IL-4 activates ULK1/Atg9a/Rab9 in asthma, NLRP3 inflammasomes, and Golgi fragmentation by increasing autophagy flux and mitochondrial oxidative stress

Redox Biol. 2024 May:71:103090. doi: 10.1016/j.redox.2024.103090. Epub 2024 Feb 15.

Abstract

During asthma, there is an intensification of pulmonary epithelial inflammation, mitochondrial oxidative stress, and Golgi apparatus fragmentation. However, the underlying mechanism remains largely unknown. Therefore, this study investigated the roles of ULK1, Atg9a, and Rab9 in epithelial inflammation, mitochondrial oxidative stress, and Golgi apparatus fragmentation. We found that ULK1 gene knockout reduced the infiltration of inflammatory cells, restored the imbalance of the Th1/Th2 ratio, and inhibited the formation of inflammatory bodies in the lung tissue of house dust mite-induced asthma mice. Moreover, we demonstrated that Atg9a interacted with ULK1 at S467. ULK1 phosphorylated Atg9a at S14. Treatment with ULK1 activator (LYN-1604) and ULK1 inhibitor (ULK-101) respectively promoted and inhibited inflammasome activation, indicating that the activation of inflammasome induced by house dust mite in asthma mice is dependent on ULK1. For validation of the in vivo results, we then used a lentivirus containing ULK1 wild type and ULK1-S467A genes to infect Beas-2b-ULK1-knockout cells and establish a stable cell line. The results suggest that the ULK1 S467 site is crucial for IL-4-induced inflammation and oxidative stress. Experimental verification confirmed that Atg9a was the superior signaling pathway of Rab9. Interestingly, we found for the first time that Rab9 played a very important role in inflammation-induced fragmentation of the Golgi apparatus. Inhibiting the activation of the ULK1/Atg9a/Rab9 signaling pathways can inhibit Golgi apparatus fragmentation and mitochondrial oxidative stress in asthma while reducing the production of NLRP3-mediated pulmonary epithelial inflammation.

Keywords: Atg9a/Rab9 signaling pathway; Golgi apparatus fragmentation; Oxidative stress; ULK1/Atg9a signaling pathway.

MeSH terms

  • Animals
  • Asthma* / genetics
  • Asthma* / metabolism
  • Autophagy
  • Golgi Apparatus / metabolism
  • Inflammasomes / metabolism
  • Inflammation / metabolism
  • Interleukin-4 / genetics
  • Interleukin-4 / metabolism
  • Mice
  • NLR Family, Pyrin Domain-Containing 3 Protein / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism
  • Oxidative Stress
  • Pneumonia* / metabolism

Substances

  • Inflammasomes
  • Interleukin-4
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Il4 protein, mouse
  • Ulk1 protein, mouse
  • Atg9A protein, mouse
  • rab9 protein, mouse
  • Nlrp3 protein, mouse