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Hox genes control vertebrate body elongation by collinear Wnt repression.

Denans N, Iimura T, Pourquié O - Elife (2015)

Bottom Line: Our data indicate that a subset of progressively more posterior Hox genes, which are collinearly activated in vertebral precursors, repress Wnt activity with increasing strength.This leads to a graded repression of the Brachyury/T transcription factor, reducing mesoderm ingression and slowing down the elongation process.Due to the continuation of somite formation, this mechanism leads to the progressive reduction of PSM size.

View Article: PubMed Central - PubMed

Affiliation: Institut de Génétique et de Biologie Moléculaire et Cellulaire, University of Strasbourg, Illkirch, France.

ABSTRACT
In vertebrates, the total number of vertebrae is precisely defined. Vertebrae derive from embryonic somites that are continuously produced posteriorly from the presomitic mesoderm (PSM) during body formation. We show that in the chicken embryo, activation of posterior Hox genes (paralogs 9-13) in the tail-bud correlates with the slowing down of axis elongation. Our data indicate that a subset of progressively more posterior Hox genes, which are collinearly activated in vertebral precursors, repress Wnt activity with increasing strength. This leads to a graded repression of the Brachyury/T transcription factor, reducing mesoderm ingression and slowing down the elongation process. Due to the continuation of somite formation, this mechanism leads to the progressive reduction of PSM size. This ultimately brings the retinoic acid (RA)-producing segmented region in close vicinity to the tail bud, potentially accounting for the termination of segmentation and axis elongation.

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Slowing down of axis elongation correlates with decreasing cellingression in the PSM.(A) Velocity of axis elongation and of somite formation.(B) PSM cell number. (C–D)Tiling of confocal sections of 20-somite (C) and 25-somite(D) stage embryos. EdU positive cells are labeled in green,phosphorylated histone H3 (pH3) in red, and nuclei in blue (DAPI).(C′, D′) Higher magnification ofPSM regions used to quantify the proliferation. (C″,D″) Confocal sections of parasagittal cryosections oftail-bud used to quantify cell proliferation.(E–F) Quantification of cellproliferation (E) and apoptosis (F) in20–22 and 25–27 somites chicken embryos. (G) Cellmotility in the posterior PSM.DOI:http://dx.doi.org/10.7554/eLife.04379.004
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fig1: Slowing down of axis elongation correlates with decreasing cellingression in the PSM.(A) Velocity of axis elongation and of somite formation.(B) PSM cell number. (C–D)Tiling of confocal sections of 20-somite (C) and 25-somite(D) stage embryos. EdU positive cells are labeled in green,phosphorylated histone H3 (pH3) in red, and nuclei in blue (DAPI).(C′, D′) Higher magnification ofPSM regions used to quantify the proliferation. (C″,D″) Confocal sections of parasagittal cryosections oftail-bud used to quantify cell proliferation.(E–F) Quantification of cellproliferation (E) and apoptosis (F) in20–22 and 25–27 somites chicken embryos. (G) Cellmotility in the posterior PSM.DOI:http://dx.doi.org/10.7554/eLife.04379.004

Mentions: We measured the variations of velocities of axis elongation and somite formation intime-lapse videos of developing chicken embryos during the formation of the first 30somites (Video 1). The velocity of somiteformation shows limited variation during this developmental window (Tenin et al., 2010) (Figure 1A, n = 4 embryos for each condition). Incontrast, axis elongation velocity increases during the formation of the first 10somites and then it decreases until the 25-somite stage, when it drops abruptly(Figure 1A and Video 2, n = 41 embryos). The number of PSM cellsdecreases over time (Figure 1B, n = 5embryos for each condition) while no significant difference in cell proliferation orapoptosis in the PSM and tail-bud is observed (Figure1C–F, n = 4 embryos for each condition). Cell motility, whichhas been implicated in the control of axis elongation (Bénazéraf et al., 2010), also decreased between 15and 27 somites (Figure 1G, n = 4embryos for each condition). Thus, a parallel decrease in cell motility and in cellflux to the PSM accompanies axis elongation slow down.Video 1.Time-lapse video of an embryo from Stage 5 HH to 29 somites showing thedifferent phases of axis elongation (Bright-field, ventral view, anterior isup).


