Upregulation of CXCL1 and LY9 contributes to BRCAness in ovarian cancer and mediates response to PARPi and immune checkpoint blockade

Br J Cancer. 2022 Sep;127(5):916-926. doi: 10.1038/s41416-022-01836-0. Epub 2022 May 26.

Abstract

Background: Mutations in BRCA1 or BRCA2 (BRCA1/2) cause homologous recombination deficiency (HRD). Ovarian cancer (OvCa) patients harbouring HRD beyond BRCA1/2 mutation result in a state referred to as "BRCAness". OvCa with BRCAness could benefit from PARP inhibitors. This study aims to identify a signature to detect the BRCAness population at the transcriptome level.

Methods: We used a rank-based algorithm to develop a qualitative BRCAness signature for OvCa. Upregulation of CXCL1 with downregulation of SV2A and upregulation of LY9 with downregulation of CHRNB3 were constructed as the BRCAness signature (2 gene pairs, 2-GPS) for OvCa.

Results: OvCa samples that were classified as BRCAness by 2-GPS showed improved overall survival, progression-free survival and exhibited increased multi-omics alterations in homologous recombination genes and enhanced sensitivity to immune checkpoint blockade. BRCAness cells were sensitive to PARP inhibitors. By biological experiments, we validated SKOV3 cells and patients with HRD exhibited higher expression of CXCL1 than SV2A and higher expression of LY9 than CHRNB3 at mRNA level. Both SKOV3 and A2780 with HRD were sensitive to mitomycin C, cisplatin and olaparib.

Conclusions: In conclusion, 2-GPS could robustly predict BRCAness OvCa at the individual level and extend the population who may benefit from PARP inhibitors.

MeSH terms

  • BRCA1 Protein / genetics
  • BRCA2 Protein / genetics
  • Carcinoma, Ovarian Epithelial / drug therapy
  • Carcinoma, Ovarian Epithelial / genetics
  • Cell Line, Tumor
  • Chemokine CXCL1* / genetics
  • Female
  • Homologous Recombination
  • Humans
  • Immune Checkpoint Inhibitors / therapeutic use
  • Ovarian Neoplasms* / drug therapy
  • Ovarian Neoplasms* / genetics
  • Poly(ADP-ribose) Polymerase Inhibitors / pharmacology
  • Poly(ADP-ribose) Polymerase Inhibitors / therapeutic use
  • Signaling Lymphocytic Activation Molecule Family* / genetics
  • Up-Regulation

Substances

  • BRCA1 Protein
  • BRCA2 Protein
  • CXCL1 protein, human
  • Chemokine CXCL1
  • Immune Checkpoint Inhibitors
  • LY9 protein, human
  • Poly(ADP-ribose) Polymerase Inhibitors
  • Signaling Lymphocytic Activation Molecule Family