Long non-coding RNA X-inactive specific transcript silencing ameliorates primary graft dysfunction following lung transplantation through microRNA-21-dependent mechanism

EBioMedicine. 2020 Feb:52:102600. doi: 10.1016/j.ebiom.2019.102600. Epub 2020 Jan 22.

Abstract

Background: Primary graft dysfunction (PGD) is a known acute lung injury (ALI) and a major cause of fatality post-lung transplantation. Though some long non-coding RNAs (lncRNAs) have been studied in ALI through regulation of microRNAs (miRNAs), their effects on PGD remain undefined. The present study aims to explore the underlying mechanism of lncRNA X-inactive specific transcript (XIST) in PGD after lung transplantation.

Methods: Initially, the expression of miR-21, IL-12A and XIST was determined by RT-qPCR and western blot analysis. The dual luciferase reporter assay, RNA pull-down and RIP assay were performed to identify the targeting relationship between miR-21 and IL-12A and the binding relationship between miR-21 and XIST. Loss- and gain-of-function investigations were conducted in rats treated with prolonged cold ischemia and polymorphonuclear neutrophils (PMNs).

Findings: miR-21 was decreased, whilst XIST and IL-12A were increased in the bronchoalveolar lavage fluid of PGD patients after lung transplantation. Enhanced miR-21 expression in rats and PMNs resulted in downregulated expression of pro-inflammatory factors and chemokines, and enhanced the apoptosis of PMNs. XIST was found to upregulate IL-12A expression in a miR-21-dependent manner. Additionally, XIST silencing enhanced the apoptosis of PMNs and inhibited the neutrophil extracellular trap (NET) formation through upregulation of miR-21 but downregulation of IL-12A in vivo.

Interpretation: In summary, lncRNA XIST upregulates IL-12A by binding to miR-21, thereby inducing NET formation and accelerating PGD after lung transplantation. This suggests that inhibition of XIST and NET may be beneficial for the treatment of PGD.

Keywords: Competing endogenous RNA; Interleukin-12A; Long non-coding RNA; MicroRNA-21; Neutrophil extracellular trap; Primary graft dysfunction; X-inactive specific transcript.

MeSH terms

  • 3' Untranslated Regions
  • Animals
  • Biomarkers
  • Biopsy
  • Extracellular Traps / genetics
  • Gene Expression Regulation
  • Gene Silencing*
  • Humans
  • Immunohistochemistry
  • Interleukin-12 Subunit p35 / genetics
  • Lung Transplantation* / adverse effects
  • Lung Transplantation* / methods
  • MicroRNAs / genetics*
  • Models, Animal
  • Primary Graft Dysfunction / etiology*
  • RNA Interference*
  • RNA, Long Noncoding / genetics*
  • RNA, Messenger
  • Rats
  • Transplantation, Homologous

Substances

  • 3' Untranslated Regions
  • Biomarkers
  • Interleukin-12 Subunit p35
  • MIRN21 microRNA, human
  • MicroRNAs
  • RNA, Long Noncoding
  • RNA, Messenger
  • XIST non-coding RNA
  • mirn21 microRNA, rat