DNA-Methylation Signatures of Tobacco Smoking in a High Cardiovascular Risk Population: Modulation by the Mediterranean Diet

Int J Environ Res Public Health. 2023 Feb 18;20(4):3635. doi: 10.3390/ijerph20043635.

Abstract

Biomarkers based on DNA methylation are relevant in the field of environmental health for precision health. Although tobacco smoking is one of the factors with a strong and consistent impact on DNA methylation, there are very few studies analyzing its methylation signature in southern European populations and none examining its modulation by the Mediterranean diet at the epigenome-wide level. We examined blood methylation smoking signatures on the EPIC 850 K array in this population (n = 414 high cardiovascular risk subjects). Epigenome-wide methylation studies (EWASs) were performed analyzing differential methylation CpG sites by smoking status (never, former, and current smokers) and the modulation by adherence to a Mediterranean diet score was explored. Gene-set enrichment analysis was performed for biological and functional interpretation. The predictive value of the top differentially methylated CpGs was analyzed using receiver operative curves. We characterized the DNA methylation signature of smoking in this Mediterranean population by identifying 46 differentially methylated CpGs at the EWAS level in the whole population. The strongest association was observed at the cg21566642 (p = 2.2 × 10-32) in the 2q37.1 region. We also detected other CpGs that have been consistently reported in prior research and discovered some novel differentially methylated CpG sites in subgroup analyses. In addition, we found distinct methylation profiles based on the adherence to the Mediterranean diet. Particularly, we obtained a significant interaction between smoking and diet modulating the cg5575921 methylation in the AHRR gene. In conclusion, we have characterized biomarkers of the methylation signature of tobacco smoking in this population, and suggest that the Mediterranean diet can increase methylation of certain hypomethylated sites.

Keywords: DNA methylation; EWAS; Mediterranean diet; dietary modulation; epigenetic biomarkers; precision health; tobacco smoking.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cardiovascular Diseases* / genetics
  • CpG Islands
  • DNA
  • DNA Methylation
  • Diet, Mediterranean*
  • Epigenesis, Genetic
  • Genome-Wide Association Study
  • Heart Disease Risk Factors
  • Humans
  • Risk Factors
  • Tobacco Smoking

Substances

  • DNA

Grants and funding

This study was partially funded, by the Conselleria de Innovación, Universidades, Ciencia y Sociedad Digital, Generalitat Valenciana (grants PROMETEO 17/2017, PROMETEO/2021/021, and APOSTD/2020/164); the Spanish Ministry of Health (Instituto de Salud Carlos III); the Ministerio de Economía y Competitividad-Fondo Europeo de Desarrollo Regional (FEDER) (grants CIBER 06/03, PI06/1326, PI13/00728, PI16/00366, PI19/00781 and SAF2016–80532-R); and Grant PID2019-108858RB-I00 funded by AEI 10.13039/501100011033 and by “ERDF A way of making Europe”.