Coordination of canonical and noncanonical Hedgehog signalling pathways mediated by WDR11 during primordial germ cell development

<p dir="ltr"><i>WDR11</i>, a gene associated with Kallmann syndrome, is important in reproductive system development but molecular understanding of its action remains incomplete. We previously reported that <i>Wdr11</i>-deficient embryos exhibit defective cili...

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Main Author: Jiyoung Lee (41796) (author)
Other Authors: Yeonjoo Kim (14191643) (author), Paris Ataliotis (9260726) (author), Hyung-Goo Kim (728597) (author), Dae-Won Kim (215689) (author), Dorothy C. Bennett (19479832) (author), Nigel A. Brown (19479835) (author), Lawrence C. Layman (13913559) (author), Soo-Hyun Kim (10655) (author)
Published: 2023
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_version_ 1864513507148431360
author Jiyoung Lee (41796)
author2 Yeonjoo Kim (14191643)
Paris Ataliotis (9260726)
Hyung-Goo Kim (728597)
Dae-Won Kim (215689)
Dorothy C. Bennett (19479832)
Nigel A. Brown (19479835)
Lawrence C. Layman (13913559)
Soo-Hyun Kim (10655)
author2_role author
author
author
author
author
author
author
author
author_facet Jiyoung Lee (41796)
Yeonjoo Kim (14191643)
Paris Ataliotis (9260726)
Hyung-Goo Kim (728597)
Dae-Won Kim (215689)
Dorothy C. Bennett (19479832)
Nigel A. Brown (19479835)
Lawrence C. Layman (13913559)
Soo-Hyun Kim (10655)
author_role author
dc.creator.none.fl_str_mv Jiyoung Lee (41796)
Yeonjoo Kim (14191643)
Paris Ataliotis (9260726)
Hyung-Goo Kim (728597)
Dae-Won Kim (215689)
Dorothy C. Bennett (19479832)
Nigel A. Brown (19479835)
Lawrence C. Layman (13913559)
Soo-Hyun Kim (10655)
dc.date.none.fl_str_mv 2023-07-29T09:00:00Z
dc.identifier.none.fl_str_mv 10.1038/s41598-023-38017-9
dc.relation.none.fl_str_mv https://figshare.com/articles/journal_contribution/Coordination_of_canonical_and_noncanonical_Hedgehog_signalling_pathways_mediated_by_WDR11_during_primordial_germ_cell_development/26827813
dc.rights.none.fl_str_mv CC BY 4.0
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Biological sciences
Biochemistry and cell biology
Genetics
WDR11
Kallmann Syndrome
Primordial Germ Cell (PGC) Development
Hedgehog (HH) Signalling
Canonical and Noncanonical HH Pathways
Ciliogenesis
dc.title.none.fl_str_mv Coordination of canonical and noncanonical Hedgehog signalling pathways mediated by WDR11 during primordial germ cell development
dc.type.none.fl_str_mv Text
Journal contribution
info:eu-repo/semantics/publishedVersion
text
contribution to journal
description <p dir="ltr"><i>WDR11</i>, a gene associated with Kallmann syndrome, is important in reproductive system development but molecular understanding of its action remains incomplete. We previously reported that <i>Wdr11</i>-deficient embryos exhibit defective ciliogenesis and developmental defects associated with Hedgehog (HH) signalling. Here we demonstrate that WDR11 is required for primordial germ cell (PGC) development, regulating canonical and noncanonical HH signalling in parallel. Loss of WDR11 disrupts PGC motility and proliferation driven by the cilia-independent, PTCH2/GAS1-dependent noncanonical HH pathway. WDR11 modulates the growth of somatic cells surrounding PGCs by regulating the cilia-dependent, PTCH1/BOC-dependent canonical HH pathway. We reveal that PTCH1/BOC or PTCH2/GAS1 receptor context dictates SMO localisation inside or outside of cilia, respectively, and loss of WDR11 affects the signalling responses of SMO in both situations. We show that GAS1 is induced by PTCH2-specific HH signalling, which is lost in the absence of WDR11. We also provide evidence supporting a role for WDR11 in ciliogenesis through regulation of anterograde intraflagellar transport potentially via its interaction with IFT20. Since WDR11 is a target of noncanonical SMO signalling, WDR11 represents a novel mechanism by which noncanonical and canonical HH signals communicate and cooperate.</p><h2>Other Information</h2><p dir="ltr">Published in: Scientific Reports<br>License: <a href="https://creativecommons.org/licenses/by/4.0" target="_blank">https://creativecommons.org/licenses/by/4.0</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1038/s41598-023-38017-9" target="_blank">https://dx.doi.org/10.1038/s41598-023-38017-9</a></p>
eu_rights_str_mv openAccess
id Manara2_8a58e893f3c7173e08e36f75ce3f39ae
