Interleukin-11 drives fibroblast metabolic reprogramming in crystalline silica-induced lung fibrosis

Sci Total Environ. 2024 Nov 1:949:174976. doi: 10.1016/j.scitotenv.2024.174976. Epub 2024 Jul 22.

Abstract

Environmental exposure to crystalline silica (CS) particles is common and occurs during natural, industrial, and agricultural activities. Prolonged inhalation of CS particles can cause silicosis, a serious and incurable pulmonary fibrosis disease. However, the underlying mechanisms remain veiled. Herein, we aim to elucidate the novel mechanisms of interleukin-11 (IL-11) driving fibroblast metabolic reprogramming during the development of silicosis. We observed that CS exposure induced lung fibrosis in mice and activated fibroblasts, accompanied by increased IL-11 expression and metabolic reprogramming switched from mitochondrial respiration to glycolysis. Besides, we innovatively uncovered that elevated IL-11 promoted the glycolysis process, thereby facilitating the fibroblast-myofibroblast transition (FMT). Mechanistically, CS-stimulated IL-11 activated the extracellular signal-regulated kinase (ERK) pathway and the latter increased the expression of hypoxia inducible factor-1α (HIF-1α) via promoting the translation and delaying the degradation of the protein. HIF-1α further facilitated glycolysis, driving the FMT process and ultimately the formation of silicosis. Moreover, either silence or neutralization of IL-11 inhibited glycolysis augmentation and attenuated CS-induced lung myofibroblast generation and fibrosis. Overall, our findings elucidate the role of IL-11 in promoting fibroblast metabolic reprogramming through the ERK-HIF-1α axis during CS-induced lung fibrosis, providing novel insights into the molecular mechanisms and potential therapeutic targets of silicosis.

Keywords: Crystalline silica; Fibroblast metabolic reprogramming; Hypoxia inducible factor-1α; Interleukin-11; Lung fibrosis.

MeSH terms

  • Animals
  • Fibroblasts* / drug effects
  • Glycolysis
  • Interleukin-11* / metabolism
  • Metabolic Reprogramming* / drug effects
  • Mice
  • Pulmonary Fibrosis* / chemically induced
  • Pulmonary Fibrosis* / metabolism
  • Silicon Dioxide* / toxicity
  • Silicosis / metabolism

Substances

  • Interleukin-11
  • Silicon Dioxide