Abstract
Genes of the coe (collier/olfactory/early B-cell factor) family encode Helix-Loop-Helix transcription factors that are widely conserved in metazoans and involved in many developmental processes, neurogenesis in particular. Whereas their functions during vertebrate neural tube formation have been well documented, very little is known about their expression and role during central nervous system (CNS) development in protostomes. Here we characterized the CNS expression of coe genes in the insect Drosophila melanogaster and the polychaete annelid Platynereis dumerilii, which belong to different subgroups of protostomes and show strikingly different modes of development. In the Drosophila ventral nerve cord, we found that the Collier-expressing cells form a subpopulation of interneurons with diverse molecular identities and neurotransmitter phenotypes. We also demonstrate that collier is required for the proper differentiation of some interneurons belonging to the Eve-Lateral cluster. In Platynereis dumerilii, we cloned a single coe gene, Pdu-coe, and found that it is exclusively expressed in post mitotic neural cells. Using an original technique of in silico 3D registration, we show that Pdu-coe is co-expressed with many different neuronal markers and therefore that, like in Drosophila, its expression defines a heterogeneous population of neurons with diverse molecular identities. Our detailed characterization and comparison of coe gene expression in the CNS of two distantly-related protostomes suggest conserved roles of coe genes in neuronal differentiation in this clade. As similar roles have also been observed in vertebrates, this function was probably already established in the last common ancestor of all bilaterians.
Highlights
The generation of neurons and glial cells is a complex and multi-step process, on which rely both the architecture and the activity of the bilaterian central nervous system (CNS)
Collier/olfactory/early B-cell factor (COE) proteins form a specific family of helix-loop-helix (HLH) proteins, characterized by the presence of three highly conserved domains: a unique DNA binding domain (DBD); an immunoglobulin / plexin / transcription (IPT) domain putatively involved in both DNA/protein and protein/protein interactions; and an atypical HLH dimerization motif [1,2,3]. coe genes have been identified in the three major bilaterian lineages, as well as in the cnidarian Nematostella vectensis, the ctenophora Mnemiopsis leidyi, and the sponge Amphimedon queenslandica [3,4,5,6], but not in plants or fungi, indicating that these genes form a metazoan specific family which would have arisen during early animal evolution
In the ventral layer of the ventral nerve cord (VNC) of stage 12 embryos, we typically found two to three Col+ phosphorylated form of histone H3 (PH3)+ cells per hemisegment probably ganglion mother cells (GMCs), but none at later stages (Figure 1A–A0, B–B0), indicating that Col is mainly or only expressed in postmitotic neural cells
Summary
The generation of neurons and glial cells is a complex and multi-step process, on which rely both the architecture and the activity of the bilaterian central nervous system (CNS). From the undifferentiated progenitors of the neural epithelium to the fully functional CNS cells, a large set of transcription factors and their combinatorial expression are required to control the different steps of commitment, patterning and differentiation Among these transcription factors, collier/olfactory/early B-cell factor (COE) proteins form a specific family of helix-loop-helix (HLH) proteins, characterized by the presence of three highly conserved domains: a unique DNA binding domain (DBD); an immunoglobulin / plexin / transcription (IPT) domain putatively involved in both DNA/protein and protein/protein interactions; and an atypical HLH dimerization motif [1,2,3]. An expression associated to the developing nervous system is found in the echinoderm Strongylocentrotus purpuratus [6], suggesting conserved functions for coe genes among deuterostomes
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
