Programmed death (PD)-1/PD-ligand 1 blockade mediates antiangiogenic effects by tumor-derived CXCL10/11 as a potential predictive biomarker

Cancer Sci. 2021 Dec;112(12):4853-4866. doi: 10.1111/cas.15161. Epub 2021 Oct 23.

Abstract

Immune checkpoint inhibitor (ICI) programmed death (PD)-1/PD-ligand 1 (PD-L1) blockade has been approved for various cancers. However, the underlying antitumor mechanisms mediated by ICIs and the predictive biomarkers remain unclear. We report the effects of anti-PD-L1/PD-1 Ab in tumor angiogenesis. In syngeneic mouse models, anti-PD-L1 Ab inhibited tumor angiogenesis and induces net-like hypoxia only in ICI-sensitive cell lines. In tumor tissue and serum of ICI-sensitive cell line-bearing mice, interferon-γ (IFN-γ) inducible angiostatic chemokines CXCL10/11 were upregulated by PD-L1 blockade. In vitro, CXCL10/11 gene upregulation by IFN-γ stimulation in tumor cell lines correlated with the sensitivity of PD-L1 blockade. The CXCL10/11 receptor CXCR3-neutralizing Ab or CXCL11 silencing in tumor cells inhibited the antiangiogenic effect of PD-L1 blockade in vivo. In pretreatment serum of lung carcinoma patients receiving anti-PD-1 Ab, the concentration of CXCL10/11 significantly correlated with the clinical outcome. Our results indicate the antiangiogenic function of PD-1/PD-L1 blockade and identify tumor-derived CXCL10/11 as a potential circulating biomarker of therapeutic sensitivity.

Keywords: CXCL10/11; angiogenesis; biomarker; immune checkpoint inhibitor; lung cancer.

MeSH terms

  • Animals
  • B7-H1 Antigen / antagonists & inhibitors
  • B7-H1 Antigen / metabolism*
  • Biomarkers, Tumor / metabolism
  • Carcinoma, Non-Small-Cell Lung / drug therapy
  • Carcinoma, Non-Small-Cell Lung / metabolism
  • Cell Line, Tumor
  • Chemokine CXCL10 / genetics
  • Chemokine CXCL10 / metabolism*
  • Chemokine CXCL11 / genetics
  • Chemokine CXCL11 / metabolism*
  • HEK293 Cells
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Interferon-gamma / metabolism
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / metabolism
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Inbred CBA
  • Mice, Nude
  • Neoplasms, Experimental / blood supply
  • Neoplasms, Experimental / drug therapy
  • Neoplasms, Experimental / metabolism*
  • Neovascularization, Pathologic / metabolism*
  • Neovascularization, Pathologic / prevention & control
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor / metabolism*
  • RNA Interference

Substances

  • B7-H1 Antigen
  • Biomarkers, Tumor
  • Chemokine CXCL10
  • Chemokine CXCL11
  • Immune Checkpoint Inhibitors
  • Programmed Cell Death 1 Receptor
  • Interferon-gamma