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Heterogeneous generation of new cells in the adult echinoderm nervous system.

Mashanov VS, Zueva OR, García-Arrarás JE - Front Neuroanat (2015)

Bottom Line: Importantly, this neurogenic activity is not evenly distributed, but is significantly more extensive in the lateral regions of the RNC than along the midline.Gene expression analysis showed that generation of new cells in the adult sea cucumber CNS is associated with transcriptional activity of genes known to be involved in regulation of various aspects of neurogenesis in other animals.Further analysis of one of those genes, the transcription factor Myc, showed that it is expressed, in some, but not all radial glial cells, suggesting heterogeneity of this CNS progenitor cell population in echinoderms.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Puerto Rico Rio Piedras, PR, USA.

ABSTRACT
Adult neurogenesis, generation of new functional cells in the mature central nervous system (CNS), has been documented in a number of diverse organisms, ranging from humans to invertebrates. However, the origin and evolution of this phenomenon is still poorly understood for many of the key phylogenetic groups. Echinoderms are one such phylum, positioned as a sister group to chordates within the monophyletic clade Deuterostomia. They are well known for the ability of their adult organs, including the CNS, to completely regenerate after injury. Nothing is known, however, about production of new cells in the nervous tissue under normal physiological conditions in these animals. In this study, we show that new cells are continuously generated in the mature radial nerve cord (RNC) of the sea cucumber Holothuria glaberrima. Importantly, this neurogenic activity is not evenly distributed, but is significantly more extensive in the lateral regions of the RNC than along the midline. Some of the new cells generated in the apical region of the ectoneural neuroepithelium leave their place of origin and migrate basally to populate the neural parenchyma. Gene expression analysis showed that generation of new cells in the adult sea cucumber CNS is associated with transcriptional activity of genes known to be involved in regulation of various aspects of neurogenesis in other animals. Further analysis of one of those genes, the transcription factor Myc, showed that it is expressed, in some, but not all radial glial cells, suggesting heterogeneity of this CNS progenitor cell population in echinoderms.

No MeSH data available.


Related in: MedlinePlus

Double fluorescent labeling with the ERG1 antibody, a maker of echinoderm radial glial cells (Mashanov et al., 2010) (green, left column), and an in situ hybridization probe for Myc (red, middle column). The right column shows overlay composite images with both markers. (A–A″) Low-magnification of a cross section through the radial nerve cord. (B–B″) Detailed view of the lateral region of the ectoneural neuroepithelium. (C–C″) Detailed view of the midline region of the ectoneural neuroepithelium. (D–D″) High-magnification view of the apical region of the ectoneural epithelium showing colocalization of the Myc in situ signal with ERG1 labeling in cell bodies of some of the radial glial cells (white arrows), whereas other glial cells do not express Myc at all (open arrows).
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Figure 7: Double fluorescent labeling with the ERG1 antibody, a maker of echinoderm radial glial cells (Mashanov et al., 2010) (green, left column), and an in situ hybridization probe for Myc (red, middle column). The right column shows overlay composite images with both markers. (A–A″) Low-magnification of a cross section through the radial nerve cord. (B–B″) Detailed view of the lateral region of the ectoneural neuroepithelium. (C–C″) Detailed view of the midline region of the ectoneural neuroepithelium. (D–D″) High-magnification view of the apical region of the ectoneural epithelium showing colocalization of the Myc in situ signal with ERG1 labeling in cell bodies of some of the radial glial cells (white arrows), whereas other glial cells do not express Myc at all (open arrows).

Mentions: In order to provide at least a partial answer, we simultaneously labeled the radial nerve cord with a specific glial marker, the ERG1 monoclonal antibody (Mashanov et al., 2010), and with a Myc in situ hybridization riboprobe. The choice of Myc was determined by phylogenetically conserved role of Myc proteins in activation of neural progenitors, which was demonstrated in animals as diverse as rat and Drosophila (Hasegawa et al., 2005; Fernández-Hernández et al., 2013). In the regenerating echinoderm radial nerve cord, Myc was also recently shown to be required for glial activation in response to injury (Mashanov et al., 2015b). In this study, the double labeling showed that many of the radial glial cells indeed expressed Myc, but these positively labeled cells were interspersed with glial cells, which showed no Myc expression (Figure 7). These results suggest that the echinoderm radial glial cells, despite being all morphologically alike, differ in expression of at least some of the key transcription factors. It remains to be determined whether or not this heterogeneity in gene expression results in heterogeneity in potency and the ability to proliferate.


