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Timed Collinear Activation of Hox Genes during Gastrulation Controls the Avian Forelimb Position
Limb position along the body is highly consistent within one species but very variable among vertebrates. Despite major advances in our understanding of limb patterning in three dimensions, how limbs reproducibly form along the antero-posterior axis remains largely unknown. Hox genes have long been...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Cell Press
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6331352/ https://www.ncbi.nlm.nih.gov/pubmed/30554902 http://dx.doi.org/10.1016/j.cub.2018.11.009 |
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author | Moreau, Chloe Caldarelli, Paolo Rocancourt, Didier Roussel, Julian Denans, Nicolas Pourquie, Olivier Gros, Jerome |
author_facet | Moreau, Chloe Caldarelli, Paolo Rocancourt, Didier Roussel, Julian Denans, Nicolas Pourquie, Olivier Gros, Jerome |
author_sort | Moreau, Chloe |
collection | PubMed |
description | Limb position along the body is highly consistent within one species but very variable among vertebrates. Despite major advances in our understanding of limb patterning in three dimensions, how limbs reproducibly form along the antero-posterior axis remains largely unknown. Hox genes have long been suspected to control limb position; however, supporting evidences are mostly correlative and their role in this process is unclear. Here, we show that limb position is determined early in development through the action of Hox genes. Dynamic lineage analysis revealed that, during gastrulation, the forelimb, interlimb, and hindlimb fields are progressively generated and concomitantly patterned by the collinear activation of Hox genes in a two-step process. First, the sequential activation of Hoxb genes controls the relative position of their own collinear domains of expression in the forming lateral plate mesoderm, as demonstrated by functional perturbations during gastrulation. Then, within these collinear domains, we show that Hoxb4 anteriorly and Hox9 genes posteriorly, respectively, activate and repress the expression of the forelimb initiation gene Tbx5 and instruct the definitive position of the forelimb. Furthermore, by comparing the dynamics of Hoxb genes activation during zebra finch, chicken, and ostrich gastrulation, we provide evidences that changes in the timing of collinear Hox gene activation might underlie natural variation in forelimb position between different birds. Altogether, our results that characterize the cellular and molecular mechanisms underlying the regulation and natural variation of forelimb positioning in avians show a direct and early role for Hox genes in this process. |
format | Online Article Text |
id | pubmed-6331352 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Cell Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-63313522019-01-22 Timed Collinear Activation of Hox Genes during Gastrulation Controls the Avian Forelimb Position Moreau, Chloe Caldarelli, Paolo Rocancourt, Didier Roussel, Julian Denans, Nicolas Pourquie, Olivier Gros, Jerome Curr Biol Article Limb position along the body is highly consistent within one species but very variable among vertebrates. Despite major advances in our understanding of limb patterning in three dimensions, how limbs reproducibly form along the antero-posterior axis remains largely unknown. Hox genes have long been suspected to control limb position; however, supporting evidences are mostly correlative and their role in this process is unclear. Here, we show that limb position is determined early in development through the action of Hox genes. Dynamic lineage analysis revealed that, during gastrulation, the forelimb, interlimb, and hindlimb fields are progressively generated and concomitantly patterned by the collinear activation of Hox genes in a two-step process. First, the sequential activation of Hoxb genes controls the relative position of their own collinear domains of expression in the forming lateral plate mesoderm, as demonstrated by functional perturbations during gastrulation. Then, within these collinear domains, we show that Hoxb4 anteriorly and Hox9 genes posteriorly, respectively, activate and repress the expression of the forelimb initiation gene Tbx5 and instruct the definitive position of the forelimb. Furthermore, by comparing the dynamics of Hoxb genes activation during zebra finch, chicken, and ostrich gastrulation, we provide evidences that changes in the timing of collinear Hox gene activation might underlie natural variation in forelimb position between different birds. Altogether, our results that characterize the cellular and molecular mechanisms underlying the regulation and natural variation of forelimb positioning in avians show a direct and early role for Hox genes in this process. Cell Press 2019-01-07 /pmc/articles/PMC6331352/ /pubmed/30554902 http://dx.doi.org/10.1016/j.cub.2018.11.009 Text en © 2018 The Author(s) http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
spellingShingle | Article Moreau, Chloe Caldarelli, Paolo Rocancourt, Didier Roussel, Julian Denans, Nicolas Pourquie, Olivier Gros, Jerome Timed Collinear Activation of Hox Genes during Gastrulation Controls the Avian Forelimb Position |
title | Timed Collinear Activation of Hox Genes during Gastrulation Controls the Avian Forelimb Position |
title_full | Timed Collinear Activation of Hox Genes during Gastrulation Controls the Avian Forelimb Position |
title_fullStr | Timed Collinear Activation of Hox Genes during Gastrulation Controls the Avian Forelimb Position |
title_full_unstemmed | Timed Collinear Activation of Hox Genes during Gastrulation Controls the Avian Forelimb Position |
title_short | Timed Collinear Activation of Hox Genes during Gastrulation Controls the Avian Forelimb Position |
title_sort | timed collinear activation of hox genes during gastrulation controls the avian forelimb position |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6331352/ https://www.ncbi.nlm.nih.gov/pubmed/30554902 http://dx.doi.org/10.1016/j.cub.2018.11.009 |
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