Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms
Resumen:
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.
2016 | |
Antero-posterior axis Cestodes FoxQ2 Metamorphosis Myocyte Phylotypic Planarian Platyhelminthes SFRP Six3/6 Wnt |
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Inglés | |
Universidad de la República | |
COLIBRI | |
https://hdl.handle.net/20.500.12008/22075 | |
Acceso abierto | |
Licencia Creative Commons Atribución (CC –BY 4.0) |
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---|---|
author | Koziol, Uriel |
author2 | Jarero, F. Olson, P.D. Brehm, Klaus |
author2_role | author author author |
author_facet | Koziol, Uriel Jarero, F. Olson, P.D. Brehm, Klaus |
author_role | author |
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collection | COLIBRI |
dc.contributor.filiacion.es.fl_str_mv | Koziol, Uriel. Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología |
dc.creator.none.fl_str_mv | Koziol, Uriel Jarero, F. Olson, P.D. Brehm, Klaus |
dc.date.accessioned.none.fl_str_mv | 2019-10-02T22:14:44Z |
dc.date.available.none.fl_str_mv | 2019-10-02T22:14:44Z |
dc.date.issued.es.fl_str_mv | 2016 |
dc.date.submitted.es.fl_str_mv | 20191001 |
dc.description.abstract.none.fl_txt_mv | 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. |
dc.format.mimetype.es.fl_str_mv | application/pdf |
dc.identifier.citation.es.fl_str_mv | Koziol, U., et al. Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms. BMC Biology, 2016, 14 (1), art. no. 10. doi: 10.1186/s12915-016-0233-x |
dc.identifier.doi.es.fl_str_mv | 10.1186/s12915-016-0233-x |
dc.identifier.issn.es.fl_str_mv | 1741-7007 |
dc.identifier.uri.none.fl_str_mv | https://hdl.handle.net/20.500.12008/22075 |
dc.language.iso.none.fl_str_mv | en eng |
dc.publisher.es.fl_str_mv | BioMed Central Ltd. |
dc.relation.ispartof.es.fl_str_mv | BMC Biology, 2016, 14 (1), art. no. 10 |
dc.rights.license.none.fl_str_mv | Licencia Creative Commons Atribución (CC –BY 4.0) |
dc.rights.none.fl_str_mv | info:eu-repo/semantics/openAccess |
dc.source.none.fl_str_mv | reponame:COLIBRI instname:Universidad de la República instacron:Universidad de la República |
dc.subject.es.fl_str_mv | Antero-posterior axis Cestodes FoxQ2 Metamorphosis Myocyte Phylotypic Planarian Platyhelminthes SFRP Six3/6 Wnt |
dc.title.none.fl_str_mv | Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms |
dc.type.es.fl_str_mv | Artículo |
dc.type.none.fl_str_mv | info:eu-repo/semantics/article |
dc.type.version.none.fl_str_mv | info:eu-repo/semantics/publishedVersion |
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. |
eu_rights_str_mv | openAccess |
format | article |
id | COLIBRI_548eaede41669fb05f48ce2263c3d226 |
identifier_str_mv | Koziol, U., et al. Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms. BMC Biology, 2016, 14 (1), art. no. 10. doi: 10.1186/s12915-016-0233-x 1741-7007 10.1186/s12915-016-0233-x |
instacron_str | Universidad de la República |
institution | Universidad de la República |
instname_str | Universidad de la República |
language | eng |
language_invalid_str_mv | en |
network_acronym_str | COLIBRI |
network_name_str | COLIBRI |
oai_identifier_str | oai:colibri.udelar.edu.uy:20.500.12008/22075 |
publishDate | 2016 |
reponame_str | COLIBRI |
repository.mail.fl_str_mv | mabel.seroubian@seciu.edu.uy |
repository.name.fl_str_mv | COLIBRI - Universidad de la República |
repository_id_str | 4771 |
rights_invalid_str_mv | Licencia Creative Commons Atribución (CC –BY 4.0) |
spelling | Koziol, Uriel. Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología2019-10-02T22:14:44Z2019-10-02T22:14:44Z201620191001Koziol, U., et al. Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms. BMC Biology, 2016, 14 (1), art. no. 10. doi: 10.1186/s12915-016-0233-x1741-7007https://hdl.handle.net/20.500.12008/2207510.1186/s12915-016-0233-xBackground: 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.Made available in DSpace on 2019-10-02T22:14:44Z (GMT). No. of bitstreams: 5 101186s129150160233x.pdf: 4265062 bytes, checksum: 7de2942b1f48c5b59ee17b8ed44ac2e1 (MD5) license_text: 38297 bytes, checksum: 4fe6ac477f5a2df0424a5ff1a9bf000c (MD5) license_url: 44 bytes, checksum: a0ebbeafb9d2ec7cbb19d7137ebc392c (MD5) license_rdf: 8067 bytes, checksum: bc1bc9659a4a06e9516479a5adfd8b0e (MD5) license.txt: 4194 bytes, checksum: 7f2e2c17ef6585de66da58d1bfa8b5e1 (MD5) Previous issue date: 2016application/pdfenengBioMed Central Ltd.BMC Biology, 2016, 14 (1), art. no. 10Las obras depositadas en el Repositorio se rigen por la Ordenanza de los Derechos de la Propiedad Intelectual de la Universidad De La República. (Res. Nº 91 de C.D.C. de 8/III/1994 – D.O. 7/IV/1994) y por la Ordenanza del Repositorio Abierto de la Universidad de la República (Res. 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- Universidad de la Repúblicafalse |
spellingShingle | Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms Koziol, Uriel Antero-posterior axis Cestodes FoxQ2 Metamorphosis Myocyte Phylotypic Planarian Platyhelminthes SFRP Six3/6 Wnt |
status_str | publishedVersion |
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 | Antero-posterior axis Cestodes FoxQ2 Metamorphosis Myocyte Phylotypic Planarian Platyhelminthes SFRP Six3/6 Wnt |
url | https://hdl.handle.net/20.500.12008/22075 |