Frontiers in Neuroanatomy (May 2014)

Investigation of spinal cerebrospinal fluid-contacting neurons expressing PKD2L1: evidence for a conserved system from fish to primates

  • Lydia eDjenoune,
  • Lydia eDjenoune,
  • Lydia eDjenoune,
  • Lydia eDjenoune,
  • Lydia eDjenoune,
  • Lydia eDjenoune,
  • Hanen eKhabou,
  • Hanen eKhabou,
  • Hanen eKhabou,
  • Hanen eKhabou,
  • Fanny eJoubert,
  • Fanny eJoubert,
  • Feng B. Quan,
  • Feng B. Quan,
  • Sophie eNunes Figueiredo,
  • Sophie eNunes Figueiredo,
  • Sophie eNunes Figueiredo,
  • Sophie eNunes Figueiredo,
  • Laurence eBodineau,
  • Laurence eBodineau,
  • Filippo eDel Bene,
  • Filippo eDel Bene,
  • Filippo eDel Bene,
  • Céline eBurcklé,
  • Céline eBurcklé,
  • Céline eBurcklé,
  • Céline eBurcklé,
  • Céline eBurcklé,
  • Hervé eTostivint,
  • Hervé eTostivint,
  • Claire eWyart,
  • Claire eWyart,
  • Claire eWyart,
  • Claire eWyart

DOI
https://doi.org/10.3389/fnana.2014.00026
Journal volume & issue
Vol. 8

Abstract

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Over ninety years ago, Kolmer and Agduhr identified spinal cerebrospinal fluid-contacting neurons (CSF-cNs) based on their morphology and location within the spinal cord. In more than two hundred vertebrate species, they observed ciliated neurons around the central canal that extended a brush of microvilli into the cerebrospinal fluid (CSF). Although their morphology is suggestive of a primitive sensory cell, their function within the vertebrate spinal cord remains unknown. The identification of specific molecular markers for these neurons in vertebrates would benefit the investigation of their physiological roles. PKD2L1, a transient receptor potential channel that could play a role as a sensory receptor, has been found in cells contacting the central canal in mouse. In this study, we demonstrate that PKD2L1 is a specific marker for CSF-cNs in the spinal cord of mouse (Mus musculus), macaque (Macaca fascicularis) and zebrafish (Danio rerio). In these species, the somata of spinal PKD2L1+ CSF-cNs were located below or within the ependymal layer and extended an apical bulbous extension into the central canal. We found GABAergic PKD2L1-expressing CSF-cNs in all three species. We took advantage of the zebrafish embryo for its transparency and rapid development to identify the progenitor domains from which pkd2l1+ CSF-cNs originate. pkd2l1+ CSF-cNs were all GABAergic and organized in two rows—one ventral and one dorsal to the central canal. Their location and marker expression is consistent with previously described Kolmer-Agduhr cells. Accordingly, pkd2l1+ CSF-cNs were derived from the progenitor domains p3 and pMN defined by the expression of nkx2.2a and olig2 transcription factors, respectively. Altogether our results suggest that a system of CSF-cNs expressing the PKD2L1 channel is conserved in the spinal cord across bony vertebrate species.

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