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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

Representative micrographs showing distribution of BrdU-positive cells in the ectoneural epithelium of the RNC sampled immediately after the last BrdU injection (A,A′) and after 8 weeks (B,B′). (A,B) show labeling with the anti-BrdU antibody in a single channel. (A′,B′) are corresponding multichannel composite micrographs, which, besides BrdU labeling, also include nuclei labeled with propidium iodide (PI) and differential interference contrast (DIC) image of the RNC. Sampling areas for cell counting are marked with dashed lines. Along the left-right axis, the RNC was divided into five columns of equal width. Each column was then subdivided into the apical (A) and basal (B) parts corresponding the the zones of dense cell body accumulation and neural parenchyma, respectively.
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Figure 2: Representative micrographs showing distribution of BrdU-positive cells in the ectoneural epithelium of the RNC sampled immediately after the last BrdU injection (A,A′) and after 8 weeks (B,B′). (A,B) show labeling with the anti-BrdU antibody in a single channel. (A′,B′) are corresponding multichannel composite micrographs, which, besides BrdU labeling, also include nuclei labeled with propidium iodide (PI) and differential interference contrast (DIC) image of the RNC. Sampling areas for cell counting are marked with dashed lines. Along the left-right axis, the RNC was divided into five columns of equal width. Each column was then subdivided into the apical (A) and basal (B) parts corresponding the the zones of dense cell body accumulation and neural parenchyma, respectively.

Mentions: Immunostained cryosections were photographed with a Nikon Eclipse 600 microscope equipped with a SPOT RT3 camera (Diagnostic Instruments, Inc.) using a 40 × objective. The acquired images were assembled into panoramic multichannel composite micrographs using the stitching plugin (Preibisch et al., 2009) in Fiji image analysis software (Schindelin et al., 2012). The cross section area of the ectoneural part of the RNC was divided into ten sampling areas as follows. The width of the RNC was divided into five areas of equal width from left to right. Each of these five areas was further subdivided into the apical zone containing dense accumulation of cell bodies and the basal zone, which included the neural parenchyma (Figures 1, 2). All clearly BrdU-labeled cells (strongly and moderately stained) were counted on every third cross-section, five sections per animal, using the Cell Counter plugin in Fiji. The total number of BrdU+-cells was divided by the total area of the corresponding sampling region to calculate the of BrdU+-cell density (Additional File 1).


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

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

Representative micrographs showing distribution of BrdU-positive cells in the ectoneural epithelium of the RNC sampled immediately after the last BrdU injection (A,A′) and after 8 weeks (B,B′). (A,B) show labeling with the anti-BrdU antibody in a single channel. (A′,B′) are corresponding multichannel composite micrographs, which, besides BrdU labeling, also include nuclei labeled with propidium iodide (PI) and differential interference contrast (DIC) image of the RNC. Sampling areas for cell counting are marked with dashed lines. Along the left-right axis, the RNC was divided into five columns of equal width. Each column was then subdivided into the apical (A) and basal (B) parts corresponding the the zones of dense cell body accumulation and neural parenchyma, respectively.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4585025&req=5

Figure 2: Representative micrographs showing distribution of BrdU-positive cells in the ectoneural epithelium of the RNC sampled immediately after the last BrdU injection (A,A′) and after 8 weeks (B,B′). (A,B) show labeling with the anti-BrdU antibody in a single channel. (A′,B′) are corresponding multichannel composite micrographs, which, besides BrdU labeling, also include nuclei labeled with propidium iodide (PI) and differential interference contrast (DIC) image of the RNC. Sampling areas for cell counting are marked with dashed lines. Along the left-right axis, the RNC was divided into five columns of equal width. Each column was then subdivided into the apical (A) and basal (B) parts corresponding the the zones of dense cell body accumulation and neural parenchyma, respectively.
Mentions: Immunostained cryosections were photographed with a Nikon Eclipse 600 microscope equipped with a SPOT RT3 camera (Diagnostic Instruments, Inc.) using a 40 × objective. The acquired images were assembled into panoramic multichannel composite micrographs using the stitching plugin (Preibisch et al., 2009) in Fiji image analysis software (Schindelin et al., 2012). The cross section area of the ectoneural part of the RNC was divided into ten sampling areas as follows. The width of the RNC was divided into five areas of equal width from left to right. Each of these five areas was further subdivided into the apical zone containing dense accumulation of cell bodies and the basal zone, which included the neural parenchyma (Figures 1, 2). All clearly BrdU-labeled cells (strongly and moderately stained) were counted on every third cross-section, five sections per animal, using the Cell Counter plugin in Fiji. The total number of BrdU+-cells was divided by the total area of the corresponding sampling region to calculate the of BrdU+-cell density (Additional File 1).

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