Acute stress disrupts intestinal homeostasis via GDNF-RET

Cell Prolif. 2020 Oct;53(10):e12889. doi: 10.1111/cpr.12889. Epub 2020 Aug 17.

Abstract

Objectives: Enterochromaffin (EC) cells have been associated with functional gastrointestinal disorders such as IBS. Recently, we found that glial cell-derived neurotrophic factor (GDNF)-rearranged during transfection (RET) localized in EC cells in human colonic epithelia. Here, we examine the role of GDNF-RET in the pathophysiology of diarrhoea-predominant irritable bowel syndrome (IBS-D).

Materials and methods: GDNF was assessed by ELISA and immunohistochemistry in biopsies from IBS-D patients and healthy controls. Stress was induced by using a wrap-restraint stress (WRS) procedure to serve as an acute stress-induced IBS model. The function of GDNF-RET axis to intestinal stem cell (ISC) homeostasis, and EC cell numbers were assessed in vivo and in vitro.

Results: GDNF-RET was expressed in EC cells in human colon. GDNF was significantly increased in IBS-D patients. WRS mice showed increased GDNF-RET levels in colon. WRS induced visceral hypersensitivity by expanding of ISC and differentiation of EC cell via GDNF-RET. Furthermore, GDNF-treated mice recapitulated the phenotype of WRS mice. In vitro, GDNF treatment amplified Wnt signal and increased serotonin levels in colonic organoids in a dose-dependent manner.

Conclusions: We identified GDNF-RET was presented in colonic epithelium of patients with IBS-D. GDNF-RET played important roles in regulating ISC and EC cell differentiation. Our findings, thus, provide RET inhibitor as new therapeutic targets for treatment of patients with IBS-D.

Keywords: enterochromaffin cell; intestinal stem cell niche; neurotrophic factor; visceral hypersensitivity.

MeSH terms

  • Adult
  • Animals
  • Enterochromaffin Cells / metabolism
  • Enterochromaffin Cells / pathology
  • Female
  • Glial Cell Line-Derived Neurotrophic Factor / metabolism*
  • Homeostasis
  • Humans
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / pathology
  • Intestines / physiopathology*
  • Irritable Bowel Syndrome / metabolism
  • Irritable Bowel Syndrome / pathology
  • Irritable Bowel Syndrome / physiopathology*
  • Male
  • Mice, Inbred C57BL
  • Middle Aged
  • Proto-Oncogene Proteins c-ret / metabolism*
  • Stress, Physiological

Substances

  • Glial Cell Line-Derived Neurotrophic Factor
  • Proto-Oncogene Proteins c-ret
  • RET protein, human
  • Ret protein, mouse