ATR kinase inhibitor AZD6738 potentiates CD8+ T cell-dependent antitumor activity following radiation

J Clin Invest. 2018 Aug 31;128(9):3926-3940. doi: 10.1172/JCI96519. Epub 2018 Aug 13.

Abstract

DNA-damaging chemotherapy and radiation therapy are integrated into the treatment paradigm of the majority of cancer patients. Recently, immunotherapy that targets the immunosuppressive interaction between programmed death 1 (PD-1) and its ligand PD-L1 has been approved for malignancies including non-small cell lung cancer, melanoma, and head and neck squamous cell carcinoma. ATR is a DNA damage-signaling kinase activated at damaged replication forks, and ATR kinase inhibitors potentiate the cytotoxicity of DNA-damaging chemotherapies. We show here that the ATR kinase inhibitor AZD6738 combines with conformal radiation therapy to attenuate radiation-induced CD8+ T cell exhaustion and potentiate CD8+ T cell activity in mouse models of Kras-mutant cancer. Mechanistically, AZD6738 blocks radiation-induced PD-L1 upregulation on tumor cells and dramatically decreases the number of tumor-infiltrating Tregs. Remarkably, AZD6738 combines with conformal radiation therapy to generate immunologic memory in complete responder mice. Our work raises the possibility that a single pharmacologic agent may enhance the cytotoxic effects of radiation while concurrently potentiating radiation-induced antitumor immune responses.

Keywords: Cancer; Immunology; Oncology.

Publication types

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

MeSH terms

  • Adenocarcinoma of Lung / drug therapy
  • Adenocarcinoma of Lung / immunology
  • Adenocarcinoma of Lung / radiotherapy
  • Animals
  • Ataxia Telangiectasia Mutated Proteins / antagonists & inhibitors
  • B7-H1 Antigen / metabolism
  • CD8-Positive T-Lymphocytes / drug effects*
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / radiation effects*
  • Cell Line, Tumor
  • Chemoradiotherapy
  • Colorectal Neoplasms / drug therapy
  • Colorectal Neoplasms / immunology
  • Colorectal Neoplasms / radiotherapy
  • Humans
  • Indoles
  • Lymphocytes, Tumor-Infiltrating / drug effects
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Lymphocytes, Tumor-Infiltrating / radiation effects
  • Mice
  • Mice, Inbred BALB C
  • Morpholines
  • Neoplasms, Experimental / drug therapy*
  • Neoplasms, Experimental / immunology
  • Neoplasms, Experimental / radiotherapy*
  • Protein Kinase Inhibitors / pharmacokinetics
  • Protein Kinase Inhibitors / pharmacology*
  • Proto-Oncogene Proteins p21(ras) / genetics
  • Pyrimidines / pharmacokinetics
  • Pyrimidines / pharmacology*
  • Radiotherapy, Conformal
  • Sulfonamides
  • Sulfoxides / pharmacokinetics
  • Sulfoxides / pharmacology*

Substances

  • B7-H1 Antigen
  • Cd274 protein, mouse
  • Indoles
  • Morpholines
  • Protein Kinase Inhibitors
  • Pyrimidines
  • Sulfonamides
  • Sulfoxides
  • ceralasertib
  • Atr protein, mouse
  • Ataxia Telangiectasia Mutated Proteins
  • Hras protein, mouse
  • Proto-Oncogene Proteins p21(ras)