Trex-1 deficiency in rheumatoid arthritis synovial fibroblasts

Arthritis Rheum. 2010 Sep;62(9):2673-9. doi: 10.1002/art.27567.

Abstract

Objective: To explore whether the increased expression of long interspersed nuclear element 1 (LINE-1; L1) messenger RNA (mRNA) and protein in rheumatoid arthritis synovial fibroblasts (RASFs) is associated with decreased expression of Trex-1, an exonuclease involved in the metabolization of L1 DNA:RNA hybrids.

Methods: Chromatin immunoprecipitation was used to detect L1-related p40 protein (L1-ORF1p) binding sequences in RASFs. Luciferase activity was measured in the synovial fibroblasts following cotransfection of the episomal plasmid with pJM105 expressing L1-ORF1p and pGL3-TS3 carrying the target sequence for L1-ORF1p. This luciferase reporter assay was used to compare the activity between RASFs and osteoarthritis synovial fibroblasts (OASFs) and to assess correlations of luciferase activity with the expression of Trex-1 measured by flow cytometry. The expression of Trex-1 mRNA and protein was also compared using real-time polymerase chain reaction, immunohistochemistry, and Western blot analyses. The role of Trex-1 in the L1-ORF1p-mediated luciferase activity assay was studied using interfering RNAs (iRNA) and a Trex-1 expression vector.

Results: Increased luciferase activity occurred after cotransfection of synovial fibroblasts with pJM105 and pGL3-TS3. L1-ORF1p activity was increased in RASFs as compared with OASFs, and this was correlated inversely with the expression of Trex-1. Levels of Trex-1 mRNA and protein were lower in RASFs than in OASFs. After transfection of the L1 expression plasmid, Trex-1 mRNA levels increased in OASFs, but not in RASFs. The addition of iRNA against Trex-1, however, resulted in an enhancement of L1-ORF1p activity in OASFs to the levels measured in RASFs. Overexpression of Trex-1 inhibited 5-azacytidine-induced expression of p38δ MAPK, a gene carrying the TS3 sequence.

Conclusion: The deficiency of Trex-1 in RASFs allows a longer half-life of gene products encoded by active endogenous L1 retrotransposons. This pathway may play a role in diseases in which the cells exhibit a "spontaneous" aggressive behavior.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arthritis, Rheumatoid / metabolism*
  • Arthritis, Rheumatoid / pathology
  • Azacitidine / pharmacology
  • Cells, Cultured
  • Down-Regulation
  • Exodeoxyribonucleases / genetics
  • Exodeoxyribonucleases / metabolism*
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism*
  • Fibroblasts / pathology
  • Flow Cytometry
  • Gene Expression
  • Gene Silencing
  • Humans
  • Immunohistochemistry
  • Long Interspersed Nucleotide Elements / genetics*
  • Oligonucleotide Array Sequence Analysis
  • Osteoarthritis / metabolism*
  • Osteoarthritis / pathology
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism*
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Synovial Membrane / drug effects
  • Synovial Membrane / metabolism*
  • Synovial Membrane / pathology
  • Transfection / methods

Substances

  • Phosphoproteins
  • RNA, Messenger
  • RNA, Small Interfering
  • Exodeoxyribonucleases
  • three prime repair exonuclease 1
  • Azacitidine