An enteroendocrine cell-enteric glia connection revealed by 3D electron microscopy.

The enteroendocrine cell is the cornerstone of gastrointestinal chemosensation. In the intestine and colon, this cell is stimulated by nutrients, tastants that elicit the perception of flavor, and bacterial by-products; and in response, the cell secretes hormones like cholecystokinin and peptide YY-...

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Main Authors: Diego V Bohórquez, Leigh A Samsa, Andrew Roholt, Satish Medicetty, Rashmi Chandra, Rodger A Liddle
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0089881&type=printable
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author Diego V Bohórquez
Leigh A Samsa
Andrew Roholt
Satish Medicetty
Rashmi Chandra
Rodger A Liddle
author_facet Diego V Bohórquez
Leigh A Samsa
Andrew Roholt
Satish Medicetty
Rashmi Chandra
Rodger A Liddle
author_sort Diego V Bohórquez
collection DOAJ
description The enteroendocrine cell is the cornerstone of gastrointestinal chemosensation. In the intestine and colon, this cell is stimulated by nutrients, tastants that elicit the perception of flavor, and bacterial by-products; and in response, the cell secretes hormones like cholecystokinin and peptide YY--both potent regulators of appetite. The development of transgenic mice with enteroendocrine cells expressing green fluorescent protein has allowed for the elucidation of the apical nutrient sensing mechanisms of the cell. However, the basal secretory aspects of the enteroendocrine cell remain largely unexplored, particularly because a complete account of the enteroendocrine cell ultrastructure does not exist. Today, the fine ultrastructure of a specific cell can be revealed in the third dimension thanks to the invention of serial block face scanning electron microscopy (SBEM). Here, we bridged confocal microscopy with SBEM to identify the enteroendocrine cell of the mouse and study its ultrastructure in the third dimension. The results demonstrated that 73.5% of the peptide-secreting vesicles in the enteroendocrine cell are contained within an axon-like basal process. We called this process a neuropod. This neuropod contains neurofilaments, which are typical structural proteins of axons. Surprisingly, the SBEM data also demonstrated that the enteroendocrine cell neuropod is escorted by enteric glia--the cells that nurture enteric neurons. We extended these structural findings into an in vitro intestinal organoid system, in which the addition of glial derived neurotrophic factors enhanced the development of neuropods in enteroendocrine cells. These findings open a new avenue of exploration in gastrointestinal chemosensation by unveiling an unforeseen physical relationship between enteric glia and enteroendocrine cells.
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spelling doaj.art-a02bd581ad2d4ee7818649df908e98cc2025-02-21T05:37:36ZengPublic Library of Science (PLoS)PLoS ONE1932-62032014-01-0192e8988110.1371/journal.pone.0089881An enteroendocrine cell-enteric glia connection revealed by 3D electron microscopy.Diego V BohórquezLeigh A SamsaAndrew RoholtSatish MedicettyRashmi ChandraRodger A LiddleThe enteroendocrine cell is the cornerstone of gastrointestinal chemosensation. In the intestine and colon, this cell is stimulated by nutrients, tastants that elicit the perception of flavor, and bacterial by-products; and in response, the cell secretes hormones like cholecystokinin and peptide YY--both potent regulators of appetite. The development of transgenic mice with enteroendocrine cells expressing green fluorescent protein has allowed for the elucidation of the apical nutrient sensing mechanisms of the cell. However, the basal secretory aspects of the enteroendocrine cell remain largely unexplored, particularly because a complete account of the enteroendocrine cell ultrastructure does not exist. Today, the fine ultrastructure of a specific cell can be revealed in the third dimension thanks to the invention of serial block face scanning electron microscopy (SBEM). Here, we bridged confocal microscopy with SBEM to identify the enteroendocrine cell of the mouse and study its ultrastructure in the third dimension. The results demonstrated that 73.5% of the peptide-secreting vesicles in the enteroendocrine cell are contained within an axon-like basal process. We called this process a neuropod. This neuropod contains neurofilaments, which are typical structural proteins of axons. Surprisingly, the SBEM data also demonstrated that the enteroendocrine cell neuropod is escorted by enteric glia--the cells that nurture enteric neurons. We extended these structural findings into an in vitro intestinal organoid system, in which the addition of glial derived neurotrophic factors enhanced the development of neuropods in enteroendocrine cells. These findings open a new avenue of exploration in gastrointestinal chemosensation by unveiling an unforeseen physical relationship between enteric glia and enteroendocrine cells.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0089881&type=printable
spellingShingle Diego V Bohórquez
Leigh A Samsa
Andrew Roholt
Satish Medicetty
Rashmi Chandra
Rodger A Liddle
An enteroendocrine cell-enteric glia connection revealed by 3D electron microscopy.
PLoS ONE
title An enteroendocrine cell-enteric glia connection revealed by 3D electron microscopy.
title_full An enteroendocrine cell-enteric glia connection revealed by 3D electron microscopy.
title_fullStr An enteroendocrine cell-enteric glia connection revealed by 3D electron microscopy.
title_full_unstemmed An enteroendocrine cell-enteric glia connection revealed by 3D electron microscopy.
title_short An enteroendocrine cell-enteric glia connection revealed by 3D electron microscopy.
title_sort enteroendocrine cell enteric glia connection revealed by 3d electron microscopy
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0089881&type=printable
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