Methotrexate inhibits NF-κB activity via long intergenic (noncoding) RNA-p21 induction

Arthritis Rheumatol. 2014 Nov;66(11):2947-57. doi: 10.1002/art.38805.

Abstract

Objective: To determine interrelationships between the expression of long intergenic (noncoding) RNA-p21 (lincRNA-p21), NF-κB activity, and responses to methotrexate (MTX) in rheumatoid arthritis (RA) by analyzing patient blood samples and cell culture models.

Methods: Expression levels of long noncoding RNA and messenger RNA (mRNA) were determined by quantitative reverse transcription-polymerase chain reaction. Western blotting and flow cytometry were used to quantify levels of intracellular proteins. Intracellular NF-κB activity was determined using an NF-κB luciferase reporter plasmid.

Results: Patients with RA expressed reduced basal levels of lincRNA-p21 and increased basal levels of phosphorylated p65 (RelA), a marker of NF-κB activation. Patients with RA who were not treated with MTX expressed lower levels of lincRNA-p21 and higher levels of phosphorylated p65 compared with RA patients treated with low-dose MTX. In cell culture using primary cells and transformed cell lines, MTX induced lincRNA-p21 through a DNA-dependent protein kinase catalytic subunit (DNA PKcs)-dependent mechanism. Deficiencies in the levels of PRKDC mRNA in patients with RA were also corrected by MTX in vivo. Furthermore, MTX reduced NF-κB activity in tumor necrosis factor α-treated cells through a DNA PKcs-dependent mechanism via induction of lincRNA-p21. Finally, we observed that depressed levels of TP53 and lincRNA-p21 increased NF-κB activity in cell lines. Decreased levels of lincRNA-p21 did not alter NFKB1 or RELA transcripts; rather, lincRNA-p21 physically bound to RELA mRNA.

Conclusion: Our findings support a model whereby depressed levels of lincRNA-p21 in RA contribute to increased NF-κB activity. MTX decreases basal levels of NF-κB activity by increasing lincRNA-p21 levels through a DNA PKcs-dependent mechanism.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural

MeSH terms

  • Adult
  • Antirheumatic Agents / pharmacology*
  • Antirheumatic Agents / therapeutic use
  • Arthritis, Rheumatoid / drug therapy
  • Arthritis, Rheumatoid / metabolism
  • Arthritis, Rheumatoid / pathology
  • Cell Line
  • Cells, Cultured
  • Cyclin-Dependent Kinase Inhibitor p21 / metabolism*
  • DNA-Activated Protein Kinase / metabolism
  • Dose-Response Relationship, Drug
  • Female
  • Humans
  • Male
  • Methotrexate / pharmacology*
  • Methotrexate / therapeutic use
  • Middle Aged
  • Monocytes / drug effects
  • Monocytes / metabolism
  • Monocytes / pathology
  • NF-kappa B / metabolism*
  • Nuclear Proteins / metabolism
  • RNA, Long Noncoding / metabolism*
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / pathology
  • Tumor Suppressor Protein p53 / metabolism
  • eIF-2 Kinase / metabolism

Substances

  • Antirheumatic Agents
  • Cyclin-Dependent Kinase Inhibitor p21
  • NF-kappa B
  • Nuclear Proteins
  • RNA, Long Noncoding
  • Tumor Suppressor Protein p53
  • DNA-Activated Protein Kinase
  • PRKDC protein, human
  • eIF-2 Kinase
  • Methotrexate