DNA and RNA Cleavage Complexes and Repair Pathway for TOP3B RNA- and DNA-Protein Crosslinks

Cell Rep. 2020 Dec 29;33(13):108569. doi: 10.1016/j.celrep.2020.108569.

Abstract

The present study demonstrates that topoisomerase 3B (TOP3B) forms both RNA and DNA cleavage complexes (TOP3Bccs) in vivo and reveals a pathway for repairing TOP3Bccs. For inducing and detecting cellular TOP3Bccs, we engineer a "self-trapping" mutant of TOP3B (R338W-TOP3B). Transfection with R338W-TOP3B induces R-loops, genomic damage, and growth defect, which highlights the importance of TOP3Bcc repair mechanisms. To determine how cells repair TOP3Bccs, we deplete tyrosyl-DNA phosphodiesterases (TDP1 and TDP2). TDP2-deficient cells show elevated TOP3Bccs both in DNA and RNA. Conversely, overexpression of TDP2 lowers cellular TOP3Bccs. Using recombinant human TDP2, we demonstrate that TDP2 can process both denatured and proteolyzed TOP3Bccs. We also show that cellular TOP3Bccs are ubiquitinated by the E3 ligase TRIM41 before undergoing proteasomal processing and excision by TDP2.

Keywords: DNA repair; TDP2; TRIM41; topoisomerase; ubiquitin-proteasome.

Publication types

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

MeSH terms

  • Amino Acid Substitution
  • DNA / metabolism*
  • DNA Cleavage
  • DNA Repair*
  • DNA Topoisomerases, Type I / physiology*
  • DNA-Binding Proteins / physiology*
  • Gene Knockout Techniques
  • HCT116 Cells
  • HEK293 Cells
  • Humans
  • Phosphoric Diester Hydrolases / genetics
  • Phosphoric Diester Hydrolases / metabolism
  • Phosphoric Diester Hydrolases / physiology*
  • Proteolysis
  • R-Loop Structures
  • RNA / metabolism*
  • RNA Cleavage
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Ubiquitin-Protein Ligases / physiology*
  • Ubiquitination

Substances

  • DNA-Binding Proteins
  • Recombinant Proteins
  • RNA
  • DNA
  • TRIM41 protein, human
  • Ubiquitin-Protein Ligases
  • Phosphoric Diester Hydrolases
  • TDP1 protein, human
  • TDP2 protein, human
  • tyrosyl-DNA phosphodiesterase
  • DNA Topoisomerases, Type I