The Human and Mouse Enteric Nervous System at Single-Cell Resolution

Cell. 2020 Sep 17;182(6):1606-1622.e23. doi: 10.1016/j.cell.2020.08.003. Epub 2020 Sep 3.

Abstract

The enteric nervous system (ENS) coordinates diverse functions in the intestine but has eluded comprehensive molecular characterization because of the rarity and diversity of cells. Here we develop two methods to profile the ENS of adult mice and humans at single-cell resolution: RAISIN RNA-seq for profiling intact nuclei with ribosome-bound mRNA and MIRACL-seq for label-free enrichment of rare cell types by droplet-based profiling. The 1,187,535 nuclei in our mouse atlas include 5,068 neurons from the ileum and colon, revealing extraordinary neuron diversity. We highlight circadian expression changes in enteric neurons, show that disease-related genes are dysregulated with aging, and identify differences between the ileum and proximal/distal colon. In humans, we profile 436,202 nuclei, recovering 1,445 neurons, and identify conserved and species-specific transcriptional programs and putative neuro-epithelial, neuro-stromal, and neuro-immune interactions. The human ENS expresses risk genes for neuropathic, inflammatory, and extra-intestinal diseases, suggesting neuronal contributions to disease.

Keywords: ENS; GWAS; aging; circadian; colon; enteric nervous system; enteric neuron; ileum; neuro-immune; single cell.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aging / genetics
  • Aging / metabolism
  • Animals
  • Circadian Clocks / genetics
  • Colon / cytology
  • Colon / metabolism
  • Endoplasmic Reticulum, Rough / genetics
  • Endoplasmic Reticulum, Rough / metabolism
  • Endoplasmic Reticulum, Rough / ultrastructure
  • Enteric Nervous System / cytology*
  • Enteric Nervous System / metabolism*
  • Epithelial Cells / metabolism
  • Female
  • Gene Expression Regulation, Developmental / genetics*
  • Genetic Predisposition to Disease / genetics
  • Humans
  • Ileum / cytology
  • Ileum / metabolism
  • Inflammation / genetics
  • Inflammation / metabolism
  • Intestinal Diseases / genetics
  • Intestinal Diseases / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Microscopy, Electron, Transmission
  • Nervous System Diseases / genetics
  • Nervous System Diseases / metabolism
  • Neuroglia / cytology
  • Neuroglia / metabolism
  • Neurons / cytology
  • Neurons / metabolism*
  • Nissl Bodies / genetics
  • Nissl Bodies / metabolism*
  • Nissl Bodies / ultrastructure
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism*
  • RNA-Seq
  • Ribosomes / metabolism
  • Ribosomes / ultrastructure
  • Single-Cell Analysis / methods*
  • Stromal Cells / metabolism

Substances

  • RNA, Messenger