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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.
Figure 1. Organization of the radial nerve cord (RNC) in the sea cucumber H. glaberrima. (A) Low magnification overview of a cross section of the body wall showing the position of the radial nerve cord (rnc) relative to other anatomical structures, such as the longitudinal muscle band (lmb), radial canal of the water-vascular system (wvc), and the connective tissue layer of the body wall (ctl). (B) Higher magnification view of the radial nerve cord. Note two parallel bands of nervous tissue, a thicker ectoneural neuroepithelium (en) and a thinner hyponeural epithelium (hn) separated by a thin connective tissue partition. The apical surface of the ectoneural and the hyponeural canals form the bottom of the epineural (ec) and hyponeural (hc) canals, respectively. Paraffin sections; hematoxylin and eosin staining.
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.
Figure 4. Expression of homologs of neural stem/progenitor cell maintenance genes in the adult radial nerve cord (RNC) of H. glaberrima. The left column (A–G) shows reference low magnification micrographs of the entire cross section profile of the RNC. The middle column (A′–G′) is a detailed view of the midline region of the ectoneural neuroepithelium. Micrographs in the right column (A″–G″) are higher magnification of the lateral region of the ectoneural neuroepithelium.
Figure 5. Expression of proglial genes, FoxJ1 (A–A″) and NFI) (B,B′), in the radial nerve cord (RNC) of H. glaberrima. (A,B) show low magnification overview micrographs of the entire cross section profile of the RNC. (A′) is a detailed view of the midline region of the ectoneural neuroepithelium. (A″,B′) show higher magnification views of the lateral region of the ectoneural neuroepithelium.
Figure 6. Expression of proneural genes in the adult radial nerve cord (RNC) of H. glaberrima. The left column (A–G) shows reference low magnification micrographs of the entire cross section profile of the RNC. The middle column (A′–G′) shows a detailed view of the midline region of the ectoneural neuroepithelium. Micrographs in the right column (A″–G″) are higher magnification of the lateral region of the ectoneural neuroepithelium.
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).
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