Dual role of autophagy in stress-induced cell death in rheumatoid arthritis synovial fibroblasts

Arthritis Rheumatol. 2014 Jan;66(1):40-8. doi: 10.1002/art.38190.

Abstract

Objective: To investigate the role of autophagy in the regulation of cell death in rheumatoid arthritis synovial fibroblasts (RASFs).

Methods: RASFs and osteoarthritis synovial fibroblasts (OASFs) were treated with thapsigargin (TG), an inducer of endoplasmic reticulum (ER) stress, and MG132, a proteasome inhibitor. Then, 3-methyladenine was used as an autophagy inhibitor and bafilomycin A1 as a lysosome inhibitor. Polyubiquitinated proteins, p62, and autophagy induction were evaluated by immunoblotting, immunofluorescence microscopy, and immunohistochemistry, respectively. OASFs were transfected with small interfering RNA targeting autophagy-linked FYVE protein (ALFY). Cell death was evaluated by flow cytometry and a caspase 3 activity assay.

Results: In RASFs, the induction of autophagy by TG and MG132 was increased compared to that in OASFs. Whereas autophagy promoted a caspase 3-independent induction of cell death under ER stress, autophagy had a protective role in apoptosis induced by proteasome inhibition. Treatment of RASFs with 3-methyladenine blocked TG-induced cell death. ER stress induced a strong accumulation of p62-positive polyubiquitinated protein aggregates, accompanied by the formation of large vacuoles in RASFs but not OASFs. Furthermore, TG-induced p62 protein expression was increased, whereas TG-induced ALFY expression was reduced, in RASFs compared to OASFs. ALFY knockdown promoted the accumulation of p62, the formation of polyubiquitinated protein aggregates, and cell death.

Conclusion: Our data provide the first evidence of a dual role of autophagy in the regulation of death pathways in RASFs. A reduced expression of ALFY and the formation of p62-positive polyubiquitinated protein aggregates promote cell death in RASFs under severe ER stress.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / drug effects
  • Adaptor Proteins, Signal Transducing / metabolism
  • Adenine / analogs & derivatives
  • Adenine / pharmacology
  • Arthritis, Rheumatoid / physiopathology*
  • Autophagy / drug effects
  • Autophagy / physiology*
  • Autophagy-Related Proteins
  • Caspase 3 / drug effects
  • Caspase 3 / metabolism
  • Cell Death / physiology
  • Cells, Cultured
  • Endoplasmic Reticulum Stress / physiology*
  • Enzyme Inhibitors / pharmacology
  • Fibroblasts / physiology*
  • Immunoblotting
  • Immunohistochemistry
  • Lysosomes / drug effects
  • Lysosomes / physiology
  • Macrolides / pharmacology
  • Membrane Proteins / drug effects
  • Membrane Proteins / metabolism
  • Microscopy, Fluorescence
  • Osteoarthritis / physiopathology
  • Polyubiquitin / drug effects
  • Polyubiquitin / metabolism
  • Sequestosome-1 Protein
  • Synovial Membrane / cytology*
  • Transcription Factors / drug effects
  • Transcription Factors / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Autophagy-Related Proteins
  • Enzyme Inhibitors
  • Macrolides
  • Membrane Proteins
  • SQSTM1 protein, human
  • Sequestosome-1 Protein
  • Transcription Factors
  • WDFY3 protein, human
  • Polyubiquitin
  • 3-methyladenine
  • bafilomycin A1
  • CASP3 protein, human
  • Caspase 3
  • Adenine