An appropriate DNA input for bisulfite conversion reveals LINE-1 and Alu hypermethylation in tissues and circulating cell-free DNA from cancers

PLoS One. 2024 Dec 30;19(12):e0316394. doi: 10.1371/journal.pone.0316394. eCollection 2024.

Abstract

The autonomous and active Long-Interspersed Element-1 (LINE-1, L1) and the non-autonomous Alu retrotransposon elements, contributing to 30% of the human genome, are the most abundant repeated sequences. With more than 90% of their sequences being methylated in normal cells, these elements undeniably contribute to the global DNA methylation level and constitute a major part of circulating-cell-free DNA (cfDNA). So far, the hypomethylation status of LINE-1 and Alu in cellular and extracellular DNA has long been considered a prevailing hallmark of ageing-related diseases and cancer. This study demonstrated that errors in LINE-1 and Alu methylation level measurements were caused by an excessive input quantity of genomic DNA used for bisulfite conversion. Using the minuscule DNA amount of 0.5 ng, much less than what has been used and recommended so far (500 ng-2 μg) or 1 μL of cfDNA extracted from 1 mL of blood, we revealed hypermethylation of LINE-1 and Alu in 407 tumour samples of primary breast, colon and lung cancers when compared with the corresponding pair-matched adjacent normal tissue samples (P < 0.05-0.001), and in cfDNA from 296 samples of lung cancers as compared with 477 samples from healthy controls (P < 0.0001). More importantly, LINE-1 hypermethylation in cfDNA is associated with healthy ageing. Our results have not only contributed to the standardized bisulfite-based protocols for DNA methylation assays, particularly in applications on repeated sequences but also provided another perspective for other repetitive sequences whose epigenetic properties may have crucial impacts on genome architecture and human health.

MeSH terms

  • Alu Elements* / genetics
  • Breast Neoplasms / genetics
  • Cell-Free Nucleic Acids* / blood
  • Cell-Free Nucleic Acids* / genetics
  • DNA Methylation*
  • Female
  • Humans
  • Long Interspersed Nucleotide Elements* / genetics
  • Male
  • Neoplasms / genetics
  • Sulfites* / chemistry

Substances

  • Sulfites
  • Cell-Free Nucleic Acids
  • hydrogen sulfite

Grants and funding

This study was funded by the Vingroup Innovation Foundation (VINIF) under project code VINIF.2022.DA00036. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.