Meteorins regulate the formation of the left-right organizer and the establishment of vertebrate body asymmetry

While the exterior of vertebrate bodies appears bilaterally symmetrical, internal organ positioning and morphology frequently exhibit left-right (L-R) asymmetries. In several vertebrates, including human, mouse, frog, and zebrafish, left-right symmetry-breaking during embryonic development is initia...

Full description

Saved in:
Bibliographic Details
Main Authors: Fanny Eggeler, Jonathan Boulanger-Weill, Flavia De Santis, Laura Belleri, Karine Duroure, Thomas O Auer, Shahad Albadri, Filippo Del Bene
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2025-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/105430
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849413248119472128
author Fanny Eggeler
Jonathan Boulanger-Weill
Flavia De Santis
Laura Belleri
Karine Duroure
Thomas O Auer
Shahad Albadri
Filippo Del Bene
author_facet Fanny Eggeler
Jonathan Boulanger-Weill
Flavia De Santis
Laura Belleri
Karine Duroure
Thomas O Auer
Shahad Albadri
Filippo Del Bene
author_sort Fanny Eggeler
collection DOAJ
description While the exterior of vertebrate bodies appears bilaterally symmetrical, internal organ positioning and morphology frequently exhibit left-right (L-R) asymmetries. In several vertebrates, including human, mouse, frog, and zebrafish, left-right symmetry-breaking during embryonic development is initiated by a ciliated organ called the Node or left-right organizer. Within the Node, a leftward flow of extraembryonic fluid named the Nodal flow mediates the asymmetric expressions of Nodal factors. Although downstream Nodal pathway components leading to the establishment of the embryonic left-right axis are well known, less is known about the development and formation of the embryonic Node itself. Here, we reveal a novel role for the Meteorin protein family in the establishment of the left-right axis and in the formation of Kupffer’s vesicle, the Node equivalent structure in zebrafish. We show that the genetic inactivation of each or all three members of the zebrafish Meteorin family (metrn, metrn-like a, and metrn-like b) leads to defects in properties of the Kupffer’s vesicle, caused by impaired assembly and migration of the Kupffer’s vesicle forming dorsal forerunner cells. In addition, we demonstrate that Meteorins genetically interact with integrins ItgαV and Itgβ1b, regulating the dorsal forerunner cell clustering, and that meteorins loss-of-function results in disturbed Nodal factor expression and consequently in randomized or symmetric heart looping and jogging. These results identify a new role for the Meteorin protein family in the left-right asymmetry patterning during embryonic vertebrate development.
format Article
id doaj-art-ebe8a96e813049f9a3f51555cf19a5fb
institution Kabale University
issn 2050-084X
language English
publishDate 2025-08-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj-art-ebe8a96e813049f9a3f51555cf19a5fb2025-08-20T03:34:10ZengeLife Sciences Publications LtdeLife2050-084X2025-08-011410.7554/eLife.105430Meteorins regulate the formation of the left-right organizer and the establishment of vertebrate body asymmetryFanny Eggeler0https://orcid.org/0009-0001-6803-1984Jonathan Boulanger-Weill1https://orcid.org/0000-0002-1580-0778Flavia De Santis2https://orcid.org/0000-0002-0988-6560Laura Belleri3https://orcid.org/0009-0001-5475-7821Karine Duroure4https://orcid.org/0000-0002-5959-569XThomas O Auer5https://orcid.org/0000-0003-3442-0567Shahad Albadri6https://orcid.org/0000-0002-3243-7018Filippo Del Bene7https://orcid.org/0000-0001-8551-2846Sorbonne Université, INSERM, CNRS, Institut de la Vision, Paris, FranceSorbonne Université, INSERM, CNRS, Institut de la Vision, Paris, FranceInstitut Curie, PSL Research University, Paris, France; ZeClinics SL. Sant Feliu de Llobregat, Barcelona, SpainSorbonne Université, INSERM, CNRS, Institut de la Vision, Paris, FranceSorbonne Université, INSERM, CNRS, Institut de la Vision, Paris, FranceInstitut Curie, PSL