Hox genes control vertebrate body elongation by collinear Wnt repression.

Denans N, Iimura T, Pourquié O - Elife (2015)

Slowing down of axis elongation correlates with decreasing cellingression in the PSM.(A) Velocity of axis elongation and of somite formation.(B) PSM cell number. (C–D)Tiling of confocal sections of 20-somite (C) and 25-somite(D) stage embryos. EdU positive cells are labeled in green,phosphorylated histone H3 (pH3) in red, and nuclei in blue (DAPI).(C′, D′) Higher magnification ofPSM regions used to quantify the proliferation. (C″,D″) Confocal sections of parasagittal cryosections oftail-bud used to quantify cell proliferation.(E–F) Quantification of cellproliferation (E) and apoptosis (F) in20–22 and 25–27 somites chicken embryos. (G) Cellmotility in the posterior PSM.DOI:http://dx.doi.org/10.7554/eLife.04379.004
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4384752&req=5

fig1: Slowing down of axis elongation correlates with decreasing cellingression in the PSM.(A) Velocity of axis elongation and of somite formation.(B) PSM cell number. (C–D)Tiling of confocal sections of 20-somite (C) and 25-somite(D) stage embryos. EdU positive cells are labeled in green,phosphorylated histone H3 (pH3) in red, and nuclei in blue (DAPI).(C′, D′) Higher magnification ofPSM regions used to quantify the proliferation. (C″,D″) Confocal sections of parasagittal cryosections oftail-bud used to quantify cell proliferation.(E–F) Quantification of cellproliferation (E) and apoptosis (F) in20–22 and 25–27 somites chicken embryos. (G) Cellmotility in the posterior PSM.DOI:http://dx.doi.org/10.7554/eLife.04379.004
Mentions: We measured the variations of velocities of axis elongation and somite formation intime-lapse videos of developing chicken embryos during the formation of the first 30somites (Video 1). The velocity of somiteformation shows limited variation during this developmental window (Tenin et al., 2010) (Figure 1A, n = 4 embryos for each condition). Incontrast, axis elongation velocity increases during the formation of the first 10somites and then it decreases until the 25-somite stage, when it drops abruptly(Figure 1A and Video 2, n = 41 embryos). The number of PSM cellsdecreases over time (Figure 1B, n = 5embryos for each condition) while no significant difference in cell proliferation orapoptosis in the PSM and tail-bud is observed (Figure1C–F, n = 4 embryos for each condition). Cell motility, whichhas been implicated in the control of axis elongation (Bénazéraf et al., 2010), also decreased between 15and 27 somites (Figure 1G, n = 4embryos for each condition). Thus, a parallel decrease in cell motility and in cellflux to the PSM accompanies axis elongation slow down.Video 1.Time-lapse video of an embryo from Stage 5 HH to 29 somites showing thedifferent phases of axis elongation (Bright-field, ventral view, anterior isup).

Bottom Line: Our data indicate that a subset of progressively more posterior Hox genes, which are collinearly activated in vertebral precursors, repress Wnt activity with increasing strength.This leads to a graded repression of the Brachyury/T transcription factor, reducing mesoderm ingression and slowing down the elongation process.Due to the continuation of somite formation, this mechanism leads to the progressive reduction of PSM size.

View Article: PubMed Central - PubMed

Affiliation: Institut de Génétique et de Biologie Moléculaire et Cellulaire, University of Strasbourg, Illkirch, France.

ABSTRACT
In vertebrates, the total number of vertebrae is precisely defined. Vertebrae derive from embryonic somites that are continuously produced posteriorly from the presomitic mesoderm (PSM) during body formation. We show that in the chicken embryo, activation of posterior Hox genes (paralogs 9-13) in the tail-bud correlates with the slowing down of axis elongation. Our data indicate that a subset of progressively more posterior Hox genes, which are collinearly activated in vertebral precursors, repress Wnt activity with increasing strength. This leads to a graded repression of the Brachyury/T transcription factor, reducing mesoderm ingression and slowing down the elongation process. Due to the continuation of somite formation, this mechanism leads to the progressive reduction of PSM size. This ultimately brings the retinoic acid (RA)-producing segmented region in close vicinity to the tail bud, potentially accounting for the termination of segmentation and axis elongation.

Show MeSH
Related in: MedlinePlus