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.

Highlights

  • In recent decades, the notion of the fixed developmental state of the adult central nervous system (CNS) has become an outdated dogma

  • The ectoneural neuroepithelium is the predominant component of the radial nerve cord in sea cucumbers

  • The ability to generate new cells in the adult CNS is widespread in the animal kingdom and has been documented in both vertebrates and invertebrates

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Summary

Introduction

The notion of the fixed developmental state of the adult central nervous system (CNS) has become an outdated dogma. Another important question is whether the ability of the mature CNS to generate new cells under physiological conditions can be harnessed to repair injuries. Neural injuries result in increased proliferation in two continuously active neurogenic zones, the subventricular zone and the hippocampal dentate gyrus, and activate quiescent neural progenitors in other brain regions (Lin and Iacovitti, 2015; Sun, 2015). This response, is not sufficient to fully restore the organization and function of the damaged mammalian CNS. Further comparative studies of post-traumatic and physiological neurogenesis in those models can yield useful insights into how the limited mammalian CNS regeneration can be improved

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