Postnatal maturation of mouse medullo-spinal cerebrospinal fluid-contacting neurons

Neuroscience. 2017 Feb 20:343:39-54. doi: 10.1016/j.neuroscience.2016.11.028. Epub 2016 Dec 7.

Abstract

The central canal along the spinal cord (SC.) and medulla is characterized by the presence of a specific population of neurons that contacts the cerebrospinal fluid (CSF). These medullo-spinal CSF-contacting neurons (CSF-cNs) are identified by the selective expression of the polycystin kidney disease 2-like 1 ionic channel (PKD2L1 or polycystin-L). In adult, they have been shown to express doublecortin (DCX) and Nkx6.1, two markers of juvenile neurons along with the neuron-specific nuclear protein (NeuN) typically expressed in mature neurons. They were therefore suggested to remain in a rather incomplete maturation state. The aim of this study was to assess whether such juvenile state is stable in postnatal animals or whether CSF-cNs may reach maturity at older stages than neurons in the parenchyma. We show, in the cervical SC. and the brainstem that, in relation to age, CSF-cN density declines and that their cell bodies become more distant from the cc, except in its ventral part. Moreover, in adults (from 1month) by comparison with neonatal mice, we show that CSF-cNs have evolved to a more mature state, as indicated by the increase in the percentage of cells positive for NeuN and of its level of expression. In parallel, CSF-cNs exhibit, in adult, lower DCX immunoreactivity and do not express PSA-NCAM and TUC4, two neurogenic markers. Nevertheless, CSF-cNs still share in adult characteristics of juvenile neurons such as the presence of phospho-CREB and DCX while NeuN expression remained low. This phenotype persists in 12-month-old animals. Thus, despite a pursuit of neuronal maturation during the postnatal period, CSF-cNs retain a durable low differentiated state.

Keywords: CSF-contacting neurons; PKD2L1; brainstem; central canal; cervical spinal cord; maturity markers.

MeSH terms

  • Aging / pathology
  • Aging / physiology
  • Animals
  • Animals, Newborn
  • Cell Count
  • Cervical Cord / cytology
  • Cervical Cord / growth & development*
  • Cervical Cord / physiology
  • DNA-Binding Proteins
  • Doublecortin Domain Proteins
  • Doublecortin Protein
  • Female
  • Fluorescent Antibody Technique
  • Male
  • Medulla Oblongata / cytology
  • Medulla Oblongata / growth & development*
  • Medulla Oblongata / physiology
  • Mice, Transgenic
  • Microtubule-Associated Proteins / metabolism
  • Nerve Tissue Proteins / metabolism
  • Neural Cell Adhesion Molecule L1 / metabolism
  • Neurons / cytology*
  • Neurons / physiology
  • Neuropeptides / metabolism
  • Nuclear Proteins / metabolism
  • Prosencephalon / cytology
  • Prosencephalon / growth & development*
  • Prosencephalon / physiology
  • Sialic Acids / metabolism

Substances

  • DNA-Binding Proteins
  • Dcx protein, mouse
  • Doublecortin Domain Proteins
  • Doublecortin Protein
  • Microtubule-Associated Proteins
  • Nerve Tissue Proteins
  • NeuN protein, mouse
  • Neural Cell Adhesion Molecule L1
  • Neuropeptides
  • Nuclear Proteins
  • Sialic Acids
  • polysialyl neural cell adhesion molecule