LINE-1 expression in cancer correlates with p53 mutation, copy number alteration, and S phase checkpoint

Proc Natl Acad Sci U S A. 2022 Feb 22;119(8):e2115999119. doi: 10.1073/pnas.2115999119.

Abstract

Retrotransposons are genomic DNA sequences that copy themselves to new genomic locations via RNA intermediates; LINE-1 is the only active and autonomous retrotransposon in the human genome. The mobility of LINE-1 is largely repressed in somatic tissues but is derepressed in many cancers, where LINE-1 retrotransposition is correlated with p53 mutation and copy number alteration (CNA). In cell lines, inducing LINE-1 expression can cause double-strand breaks (DSBs) and replication stress. Reanalyzing multiomic data from breast, ovarian, endometrial, and colon cancers, we confirmed correlations between LINE-1 expression, p53 mutation status, and CNA. We observed a consistent correlation between LINE-1 expression and the abundance of DNA replication complex components, indicating that LINE-1 may also induce replication stress in human tumors. In endometrial cancer, high-quality phosphoproteomic data allowed us to identify the DSB-induced ATM-MRN-SMC S phase checkpoint pathway as the primary DNA damage response (DDR) pathway associated with LINE-1 expression. Induction of LINE-1 expression in an in vitro model led to increased phosphorylation of MRN complex member RAD50, suggesting that LINE-1 directly activates this pathway.

Keywords: DNA damage response; LINE-1; cancer; copy number alteration; retrotransposon.

MeSH terms

  • Cell Cycle / genetics
  • Cell Cycle Proteins / metabolism
  • DNA Breaks, Double-Stranded
  • DNA Copy Number Variations / genetics*
  • DNA Repair / genetics
  • DNA-Binding Proteins / metabolism
  • Databases, Genetic
  • Gene Expression / genetics
  • Gene Expression Regulation, Neoplastic / genetics
  • Humans
  • Long Interspersed Nucleotide Elements / genetics*
  • Long Interspersed Nucleotide Elements / physiology
  • Neoplasms / genetics
  • Nuclear Proteins / metabolism
  • Proteins / genetics
  • Proteins / metabolism
  • Retroelements / genetics
  • S Phase Cell Cycle Checkpoints / genetics
  • Tumor Suppressor Protein p53 / genetics*
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • L1TD1 protein, human
  • Nuclear Proteins
  • Proteins
  • Retroelements
  • Tumor Suppressor Protein p53