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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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The differentiation of a subpopulation of EL interneurons is impaired in Col mutants.(A, C) In stage 15 wild type embryos, Eve staining allows for the identification of the aCC and RP2 motoneurons (arrows and arrowheads respectively) and for the pCC interneuron (double arrowheads) in the dorsal region of the VNC (A). In the intermediate/ventral region of the VNC (C), Eve staining decorates the 5 U/CQ motoneurons (U1–5) (asterisks) and the cluster of 8/10 EL (Eve Lateral) interneurons (dashed circle). (B, D) In stage 15 Col mutant embryos, while the aCC, RP2, pCC and U/CQ neurons develop normally (B), the EL interneuron cluster (D) is reduced to 4/5 neurons in most of the segment analyzed. In all panels two consecutive segments are shown.
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pone-0021213-g006: The differentiation of a subpopulation of EL interneurons is impaired in Col mutants.(A, C) In stage 15 wild type embryos, Eve staining allows for the identification of the aCC and RP2 motoneurons (arrows and arrowheads respectively) and for the pCC interneuron (double arrowheads) in the dorsal region of the VNC (A). In the intermediate/ventral region of the VNC (C), Eve staining decorates the 5 U/CQ motoneurons (U1–5) (asterisks) and the cluster of 8/10 EL (Eve Lateral) interneurons (dashed circle). (B, D) In stage 15 Col mutant embryos, while the aCC, RP2, pCC and U/CQ neurons develop normally (B), the EL interneuron cluster (D) is reduced to 4/5 neurons in most of the segment analyzed. In all panels two consecutive segments are shown.

Mentions: Previous studies have shown that col is required for the proper differentiation of the dAp interneurons in the VNC [30], and a subset of the so-called multidendritic neurons in the PNS [27], [28], [29]. Here, we questioned whether a function for col in neuronal differentiation can be extended to other neurons. We focused on the well characterized EL cluster which contains, in the wild-type, 9–10 Eve+ neurons (100% of the hemisegments, n = 50; Figure 6) among which 4–5 express Col (Figure 3D–D″). We used two different col loss-of-function mutants, col1 ( mutation) and col2 (strong hypomorphic allele) [20], to assess the function of col in the differentiation of the EL neurons. With both alleles, we found a significant reduction of the number of EL neurons expressing Eve (Figure 6). In col1 homozygous embryos, we found 4–5 Eve+ neurons in 58% of the hemisegments and 2–3 Eve+ neurons in 42% of the hemisegments (n = 73); in col2 homozygous embryos, we found 4–5 Eve+ neurons in 89% of the hemisegments and 2–3 Eve+ neurons in 11% of the hemisegments (n = 48). We did not observe any effect on other Eve expressing neurons (which do not express Col in the wild-type), such as the aforementioned Eve+ motor neurons and the Eve+ pCC interneurons (Figure 6).


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)

The differentiation of a subpopulation of EL interneurons is impaired in Col mutants.(A, C) In stage 15 wild type embryos, Eve staining allows for the identification of the aCC and RP2 motoneurons (arrows and arrowheads respectively) and for the pCC interneuron (double arrowheads) in the dorsal region of the VNC (A). In the intermediate/ventral region of the VNC (C), Eve staining decorates the 5 U/CQ motoneurons (U1–5) (asterisks) and the cluster of 8/10 EL (Eve Lateral) interneurons (dashed circle). (B, D) In stage 15 Col mutant embryos, while the aCC, RP2, pCC and U/CQ neurons develop normally (B), the EL interneuron cluster (D) is reduced to 4/5 neurons in most of the segment analyzed. In all panels two consecutive segments are shown.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3117877&req=5

pone-0021213-g006: The differentiation of a subpopulation of EL interneurons is impaired in Col mutants.(A, C) In stage 15 wild type embryos, Eve staining allows for the identification of the aCC and RP2 motoneurons (arrows and arrowheads respectively) and for the pCC interneuron (double arrowheads) in the dorsal region of the VNC (A). In the intermediate/ventral region of the VNC (C), Eve staining decorates the 5 U/CQ motoneurons (U1–5) (asterisks) and the cluster of 8/10 EL (Eve Lateral) interneurons (dashed circle). (B, D) In stage 15 Col mutant embryos, while the aCC, RP2, pCC and U/CQ neurons develop normally (B), the EL interneuron cluster (D) is reduced to 4/5 neurons in most of the segment analyzed. In all panels two consecutive segments are shown.
Mentions: Previous studies have shown that col is required for the proper differentiation of the dAp interneurons in the VNC [30], and a subset of the so-called multidendritic neurons in the PNS [27], [28], [29]. Here, we questioned whether a function for col in neuronal differentiation can be extended to other neurons. We focused on the well characterized EL cluster which contains, in the wild-type, 9–10 Eve+ neurons (100% of the hemisegments, n = 50; Figure 6) among which 4–5 express Col (Figure 3D–D″). We used two different col loss-of-function mutants, col1 ( mutation) and col2 (strong hypomorphic allele) [20], to assess the function of col in the differentiation of the EL neurons. With both alleles, we found a significant reduction of the number of EL neurons expressing Eve (Figure 6). In col1 homozygous embryos, we found 4–5 Eve+ neurons in 58% of the hemisegments and 2–3 Eve+ neurons in 42% of the hemisegments (n = 73); in col2 homozygous embryos, we found 4–5 Eve+ neurons in 89% of the hemisegments and 2–3 Eve+ neurons in 11% of the hemisegments (n = 48). We did not observe any effect on other Eve expressing neurons (which do not express Col in the wild-type), such as the aforementioned Eve+ motor neurons and the Eve+ pCC interneurons (Figure 6).

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