ADP-ribosylome analysis reveals homogeneous DNA-damage-induced serine ADP-ribosylation across wild-type and BRCA-mutant breast cancer cell lines

Cell Rep. 2024 Jul 23;43(7):114433. doi: 10.1016/j.celrep.2024.114433. Epub 2024 Jul 9.

Abstract

ADP-ribosylation (ADPr) signaling plays a crucial role in DNA damage response. Inhibitors against the main enzyme catalyzing ADPr after DNA damage, poly(ADP-ribose) polymerase 1 (PARP1), are used to treat patients with breast cancer harboring BRCA1/2 mutations. However, resistance to PARP inhibitors (PARPi) is a major obstacle in treating patients. To understand the role of ADPr in PARPi sensitivity, we use liquid chromatography-tandem mass spectrometry (LC-MS/MS) to analyze ADPr in six breast cancer cell lines exhibiting different PARPi sensitivities. We identify 1,632 sites on 777 proteins across all cell lines, primarily on serine residues, with site-specific overlap of targeted residues across DNA-damage-related proteins across all cell lines, demonstrating high conservation of serine ADPr-signaling networks upon DNA damage. Furthermore, we observe site-specific differences in ADPr intensities in PARPi-sensitive BRCA mutants and unique ADPr sites in PARPi-resistant BRCA-mutant HCC1937 cells, which have low poly(ADP-ribose) glycohydrolase (PARG) levels and longer ADPr chains on PARP1.

Keywords: ADP-ribosylation; ADP-ribosylome; Af1521 macrodomain; CP: Cancer; CP: Molecular biology; EThcD; PARG; PARP; PARP inhibitor sensitivity; mass spectrometry; proteomics.

MeSH terms

  • ADP-Ribosylation*
  • BRCA1 Protein* / genetics
  • BRCA1 Protein* / metabolism
  • BRCA2 Protein / genetics
  • BRCA2 Protein / metabolism
  • Breast Neoplasms* / genetics
  • Breast Neoplasms* / metabolism
  • Breast Neoplasms* / pathology
  • Cell Line, Tumor
  • DNA Damage*
  • Female
  • Glycoside Hydrolases / genetics
  • Glycoside Hydrolases / metabolism
  • Humans
  • Mutation / genetics
  • Poly (ADP-Ribose) Polymerase-1 / genetics
  • Poly (ADP-Ribose) Polymerase-1 / metabolism
  • Poly(ADP-ribose) Polymerase Inhibitors / pharmacology
  • Serine* / metabolism

Substances

  • Serine
  • BRCA1 Protein
  • BRCA2 Protein
  • Poly(ADP-ribose) Polymerase Inhibitors
  • Glycoside Hydrolases
  • BRCA1 protein, human
  • BRCA2 protein, human
  • Poly (ADP-Ribose) Polymerase-1