Presence of intramucosal neuroglial cells in normal and aganglionic human colon

Am J Physiol Gastrointest Liver Physiol. 2014 Nov 15;307(10):G1002-12. doi: 10.1152/ajpgi.00164.2014. Epub 2014 Sep 11.

Abstract

The enteric nervous system (ENS) is composed of neural crest-derived neurons (also known as ganglion cells) the cell bodies of which are located in the submucosal and myenteric plexuses of the intestinal wall. Intramucosal ganglion cells are known to exist but are rare and often considered ectopic. Also derived from the neural crest are enteric glial cells that populate the ganglia and the associated nerves, as well as the lamina propria of the intestinal mucosa. In Hirschsprung disease (HSCR), ganglion cells are absent from the distal gut because of a failure of neural crest-derived progenitor cells to complete their rostrocaudal migration during embryogenesis. The fate of intramucosal glial cells in human HSCR is essentially unknown. We demonstrate a network of intramucosal cells that exhibit dendritic morphology typical of neurons and glial cells. These dendritic cells are present throughout the human gut and express Tuj1, S100, glial fibrillary acidic protein, CD56, synaptophysin, and calretinin, consistent with mixed or overlapping neuroglial differentiation. The cells are present in aganglionic colon from patients with HSCR, but with an altered immunophenotype. Coexpression of Tuj1 and HNK1 in this cell population supports a neural crest origin. These findings extend and challenge the current understanding of ENS microanatomy and suggest the existence of an intramucosal population of neural crest-derived cells, present in HSCR, with overlapping immunophenotype of neurons and glia. Intramucosal neuroglial cells have not been previously recognized, and their presence in HSCR poses new questions about ENS development and the pathobiology of HSCR that merit further investigation.

Keywords: Hirschsprung disease; enteric glial cells; enteric nervous system.

MeSH terms

  • Biomarkers / analysis
  • CD56 Antigen / analysis
  • CD57 Antigens / analysis
  • Calbindin 2 / analysis
  • Case-Control Studies
  • Cell Differentiation
  • Cell Lineage
  • Cell Shape
  • Colon / chemistry
  • Colon / pathology*
  • Glial Fibrillary Acidic Protein / analysis
  • Hirschsprung Disease / metabolism
  • Hirschsprung Disease / pathology*
  • Humans
  • Intestinal Mucosa / chemistry
  • Intestinal Mucosa / pathology*
  • Neuroglia / chemistry
  • Neuroglia / pathology*
  • S100 Proteins / analysis
  • Synaptophysin / analysis
  • Tubulin / analysis

Substances

  • Biomarkers
  • CALB2 protein, human
  • CD56 Antigen
  • CD57 Antigens
  • Calbindin 2
  • Glial Fibrillary Acidic Protein
  • NCAM1 protein, human
  • S100 Proteins
  • SYP protein, human
  • Synaptophysin
  • TUBB3 protein, human
  • Tubulin