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Coe genes are expressed in differentiating neurons in the central nervous system of protostomes.

Demilly A, Simionato E, Ohayon D, Kerner P, Garcès A, Vervoort M - PLoS ONE (2011)

Bottom Line: In Platynereis dumerilii, we cloned a single coe gene, Pdu-coe, and found that it is exclusively expressed in post mitotic neural cells.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.

View Article: PubMed Central - PubMed

Affiliation: University of Paris Diderot, Sorbonne Paris Cité, Institut Jacques Monod, UMR 7592 CNRS, Paris, France.

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.

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Col is expressed in discrete subsets of interneurons.Stage 15 embryos stained with Col and different interneuron markers. (A–A″) Col is expressed by the dAp (dorsal Apterous) interneuron (ApGal4+) and by the dCID interneuron (indicated by arrows). (B–B″) In the dorsal region of the VNC Col is only found expressed in one Dachshund (DacGal4) expressing interneuron that we have named dCID (dorsal Col, Islet, Dachshund) neuron (see also Figure 2). Note that the dCID is found at the vicinity of dAp. (C–C″) In the intermediate region of the VNC Col expression is found in 2 laterally located Dac+ interneurons indicated by the arrows. (D–D″) Overlap between Col and Eve is found in 4/5 EL (Eve Lateral) Eve+ interneurons. (E–E″) In the dorsal region of the VNC Col is not expressed with Eagle (EgGal4). Nevertheless note that the dAp and the dCID interneurons are located in a region where two Eg+ neurons are found. Note that here only two consecutive segments are shown. (F–F″) In the intermediate region of the VNC Col is not found expressed in the 3 Eg expressing serotoninergic neurons (EW1–3) but it is expressed in 3/4 Eg+ laterally located interneurons that belong the EL (Eve+) cluster. (G–G″) Col and Engrailed (En) expression only overlaps in 2 interneurons that are located in the lateral and intermediate region of the VNC.
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pone-0021213-g003: Col is expressed in discrete subsets of interneurons.Stage 15 embryos stained with Col and different interneuron markers. (A–A″) Col is expressed by the dAp (dorsal Apterous) interneuron (ApGal4+) and by the dCID interneuron (indicated by arrows). (B–B″) In the dorsal region of the VNC Col is only found expressed in one Dachshund (DacGal4) expressing interneuron that we have named dCID (dorsal Col, Islet, Dachshund) neuron (see also Figure 2). Note that the dCID is found at the vicinity of dAp. (C–C″) In the intermediate region of the VNC Col expression is found in 2 laterally located Dac+ interneurons indicated by the arrows. (D–D″) Overlap between Col and Eve is found in 4/5 EL (Eve Lateral) Eve+ interneurons. (E–E″) In the dorsal region of the VNC Col is not expressed with Eagle (EgGal4). Nevertheless note that the dAp and the dCID interneurons are located in a region where two Eg+ neurons are found. Note that here only two consecutive segments are shown. (F–F″) In the intermediate region of the VNC Col is not found expressed in the 3 Eg expressing serotoninergic neurons (EW1–3) but it is expressed in 3/4 Eg+ laterally located interneurons that belong the EL (Eve+) cluster. (G–G″) Col and Engrailed (En) expression only overlaps in 2 interneurons that are located in the lateral and intermediate region of the VNC.

Mentions: Stage 15 embryos stained with Col and different motor neuron markers. (A–B″) No overlap between Col and pMad is found in any of the different regions of the VNC examined. (C–C″) Col and Zfh1 expression only overlaps in the dorsal apterous neuron (dAp). (D–D″) Col is only found expressed in one Islet-tau-mycEGFP+ interneuron (see also Figure 3) that we have named dCID (dorsal Col, Islet, Dachshund) neuron and excluded from the identifiable Islet+ motor neurons RP1–5. (E–E″) Expression of Col and HB9Gal4 is mutually exclusive. (F–G″) Col is not expressed by the Eve+ aCC, RP2 and U1–5 motor neurons neither by the pCC interneuron. Arrowheads: RP2 motor neuron; arrows: aCC motor neuron; arrows in (C–D″) indicate dCID interneuron; asterisks: U/CQ motor neurons (U1–5); brackets: RP1, 3, 4, 5 motor neurons; double arrowheads: pCC interneuron.


