Sustained Type I interferon signaling as a mechanism of resistance to PD-1 blockade

Cell Res. 2019 Oct;29(10):846-861. doi: 10.1038/s41422-019-0224-x. Epub 2019 Sep 3.

Abstract

PD-1 blockade represents a major therapeutic avenue in anticancer immunotherapy. Delineating mechanisms of secondary resistance to this strategy is increasingly important. Here, we identified the deleterious role of signaling via the type I interferon (IFN) receptor in tumor and antigen presenting cells, that induced the expression of nitric oxide synthase 2 (NOS2), associated with intratumor accumulation of regulatory T cells (Treg) and myeloid cells and acquired resistance to anti-PD-1 monoclonal antibody (mAb). Sustained IFNβ transcription was observed in resistant tumors, in turn inducing PD-L1 and NOS2 expression in both tumor and dendritic cells (DC). Whereas PD-L1 was not involved in secondary resistance to anti-PD-1 mAb, pharmacological or genetic inhibition of NOS2 maintained long-term control of tumors by PD-1 blockade, through reduction of Treg and DC activation. Resistance to immunotherapies, including anti-PD-1 mAb in melanoma patients, was also correlated with the induction of a type I IFN signature. Hence, the role of type I IFN in response to PD-1 blockade should be revisited as sustained type I IFN signaling may contribute to resistance to therapy.

MeSH terms

  • Animals
  • Antibodies, Monoclonal / immunology
  • Antibodies, Monoclonal / pharmacology*
  • Antibodies, Monoclonal / therapeutic use
  • B7-H1 Antigen / metabolism
  • Cell Line, Tumor
  • Dendritic Cells / cytology
  • Dendritic Cells / metabolism
  • Drug Resistance, Neoplasm
  • Humans
  • Interferon Type I / metabolism*
  • Kaplan-Meier Estimate
  • Melanoma / drug therapy
  • Melanoma / mortality
  • Melanoma / pathology
  • Mice
  • Mice, Inbred C57BL
  • Neoplasms / drug therapy
  • Neoplasms / mortality
  • Neoplasms / pathology
  • Nitric Oxide Synthase Type II / metabolism
  • Programmed Cell Death 1 Receptor / immunology*
  • Signal Transduction / drug effects*
  • T-Lymphocytes, Regulatory / cytology
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism

Substances

  • Antibodies, Monoclonal
  • B7-H1 Antigen
  • CD274 protein, human
  • Interferon Type I
  • Programmed Cell Death 1 Receptor
  • Nitric Oxide Synthase Type II