identifier_str_mv 10.1038/s41598-023-38017-9
network_acronym_str Manara2
network_name_str Manara2
oai_identifier_str oai:figshare.com:article/26827813
publishDate 2023
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rights_invalid_str_mv CC BY 4.0
spelling Coordination of canonical and noncanonical Hedgehog signalling pathways mediated by WDR11 during primordial germ cell developmentJiyoung Lee (41796)Yeonjoo Kim (14191643)Paris Ataliotis (9260726)Hyung-Goo Kim (728597)Dae-Won Kim (215689)Dorothy C. Bennett (19479832)Nigel A. Brown (19479835)Lawrence C. Layman (13913559)Soo-Hyun Kim (10655)Biological sciencesBiochemistry and cell biologyGeneticsWDR11Kallmann SyndromePrimordial Germ Cell (PGC) DevelopmentHedgehog (HH) SignallingCanonical and Noncanonical HH PathwaysCiliogenesis<p dir="ltr"><i>WDR11</i>, a gene associated with Kallmann syndrome, is important in reproductive system development but molecular understanding of its action remains incomplete. We previously reported that <i>Wdr11</i>-deficient embryos exhibit defective ciliogenesis and developmental defects associated with Hedgehog (HH) signalling. Here we demonstrate that WDR11 is required for primordial germ cell (PGC) development, regulating canonical and noncanonical HH signalling in parallel. Loss of WDR11 disrupts PGC motility and proliferation driven by the cilia-independent, PTCH2/GAS1-dependent noncanonical HH pathway. WDR11 modulates the growth of somatic cells surrounding PGCs by regulating the cilia-dependent, PTCH1/BOC-dependent canonical HH pathway. We reveal that PTCH1/BOC or PTCH2/GAS1 receptor context dictates SMO localisation inside or outside of cilia, respectively, and loss of WDR11 affects the signalling responses of SMO in both situations. We show that GAS1 is induced by PTCH2-specific HH signalling, which is lost in the absence of WDR11. We also provide evidence supporting a role for WDR11 in ciliogenesis through regulation of anterograde intraflagellar transport potentially via its interaction with IFT20. Since WDR11 is a target of noncanonical SMO signalling, WDR11 represents a novel mechanism by which noncanonical and canonical HH signals communicate and cooperate.</p><h2>Other Information</h2><p dir="ltr">Published in: Scientific Reports<br>License: <a href="https://creativecommons.org/licenses/by/4.0" target="_blank">https://creativecommons.org/licenses/by/4.0</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1038/s41598-023-38017-9" target="_blank">https://dx.doi.org/10.1038/s41598-023-38017-9</a></p>2023-07-29T09:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1038/s41598-023-38017-9https://figshare.com/articles/journal_contribution/Coordination_of_canonical_and_noncanonical_Hedgehog_signalling_pathways_mediated_by_WDR11_during_primordial_germ_cell_development/26827813CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/268278132023-07-29T09:00:00Z
spellingShingle Coordination of canonical and noncanonical Hedgehog signalling pathways mediated by WDR11 during primordial germ cell development
Jiyoung Lee (41796)
Biological sciences
Biochemistry and cell biology
Genetics
WDR11
Kallmann Syndrome
Primordial Germ Cell (PGC) Development
Hedgehog (HH) Signalling
Canonical and Noncanonical HH Pathways
Ciliogenesis
status_str publishedVersion
title Coordination of canonical and noncanonical Hedgehog signalling pathways mediated by WDR11 during primordial germ cell development
title_full Coordination of canonical and noncanonical Hedgehog signalling pathways mediated by WDR11 during primordial germ cell development
title_fullStr Coordination of canonical and noncanonical Hedgehog signalling pathways mediated by WDR11 during primordial germ cell development
title_full_unstemmed Coordination of canonical and noncanonical Hedgehog signalling pathways mediated by WDR11 during primordial germ cell development
title_short Coordination of canonical and noncanonical Hedgehog signalling pathways mediated by WDR11 during primordial germ cell development
title_sort Coordination of canonical and noncanonical Hedgehog signalling pathways mediated by WDR11 during primordial germ cell development
topic Biological sciences
Biochemistry and cell biology
Genetics
WDR11
Kallmann Syndrome
Primordial Germ Cell (PGC) Development
Hedgehog (HH) Signalling
Canonical and Noncanonical HH Pathways
Ciliogenesis