Cargando…

Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis

During Caenorhabditis elegans vulval development, the uterine anchor cell (AC) first secretes an epidermal growth factor (EGF) to specify the vulval cell fates and then invades the underlying vulval epithelium. By doing so, the AC establishes direct contact with the invaginating primary vulF cells a...

Descripción completa

Detalles Bibliográficos
Autores principales: Spiri, Silvan, Berger, Simon, Mereu, Louisa, DeMello, Andrew, Hajnal, Alex
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8783044/
https://www.ncbi.nlm.nih.gov/pubmed/34982813
http://dx.doi.org/10.1242/dev.199900
_version_ 1784638436665196544
author Spiri, Silvan
Berger, Simon
Mereu, Louisa
DeMello, Andrew
Hajnal, Alex
author_facet Spiri, Silvan
Berger, Simon
Mereu, Louisa
DeMello, Andrew
Hajnal, Alex
author_sort Spiri, Silvan
collection PubMed
description During Caenorhabditis elegans vulval development, the uterine anchor cell (AC) first secretes an epidermal growth factor (EGF) to specify the vulval cell fates and then invades the underlying vulval epithelium. By doing so, the AC establishes direct contact with the invaginating primary vulF cells and attaches the developing uterus to the vulva. The signals involved and the exact sequence of events joining these two organs are not fully understood. Using a conditional let-23 EGF receptor (EGFR) allele along with novel microfluidic short- and long-term imaging methods, we discovered a specific function of the EGFR in the AC during vulval lumen morphogenesis. Tissue-specific inactivation of let-23 in the AC resulted in imprecise alignment of the AC with the primary vulval cells, delayed AC invasion and disorganized adherens junctions at the contact site forming between the AC and the dorsal vulF toroid. We propose that EGFR signaling, activated by a reciprocal EGF cue from the primary vulval cells, positions the AC at the vulval midline, guides it during invasion and assembles a cytoskeletal scaffold organizing the adherens junctions that connect the developing uterus to the dorsal vulF toroid. Thus, EGFR signaling in the AC ensures the precise alignment of the two developing organs.
format Online
Article
Text
id pubmed-8783044
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher The Company of Biologists Ltd
record_format MEDLINE/PubMed
spelling pubmed-87830442022-03-16 Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis Spiri, Silvan Berger, Simon Mereu, Louisa DeMello, Andrew Hajnal, Alex Development Research Article During Caenorhabditis elegans vulval development, the uterine anchor cell (AC) first secretes an epidermal growth factor (EGF) to specify the vulval cell fates and then invades the underlying vulval epithelium. By doing so, the AC establishes direct contact with the invaginating primary vulF cells and attaches the developing uterus to the vulva. The signals involved and the exact sequence of events joining these two organs are not fully understood. Using a conditional let-23 EGF receptor (EGFR) allele along with novel microfluidic short- and long-term imaging methods, we discovered a specific function of the EGFR in the AC during vulval lumen morphogenesis. Tissue-specific inactivation of let-23 in the AC resulted in imprecise alignment of the AC with the primary vulval cells, delayed AC invasion and disorganized adherens junctions at the contact site forming between the AC and the dorsal vulF toroid. We propose that EGFR signaling, activated by a reciprocal EGF cue from the primary vulval cells, positions the AC at the vulval midline, guides it during invasion and assembles a cytoskeletal scaffold organizing the adherens junctions that connect the developing uterus to the dorsal vulF toroid. Thus, EGFR signaling in the AC ensures the precise alignment of the two developing organs. The Company of Biologists Ltd 2022-01-04 /pmc/articles/PMC8783044/ /pubmed/34982813 http://dx.doi.org/10.1242/dev.199900 Text en © 2022. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Spiri, Silvan
Berger, Simon
Mereu, Louisa
DeMello, Andrew
Hajnal, Alex
Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis
title Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis
title_full Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis
title_fullStr Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis
title_full_unstemmed Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis
title_short Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis
title_sort reciprocal egfr signaling in the anchor cell ensures precise inter-organ connection during caenorhabditis elegans vulval morphogenesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8783044/
https://www.ncbi.nlm.nih.gov/pubmed/34982813
http://dx.doi.org/10.1242/dev.199900
work_keys_str_mv AT spirisilvan reciprocalegfrsignalingintheanchorcellensurespreciseinterorganconnectionduringcaenorhabditiselegansvulvalmorphogenesis
AT bergersimon reciprocalegfrsignalingintheanchorcellensurespreciseinterorganconnectionduringcaenorhabditiselegansvulvalmorphogenesis
AT mereulouisa reciprocalegfrsignalingintheanchorcellensurespreciseinterorganconnectionduringcaenorhabditiselegansvulvalmorphogenesis
AT demelloandrew reciprocalegfrsignalingintheanchorcellensurespreciseinterorganconnectionduringcaenorhabditiselegansvulvalmorphogenesis
AT hajnalalex reciprocalegfrsignalingintheanchorcellensurespreciseinterorganconnectionduringcaenorhabditiselegansvulvalmorphogenesis