Ten-eleven translocation 1 (TET1) methylation is associated with childhood asthma and traffic-related air pollution

J Allergy Clin Immunol. 2016 Mar;137(3):797-805.e5. doi: 10.1016/j.jaci.2015.10.021. Epub 2015 Dec 10.

Abstract

Background: Asthma is a complex disorder influenced by genetics and the environment. Recent findings have linked abnormal DNA methylation in T cells with asthma; however, the potential dysregulation of methylation in airway epithelial cells is unknown. Studies of mouse models of asthma have observed greater levels of 5-hydroxymethylcytosine (5-hmC) and ten-eleven translocation 1 (TET1) expression in lungs. TET proteins are known to catalyze methylation through modification of 5-methylcytosine to 5-hmC.

Objective: We sought to examine the association of TET1 methylation with asthma and traffic-related air pollution (TRAP).

Methods: TET1 methylation levels from DNA derived from nasal airway epithelial cells collected from 12 African American children with physician-diagnosed asthma and their nonasthmatic siblings were measured by using Illumina 450K arrays. Regions of interest were verified by means of locus-specific pyrosequencing in 35 sibling pairs and replicated in an independent population (n = 186). Exposure to TRAP in participants' early life and at current home addresses was estimated by using a land-use regression model. Methylation studies in saliva, PBMCs, and human bronchial epithelial cells were done to support our findings.

Results: Loss of methylation at a single CpG site in the TET1 promoter (cg23602092) and increased global 5-hmC levels were significantly associated with asthma. In contrast, TRAP exposure at participants' current homes significantly increased methylation at the same site. Patterns were consistent across tissue sample types. 5-Aza-2'-deoxycytidine and diesel exhaust particle exposure in human bronchial epithelial cells was associated with altered TET1 methylation and expression and global 5-hmC levels.

Conclusions: Our findings suggest a possible role of TET1 methylation in asthmatic patients and response to TRAP.

Keywords: 5-hmC; DNA methylation; TET1; asthma; cross-tissue marker; nasal epithelial cells; traffic-related air pollution.

Publication types

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

MeSH terms

  • 5-Methylcytosine / analogs & derivatives
  • Adolescent
  • Air Pollution / adverse effects*
  • Alleles
  • Asthma / etiology*
  • Asthma / metabolism
  • Case-Control Studies
  • Child
  • CpG Islands
  • Cytosine / analogs & derivatives
  • Cytosine / metabolism
  • DNA Methylation*
  • DNA-Binding Proteins / genetics*
  • Epigenesis, Genetic
  • Epithelial Cells
  • Female
  • Gene Expression
  • Humans
  • Male
  • Mixed Function Oxygenases
  • Nasal Mucosa / metabolism
  • Promoter Regions, Genetic
  • Proto-Oncogene Proteins / genetics*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Risk Factors
  • Vehicle Emissions*

Substances

  • DNA-Binding Proteins
  • Proto-Oncogene Proteins
  • RNA, Messenger
  • Vehicle Emissions
  • 5-hydroxymethylcytosine
  • 5-Methylcytosine
  • Cytosine
  • Mixed Function Oxygenases
  • TET1 protein, human