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Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms

BACKGROUND: Early developmental patterns of flatworms are extremely diverse and difficult to compare between distant groups. In parasitic flatworms, such as tapeworms, this is confounded by highly derived life cycles involving indirect development, and even the true orientation of the tapeworm anter...

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Autores principales: Koziol, Uriel, Jarero, Francesca, Olson, Peter D., Brehm, Klaus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4778295/
https://www.ncbi.nlm.nih.gov/pubmed/26941070
http://dx.doi.org/10.1186/s12915-016-0233-x
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author Koziol, Uriel
Jarero, Francesca
Olson, Peter D.
Brehm, Klaus
author_facet Koziol, Uriel
Jarero, Francesca
Olson, Peter D.
Brehm, Klaus
author_sort Koziol, Uriel
collection PubMed
description BACKGROUND: Early developmental patterns of flatworms are extremely diverse and difficult to compare between distant groups. In parasitic flatworms, such as tapeworms, this is confounded by highly derived life cycles involving indirect development, and even the true orientation of the tapeworm antero-posterior (AP) axis has been a matter of controversy. In planarians, and metazoans generally, the AP axis is specified by the canonical Wnt pathway, and we hypothesized that it could also underpin axial formation during larval metamorphosis in tapeworms. RESULTS: By comparative gene expression analysis of Wnt components and conserved AP markers in the tapeworms Echinococcus multilocularis and Hymenolepis microstoma, we found remarkable similarities between the early stages of larval metamorphosis in tapeworms and late embryonic and adult development in planarians. We demonstrate posterior expression of specific Wnt factors during larval metamorphosis and show that scolex formation is preceded by localized expression of Wnt inhibitors. In the highly derived larval form of E. multilocularis, which proliferates asexually within the mammalian host, we found ubiquitous expression of posterior Wnt factors combined with localized expression of Wnt inhibitors that correlates with the asexual budding of scoleces. As in planarians, muscle cells are shown to be a source of secreted Wnt ligands, providing an explanation for the retention of a muscle layer in the immotile E. multilocularis larva. CONCLUSIONS: The strong conservation of gene expression between larval metamorphosis in tapeworms and late embryonic development in planarians suggests, for the first time, a homologous developmental period across this diverse phylum. We postulate these to represent the phylotypic stages of these flatworm groups. Our results support the classical notion that the scolex is the true anterior end of tapeworms. Furthermore, the up-regulation of Wnt inhibitors during the specification of multiple anterior poles suggests a mechanism for the unique asexual reproduction of E. multilocularis larvae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-016-0233-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-47782952016-03-05 Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms Koziol, Uriel Jarero, Francesca Olson, Peter D. Brehm, Klaus BMC Biol Research Article BACKGROUND: Early developmental patterns of flatworms are extremely diverse and difficult to compare between distant groups. In parasitic flatworms, such as tapeworms, this is confounded by highly derived life cycles involving indirect development, and even the true orientation of the tapeworm antero-posterior (AP) axis has been a matter of controversy. In planarians, and metazoans generally, the AP axis is specified by the canonical Wnt pathway, and we hypothesized that it could also underpin axial formation during larval metamorphosis in tapeworms. RESULTS: By comparative gene expression analysis of Wnt components and conserved AP markers in the tapeworms Echinococcus multilocularis and Hymenolepis microstoma, we found remarkable similarities between the early stages of larval metamorphosis in tapeworms and late embryonic and adult development in planarians. We demonstrate posterior expression of specific Wnt factors during larval metamorphosis and show that scolex formation is preceded by localized expression of Wnt inhibitors. In the highly derived larval form of E. multilocularis, which proliferates asexually within the mammalian host, we found ubiquitous expression of posterior Wnt factors combined with localized expression of Wnt inhibitors that correlates with the asexual budding of scoleces. As in planarians, muscle cells are shown to be a source of secreted Wnt ligands, providing an explanation for the retention of a muscle layer in the immotile E. multilocularis larva. CONCLUSIONS: The strong conservation of gene expression between larval metamorphosis in tapeworms and late embryonic development in planarians suggests, for the first time, a homologous developmental period across this diverse phylum. We postulate these to represent the phylotypic stages of these flatworm groups. Our results support the classical notion that the scolex is the true anterior end of tapeworms. Furthermore, the up-regulation of Wnt inhibitors during the specification of multiple anterior poles suggests a mechanism for the unique asexual reproduction of E. multilocularis larvae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-016-0233-x) contains supplementary material, which is available to authorized users. BioMed Central 2016-03-04 /pmc/articles/PMC4778295/ /pubmed/26941070 http://dx.doi.org/10.1186/s12915-016-0233-x Text en © Koziol et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Koziol, Uriel
Jarero, Francesca
Olson, Peter D.
Brehm, Klaus
Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms
title Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms
title_full Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms
title_fullStr Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms
title_full_unstemmed Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms
title_short Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms
title_sort comparative analysis of wnt expression identifies a highly conserved developmental transition in flatworms
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4778295/
https://www.ncbi.nlm.nih.gov/pubmed/26941070
http://dx.doi.org/10.1186/s12915-016-0233-x
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