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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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Posterior Hox genes control the axis elongationvelocity in a collinear fashion.(A–B) Time-lapse series of chicken embryoselectroporated either with control (A) orHoxa13 (B). Red line: position ofHensen's node. ss = somite-stage. (C) Velocity ofaxis elongation of embryos electroporated with either a control,Hoxa9, Hoxc9, Hoxd10,Hoxd11, Hoxc11, Hoxa13, Hoxb13, orHoxc13 expressing constructs. Stars: p-value oftwo-tailed Student's t-test applied between thedifferent conditions. *p < 0.05. Error bars: standard error tothe mean (SEM).DOI:http://dx.doi.org/10.7554/eLife.04379.020
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fig5: Posterior Hox genes control the axis elongationvelocity in a collinear fashion.(A–B) Time-lapse series of chicken embryoselectroporated either with control (A) orHoxa13 (B). Red line: position ofHensen's node. ss = somite-stage. (C) Velocity ofaxis elongation of embryos electroporated with either a control,Hoxa9, Hoxc9, Hoxd10,Hoxd11, Hoxc11, Hoxa13, Hoxb13, orHoxc13 expressing constructs. Stars: p-value oftwo-tailed Student's t-test applied between thedifferent conditions. *p < 0.05. Error bars: standard error tothe mean (SEM).DOI:http://dx.doi.org/10.7554/eLife.04379.020

Mentions: We next tested the effect of over-expressing posterior Hox genes onaxis elongation (Figure 5A–C, Video 4, n = 47 embryos).Over-expression of either Hoxa9, Hoxc9, Hoxd10, Hoxd11, Hoxc11, Hoxa13,Hoxb13 or Hoxc13 but not of Hoxa10, Hoxc10,Hoxa11, Hoxc12, Hoxd12 and Hoxd13 in PM precursorscaused a significant decrease of elongation velocity (Figure 5A–C and not shown). The effect of Hoxgenes becomes progressively stronger for more posterior genes (Figure 5C and not shown, Video 4). Therefore, the same posterior Hox genes canalter cell ingression and axis elongation with a similar collinear trend (Figures 3C and 5C). The cell-autonomouscontrol of ingression by posterior Hox genes (Figure 4F–H) is expected to reduce the supply of motilecells in the posterior PSM. This should slow down elongation movements and couldexplain why such a non-cell autonomous effect on axis elongation is observed whileonly 30–50% PM cells express the Hox constructs. These datasuggest that a subset of posterior Hox genes controls the slowingdown of axis elongation by regulating ingression of PM precursors.10.7554/eLife.04379.020Figure 5.Posterior Hox genes control the axis elongationvelocity in a collinear fashion.


Hox genes control vertebrate body elongation by collinear Wnt repression.

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

Posterior Hox genes control the axis elongationvelocity in a collinear fashion.(A–B) Time-lapse series of chicken embryoselectroporated either with control (A) orHoxa13 (B). Red line: position ofHensen's node. ss = somite-stage. (C) Velocity ofaxis elongation of embryos electroporated with either a control,Hoxa9, Hoxc9, Hoxd10,Hoxd11, Hoxc11, Hoxa13, Hoxb13, orHoxc13 expressing constructs. Stars: p-value oftwo-tailed Student's t-test applied between thedifferent conditions. *p < 0.05. Error bars: standard error tothe mean (SEM).DOI:http://dx.doi.org/10.7554/eLife.04379.020
© Copyright Policy
Related In: Results  -  Collection

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

fig5: Posterior Hox genes control the axis elongationvelocity in a collinear fashion.(A–B) Time-lapse series of chicken embryoselectroporated either with control (A) orHoxa13 (B). Red line: position ofHensen's node. ss = somite-stage. (C) Velocity ofaxis elongation of embryos electroporated with either a control,Hoxa9, Hoxc9, Hoxd10,Hoxd11, Hoxc11, Hoxa13, Hoxb13, orHoxc13 expressing constructs. Stars: p-value oftwo-tailed Student's t-test applied between thedifferent conditions. *p < 0.05. Error bars: standard error tothe mean (SEM).DOI:http://dx.doi.org/10.7554/eLife.04379.020
Mentions: We next tested the effect of over-expressing posterior Hox genes onaxis elongation (Figure 5A–C, Video 4, n = 47 embryos).Over-expression of either Hoxa9, Hoxc9, Hoxd10, Hoxd11, Hoxc11, Hoxa13,Hoxb13 or Hoxc13 but not of Hoxa10, Hoxc10,Hoxa11, Hoxc12, Hoxd12 and Hoxd13 in PM precursorscaused a significant decrease of elongation velocity (Figure 5A–C and not shown). The effect of Hoxgenes becomes progressively stronger for more posterior genes (Figure 5C and not shown, Video 4). Therefore, the same posterior Hox genes canalter cell ingression and axis elongation with a similar collinear trend (Figures 3C and 5C). The cell-autonomouscontrol of ingression by posterior Hox genes (Figure 4F–H) is expected to reduce the supply of motilecells in the posterior PSM. This should slow down elongation movements and couldexplain why such a non-cell autonomous effect on axis elongation is observed whileonly 30–50% PM cells express the Hox constructs. These datasuggest that a subset of posterior Hox genes controls the slowingdown of axis elongation by regulating ingression of PM precursors.10.7554/eLife.04379.020Figure 5.Posterior Hox genes control the axis elongationvelocity in a collinear fashion.

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