Radiotherapy and MVA-MUC1-IL-2 vaccine act synergistically for inducing specific immunity to MUC-1 tumor antigen

Background We previously demonstrated that tumor irradiation potentiates cancer vaccines using genetic modification of tumor cells in murine tumor models. To investigate whether tumor irradiation augments the immune response to MUC1 tumor antigen, we have tested the efficacy of tumor irradiation com...

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Main Authors: Philippe Slos, Gilda G. Hillman, Lyndsey A. Reich, Shoshana E. Rothstein, Lisa M. Abernathy, Matthew D. Fountain, Kali Hankerd, Christopher K. Yunker, Joseph T. Rakowski, Eric Quemeneur
Format: Article
Language:English
Published: BMJ Publishing Group 2017-11-01
Series:Journal for ImmunoTherapy of Cancer
Online Access:https://jitc.bmj.com/content/5/1/4.full
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author Philippe Slos
Gilda G. Hillman
Lyndsey A. Reich
Shoshana E. Rothstein
Lisa M. Abernathy
Matthew D. Fountain
Kali Hankerd
Christopher K. Yunker
Joseph T. Rakowski
Eric Quemeneur
author_facet Philippe Slos
Gilda G. Hillman
Lyndsey A. Reich
Shoshana E. Rothstein
Lisa M. Abernathy
Matthew D. Fountain
Kali Hankerd
Christopher K. Yunker
Joseph T. Rakowski
Eric Quemeneur
author_sort Philippe Slos
collection DOAJ
description Background We previously demonstrated that tumor irradiation potentiates cancer vaccines using genetic modification of tumor cells in murine tumor models. To investigate whether tumor irradiation augments the immune response to MUC1 tumor antigen, we have tested the efficacy of tumor irradiation combined with an MVA-MUC1-IL2 cancer vaccine (Transgene TG4010) for murine renal adenocarcinoma (Renca) cells transfected with MUC1.Methods Established subcutaneous Renca-MUC1 tumors were treated with 8 Gy radiation on day 11 and peritumoral injections of MVA-MUC1-IL2 vector on day 12 and 17, or using a reverse sequence of vaccine followed by radiation. Growth delays were monitored by tumor measurements and histological responses were evaluated by immunohistochemistry. Specific immunity was assessed by challenge with Renca-MUC1 cells. Generation of tumor-specific T cells was detected by IFN-γ production from splenocytes stimulated in vitro with tumor lysates using ELISPOT assays.Results Tumor growth delays observed by tumor irradiation combined with MVA-MUC1-IL-2 vaccine were significantly more prolonged than those observed by vaccine, radiation, or radiation with MVA empty vector. The sequence of cancer vaccine followed by radiation two days later resulted in 55–58% complete responders and 60% mouse long-term survival. This sequence was more effective than that of radiation followed by vaccine leading to 24–30% complete responders and 30% mouse survival. Responding mice were immune to challenge with Renca-MUC1 cells, indicating the induction of specific tumor immunity. Histology studies of regressing tumors at 1 week after therapy, revealed extensive tumor destruction and a heavy infiltration of CD45+ leukocytes including F4/80+ macrophages, CD8+ cytotoxic T cells and CD4+ helper T cells. The generation of tumor-specific T cells by combined therapy was confirmed by IFN-γ secretion in tumor-stimulated splenocytes. An abscopal effect was measured by rejection of an untreated tumor on the contralateral flank to the tumor treated with radiation and vaccine.Conclusions These findings suggest that cancer vaccine given prior to local tumor irradiation augments an immune response targeted at tumor antigens that results in specific anti-tumor immunity. These findings support further exploration of the combination of radiotherapy with cancer vaccines for the treatment of cancer.
