DNA methylation of the TPMT gene and azathioprine pharmacokinetics in children with very early onset inflammatory bowel disease

Biomed Pharmacother. 2023 Jan:157:113901. doi: 10.1016/j.biopha.2022.113901. Epub 2022 Nov 30.

Abstract

Background: Thiopurine methyltransferase (TPMT) is a crucial enzyme for azathioprine biotransformation and its activity is higher in very early onset inflammatory bowel disease (VEO-IBD) patients than in adolescents with IBD (aIBD).

Aims: The aims of this pharmacoepigenetic study were to evaluate differences in peripheral blood DNA methylation of the TPMT gene and in azathioprine pharmacokinetics in patients with VEO-IBD compared to aIBD.

Methods: The association of age with whole genome DNA methylation profile was evaluated in a pilot group of patients and confirmed by a meta-analysis on 3 cohorts of patients available on the public functional genomics data repository. Effects of candidate CpG sites in the TPMT gene were validated in a larger cohort using pyrosequencing. TPMT activity and azathioprine metabolites (TGN) were measured in patients' erythrocytes by HPLC and associated with patients' age group and TPMT DNA methylation.

Results: Whole genome DNA methylation pilot analysis, combined with the meta-analysis revealed cg22736354, located on TPMT downstream neighboring region, as the only statistically significant CpG whose methylation increases with age, resulting lower in VEO-IBD patients compared to aIBD (median 9.6% vs 12%, p = 0.029). Pyrosequencing confirmed lower cg22736354 methylation in VEO-IBD patients (median 4.0% vs 6.0%, p = 4.6 ×10-5). No differences in TPMT promoter methylation were found. Reduced cg22736354 methylation was associated with lower TGN concentrations (rho = 0.31, p = 0.01) in patients with VEO-IBD and aIBD.

Conclusion: Methylation of cg22736354 in TPMT gene neighborhood is lower in patients with VEO-IBD and is associated with reduced azathioprine inactivation and increased TGN concentrations.

Keywords: Azathioprine; DNA methylation; TPMT; Very early onset inflammatory bowel disease.

Publication types

  • Meta-Analysis

MeSH terms

  • Adolescent
  • Azathioprine* / therapeutic use
  • Child
  • DNA Methylation / genetics
  • Humans
  • Immunosuppressive Agents / therapeutic use
  • Inflammatory Bowel Diseases* / drug therapy
  • Inflammatory Bowel Diseases* / genetics
  • Methyltransferases / genetics
  • Methyltransferases / metabolism

Substances

  • Azathioprine
  • thiopurine methyltransferase
  • Methyltransferases
  • Immunosuppressive Agents