Neuronal and nonneuronal cholinergic structures in the mouse gastrointestinal tract and spleen

Laurent Gautron, Joseph M. Rutkowski, Michael D. Burton, Wei Wei, Yihong Wan, Joel K. Elmquist

Research output: Contribution to journalArticle

61 Citations (Scopus)

Abstract

Accumulating evidence demonstrates that acetylcholine can directly modulate immune function in peripheral tissues including the spleen and gastrointestinal tract. However, the anatomical relationships between the peripheral cholinergic system and immune cells located in these lymphoid tissues remain unclear due to inherent technical difficulties with currently available neuroanatomical methods. In this study, mice with specific expression of the tdTomato fluorescent protein in choline acetyltransferase (ChAT)-expressing cells were used to label preganglionic and postganglionic cholinergic neurons and their projections to lymphoid tissues. Notably, our anatomical observations revealed an abundant innervation in the intestinal lamina propria of the entire gastrointestinal tract principally originating from cholinergic enteric neurons. The aforementioned innervation frequently approached macrophages, plasma cells, and lymphocytes located in the lamina propria and, to a lesser extent, lymphocytes in the interfollicular areas of Peyer's patches. In addition to the above innervation, we observed labeled epithelial cells in the gallbladder and lower intestines, as well as Microfold cells and T-cells within Peyer's patches. In contrast, we found only a sparse innervation in the spleen consisting of neuronal fibers of spinal origin present around arterioles and in lymphocyte-containing areas of the white pulp. Lastly, a small population of ChAT-expressing lymphocytes was identified in the spleen including both Tand B-cells. In summary, this study describes the variety of cholinergic neuronal and nonneuronal cells in a position to modulate gastrointestinal and splenic immunity in the mouse.

Original languageEnglish (US)
Pages (from-to)3741-3767
Number of pages27
JournalJournal of Comparative Neurology
Volume521
Issue number16
DOIs
StatePublished - 2013

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Cholinergic Agents
Gastrointestinal Tract
Spleen
Lymphocytes
Peyer's Patches
Cholinergic Neurons
Choline O-Acetyltransferase
Lymphoid Tissue
Mucous Membrane
Arterioles
Plasma Cells
Gallbladder
Acetylcholine
Intestines
Immune System
Immunity
B-Lymphocytes
Epithelial Cells
Macrophages
T-Lymphocytes

Keywords

  • Anterograde tracing
  • Enteric
  • Genetic
  • Immunity
  • Parasympathetic

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Neuronal and nonneuronal cholinergic structures in the mouse gastrointestinal tract and spleen. / Gautron, Laurent; Rutkowski, Joseph M.; Burton, Michael D.; Wei, Wei; Wan, Yihong; Elmquist, Joel K.

In: Journal of Comparative Neurology, Vol. 521, No. 16, 2013, p. 3741-3767.

Research output: Contribution to journalArticle

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