Sphingosine kinase 1-mediated inhibition of Fas death signaling in rheumatoid arthritis B lymphoblastoid cells

Arthritis Rheum. 2006 Mar;54(3):754-64. doi: 10.1002/art.21635.

Abstract

Objective: It is becoming increasingly apparent that B cells play an important role in the pathogenesis of rheumatoid arthritis (RA). Due to the scarcity of B cells in RA, it has been technically difficult to functionally characterize B cell apoptosis in this disease. As a necessary first step to identify candidate aberrations, we investigated Fas-mediated signaling events in immortalized peripheral blood B lymphoblastoid cell lines (LCLs) from patients with RA and controls.

Methods: Cell death was determined by the MTS assay, and apoptosis was detected by the TUNEL assay and DNA laddering. Proteolytic activation of caspase 3 was determined by immunoblotting, and its enzymatic activity was determined by a fluorometric technique. Messenger RNA (mRNA) expression was quantified by real-time polymerase chain reaction (PCR) analysis. The functional role of sphingosine kinase (SPHK) was determined by measuring its enzymatic activity, by quantifying the levels of its product, sphingosine 1-phosphate (S1P), and by investigating the ability of the SPHK inhibitor N,N-dimethylsphingosine and isozyme-specific small interfering RNA (siRNA) oligonucleotides to reverse signaling aberrations.

Results: LCLs from patients with RA displayed disease-specific Fas-mediated signal transduction impairment with consequent resistance to cell death. RA LCLs displayed high constitutive SPHK activity and increased levels of S1P. Real-time PCR analysis showed higher SPHK-1 mRNA expression levels in RA patients compared with paired controls. Increased SPHK-1 (but not SPHK-2) mRNA levels were observed in synovial tissue from RA patients. Competitive inhibitors of SPHK reversed the resistance of RA LCLs to Fas-induced apoptosis. Additionally, resistance to Fas-mediated signaling was reversed by siRNA oligonucleotides specific for SPHK-1 but not by oligonucleotides specific for SPHK-2.

Conclusion: These findings demonstrate disease-specific resistance to Fas-mediated death signaling in patients with RA and implicate increased SPHK-1 activity as the cause of this aberration.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / pharmacology
  • Adult
  • Aged
  • Apoptosis / physiology
  • Arthritis, Rheumatoid / immunology*
  • Arthritis, Rheumatoid / metabolism
  • B-Lymphocytes / immunology*
  • Caspase 3
  • Caspases / metabolism
  • Cell Death / physiology*
  • Enzyme Activation
  • Female
  • Humans
  • In Situ Nick-End Labeling
  • Male
  • Middle Aged
  • Phosphotransferases (Alcohol Group Acceptor) / physiology*
  • Polymerase Chain Reaction
  • RNA, Messenger / analysis
  • Signal Transduction / physiology
  • fas Receptor / immunology*

Substances

  • Adaptor Proteins, Signal Transducing
  • RNA, Messenger
  • SPHKAP protein, human
  • fas Receptor
  • Phosphotransferases (Alcohol Group Acceptor)
  • sphingosine kinase
  • CASP3 protein, human
  • Caspase 3
  • Caspases