β-Arrestin1-mediated decrease in endoplasmic reticulum stress impairs intestinal stem cell proliferation following radiation

FASEB J. 2019 Sep;33(9):10165-10176. doi: 10.1096/fj.201900376RRR. Epub 2019 Jun 19.

Abstract

Gastrointestinal toxicity limits the clinical application of abdominal and pelvic radiotherapy and currently has no effective treatment. Intestinal leucine-rich-repeat-containing GPCR 5 (Lgr5)-positive stem cell depletion and loss of proliferative ability due to radiation may be the primary factors causing intestinal injury following radiation. Here, we report the critical role of β-arrestin1 (βarr1) in radiation-induced intestinal injury. Intestinal βarr1 was highly expressed in radiation enteritis and in a radiation model. βarr1 knockout (KO) or knockdown mice exhibited increased proliferation in intestinal Lgr5+ stem cell, crypt reproduction, and survival following radiation. Unexpectedly, the beneficial effects of βarr1 deficiency on intestinal stem cells in response to radiation were compromised when the endoplasmic reticulum stress-related protein kinase RNA-like ER kinase (PERK)/eukaryotic initiation factor-2α (eIF2α) pathway was inhibited, and this result was further supported in vitro. Furthermore, we found that βarr1 knockdown with small interfering RNA significantly enhanced intestinal Lgr5+ stem cell proliferation after radiation via directly targeting PERK. βarr1 offers a promising target for mitigating radiation-induced intestinal injury.-Liu, Z., Jiang, J., He, Q., Liu, Z., Yang, Z., Xu, J., Huang, Z., Wu, B. β-Arrestin1-mediated decrease in endoplasmic reticulum stress impairs intestinal stem cell proliferation following radiation.

Keywords: PERK; intestinal injury; intestinal stem/progenitor cell.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Animals
  • Cell Division / radiation effects
  • Colony-Forming Units Assay
  • Endoplasmic Reticulum Stress / physiology*
  • Enteritis / etiology
  • Enteritis / pathology*
  • Enteritis / physiopathology
  • Eukaryotic Initiation Factor-2 / physiology
  • Female
  • Gene Knockdown Techniques
  • Humans
  • Intestines / radiation effects*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Middle Aged
  • RNA Interference
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / pharmacology
  • Radiation Chimera
  • Radiation Injuries / pathology*
  • Radiation Injuries / physiopathology
  • Radiation Injuries, Experimental / pathology*
  • Radiation Injuries, Experimental / physiopathology
  • Radiotherapy / adverse effects
  • Receptors, G-Protein-Coupled / analysis
  • Regeneration
  • Signal Transduction / physiology
  • Stem Cells / pathology
  • Stem Cells / radiation effects*
  • beta-Arrestin 1 / deficiency
  • beta-Arrestin 1 / genetics
  • beta-Arrestin 1 / physiology*
  • eIF-2 Kinase / physiology*

Substances

  • Eukaryotic Initiation Factor-2
  • Lgr5 protein, mouse
  • RNA, Small Interfering
  • Receptors, G-Protein-Coupled
  • beta-Arrestin 1
  • PERK kinase
  • eIF-2 Kinase