Coe genes are expressed in differentiating neurons in the central nervous system of protostomes.

Demilly A, Simionato E, Ohayon D, Kerner P, Garcès A, Vervoort M - PLoS ONE (2011)

Col is expressed in discrete subsets of interneurons.Stage 15 embryos stained with Col and different interneuron markers. (A–A″) Col is expressed by the dAp (dorsal Apterous) interneuron (ApGal4+) and by the dCID interneuron (indicated by arrows). (B–B″) In the dorsal region of the VNC Col is only found expressed in one Dachshund (DacGal4) expressing interneuron that we have named dCID (dorsal Col, Islet, Dachshund) neuron (see also Figure 2). Note that the dCID is found at the vicinity of dAp. (C–C″) In the intermediate region of the VNC Col expression is found in 2 laterally located Dac+ interneurons indicated by the arrows. (D–D″) Overlap between Col and Eve is found in 4/5 EL (Eve Lateral) Eve+ interneurons. (E–E″) In the dorsal region of the VNC Col is not expressed with Eagle (EgGal4). Nevertheless note that the dAp and the dCID interneurons are located in a region where two Eg+ neurons are found. Note that here only two consecutive segments are shown. (F–F″) In the intermediate region of the VNC Col is not found expressed in the 3 Eg expressing serotoninergic neurons (EW1–3) but it is expressed in 3/4 Eg+ laterally located interneurons that belong the EL (Eve+) cluster. (G–G″) Col and Engrailed (En) expression only overlaps in 2 interneurons that are located in the lateral and intermediate region of the VNC.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3117877&req=5

pone-0021213-g003: Col is expressed in discrete subsets of interneurons.Stage 15 embryos stained with Col and different interneuron markers. (A–A″) Col is expressed by the dAp (dorsal Apterous) interneuron (ApGal4+) and by the dCID interneuron (indicated by arrows). (B–B″) In the dorsal region of the VNC Col is only found expressed in one Dachshund (DacGal4) expressing interneuron that we have named dCID (dorsal Col, Islet, Dachshund) neuron (see also Figure 2). Note that the dCID is found at the vicinity of dAp. (C–C″) In the intermediate region of the VNC Col expression is found in 2 laterally located Dac+ interneurons indicated by the arrows. (D–D″) Overlap between Col and Eve is found in 4/5 EL (Eve Lateral) Eve+ interneurons. (E–E″) In the dorsal region of the VNC Col is not expressed with Eagle (EgGal4). Nevertheless note that the dAp and the dCID interneurons are located in a region where two Eg+ neurons are found. Note that here only two consecutive segments are shown. (F–F″) In the intermediate region of the VNC Col is not found expressed in the 3 Eg expressing serotoninergic neurons (EW1–3) but it is expressed in 3/4 Eg+ laterally located interneurons that belong the EL (Eve+) cluster. (G–G″) Col and Engrailed (En) expression only overlaps in 2 interneurons that are located in the lateral and intermediate region of the VNC.
Mentions: Stage 15 embryos stained with Col and different motor neuron markers. (A–B″) No overlap between Col and pMad is found in any of the different regions of the VNC examined. (C–C″) Col and Zfh1 expression only overlaps in the dorsal apterous neuron (dAp). (D–D″) Col is only found expressed in one Islet-tau-mycEGFP+ interneuron (see also Figure 3) that we have named dCID (dorsal Col, Islet, Dachshund) neuron and excluded from the identifiable Islet+ motor neurons RP1–5. (E–E″) Expression of Col and HB9Gal4 is mutually exclusive. (F–G″) Col is not expressed by the Eve+ aCC, RP2 and U1–5 motor neurons neither by the pCC interneuron. Arrowheads: RP2 motor neuron; arrows: aCC motor neuron; arrows in (C–D″) indicate dCID interneuron; asterisks: U/CQ motor neurons (U1–5); brackets: RP1, 3, 4, 5 motor neurons; double arrowheads: pCC interneuron.

Bottom Line: In Platynereis dumerilii, we cloned a single coe gene, Pdu-coe, and found that it is exclusively expressed in post mitotic neural cells.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.

View Article: PubMed Central - PubMed

Affiliation: University of Paris Diderot, Sorbonne Paris Cité, Institut Jacques Monod, UMR 7592 CNRS, Paris, France.

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.

Show MeSH
Related in: MedlinePlus