Induction of interleukin 21 receptor expression via enhanced intracellular metabolism in B cells and its relevance to the disease activity in systemic lupus erythematosus

RMD Open. 2024 Dec 31;10(4):e004567. doi: 10.1136/rmdopen-2024-004567.

Abstract

Objective: To elucidate the association between the changes in intracellular metabolism in the early stage of B cell activation and systemic lupus erythematosus (SLE) pathogenesis.

Methods: CD19+ or CD19+CD27- (naïve) cells from the peripheral blood of healthy controls and lupus patients were cultured under different stimuli. The changes in intracellular metabolism and signalling pathways in these cells were evaluated.

Results: Stimulation with CpG (Toll-like receptor 9 (TLR9) ligand) in vitro induced enhanced interleukin 21 (IL-21) receptor expression in CD19+CD27- cells after 24 hours. The addition of IL-21 to the CpG stimulation enhanced the extracellular acidification rate, which indicates glycolysis, within 30 min. IL-21 receptor (IL-21R) expression induced by CpG stimulation was selectively inhibited by 2-deoxy-D-glucose (hexokinase 2 (HK2) inhibitor) and heptelidic acid (glyceraldehyde 3-phosphate dehydrogenase (GAPDH) inhibitor). RNA immunoprecipitation with anti-GAPDH antibody revealed that CpG stimulation dissociated the binding between IL-21R messenger RNA (mRNA) and GAPDH under no stimulation. HK2 and GAPDH expression were higher in CD19+CD27- cells of lupus patients than in those of healthy controls, and GAPDH expression was correlated with the plasmocyte count and disease activity score.

Conclusion: IL-21R mRNA-GAPDH binding dissociation associated with rapid glycolytic enhancement by the TLR9 ligand in B cells may induce plasmocyte differentiation through IL-21 signals and be involved in exacerbating SLE.

Keywords: Autoimmune Diseases; Immune System Diseases; Lupus Erythematosus, Systemic.

MeSH terms

  • Adult
  • B-Lymphocytes* / immunology
  • B-Lymphocytes* / metabolism
  • Case-Control Studies
  • Cells, Cultured
  • Female
  • Gene Expression Regulation
  • Glycolysis
  • Humans
  • Interleukins
  • Lupus Erythematosus, Systemic* / immunology
  • Lupus Erythematosus, Systemic* / metabolism
  • Lymphocyte Activation / immunology
  • Male
  • Middle Aged
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptors, Interleukin-21* / genetics
  • Receptors, Interleukin-21* / metabolism
  • Signal Transduction
  • Toll-Like Receptor 9 / metabolism

Substances

  • Receptors, Interleukin-21
  • Toll-Like Receptor 9
  • interleukin-21
  • RNA, Messenger
  • Interleukins