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spelling doaj-art-fe030e74722946d4a38f0b5332c2c2f32025-08-20T03:10:50ZengBMJ Publishing GroupJournal for ImmunoTherapy of Cancer2051-14262017-11-015110.1186/s40425-016-0204-3Radiotherapy and MVA-MUC1-IL-2 vaccine act synergistically for inducing specific immunity to MUC-1 tumor antigenPhilippe Slos0Gilda G. Hillman1Lyndsey A. Reich2Shoshana E. Rothstein3Lisa M. Abernathy4Matthew D. Fountain5Kali Hankerd6Christopher K. Yunker7Joseph T. Rakowski8Eric Quemeneur9Aff5 Present address: Oncodesign 20, rue Jean Mazen 21076 Dijon Cedex FranceAff1 grid.254444.70000000114567807Department of OncologyWayne State University School of Medicine, Karmanos Cancer Institute Hudson Webber Cancer Research Center, room 515, 4100 John R 48201 Detroit MI USAAff2 grid.254444.70000000114567807Radiation Oncology Division, Immunology & MicrobiologyWayne State University School of Medicine, Karmanos Cancer Institute 48201 Detroit MI USAAff1 grid.254444.70000000114567807Department of OncologyWayne State University School of Medicine, Karmanos Cancer Institute Hudson Webber Cancer Research Center, room 515, 4100 John R 48201 Detroit MI USAAff1 grid.254444.70000000114567807Department of OncologyWayne State University School of Medicine, Karmanos Cancer Institute Hudson Webber Cancer Research Center, room 515, 4100 John R 48201 Detroit MI USAAff1 grid.254444.70000000114567807Department of OncologyWayne State University School of Medicine, Karmanos Cancer Institute Hudson Webber Cancer Research Center, room 515, 4100 John R 48201 Detroit MI USAAff1 grid.254444.70000000114567807Department of OncologyWayne State University School of Medicine, Karmanos Cancer Institute Hudson Webber Cancer Research Center, room 515, 4100 John R 48201 Detroit MI USAAff1 grid.254444.70000000114567807Department of OncologyWayne State University School of Medicine, Karmanos Cancer Institute Hudson Webber Cancer Research Center, room 515, 4100 John R 48201 Detroit MI USAAff1 grid.254444.70000000114567807Department of OncologyWayne State University School of Medicine, Karmanos Cancer Institute Hudson Webber Cancer Research Center, room 515, 4100 John R 48201 Detroit MI USA3Transgene, Illkirch-Graffenstaden, FranceBackground We previously demonstrated that tumor irradiation potentiates cancer vaccines using genetic modification of tumor cells in murine tumor models. To investigate whether tumor irradiation augments the immune response to MUC1 tumor antigen, we have tested the efficacy of tumor irradiation combined with an MVA-MUC1-IL2 cancer vaccine (Transgene TG4010) for murine renal adenocarcinoma (Renca) cells transfected with MUC1.Methods Established subcutaneous Renca-MUC1 tumors were treated with 8 Gy radiation on day 11 and peritumoral injections of MVA-MUC1-IL2 vector on day 12 and 17, or using a reverse sequence of vaccine followed by radiation. Growth delays were monitored by tumor measurements and histological responses were evaluated by immunohistochemistry. Specific immunity was assessed by challenge with Renca-MUC1 cells. Generation of tumor-specific T cells was detected by IFN-γ production from splenocytes stimulated in vitro with tumor lysates using ELISPOT assays.Results Tumor growth delays observed by tumor irradiation combined with MVA-MUC1-IL-2 vaccine were significantly more prolonged than those observed by vaccine, radiation, or radiation with MVA empty vector. The sequence of cancer vaccine followed by radiation two days later resulted in 55–58% complete responders and 60% mouse long-term survival. This sequence was more effective than that of radiation followed by vaccine leading to 24–30% complete responders and 30% mouse survival. Responding mice were immune to challenge with Renca-MUC1 cells, indicating the induction of specific tumor immunity. Histology studies of regressing tumors at 1 week after therapy, revealed extensive tumor destruction and a heavy infiltration of CD45+ leukocytes including F4/80+ macrophages, CD8+ cytotoxic T cells and CD4+ helper T cells. The generation of tumor-specific T cells by combined therapy was confirmed by IFN-γ secretion in tumor-stimulated splenocytes. An abscopal effect was measured by rejection of an untreated tumor on the contralateral flank to the tumor treated with radiation and vaccine.Conclusions These findings suggest that cancer vaccine given prior to local tumor irradiation augments an immune response targeted at tumor antigens that results in specific anti-tumor immunity. These findings support further exploration of the combination of radiotherapy with cancer vaccines for the treatment of cancer.https://jitc.bmj.com/content/5/1/4.full
spellingShingle Philippe Slos
Gilda G. Hillman
Lyndsey A. Reich
Shoshana E. Rothstein
Lisa M. Abernathy
Matthew D. Fountain
Kali Hankerd
Christopher K. Yunker
Joseph T. Rakowski
Eric Quemeneur
Radiotherapy and MVA-MUC1-IL-2 vaccine act synergistically for inducing specific immunity to MUC-1 tumor antigen
Journal for ImmunoTherapy of Cancer
title Radiotherapy and MVA-MUC1-IL-2 vaccine act synergistically for inducing specific immunity to MUC-1 tumor antigen
title_full Radiotherapy and MVA-MUC1-IL-2 vaccine act synergistically for inducing specific immunity to MUC-1 tumor antigen
title_fullStr Radiotherapy and MVA-MUC1-IL-2 vaccine act synergistically for inducing specific immunity to MUC-1 tumor antigen
title_full_unstemmed Radiotherapy and MVA-MUC1-IL-2 vaccine act synergistically for inducing specific immunity to MUC-1 tumor antigen
title_short Radiotherapy and MVA-MUC1-IL-2 vaccine act synergistically for inducing specific immunity to MUC-1 tumor antigen
title_sort radiotherapy and mva muc1 il 2 vaccine act synergistically for inducing specific immunity to muc 1 tumor antigen
url https://jitc.bmj.com/content/5/1/4.full
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