Deletion of F4L (ribonucleotide reductase) in vaccinia virus produces a selective oncolytic virus and promotes anti-tumor immunity with superior safety in bladder cancer models

EMBO Mol Med. 2017 May;9(5):638-654. doi: 10.15252/emmm.201607296.

Abstract

Bladder cancer has a recurrence rate of up to 80% and many patients require multiple treatments that often fail, eventually leading to disease progression. In particular, standard of care for high-grade disease, Bacillus Calmette-Guérin (BCG), fails in 30% of patients. We have generated a novel oncolytic vaccinia virus (VACV) by mutating the F4L gene that encodes the virus homolog of the cell-cycle-regulated small subunit of ribonucleotide reductase (RRM2). The F4L-deleted VACVs are highly attenuated in normal tissues, and since cancer cells commonly express elevated RRM2 levels, have tumor-selective replication and cell killing. These F4L-deleted VACVs replicated selectively in immune-competent rat AY-27 and xenografted human RT112-luc orthotopic bladder cancer models, causing significant tumor regression or complete ablation with no toxicity. It was also observed that rats cured of AY-27 tumors by VACV treatment developed anti-tumor immunity as evidenced by tumor rejection upon challenge and by ex vivo cytotoxic T-lymphocyte assays. Finally, F4L-deleted VACVs replicated in primary human bladder cancer explants. Our findings demonstrate the enhanced safety and selectivity of F4L-deleted VACVs, with application as a promising therapy for patients with BCG-refractory cancers and immune dysregulation.

Keywords: bladder cancer; immunotherapy; oncolytic virus; ribonucleotide reductase; vaccinia virus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Female
  • Gene Deletion*
  • Humans
  • Immunity
  • Mice, Inbred BALB C
  • Mice, Nude
  • Oncolytic Virotherapy
  • Oncolytic Viruses / genetics*
  • Oncolytic Viruses / immunology
  • Oncolytic Viruses / physiology
  • Rats
  • Ribonucleotide Reductases / genetics*
  • Ribonucleotide Reductases / immunology
  • Tumor Cells, Cultured
  • Urinary Bladder / immunology
  • Urinary Bladder / pathology
  • Urinary Bladder Neoplasms / immunology
  • Urinary Bladder Neoplasms / pathology
  • Urinary Bladder Neoplasms / therapy*
  • Vaccinia virus / genetics*
  • Vaccinia virus / immunology
  • Vaccinia virus / physiology
  • Viral Proteins / genetics*
  • Viral Proteins / immunology
  • Virus Replication

Substances

  • Viral Proteins
  • Ribonucleotide Reductases