alar forebrain (red arrow). These results therefore strongly suggest that the final location of the different diencephalic areas found in prim5 brains is taken during the beginning of somitogenesis, as the neural plate is “keeling.”

Bottom Line: In this study, we draw an extended expression map of the rostral neural plate that reveals discrete domains inside the presumptive posterior forebrain.Finally, transplantation of these precursors, in the rostral-most neural epithelium, induces changes in cell identity in the surrounding host forebrain.This cell-non-autonomous property led us to propose that these committed prethalamic precursors may play an instructive role in the regionalization of the developing diencephalon.

View Article: PubMed Central - PubMed

Affiliation: Medical Research Council Centre for Developmental Neurobiology, King's College London, London, United Kingdom.

ABSTRACT
The vertebrate neural plate contains distinct domains of gene expression, prefiguring the future brain areas. In this study, we draw an extended expression map of the rostral neural plate that reveals discrete domains inside the presumptive posterior forebrain. We show, by fate mapping, that these well-defined cell populations will develop into specific diencephalic regions. To address whether these early subterritories are already committed to restricted identities, we began to analyse the consequences of ablation and transplantation of these specific cell populations. We found that precursors of the prethalamus are already specified and irreplaceable at late gastrula stage, because ablation of these cells results in loss of prethalamic markers. Moreover, when transplanted into the ectopic environment of the presumptive hindbrain, these cells still pursue their prethalamic differentiation program. Finally, transplantation of these precursors, in the rostral-most neural epithelium, induces changes in cell identity in the surrounding host forebrain. This cell-non-autonomous property led us to propose that these committed prethalamic precursors may play an instructive role in the regionalization of the developing diencephalon.

Show MeSH
Related in: MedlinePlus