Dysregulation of miR-21-associated miRNA regulatory networks by chronic ethanol consumption impairs liver regeneration

Physiol Genomics. 2021 Dec 1;53(12):546-555. doi: 10.1152/physiolgenomics.00113.2021. Epub 2021 Nov 19.

Abstract

Impaired liver regeneration has been considered as a hallmark of progression of alcohol-associated liver disease. Our previous studies demonstrated that in vivo inhibition of the microRNA (miRNA) miR21 can restore regenerative capacity of the liver in chronic ethanol-fed animals. The present study focuses on the role of microRNA regulatory networks that are likely to mediate the miR-21 action. Rats were chronically fed an ethanol-enriched diet along with pair-fed control animals and treated with AM21 (anti-miR-21), a locked nucleic acid antisense to miR-21. Partial hepatectomy (PHx) was performed and miRNA expression profiling over the course of liver regeneration was assessed. Our results showed dynamic expression changes in several miRNAs after PHx, notably with altered miRNA expression profiles between ethanol and control groups. We found that in vivo inhibition of miR-21 led to correlated differential expression of miR-340-5p and anticorrelated expression of miR-365, let-7a, miR-1224, and miR-146a across all sample groups after PHx. Gene set enrichment analysis identified a miRNA signature significantly associated with hepatic stellate cell activation within whole liver tissue data. We hypothesized that at least part of the PHx-induced miRNA network changes responsive to miR-21 inhibition is localized to hepatic stellate cells. We validated this hypothesis using AM21 and TGF-β treatments in LX-2 human hepatic stellate cells in culture and measured expression levels of select miRNAs by quantitative RT-PCR. Based on the in vivo and in vitro results, we propose a hepatic stellate cell miRNA regulatory network as contributing to the restoration of liver regenerative capacity by miR-21 inhibition.

Keywords: alcoholic liver disease; hepatic stellate cells; liver regeneration; microRNA networks.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Alcohol Drinking / adverse effects*
  • Animals
  • Cell Line
  • Diet / methods
  • Disease Models, Animal
  • Ethanol / adverse effects*
  • Gene Regulatory Networks / drug effects*
  • Hepatectomy / methods
  • Hepatic Stellate Cells / metabolism*
  • Humans
  • Liver Diseases, Alcoholic / genetics*
  • Liver Diseases, Alcoholic / surgery
  • Liver Regeneration / genetics*
  • Male
  • MicroRNAs / antagonists & inhibitors
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism*
  • Oligonucleotides / administration & dosage
  • Rats
  • Rats, Sprague-Dawley
  • Signal Transduction / drug effects
  • Signal Transduction / genetics*
  • Transcriptome / drug effects
  • Transcriptome / genetics
  • Transfection
  • Transforming Growth Factor beta / pharmacology

Substances

  • MIRN21 microRNA, human
  • MicroRNAs
  • Oligonucleotides
  • Transforming Growth Factor beta
  • locked nucleic acid
  • mirn21 microRNA, rat
  • Ethanol