The ancestral role of nodal signalling in breaking L/R symmetry in the vertebrate forebrain

Ronan Lagadec; Laurent Laguerre; Arnaud Menuet; Anis Amara; Claire Rocancourt; Pierre Péricard; Benoît G Godard; Maria Celina Rodicio; Isabel Rodriguez-Moldes; Hélène Mayeur; Quentin Rougemont; Sylvie Mazan; Agnès Boutet

doi:10.1038/ncomms7686

The ancestral role of nodal signalling in breaking L/R symmetry in the vertebrate forebrain

Nat Commun. 2015 Mar 30:6:6686. doi: 10.1038/ncomms7686.

Affiliations

¹ CNRS, Sorbonne Universités, UPMC Univ Paris 06, FR2424, Development and Evolution of Vertebrates Group, Station Biologique, F-29688 Roscoff, France.
² UMR7355, CNRS, Experimental and Molecular Immunology and Neurogenetics, University of Orleans, 3b rue de la Férollerie, F-45071 Orleans Cedex 2, France.
³ CNRS, Sorbonne Universités, UPMC Univ Paris 06, FR2424, ABiMS, Station Biologique de Roscoff, F-29688 Roscoff, France.
⁴ Department of Cell Biology and Ecology, University of Santiago de Compostela, 15782 Santiago de Compostela, Spain.
⁵ INRA, Agrocampus Ouest, UMR 985 Ecologie et Santé des Ecosystèmes, F-35042 Rennes, France.

PMID: 25819227
DOI: 10.1038/ncomms7686

Abstract

Left-right asymmetries in the epithalamic region of the brain are widespread across vertebrates, but their magnitude and laterality varies among species. Whether these differences reflect independent origins of forebrain asymmetries or taxa-specific diversifications of an ancient vertebrate feature remains unknown. Here we show that the catshark Scyliorhinus canicula and the lampreys Petromyzon marinus and Lampetra planeri exhibit conserved molecular asymmetries between the left and right developing habenulae. Long-term pharmacological treatments in these species show that nodal signalling is essential to their generation, rather than their directionality as in teleosts. Moreover, in contrast to zebrafish, habenular left-right differences are observed in the absence of overt asymmetry of the adjacent pineal field. These data support an ancient origin of epithalamic asymmetry, and suggest that a nodal-dependent asymmetry programme operated in the forebrain of ancestral vertebrates before evolving into a variable trait in bony fish.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Base Sequence
Diencephalon / embryology
Diencephalon / metabolism
Embryo, Nonmammalian
Fibroblast Growth Factors / genetics
Fibroblast Growth Factors / metabolism
Functional Laterality / genetics*
Gene Expression Regulation, Developmental*
Homeodomain Proteins / genetics
Homeodomain Proteins / metabolism
Lampreys / genetics
Left-Right Determination Factors / genetics
Left-Right Determination Factors / metabolism
Molecular Sequence Data
Nodal Protein / genetics
Nodal Protein / metabolism
Nodal Signaling Ligands / genetics*
Nodal Signaling Ligands / metabolism
Petromyzon / genetics*
Prosencephalon / embryology*
Prosencephalon / metabolism
Sharks / genetics*
Signal Transduction
Transforming Growth Factor beta / genetics
Transforming Growth Factor beta / metabolism

Substances

Homeodomain Proteins
Left-Right Determination Factors
Nodal Protein
Nodal Signaling Ligands
Transforming Growth Factor beta
Fibroblast Growth Factors

Associated data

GENBANK/KF190312
GENBANK/KF190313
GENBANK/KF190314
GENBANK/KF190315
GENBANK/KF190316
GENBANK/KJ623814
GENBANK/KJ623815
GENBANK/KM041048
GENBANK/KM041049