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Wnt/β-catenin signaling integrates patterning and metabolism of the insect growth zone

Wnt/β-catenin and hedgehog (Hh) signaling are essential for transmitting signals across cell membranes in animal embryos. Early patterning of the principal insect model, Drosophila melanogaster, occurs in the syncytial blastoderm, where diffusion of transcription factors obviates the need for signal...

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Autores principales: Oberhofer, Georg, Grossmann, Daniela, Siemanowski, Janna L., Beissbarth, Tim, Bucher, Gregor
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4299277/
https://www.ncbi.nlm.nih.gov/pubmed/25395458
http://dx.doi.org/10.1242/dev.112797
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author Oberhofer, Georg
Grossmann, Daniela
Siemanowski, Janna L.
Beissbarth, Tim
Bucher, Gregor
author_facet Oberhofer, Georg
Grossmann, Daniela
Siemanowski, Janna L.
Beissbarth, Tim
Bucher, Gregor
author_sort Oberhofer, Georg
collection PubMed
description Wnt/β-catenin and hedgehog (Hh) signaling are essential for transmitting signals across cell membranes in animal embryos. Early patterning of the principal insect model, Drosophila melanogaster, occurs in the syncytial blastoderm, where diffusion of transcription factors obviates the need for signaling pathways. However, in the cellularized growth zone of typical short germ insect embryos, signaling pathways are predicted to play a more fundamental role. Indeed, the Wnt/β-catenin pathway is required for posterior elongation in most arthropods, although which target genes are activated in this context remains elusive. Here, we use the short germ beetle Tribolium castaneum to investigate two Wnt and Hh signaling centers located in the head anlagen and in the growth zone of early embryos. We find that Wnt/β-catenin signaling acts upstream of Hh in the growth zone, whereas the opposite interaction occurs in the head. We determine the target gene sets of the Wnt/β-catenin and Hh pathways and find that the growth zone signaling center activates a much greater number of genes and that the Wnt and Hh target gene sets are essentially non-overlapping. The Wnt pathway activates key genes of all three germ layers, including pair-rule genes, and Tc-caudal and Tc-twist. Furthermore, the Wnt pathway is required for hindgut development and we identify Tc-senseless as a novel hindgut patterning gene required in the early growth zone. At the same time, Wnt acts on growth zone metabolism and cell division, thereby integrating growth with patterning. Posterior Hh signaling activates several genes potentially involved in a proteinase cascade of unknown function.
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spelling pubmed-42992772015-01-29 Wnt/β-catenin signaling integrates patterning and metabolism of the insect growth zone Oberhofer, Georg Grossmann, Daniela Siemanowski, Janna L. Beissbarth, Tim Bucher, Gregor Development Research Articles Wnt/β-catenin and hedgehog (Hh) signaling are essential for transmitting signals across cell membranes in animal embryos. Early patterning of the principal insect model, Drosophila melanogaster, occurs in the syncytial blastoderm, where diffusion of transcription factors obviates the need for signaling pathways. However, in the cellularized growth zone of typical short germ insect embryos, signaling pathways are predicted to play a more fundamental role. Indeed, the Wnt/β-catenin pathway is required for posterior elongation in most arthropods, although which target genes are activated in this context remains elusive. Here, we use the short germ beetle Tribolium castaneum to investigate two Wnt and Hh signaling centers located in the head anlagen and in the growth zone of early embryos. We find that Wnt/β-catenin signaling acts upstream of Hh in the growth zone, whereas the opposite interaction occurs in the head. We determine the target gene sets of the Wnt/β-catenin and Hh pathways and find that the growth zone signaling center activates a much greater number of genes and that the Wnt and Hh target gene sets are essentially non-overlapping. The Wnt pathway activates key genes of all three germ layers, including pair-rule genes, and Tc-caudal and Tc-twist. Furthermore, the Wnt pathway is required for hindgut development and we identify Tc-senseless as a novel hindgut patterning gene required in the early growth zone. At the same time, Wnt acts on growth zone metabolism and cell division, thereby integrating growth with patterning. Posterior Hh signaling activates several genes potentially involved in a proteinase cascade of unknown function. The Company of Biologists 2014-12-15 /pmc/articles/PMC4299277/ /pubmed/25395458 http://dx.doi.org/10.1242/dev.112797 Text en © 2014. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/3.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Oberhofer, Georg
Grossmann, Daniela
Siemanowski, Janna L.
Beissbarth, Tim
Bucher, Gregor
Wnt/β-catenin signaling integrates patterning and metabolism of the insect growth zone
title Wnt/β-catenin signaling integrates patterning and metabolism of the insect growth zone
title_full Wnt/β-catenin signaling integrates patterning and metabolism of the insect growth zone
title_fullStr Wnt/β-catenin signaling integrates patterning and metabolism of the insect growth zone
title_full_unstemmed Wnt/β-catenin signaling integrates patterning and metabolism of the insect growth zone
title_short Wnt/β-catenin signaling integrates patterning and metabolism of the insect growth zone
title_sort wnt/β-catenin signaling integrates patterning and metabolism of the insect growth zone
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4299277/
https://www.ncbi.nlm.nih.gov/pubmed/25395458
http://dx.doi.org/10.1242/dev.112797
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