Cargando…

Rab7-Mediated Endocytosis Establishes Patterning of Wnt Activity through Inactivation of Dkk Antagonism

Endocytosis has been proposed to modulate cell signaling activities. However, the role of endocytosis in embryogenesis, which requires coordination of multiple signaling inputs, has remained less understood. We previously showed that mouse embryos lacking a small guanosine triphosphate (GTP)-binding...

Descripción completa

Detalles Bibliográficos
Autores principales: Kawamura, Nobuyuki, Takaoka, Katsuyoshi, Hamada, Hiroshi, Hadjantonakis, Anna-Katerina, Sun-Wada, Ge-Hong, Wada, Yoh
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8171381/
https://www.ncbi.nlm.nih.gov/pubmed/32521258
http://dx.doi.org/10.1016/j.celrep.2020.107733
_version_ 1783702418754633728
author Kawamura, Nobuyuki
Takaoka, Katsuyoshi
Hamada, Hiroshi
Hadjantonakis, Anna-Katerina
Sun-Wada, Ge-Hong
Wada, Yoh
author_facet Kawamura, Nobuyuki
Takaoka, Katsuyoshi
Hamada, Hiroshi
Hadjantonakis, Anna-Katerina
Sun-Wada, Ge-Hong
Wada, Yoh
author_sort Kawamura, Nobuyuki
collection PubMed
description Endocytosis has been proposed to modulate cell signaling activities. However, the role of endocytosis in embryogenesis, which requires coordination of multiple signaling inputs, has remained less understood. We previously showed that mouse embryos lacking a small guanosine triphosphate (GTP)-binding protein Rab7 implicated in endocytic flow are defective in gastrulation. Here, we investigate how subcellular defects associated with Rab7 deficiency are related to the observed developmental defects. Rab7-deficient embryos fail to organize mesodermal tissues due to defects in Wnt-β-catenin signaling. Visceral endoderm (VE)-specific ablation of Rab7 results in patterning defects similar to systemic Rab7 deletion. Rab7 mutants accumulate the Wnt antagonist Dkk1 in the extracellular space and in intracellular compartments throughout the VE epithelium. These data indicate that Rab7-dependent endocytosis regulates the concentration and availability of extracellular Dkk1, thereby relieving the epiblast of antagonism. This intercellular mechanism therefore organizes distinct spatiotemporal patterns of canonical Wnt activity during the peri-gastrulation stages of embryonic development.
format Online
Article
Text
id pubmed-8171381
institution National Center for Biotechnology Information
language English
publishDate 2020
record_format MEDLINE/PubMed
spelling pubmed-81713812021-06-02 Rab7-Mediated Endocytosis Establishes Patterning of Wnt Activity through Inactivation of Dkk Antagonism Kawamura, Nobuyuki Takaoka, Katsuyoshi Hamada, Hiroshi Hadjantonakis, Anna-Katerina Sun-Wada, Ge-Hong Wada, Yoh Cell Rep Article Endocytosis has been proposed to modulate cell signaling activities. However, the role of endocytosis in embryogenesis, which requires coordination of multiple signaling inputs, has remained less understood. We previously showed that mouse embryos lacking a small guanosine triphosphate (GTP)-binding protein Rab7 implicated in endocytic flow are defective in gastrulation. Here, we investigate how subcellular defects associated with Rab7 deficiency are related to the observed developmental defects. Rab7-deficient embryos fail to organize mesodermal tissues due to defects in Wnt-β-catenin signaling. Visceral endoderm (VE)-specific ablation of Rab7 results in patterning defects similar to systemic Rab7 deletion. Rab7 mutants accumulate the Wnt antagonist Dkk1 in the extracellular space and in intracellular compartments throughout the VE epithelium. These data indicate that Rab7-dependent endocytosis regulates the concentration and availability of extracellular Dkk1, thereby relieving the epiblast of antagonism. This intercellular mechanism therefore organizes distinct spatiotemporal patterns of canonical Wnt activity during the peri-gastrulation stages of embryonic development. 2020-06-09 /pmc/articles/PMC8171381/ /pubmed/32521258 http://dx.doi.org/10.1016/j.celrep.2020.107733 Text en https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ).
spellingShingle Article
Kawamura, Nobuyuki
Takaoka, Katsuyoshi
Hamada, Hiroshi
Hadjantonakis, Anna-Katerina
Sun-Wada, Ge-Hong
Wada, Yoh
Rab7-Mediated Endocytosis Establishes Patterning of Wnt Activity through Inactivation of Dkk Antagonism
title Rab7-Mediated Endocytosis Establishes Patterning of Wnt Activity through Inactivation of Dkk Antagonism
title_full Rab7-Mediated Endocytosis Establishes Patterning of Wnt Activity through Inactivation of Dkk Antagonism
title_fullStr Rab7-Mediated Endocytosis Establishes Patterning of Wnt Activity through Inactivation of Dkk Antagonism
title_full_unstemmed Rab7-Mediated Endocytosis Establishes Patterning of Wnt Activity through Inactivation of Dkk Antagonism
title_short Rab7-Mediated Endocytosis Establishes Patterning of Wnt Activity through Inactivation of Dkk Antagonism
title_sort rab7-mediated endocytosis establishes patterning of wnt activity through inactivation of dkk antagonism
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8171381/
https://www.ncbi.nlm.nih.gov/pubmed/32521258
http://dx.doi.org/10.1016/j.celrep.2020.107733
work_keys_str_mv AT kawamuranobuyuki rab7mediatedendocytosisestablishespatterningofwntactivitythroughinactivationofdkkantagonism
AT takaokakatsuyoshi rab7mediatedendocytosisestablishespatterningofwntactivitythroughinactivationofdkkantagonism
AT hamadahiroshi rab7mediatedendocytosisestablishespatterningofwntactivitythroughinactivationofdkkantagonism
AT hadjantonakisannakaterina rab7mediatedendocytosisestablishespatterningofwntactivitythroughinactivationofdkkantagonism
AT sunwadagehong rab7mediatedendocytosisestablishespatterningofwntactivitythroughinactivationofdkkantagonism
AT wadayoh rab7mediatedendocytosisestablishespatterningofwntactivitythroughinactivationofdkkantagonism