Indole-3-acetic acid attenuates pulmonary fibrosis by modulating lung microbiota, inhibiting fibroblast activation, and alleviating alveolar epithelial cell senescence

Life Sci. 2024 Dec 15:359:123191. doi: 10.1016/j.lfs.2024.123191. Epub 2024 Oct 29.

Abstract

Aim: Pulmonary fibrosis (PF) is a relentlessly progressive disorder characterized by high mortality and limited effective therapeutic options. Indole-3-acetic acid (IAA), originally recognized as a plant hormone, is also identified as a tryptophan-derived metabolite catabolized from microbiota in mammals. IAA has exhibited antioxidative, anti-inflammatory, and anti-tumor effects in various disorders, yet its role in PF remains elusive.

Main methods: Bleomycin (BLM) was employed to induce PF in a mouse model. TGF-β1 was utilized in primary mouse lung fibroblasts (pMLFs) to establish a pro-fibrotic in vitro cellular model, and in A549 cells to create an in vitro cellular senescence model. The therapeutic effects of IAA on PF were evaluated using hematoxylin-eosin staining, immunofluorescence staining, western blotting, SA-β-gal assay, and network pharmacology analysis. Additionally, the effect of IAA on lung microbiota of PF was investigated using 16S rRNA gene sequencing analysis.

Key findings: we observed a significant reduction in IAA levels in both PF patients and mouse models. Moreover, we demonstrated the therapeutic potential of IAA in alleviating PF in BLM-induced mouse models, showing a dose-dependent response. Mechanistically, we delineated three perspectives. Firstly, IAA promoted autophagic flux by inhibiting the PI3K/AKT/mTOR pathway, thereby suppressing lung fibroblast differentiation and extracellular matrix (ECM) deposition. Secondly, IAA attenuated alveolar epithelial cell senescence by modulating the PI3K/AKT and HIF-1 pathways. Lastly, IAA displayed the ability to mitigate PF by modulating the structure and composition of lung microbiota.

Significance: Our study demonstrates that IAA alleviates PF through multiple pathways, highlighting its potential as a therapeutic agent.

Keywords: Autophagy; Cell senescence; Indole-3-acetic acid; Microbiota; Pulmonary fibrosis.

MeSH terms

  • A549 Cells
  • Alveolar Epithelial Cells* / drug effects
  • Alveolar Epithelial Cells* / metabolism
  • Alveolar Epithelial Cells* / pathology
  • Animals
  • Bleomycin
  • Cellular Senescence* / drug effects
  • Disease Models, Animal
  • Fibroblasts* / drug effects
  • Fibroblasts* / metabolism
  • Humans
  • Indoleacetic Acids* / metabolism
  • Indoleacetic Acids* / pharmacology
  • Lung* / drug effects
  • Lung* / metabolism
  • Lung* / microbiology
  • Lung* / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Microbiota / drug effects
  • Pulmonary Fibrosis* / drug therapy
  • Pulmonary Fibrosis* / metabolism
  • Pulmonary Fibrosis* / pathology
  • Signal Transduction / drug effects

Substances

  • Indoleacetic Acids
  • indoleacetic acid
  • Bleomycin