A global increase in 5-hydroxymethylcytosine levels marks osteoarthritic chondrocytes

Arthritis Rheumatol. 2014 Jan;66(1):90-100. doi: 10.1002/art.38200.

Abstract

Objective: To investigate the role of the newly discovered epigenetic mark 5-hydroxymethylcytosine (5hmC) and its regulators in altered gene expression in osteoarthritis (OA).

Methods: Cartilage was obtained from OA patients undergoing total knee arthroplasty and from control patients undergoing anterior cruciate ligament reconstruction. Global levels of 5hmC and 5-methylcytosine (5mC) were investigated using immunoblotting, enzyme-linked immunosorbent assays, and cellular staining. Gene expression changes were monitored by quantitative polymerase chain reaction (PCR) analysis. Levels of locus-specific 5hmC and 5mC at CpG sites in the matrix metalloproteinase 1 (MMP-1), MMP-3, ADAMTS-5, and hypoxanthine guanine phosphoribosyltransferase 1 (HPRT-1) promoters were quantified using a glucosylation and enzyme digestion-based method followed by quantitative PCR analysis. Global and locus-specific 5hmC levels and gene expression changes were monitored in normal chondrocytes stimulated with inflammatory cytokines to identify the effect of joint inflammation.

Results: A global 5-6-fold increase in 5hmC concomitant with a loss of TET1 was observed in human OA chondrocytes compared to normal chondrocytes. Enrichment of 5hmC was observed in promoters of enzymes critical to OA pathology, MMP-1 and MMP-3. Short-term treatment of normal chondrocytes with inflammatory cytokines induced a rapid decrease in TET1 expression but no global or locus-specific 5hmC enrichment.

Conclusion: This study provides the first evidence of an epigenetic imbalance of the 5hmC homeostasis in OA leading to TET1 down-regulation and 5hmC accumulation. Our experiments identify 5hmC and its regulators as potential diagnostic and therapeutic targets in OA.

MeSH terms

  • 5-Methylcytosine / metabolism
  • ADAM Proteins / genetics
  • ADAMTS5 Protein
  • Adolescent
  • Adult
  • Aged
  • Aged, 80 and over
  • Anterior Cruciate Ligament Reconstruction
  • Arthroplasty, Replacement, Knee
  • Biomarkers / metabolism
  • Cartilage, Articular / cytology
  • Case-Control Studies
  • Child
  • Child, Preschool
  • Chondrocytes / enzymology
  • Chondrocytes / metabolism*
  • CpG Islands
  • Cytokines
  • Cytosine / analogs & derivatives*
  • Cytosine / metabolism
  • DNA Methylation*
  • DNA-Binding Proteins / metabolism
  • Down-Regulation / genetics
  • Enzyme-Linked Immunosorbent Assay
  • Epigenesis, Genetic
  • Female
  • Gene Expression
  • Humans
  • Hypoxanthine Phosphoribosyltransferase / genetics
  • Infant
  • Male
  • Matrix Metalloproteinase 1 / genetics
  • Matrix Metalloproteinase 3 / genetics
  • Middle Aged
  • Mixed Function Oxygenases
  • Osteoarthritis, Knee / enzymology
  • Osteoarthritis, Knee / genetics
  • Osteoarthritis, Knee / metabolism*
  • Promoter Regions, Genetic / genetics
  • Proto-Oncogene Proteins / metabolism
  • Young Adult

Substances

  • Biomarkers
  • Cytokines
  • DNA-Binding Proteins
  • Proto-Oncogene Proteins
  • 5-hydroxymethylcytosine
  • 5-Methylcytosine
  • Cytosine
  • Mixed Function Oxygenases
  • TET1 protein, human
  • Hypoxanthine Phosphoribosyltransferase
  • ADAM Proteins
  • ADAMTS5 Protein
  • ADAMTS5 protein, human
  • MMP3 protein, human
  • Matrix Metalloproteinase 3
  • MMP1 protein, human
  • Matrix Metalloproteinase 1