Overcoming Genetically Based Resistance Mechanisms to PD-1 Blockade

Cancer Discov. 2020 Aug;10(8):1140-1157. doi: 10.1158/2159-8290.CD-19-1409. Epub 2020 May 28.

Abstract

Mechanism-based strategies to overcome resistance to PD-1 blockade therapy are urgently needed. We developed genetic acquired resistant models of JAK1, JAK2, and B2M loss-of-function mutations by gene knockout in human and murine cell lines. Human melanoma cell lines with JAK1/2 knockout became insensitive to IFN-induced antitumor effects, while B2M knockout was no longer recognized by antigen-specific T cells and hence was resistant to cytotoxicity. All of these mutations led to resistance to anti-PD-1 therapy in vivo. JAK1/2-knockout resistance could be overcome with the activation of innate and adaptive immunity by intratumoral Toll-like receptor 9 agonist administration together with anti-PD-1, mediated by natural killer (NK) and CD8 T cells. B2M-knockout resistance could be overcome by NK-cell and CD4 T-cell activation using the CD122 preferential IL2 agonist bempegaldesleukin. Therefore, mechanistically designed combination therapies can overcome genetic resistance to PD-1 blockade therapy. SIGNIFICANCE: The activation of IFN signaling through pattern recognition receptors and the stimulation of NK cells overcome genetic mechanisms of resistance to PD-1 blockade therapy mediated through deficient IFN receptor and antigen presentation pathways. These approaches are being tested in the clinic to improve the antitumor activity of PD-1 blockade therapy.This article is highlighted in the In This Issue feature, p. 1079.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / immunology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Drug Resistance, Neoplasm / genetics*
  • Humans
  • Interferons / pharmacology
  • Interleukin-2 / analogs & derivatives
  • Interleukin-2 / immunology
  • Interleukin-2 / pharmacology
  • Interleukin-2 / therapeutic use
  • Janus Kinase 1 / genetics*
  • Janus Kinase 2 / genetics*
  • Killer Cells, Natural / immunology
  • Loss of Function Mutation
  • Mice, Inbred C57BL
  • Neoplasms / drug therapy
  • Neoplasms / genetics
  • Neoplasms / immunology
  • Polyethylene Glycols / pharmacology
  • Polyethylene Glycols / therapeutic use
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors*
  • Toll-Like Receptor 9 / immunology
  • beta 2-Microglobulin / genetics*

Substances

  • Interleukin-2
  • Programmed Cell Death 1 Receptor
  • Toll-Like Receptor 9
  • beta 2-Microglobulin
  • Polyethylene Glycols
  • Interferons
  • bempegaldesleukin
  • Janus Kinase 1
  • Janus Kinase 2