Oncolytic Maraba virus armed with tumor antigen boosts vaccine priming and reveals diverse therapeutic response patterns when combined with checkpoint blockade in ovarian cancer

J Immunother Cancer. 2019 Jul 17;7(1):189. doi: 10.1186/s40425-019-0641-x.

Abstract

Background: Cancer immunotherapies are emerging as promising treatment strategies for ovarian cancer patients that experience disease relapse following first line therapy. As such, identifying strategies to bolster anti-tumor immunity and limit immune suppression, while recognizing diverse patterns of tumor response to immunotherapy is critical to selecting treatment combinations that lead to durable therapeutic benefit.

Methods: Using a pre-clinical mouse model, we evaluated a heterologous prime/boost vaccine in combination with checkpoint blockade to treat metastatic intraperitoneal ovarian cancer. Vaccine-elicited CD8+ T cell responses and changes in the tumor microenvironment following treatment were analyzed and compared to treatment outcome. Kinetics of intraperitoneal tumor growth were assessed using non-invasive magnetic resonance imaging (MRI).

Results: Vaccine priming followed by antigen-armed oncolytic Maraba virus boosting elicited robust tumor-specific CD8+ T cell responses that improved tumor control and led to unique immunological changes in the tumor, including a signature that correlated with improved clinical outcome of ovarian cancer patients. However, this treatment was not curative and T cells in the tumor microenvironment (TME) were functionally suppressed. Combination PD-1 blockade partially overcame the adaptive resistance in the tumor observed in response to prime/boost vaccination, restoring CD8+ T cell function in the TME and enhancing the therapeutic response. Non-invasive MRI of tumors during the course of combination treatment revealed heterogeneous radiologic response patterns following treatment, including pseudo-progression, which was associated with improved tumor control prior to relapse.

Conclusions: Our findings point to a key hierarchical role for PD-1 signaling and adaptive immune resistance in the ovarian TME in determining the functional fate of tumor-specific CD8+ T cells, even in the context of robust therapy mediated anti-tumor immunity, as well as the ability of multiple unique patterns of therapeutic response to result in durable tumor control.

Keywords: Adaptive immune resistance; Cancer; Cancer vaccine; Immunotherapy; MRI; Oncolytic virus; Ovarian cancer; PD-1 blockade.

Publication types

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

MeSH terms

  • Animals
  • Antigens, Neoplasm / genetics*
  • Antigens, Neoplasm / immunology
  • CD8-Positive T-Lymphocytes / immunology
  • Cancer Vaccines / administration & dosage*
  • Cancer Vaccines / immunology
  • Cell Line, Tumor
  • Combined Modality Therapy
  • Female
  • Humans
  • Intramolecular Oxidoreductases / genetics*
  • Intramolecular Oxidoreductases / immunology
  • Mice
  • Neoplasm Metastasis
  • Oncolytic Viruses / genetics
  • Oncolytic Viruses / physiology
  • Ovalbumin / genetics*
  • Ovalbumin / immunology
  • Ovarian Neoplasms / diagnostic imaging
  • Ovarian Neoplasms / immunology
  • Ovarian Neoplasms / therapy*
  • Treatment Outcome
  • Tumor Microenvironment
  • Vesiculovirus / genetics
  • Vesiculovirus / physiology*
  • Xenograft Model Antitumor Assays

Substances

  • Antigens, Neoplasm
  • Cancer Vaccines
  • MIS416 vaccine
  • Ovalbumin
  • Intramolecular Oxidoreductases
  • dopachrome isomerase