Universal off-the-shelf combination immunotherapy using oncolytic viruses to redirect T cell engagers to target solid tumors

Background Bispecific T cell engager (BiTE), such as blinatumomab, has demonstrated significant clinical success in treating hematological malignancies like B cell acute lymphoblastic leukemia and non-Hodgkin's lymphoma. However, the application of BiTEs in solid tumors has proven challenging,...

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Main Authors: Stephen J Forman, Wen-Chung Chang, Xiuli Wang, Anthony K Park, Ryan Urak, Yuman Fong, Monil Shah, Colin Cook, Yukiko Yamaguchi, Saul J Priceman, Cathy Lu, Shyambabu Chaurasiya, Isabel Monroy, Yuwei Ren, Hannah Valencia, Jackson Lent-Koop, Seonah Kang, Lupita Lopez, John P Murad, Leslie Mi Ok Chong
Format: Article
Language:English
Published: BMJ Publishing Group 2025-08-01
Series:Journal for ImmunoTherapy of Cancer
Online Access:https://jitc.bmj.com/content/13/8/e011051.full
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author Stephen J Forman
Wen-Chung Chang
Xiuli Wang
Anthony K Park
Ryan Urak
Yuman Fong
Monil Shah
Colin Cook
Yukiko Yamaguchi
Saul J Priceman
Cathy Lu
Shyambabu Chaurasiya
Isabel Monroy
Yuwei Ren
Hannah Valencia
Jackson Lent-Koop
Seonah Kang
Lupita Lopez
John P Murad
Leslie Mi Ok Chong
author_facet Stephen J Forman
Wen-Chung Chang
Xiuli Wang
Anthony K Park
Ryan Urak
Yuman Fong
Monil Shah
Colin Cook
Yukiko Yamaguchi
Saul J Priceman
Cathy Lu
Shyambabu Chaurasiya
Isabel Monroy
Yuwei Ren
Hannah Valencia
Jackson Lent-Koop
Seonah Kang
Lupita Lopez
John P Murad
Leslie Mi Ok Chong
author_sort Stephen J Forman
collection DOAJ
description Background Bispecific T cell engager (BiTE), such as blinatumomab, has demonstrated significant clinical success in treating hematological malignancies like B cell acute lymphoblastic leukemia and non-Hodgkin's lymphoma. However, the application of BiTEs in solid tumors has proven challenging, primarily due to the lack of targetable tumor antigens and the immunologically “cold” nature of the tumor microenvironment, which limits immune system activation.Methods We developed a novel oncolytic virus (OV) platform by engineering a chimeric vaccinia virus to express either a truncated non-signaling CD19 antigen (CD19t) or truncated B cell maturation antigen (BCMAt) on the surface of infected tumor cells. Here, we advance a combinatorial platform using an OV to redirect CD19-targeted or BCMA-targeted T cell engagers (TCEs) to drive antitumor responses against multiple solid tumors.Results We found that OV-infected tumor cells in combination with TCEs significantly improved tumor cell killing against solid tumor models, with efficacy comparable to that of chimeric antigen receptor T cells. This combination approach enhanced antitumor responses using in vivo human tumor xenograft models and promoted more effective elimination of solid tumor cells than either therapy alone. Our studies highlight OVs combined with clinically approved TCEs as a readily translatable, tumor-agnostic, off-the-shelf strategy to effectively target solid tumors.Conclusions Our findings demonstrate that the combination of OV and TCEs offers a promising strategy to drive antitumor immune responses against solid tumors. This approach represents a novel and universal platform currently in phase 1 clinical trial combining TCE therapy with oncolytic virotherapy, overcoming antigen heterogeneity and immunological barriers for the effective treatment of solid tumors.