Heterogeneous generation of new cells in the adult echinoderm nervous system.

Mashanov VS, Zueva OR, García-Arrarás JE - Front Neuroanat (2015)

Double fluorescent labeling with the ERG1 antibody, a maker of echinoderm radial glial cells (Mashanov et al., 2010) (green, left column), and an in situ hybridization probe for Myc (red, middle column). The right column shows overlay composite images with both markers. (A–A″) Low-magnification of a cross section through the radial nerve cord. (B–B″) Detailed view of the lateral region of the ectoneural neuroepithelium. (C–C″) Detailed view of the midline region of the ectoneural neuroepithelium. (D–D″) High-magnification view of the apical region of the ectoneural epithelium showing colocalization of the Myc in situ signal with ERG1 labeling in cell bodies of some of the radial glial cells (white arrows), whereas other glial cells do not express Myc at all (open arrows).
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Related In: Results  -  Collection

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Figure 7: Double fluorescent labeling with the ERG1 antibody, a maker of echinoderm radial glial cells (Mashanov et al., 2010) (green, left column), and an in situ hybridization probe for Myc (red, middle column). The right column shows overlay composite images with both markers. (A–A″) Low-magnification of a cross section through the radial nerve cord. (B–B″) Detailed view of the lateral region of the ectoneural neuroepithelium. (C–C″) Detailed view of the midline region of the ectoneural neuroepithelium. (D–D″) High-magnification view of the apical region of the ectoneural epithelium showing colocalization of the Myc in situ signal with ERG1 labeling in cell bodies of some of the radial glial cells (white arrows), whereas other glial cells do not express Myc at all (open arrows).
Mentions: In order to provide at least a partial answer, we simultaneously labeled the radial nerve cord with a specific glial marker, the ERG1 monoclonal antibody (Mashanov et al., 2010), and with a Myc in situ hybridization riboprobe. The choice of Myc was determined by phylogenetically conserved role of Myc proteins in activation of neural progenitors, which was demonstrated in animals as diverse as rat and Drosophila (Hasegawa et al., 2005; Fernández-Hernández et al., 2013). In the regenerating echinoderm radial nerve cord, Myc was also recently shown to be required for glial activation in response to injury (Mashanov et al., 2015b). In this study, the double labeling showed that many of the radial glial cells indeed expressed Myc, but these positively labeled cells were interspersed with glial cells, which showed no Myc expression (Figure 7). These results suggest that the echinoderm radial glial cells, despite being all morphologically alike, differ in expression of at least some of the key transcription factors. It remains to be determined whether or not this heterogeneity in gene expression results in heterogeneity in potency and the ability to proliferate.

Bottom Line: Importantly, this neurogenic activity is not evenly distributed, but is significantly more extensive in the lateral regions of the RNC than along the midline.Gene expression analysis showed that generation of new cells in the adult sea cucumber CNS is associated with transcriptional activity of genes known to be involved in regulation of various aspects of neurogenesis in other animals.Further analysis of one of those genes, the transcription factor Myc, showed that it is expressed, in some, but not all radial glial cells, suggesting heterogeneity of this CNS progenitor cell population in echinoderms.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Puerto Rico Rio Piedras, PR, USA.

ABSTRACT
Adult neurogenesis, generation of new functional cells in the mature central nervous system (CNS), has been documented in a number of diverse organisms, ranging from humans to invertebrates. However, the origin and evolution of this phenomenon is still poorly understood for many of the key phylogenetic groups. Echinoderms are one such phylum, positioned as a sister group to chordates within the monophyletic clade Deuterostomia. They are well known for the ability of their adult organs, including the CNS, to completely regenerate after injury. Nothing is known, however, about production of new cells in the nervous tissue under normal physiological conditions in these animals. In this study, we show that new cells are continuously generated in the mature radial nerve cord (RNC) of the sea cucumber Holothuria glaberrima. Importantly, this neurogenic activity is not evenly distributed, but is significantly more extensive in the lateral regions of the RNC than along the midline. Some of the new cells generated in the apical region of the ectoneural neuroepithelium leave their place of origin and migrate basally to populate the neural parenchyma. Gene expression analysis showed that generation of new cells in the adult sea cucumber CNS is associated with transcriptional activity of genes known to be involved in regulation of various aspects of neurogenesis in other animals. Further analysis of one of those genes, the transcription factor Myc, showed that it is expressed, in some, but not all radial glial cells, suggesting heterogeneity of this CNS progenitor cell population in echinoderms.

No MeSH data available.


Related in: MedlinePlus