LncRNA BRE-AS1 regulates the JAK2/STAT3-mediated inflammatory activation via the miR-30b-5p/SOC3 axis in THP-1 cells

Sci Rep. 2024 Oct 28;14(1):25726. doi: 10.1038/s41598-024-77265-1.

Abstract

Long non-coding RNAs (lncRNAs) have emerged as pivotal regulators in numerous biological processes, including macrophage-mediated inflammatory responses, which play a critical role in the progress of diverse diseases. This study focuses on the regulatory function of lncRNA brain and reproductive organ-expressed protein (BRE) antisense RNA 1 (BRE-AS1) in modulating the inflammatory activation of monocytes/macrophages. Employing the THP-1 cell line as a model, we demonstrate that lipopolysaccharide (LPS) treatment significantly upregulates BRE-AS1 expression. Notably, specific knockdown of BRE-AS1 via siRNA transfection enhances LPS-induced expression of interleukin (IL)-6 and IL-1β, while not affecting tumor necrosis factor (TNF)-α levels. This selective augmentation of pro-inflammatory cytokine production coincides with increased phosphorylation of Janus kinase (JAK)2 and signal transducer and activator of transcription (STAT)3. Furthermore, BRE-AS1 suppression results in the downregulation of suppressor of cytokine signaling (SOCS)3, an established inhibitor of the JAK2/STAT3 pathway. Bioinformatics analysis identified binding sites for miR-30b-5p on both BRE-AS1 and SOCS3 mRNA. Intervention with a miR-30b-5p inhibitor and a synthetic RNA fragment that represents the miR-30b-5p binding site on BRE-AS1 attenuates the pro-inflammatory effects of BRE-AS1 knockdown. Conversely, a miR-30b-5p mimic replicated the BRE-AS1 attenuation outcomes. Our findings elucidate the role of lncRNA BRE-AS1 in modulating inflammatory activation in THP-1 cells via the miR-30b-5p/SOCS3/JAK2/STAT3 signaling pathway, proposing that manipulation of macrophage BRE-AS1 activity may offer a novel therapeutic avenue in diseases characterized by macrophage-driven pathogenesis.

Keywords: JAK2; LncRNA; SOCS3; STAT3; miRNA.

MeSH terms

  • Gene Expression Regulation
  • Humans
  • Inflammation* / genetics
  • Inflammation* / metabolism
  • Inflammation* / pathology
  • Janus Kinase 2* / genetics
  • Janus Kinase 2* / metabolism
  • Lipopolysaccharides* / pharmacology
  • Macrophages / metabolism
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • RNA, Antisense
  • RNA, Long Noncoding* / genetics
  • RNA, Long Noncoding* / metabolism
  • STAT3 Transcription Factor* / metabolism
  • Signal Transduction*
  • Suppressor of Cytokine Signaling 3 Protein / genetics
  • Suppressor of Cytokine Signaling 3 Protein / metabolism
  • Suppressor of Cytokine Signaling Proteins / genetics
  • Suppressor of Cytokine Signaling Proteins / metabolism
  • THP-1 Cells

Substances

  • BABAM2 protein, human
  • JAK2 protein, human
  • Janus Kinase 2
  • Lipopolysaccharides
  • MicroRNAs
  • MIRN30b microRNA, human
  • RNA, Long Noncoding
  • SOCS3 protein, human
  • STAT3 protein, human
  • STAT3 Transcription Factor
  • Suppressor of Cytokine Signaling 3 Protein
  • Suppressor of Cytokine Signaling Proteins
  • RNA, Antisense