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

Koziol, Uriel - Jarero, F. - Olson, P.D. - Brehm, Klaus

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.


Detalles Bibliográficos
2016
Antero-posterior axis
Cestodes
FoxQ2
Metamorphosis
Myocyte
Phylotypic
Planarian
Platyhelminthes
SFRP
Six3/6
Wnt
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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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.
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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
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instname_str Universidad de la República
language eng
language_invalid_str_mv en
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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). 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Nº 16 de C.D.C. de 07/10/2014)info:eu-repo/semantics/openAccessLicencia Creative Commons Atribución (CC –BY 4.0)Antero-posterior axisCestodesFoxQ2MetamorphosisMyocytePhylotypicPlanarianPlatyhelminthesSFRPSix3/6WntComparative analysis of Wnt expression identifies a highly conserved developmental transition in flatwormsArtículoinfo:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionreponame:COLIBRIinstname:Universidad de la Repúblicainstacron:Universidad de la RepúblicaKoziol, UrielJarero, F.Olson, P.D.Brehm, 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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