Research University, Paris, France; Department of Biology, University of Fribourg, Fribourg, SwitzerlandSorbonne Université, INSERM, CNRS, Institut de la Vision, Paris, FranceSorbonne Université, INSERM, CNRS, Institut de la Vision, Paris, FranceWhile the exterior of vertebrate bodies appears bilaterally symmetrical, internal organ positioning and morphology frequently exhibit left-right (L-R) asymmetries. In several vertebrates, including human, mouse, frog, and zebrafish, left-right symmetry-breaking during embryonic development is initiated by a ciliated organ called the Node or left-right organizer. Within the Node, a leftward flow of extraembryonic fluid named the Nodal flow mediates the asymmetric expressions of Nodal factors. Although downstream Nodal pathway components leading to the establishment of the embryonic left-right axis are well known, less is known about the development and formation of the embryonic Node itself. Here, we reveal a novel role for the Meteorin protein family in the establishment of the left-right axis and in the formation of Kupffer’s vesicle, the Node equivalent structure in zebrafish. We show that the genetic inactivation of each or all three members of the zebrafish Meteorin family (metrn, metrn-like a, and metrn-like b) leads to defects in properties of the Kupffer’s vesicle, caused by impaired assembly and migration of the Kupffer’s vesicle forming dorsal forerunner cells. In addition, we demonstrate that Meteorins genetically interact with integrins ItgαV and Itgβ1b, regulating the dorsal forerunner cell clustering, and that meteorins loss-of-function results in disturbed Nodal factor expression and consequently in randomized or symmetric heart looping and jogging. These results identify a new role for the Meteorin protein family in the left-right asymmetry patterning during embryonic vertebrate development.https://elifesciences.org/articles/105430Meteorinleft-right asymmetryembryonic development
spellingShingle Fanny Eggeler
Jonathan Boulanger-Weill
Flavia De Santis
Laura Belleri
Karine Duroure
Thomas O Auer
Shahad Albadri
Filippo Del Bene
Meteorins regulate the formation of the left-right organizer and the establishment of vertebrate body asymmetry
eLife
Meteorin
left-right asymmetry
embryonic development
title Meteorins regulate the formation of the left-right organizer and the establishment of vertebrate body asymmetry
title_full Meteorins regulate the formation of the left-right organizer and the establishment of vertebrate body asymmetry
title_fullStr Meteorins regulate the formation of the left-right organizer and the establishment of vertebrate body asymmetry
title_full_unstemmed Meteorins regulate the formation of the left-right organizer and the establishment of vertebrate body asymmetry
title_short Meteorins regulate the formation of the left-right organizer and the establishment of vertebrate body asymmetry
title_sort meteorins regulate the formation of the left right organizer and the establishment of vertebrate body asymmetry
topic Meteorin
left-right asymmetry
embryonic development
url https://elifesciences.org/articles/105430
work_keys_str_mv AT fannyeggeler meteorinsregulatetheformationoftheleftrightorganizerandtheestablishmentofvertebratebodyasymmetry
AT jonathanboulangerweill meteorinsregulatetheformationoftheleftrightorganizerandtheestablishmentofvertebratebodyasymmetry
AT flaviadesantis meteorinsregulatetheformationoftheleftrightorganizerandtheestablishmentofvertebratebodyasymmetry
AT laurabelleri meteorinsregulatetheformationoftheleftrightorganizerandtheestablishmentofvertebratebodyasymmetry
AT karineduroure meteorinsregulatetheformationoftheleftrightorganizerandtheestablishmentofvertebratebodyasymmetry
AT thomasoauer meteorinsregulatetheformationoftheleftrightorganizerandtheestablishmentofvertebratebodyasymmetry
AT shahadalbadri meteorinsregulatetheformationoftheleftrightorganizerandtheestablishmentofvertebratebodyasymmetry
AT filippodelbene meteorinsregulatetheformationoftheleftrightorganizerandtheestablishmentofvertebratebodyasymmetry