Immunotherapeutic synergy between anti-CD137 mAb and intratumoral administration of a cytopathic Semliki Forest virus encoding IL-12

Mol Ther. 2012 Sep;20(9):1664-75. doi: 10.1038/mt.2012.56. Epub 2012 Jun 26.

Abstract

Intratumoral injection of Semliki Forest virus encoding interleukin-12 (SFV-IL-12) combines acute expression of IL-12 and stressful apoptosis of infected malignant cells. Agonist antibodies directed to costimulatory receptor CD137 (4-1BB) strongly amplify pre-existing cellular immune responses toward weak tumor antigens. In this study, we provide evidence for powerful synergistic effects of a combined strategy consisting of intratumoral injection of SFV-IL-12 and systemic delivery of agonist anti-CD137 monoclonal antibodies (mAbs), which was substantiated against poorly immunogenic B16 melanomas (B16-OVA and B16.F10) and TC-1 lung carcinomas. Effector CD8(β)(+) T cells were sufficient to mediate complete tumor eradications. Accordingly, there was an intensely synergistic in vivo enhancement of cytotoxic T lymphocytes (CTL)-mediated immunity against the tumor antigens OVA and tyrosine-related protein-2 (TRP-2). This train of phenomena led to long-lasting tumor-specific immunity against rechallenge, attained transient control of the progression of concomitant tumor lesions that were not directly treated with SFV-IL-12 and caused autoimmune vitiligo. Importantly, we found that SFV-IL-12 intratumoral injection induces bright expression of CD137 on most tumor-infiltrating CD8(+) T lymphocytes, thereby providing more abundant targets for the action of the agonist antibody. This efficacious combinatorial immunotherapy strategy offers feasibility for clinical translation since anti-CD137 mAbs are already undergoing clinical trials and development of clinical-grade SFV-IL-12 vectors is in progress.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Monoclonal / administration & dosage
  • Antibodies, Monoclonal / immunology*
  • Apoptosis / drug effects
  • CD8-Positive T-Lymphocytes / drug effects
  • CD8-Positive T-Lymphocytes / immunology
  • Carcinoma / immunology
  • Carcinoma / mortality
  • Carcinoma / therapy*
  • Cell Line, Tumor
  • Cricetinae
  • Gene Expression / drug effects
  • Immunity, Cellular / drug effects
  • Immunologic Memory / drug effects
  • Immunotherapy / methods
  • Injections, Intralesional
  • Injections, Intravenous
  • Interleukin-12 / administration & dosage
  • Interleukin-12 / genetics
  • Interleukin-12 / immunology*
  • Intramolecular Oxidoreductases / genetics
  • Intramolecular Oxidoreductases / immunology
  • Lung Neoplasms / immunology
  • Lung Neoplasms / mortality
  • Lung Neoplasms / therapy*
  • Melanoma, Experimental / immunology
  • Melanoma, Experimental / mortality
  • Melanoma, Experimental / therapy*
  • Mice
  • Semliki forest virus / genetics
  • Semliki forest virus / immunology*
  • Skin Neoplasms / immunology
  • Skin Neoplasms / mortality
  • Skin Neoplasms / therapy*
  • Survival Rate
  • T-Lymphocytes, Cytotoxic / drug effects
  • T-Lymphocytes, Cytotoxic / immunology
  • Tumor Necrosis Factor Receptor Superfamily, Member 9 / agonists
  • Tumor Necrosis Factor Receptor Superfamily, Member 9 / immunology

Substances

  • Antibodies, Monoclonal
  • Tumor Necrosis Factor Receptor Superfamily, Member 9
  • Interleukin-12
  • Intramolecular Oxidoreductases
  • dopachrome isomerase