Immune cell-poor melanomas benefit from PD-1 blockade after targeted type I IFN activation

Cancer Discov. 2014 Jun;4(6):674-87. doi: 10.1158/2159-8290.CD-13-0458. Epub 2014 Mar 3.

Abstract

Infiltration of human melanomas with cytotoxic immune cells correlates with spontaneous type I IFN activation and a favorable prognosis. Therapeutic blockade of immune-inhibitory receptors in patients with preexisting lymphocytic infiltrates prolongs survival, but new complementary strategies are needed to activate cellular antitumor immunity in immune cell-poor melanomas. Here, we show that primary melanomas in Hgf-Cdk4(R24C) mice, which imitate human immune cell-poor melanomas with a poor outcome, escape IFN-induced immune surveillance and editing. Peritumoral injections of immunostimulatory RNA initiated a cytotoxic inflammatory response in the tumor microenvironment and significantly impaired tumor growth. This critically required the coordinated induction of type I IFN responses by dendritic, myeloid, natural killer, and T cells. Importantly, antibody-mediated blockade of the IFN-induced immune-inhibitory interaction between PD-L1 and PD-1 receptors further prolonged the survival. These results highlight important interconnections between type I IFNs and immune-inhibitory receptors in melanoma pathogenesis, which serve as targets for combination immunotherapies.

Significance: Using a genetically engineered mouse melanoma model, we demonstrate that targeted activation of the type I IFN system with immunostimulatory RNA in combination with blockade of immune-inhibitory receptors is a rational strategy to expose immune cell-poor tumors to cellular immune surveillance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 9,10-Dimethyl-1,2-benzanthracene
  • Animals
  • B7-H1 Antigen / immunology
  • Carcinogens
  • Immunoglobulin G / administration & dosage
  • Immunologic Factors / administration & dosage
  • Interferon Type I / immunology*
  • Melanoma, Experimental / drug therapy*
  • Melanoma, Experimental / immunology
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Poly I-C / administration & dosage
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors*
  • Programmed Cell Death 1 Receptor / immunology
  • RNA / administration & dosage
  • Tumor Microenvironment / immunology

Substances

  • B7-H1 Antigen
  • Carcinogens
  • Cd274 protein, mouse
  • Immunoglobulin G
  • Immunologic Factors
  • Interferon Type I
  • Programmed Cell Death 1 Receptor
  • 9,10-Dimethyl-1,2-benzanthracene
  • RNA
  • Poly I-C