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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

Quantification of newly born cells in the ectoneural epithelium fo the RNC. (A) Lateral regions of the RNC have significantly higher density of BrdU+ cells than the mid-line regions. Notched box and whisker plots. Boxes show the interquartile range (the values between the 25 and 75% percentiles), the line within the box is the median of the data, and the whiskers represent adjacent values within the 1.5 × interquartile range outside the box. (B,B′) Box and whisker plot showing density of BrdU+ cells in the apical (B) and basal(B′) regions of the ectoneural neuroepithelium of the RNC as a function of the length of time after the last BrdU injection. (C,C′) Box and whisker plots showing comparison of density of BrdU-labeled cells between the apical and basal regions of the RNC immediately after the last BrdU injection (C) and after 8 weeks (C′).*P < 0.05; **P < 0.01; ***P < 0.001.
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Figure 3: Quantification of newly born cells in the ectoneural epithelium fo the RNC. (A) Lateral regions of the RNC have significantly higher density of BrdU+ cells than the mid-line regions. Notched box and whisker plots. Boxes show the interquartile range (the values between the 25 and 75% percentiles), the line within the box is the median of the data, and the whiskers represent adjacent values within the 1.5 × interquartile range outside the box. (B,B′) Box and whisker plot showing density of BrdU+ cells in the apical (B) and basal(B′) regions of the ectoneural neuroepithelium of the RNC as a function of the length of time after the last BrdU injection. (C,C′) Box and whisker plots showing comparison of density of BrdU-labeled cells between the apical and basal regions of the RNC immediately after the last BrdU injection (C) and after 8 weeks (C′).*P < 0.05; **P < 0.01; ***P < 0.001.

Mentions: Our statistical analysis (Additional File 3) involving generalized linear modeling approach with time, apical-basal position, and left-right position as factors, showed that the density of BrdU+-cells varied significantly (F-test, P = 1.6 × 10−11) along the left-right axis of the ectoneural layer of the radial nerve cord, with the lateral areas (area 1 and area 5) containing significantly more labeled cells per μm2 of cross-sectioned area than the midline area (area 3) (Figure 3A). For example, 8 weeks after the last BrdU injection, the mean density of BrdU-labeled cells in the lateral regions is about 2.4–3 times greater than in the midline region. There was no interaction between the mediolateral position and the other two factors, suggesting that the observed pattern of distribution of BrdU-labeled cells along the left-right axis does not change with time or with position along the apical-basal axis.


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

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

Quantification of newly born cells in the ectoneural epithelium fo the RNC. (A) Lateral regions of the RNC have significantly higher density of BrdU+ cells than the mid-line regions. Notched box and whisker plots. Boxes show the interquartile range (the values between the 25 and 75% percentiles), the line within the box is the median of the data, and the whiskers represent adjacent values within the 1.5 × interquartile range outside the box. (B,B′) Box and whisker plot showing density of BrdU+ cells in the apical (B) and basal(B′) regions of the ectoneural neuroepithelium of the RNC as a function of the length of time after the last BrdU injection. (C,C′) Box and whisker plots showing comparison of density of BrdU-labeled cells between the apical and basal regions of the RNC immediately after the last BrdU injection (C) and after 8 weeks (C′).*P < 0.05; **P < 0.01; ***P < 0.001.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 3: Quantification of newly born cells in the ectoneural epithelium fo the RNC. (A) Lateral regions of the RNC have significantly higher density of BrdU+ cells than the mid-line regions. Notched box and whisker plots. Boxes show the interquartile range (the values between the 25 and 75% percentiles), the line within the box is the median of the data, and the whiskers represent adjacent values within the 1.5 × interquartile range outside the box. (B,B′) Box and whisker plot showing density of BrdU+ cells in the apical (B) and basal(B′) regions of the ectoneural neuroepithelium of the RNC as a function of the length of time after the last BrdU injection. (C,C′) Box and whisker plots showing comparison of density of BrdU-labeled cells between the apical and basal regions of the RNC immediately after the last BrdU injection (C) and after 8 weeks (C′).*P < 0.05; **P < 0.01; ***P < 0.001.
Mentions: Our statistical analysis (Additional File 3) involving generalized linear modeling approach with time, apical-basal position, and left-right position as factors, showed that the density of BrdU+-cells varied significantly (F-test, P = 1.6 × 10−11) along the left-right axis of the ectoneural layer of the radial nerve cord, with the lateral areas (area 1 and area 5) containing significantly more labeled cells per μm2 of cross-sectioned area than the midline area (area 3) (Figure 3A). For example, 8 weeks after the last BrdU injection, the mean density of BrdU-labeled cells in the lateral regions is about 2.4–3 times greater than in the midline region. There was no interaction between the mediolateral position and the other two factors, suggesting that the observed pattern of distribution of BrdU-labeled cells along the left-right axis does not change with time or with position along the apical-basal axis.

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