LIN28A-dependent lncRNA NEAT1 aggravates sepsis-induced acute respiratory distress syndrome through destabilizing ACE2 mRNA by RNA methylation

J Transl Med. 2025 Jan 6;23(1):15. doi: 10.1186/s12967-024-06032-7.

Abstract

Background: Acute respiratory distress syndrome (ARDS) is a life-threatening and heterogeneous disorder leading to lung injury. To date, effective therapies for ARDS remain limited. Sepsis is a frequent inducer of ARDS. However, the precise mechanisms underlying sepsis-induced ARDS remain unclear.

Methods: Here RNA methylation was detected by methylated RNA immunoprecipitation (MeRIP), RNA stability was determined by RNA decay assay while RNA antisense purification (RAP) was used to identify RNA-protein interaction. Besides, co-immunoprecipitation (Co-IP) was utilized to detect protein-protein interaction. Moreover, mice were injected with lipopolysaccharide (LPS) to establish sepsis-induced ARDS model in vivo.

Results: This study revealed that long non-coding RNA (lncRNA) nuclear-enriched abundant transcript 1 (NEAT1) aggravated lung injury through suppressing angiotensin-converting enzyme 2 (ACE2) in sepsis-induced ARDS models in vitro and in vivo. Mechanistically, NEAT1 declined ACE2 mRNA stability through heterogeneous nuclear ribonucleoprotein A2/B1 (hnRNPA2B1) in lipopolysaccharide (LPS)-treated alveolar type II epithelial cells (AT-II cells). Besides, NEAT1 destabilized ACE2 mRNA depending on RNA methylation by forming methylated NEAT1/hnRNPA2B1/ACE2 mRNA complex in LPS-treated AT-II cells. Moreover, lin-28 homolog A (LIN28A) improved NEAT1 stability whereas insulin-like growth factor 2 mRNA binding protein 3 (IGF2BP3) augmented NEAT1 destabilization by associating with LIN28A to disrupt the combination of LIN28A and NEAT1 in LPS-treated AT-II cells. Nevertheless, hnRNPA2B1 increased NEAT1 stability by blocking the interaction between LIN28A and IGF2BP3 in LPS-treated AT-II cells.

Conclusions: These findings uncover mechanisms of sepsis-triggering ARDS and provide promising therapeutic targets for sepsis-induced ARDS.

Keywords: ACE2; Acute respiratory distress syndrome; NEAT1; RNA methylation; RNA stability; Sepsis.

MeSH terms

  • Angiotensin-Converting Enzyme 2* / genetics
  • Angiotensin-Converting Enzyme 2* / metabolism
  • Animals
  • Humans
  • Lipopolysaccharides* / pharmacology
  • Male
  • Methylation
  • Mice
  • Mice, Inbred C57BL
  • Peptidyl-Dipeptidase A / genetics
  • Peptidyl-Dipeptidase A / metabolism
  • RNA Methylation
  • RNA Stability* / genetics
  • RNA, Long Noncoding* / genetics
  • RNA, Long Noncoding* / metabolism
  • RNA, Messenger* / genetics
  • RNA, Messenger* / metabolism
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Respiratory Distress Syndrome* / genetics
  • Respiratory Distress Syndrome* / metabolism
  • Respiratory Distress Syndrome* / pathology
  • Sepsis* / complications
  • Sepsis* / genetics
  • Sepsis* / metabolism

Substances

  • RNA, Long Noncoding
  • RNA, Messenger
  • Lipopolysaccharides
  • Angiotensin-Converting Enzyme 2
  • RNA-Binding Proteins
  • NEAT1 long non-coding RNA, mouse
  • Peptidyl-Dipeptidase A
  • Ace2 protein, mouse