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Cancer Immunology Research
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Deciphering the Immunomodulatory Capacity of Oncolytic Vaccinia Virus to Enhance the Immune Response to Breast Cancer

Brittany A. Umer, Ryan S. Noyce, Brian C. Franczak, Mira M. Shenouda, Rees G. Kelly, Nicole A. Favis, Megan Desaulniers, Troy A. Baldwin, Mary M. Hitt and David H. Evans
Brittany A. Umer
1Department of Medical Microbiology & Immunology, University of Alberta, Edmonton, Alberta, Canada.
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Ryan S. Noyce
1Department of Medical Microbiology & Immunology, University of Alberta, Edmonton, Alberta, Canada.
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Brian C. Franczak
2Department of Statistics, MacEwan University, Edmonton, Alberta, Canada.
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Mira M. Shenouda
1Department of Medical Microbiology & Immunology, University of Alberta, Edmonton, Alberta, Canada.
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Rees G. Kelly
1Department of Medical Microbiology & Immunology, University of Alberta, Edmonton, Alberta, Canada.
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Nicole A. Favis
1Department of Medical Microbiology & Immunology, University of Alberta, Edmonton, Alberta, Canada.
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Megan Desaulniers
1Department of Medical Microbiology & Immunology, University of Alberta, Edmonton, Alberta, Canada.
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Troy A. Baldwin
1Department of Medical Microbiology & Immunology, University of Alberta, Edmonton, Alberta, Canada.
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Mary M. Hitt
3Department of Oncology, University of Alberta, Edmonton, Alberta, Canada.
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  • ORCID record for Mary M. Hitt
David H. Evans
1Department of Medical Microbiology & Immunology, University of Alberta, Edmonton, Alberta, Canada.
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  • For correspondence: devans@ualberta.ca
DOI: 10.1158/2326-6066.CIR-19-0703 Published May 2020
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Abstract

Vaccinia virus (VACV) is a double-stranded DNA virus that devotes a large portion of its 200 kbp genome to suppressing and manipulating the immune response of its host. Here, we investigated how targeted removal of immunomodulatory genes from the VACV genome impacted immune cells in the tumor microenvironment with the intention of improving the therapeutic efficacy of VACV in breast cancer. We performed a head-to-head comparison of six mutant oncolytic VACVs, each harboring deletions in genes that modulate different cellular pathways, such as nucleotide metabolism, apoptosis, inflammation, and chemokine and interferon signaling. We found that even minor changes to the VACV genome can impact the immune cell compartment in the tumor microenvironment. Viral genome modifications had the capacity to alter lymphocytic and myeloid cell compositions in tumors and spleens, PD-1 expression, and the percentages of virus-targeted and tumor-targeted CD8+ T cells. We observed that while some gene deletions improved responses in the nonimmunogenic 4T1 tumor model, very little therapeutic improvement was seen in the immunogenic HER2/neu TuBo model with the various genome modifications. We observed that the most promising candidate genes for deletion were those that interfere with interferon signaling. Collectively, this research helped focus attention on the pathways that modulate the immune response in the context of VACV oncolytic virotherapy. They also suggest that the greatest benefits to be obtained with these treatments may not always be seen in “hot tumors.”

Footnotes

  • Note: Supplementary data for this article are available at Cancer Immunology Research Online (http://cancerimmunolres.aacrjournals.org/).

  • Cancer Immunol Res 2020;8:618–31

  • Received September 18, 2019.
  • Revision received December 12, 2019.
  • Accepted February 27, 2020.
  • Published first March 3, 2020.
  • ©2020 American Association for Cancer Research.
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Cancer Immunology Research: 8 (5)
May 2020
Volume 8, Issue 5
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Deciphering the Immunomodulatory Capacity of Oncolytic Vaccinia Virus to Enhance the Immune Response to Breast Cancer
Brittany A. Umer, Ryan S. Noyce, Brian C. Franczak, Mira M. Shenouda, Rees G. Kelly, Nicole A. Favis, Megan Desaulniers, Troy A. Baldwin, Mary M. Hitt and David H. Evans
Cancer Immunol Res May 1 2020 (8) (5) 618-631; DOI: 10.1158/2326-6066.CIR-19-0703

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Deciphering the Immunomodulatory Capacity of Oncolytic Vaccinia Virus to Enhance the Immune Response to Breast Cancer
Brittany A. Umer, Ryan S. Noyce, Brian C. Franczak, Mira M. Shenouda, Rees G. Kelly, Nicole A. Favis, Megan Desaulniers, Troy A. Baldwin, Mary M. Hitt and David H. Evans
Cancer Immunol Res May 1 2020 (8) (5) 618-631; DOI: 10.1158/2326-6066.CIR-19-0703
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