Endoplasmic Reticulum Stress Induces ROS Production and Activates NLRP3 Inflammasome Via the PERK-CHOP Signaling Pathway in Dry Eye Disease

Invest Ophthalmol Vis Sci. 2024 Dec 2;65(14):34. doi: 10.1167/iovs.65.14.34.

Abstract

Purpose: The purpose of this study was to investigate the potential roles of endoplasmic reticulum (ER) stress in the development of dry eye disease (DED).

Methods: Single-cell RNA sequencing (scRNA-seq) data from the Gene Expression Omnibus (GEO) database, derived from corneal tissues of a dry eye mouse model, was processed using the Seurat R program. The results were validated using a scopolamine-induced dry eye mouse model and a hyperosmotic-induced cell model involving primary human corneal epithelial cells (HCECs) and immortalized human corneal epithelial (HCE-2) cells. The HCE-2 cells were treated with 4-phenylbutyric acid (4-PBA) or tunicamycin (TM) to modulate ER stress. TXNIP and PERK knockdown were performed by siRNA transfection. Immunofluorescence, Western blotting, and real-time PCR were used to assess oxidative stress, ER stress, unfolded protein response (UPR) marker proteins, and TXNIP/NLRP3 axis activation.

Results: The analysis of scRNAseq data shows an increase in the ER stress marker GRP78, and the activation of the PERK-CHOP of UPR in DED mouse. These findings were confirmed both in vivo and in vitro. Additionally, HCE-2 cells treated with 4-PBA or TM showed significant effects on the production of reactive oxygen species (ROS) and the activation of the TXNIP/NLRP3-IL1β signaling pathway. Furthermore, siRNA knockdown of PERK or TXNIP, which alleviated the TXNIP/NLRP3-IL1β signaling axis, showed protective effects on HCECs.

Conclusions: This study explores the role of ER stress-induced oxidative stress and NLRP3-IL-1β mediated inflammation in DED, and highlights the therapeutic potential of PERK-CHOP axis and TXNIP in the treatment of DED.

MeSH terms

  • Animals
  • Blotting, Western
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cells, Cultured
  • Disease Models, Animal*
  • Dry Eye Syndromes* / genetics
  • Dry Eye Syndromes* / metabolism
  • Endoplasmic Reticulum Chaperone BiP*
  • Endoplasmic Reticulum Stress* / physiology
  • Epithelium, Corneal / drug effects
  • Epithelium, Corneal / metabolism
  • Humans
  • Inflammasomes* / metabolism
  • Mice
  • Mice, Inbred C57BL*
  • NLR Family, Pyrin Domain-Containing 3 Protein* / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein* / metabolism
  • Oxidative Stress
  • Reactive Oxygen Species* / metabolism
  • Real-Time Polymerase Chain Reaction
  • Signal Transduction* / physiology
  • Thioredoxins
  • Transcription Factor CHOP* / genetics
  • Transcription Factor CHOP* / metabolism
  • Unfolded Protein Response
  • eIF-2 Kinase* / genetics
  • eIF-2 Kinase* / metabolism

Substances

  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Hspa5 protein, mouse
  • Endoplasmic Reticulum Chaperone BiP
  • eIF-2 Kinase
  • Reactive Oxygen Species
  • HSPA5 protein, human
  • Inflammasomes
  • Transcription Factor CHOP
  • Nlrp3 protein, mouse
  • PERK kinase
  • Ddit3 protein, mouse
  • Txnip protein, mouse
  • Carrier Proteins
  • Thioredoxins