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spelling doaj-art-d401acd295ee46dbb013b49b3c2ae5c42025-08-20T03:41:18ZengBMJ Publishing GroupJournal for ImmunoTherapy of Cancer2051-14262025-08-0113810.1136/jitc-2024-011051Universal off-the-shelf combination immunotherapy using oncolytic viruses to redirect T cell engagers to target solid tumorsStephen J Forman0Wen-Chung Chang1Xiuli Wang2Anthony K Park3Ryan Urak4Yuman Fong5Monil Shah6Colin Cook7Yukiko Yamaguchi8Saul J Priceman9Cathy Lu10Shyambabu Chaurasiya11Isabel Monroy12Yuwei Ren13Hannah Valencia14Jackson Lent-Koop15Seonah Kang16Lupita Lopez17John P Murad18Leslie Mi Ok Chong191 Department of Hematology and Hematopoietic Cell Transplantation, City of Hope National Medical Center, Duarte, California, USA1 Department of Hematology and Hematopoietic Cell Transplantation, City of Hope National Medical Center, Duarte, California, USA1 Department of Hematology and Hematopoietic Cell Transplantation, City of Hope National Medical Center, Duarte, California, USA1 Department of Hematology and Hematopoietic Cell Transplantation, City of Hope National Medical Center, Duarte, California, USA1 Department of Hematology and Hematopoietic Cell Transplantation, City of Hope National Medical Center, Duarte, California, USA3 Department of Surgery, City of Hope National Medical Center, Duarte, California, USA4 Imugene, Sydney, New South Wales, Australia3 Department of Surgery, City of Hope National Medical Center, Duarte, California, USA2 Department of Medicine, University of Southern California Keck School of Medicine, Los Angeles, California, USA5 KSOM/Norris Center for Cancer Cellular Immunotherapy Research, University of Southern California, Los Angeles, California, USA2 Department of Medicine, University of Southern California Keck School of Medicine, Los Angeles, California, USA3 Department of Surgery, City of Hope National Medical Center, Duarte, California, USA1 Department of Hematology and Hematopoietic Cell Transplantation, City of Hope National Medical Center, Duarte, California, USA2 Department of Medicine, University of Southern California Keck School of Medicine, Los Angeles, California, USA3 Department of Surgery, City of Hope National Medical Center, Duarte, California, USA1 Department of Hematology and Hematopoietic Cell Transplantation, City of Hope National Medical Center, Duarte, California, USA3 Department of Surgery, City of Hope National Medical Center, Duarte, California, USA2 Department of Medicine, University of Southern California Keck School of Medicine, Los Angeles, California, USA2 Department of Medicine, University of Southern California Keck School of Medicine, Los Angeles, California, USA4 Imugene, Sydney, New South Wales, AustraliaBackground Bispecific T cell engager (BiTE), such as blinatumomab, has demonstrated significant clinical success in treating hematological malignancies like B cell acute lymphoblastic leukemia and non-Hodgkin's lymphoma. However, the application of BiTEs in solid tumors has proven challenging, primarily due to the lack of targetable tumor antigens and the immunologically “cold” nature of the tumor microenvironment, which limits immune system activation.Methods We developed a novel oncolytic virus (OV) platform by engineering a chimeric vaccinia virus to express either a truncated non-signaling CD19 antigen (CD19t) or truncated B cell maturation antigen (BCMAt) on the surface of infected tumor cells. Here, we advance a combinatorial platform using an OV to redirect CD19-targeted or BCMA-targeted T cell engagers (TCEs) to drive antitumor responses against multiple solid tumors.Results We found that OV-infected tumor cells in combination with TCEs significantly improved tumor cell killing against solid tumor models, with efficacy comparable to that of chimeric antigen receptor T cells. This combination approach enhanced antitumor responses using in vivo human tumor xenograft models and promoted more effective elimination of solid tumor cells than either therapy alone. Our studies highlight OVs combined with clinically approved TCEs as a readily translatable, tumor-agnostic, off-the-shelf strategy to effectively target solid tumors.Conclusions Our findings demonstrate that the combination of OV and TCEs offers a promising strategy to drive antitumor immune responses against solid tumors. This approach represents a novel and universal platform currently in phase 1 clinical trial combining TCE therapy with oncolytic virotherapy, overcoming antigen heterogeneity and immunological barriers for the effective treatment of solid tumors.https://jitc.bmj.com/content/13/8/e011051.full
spellingShingle Stephen J Forman
Wen-Chung Chang
Xiuli Wang
Anthony K Park
Ryan Urak
Yuman Fong
Monil Shah
Colin Cook
Yukiko Yamaguchi
Saul J Priceman
Cathy Lu
Shyambabu Chaurasiya
Isabel Monroy
Yuwei Ren
Hannah Valencia
Jackson Lent-Koop
Seonah Kang
Lupita Lopez
John P Murad
Leslie Mi Ok Chong
Universal off-the-shelf combination immunotherapy using oncolytic viruses to redirect T cell engagers to target solid tumors
Journal for ImmunoTherapy of Cancer
title Universal off-the-shelf combination immunotherapy using oncolytic viruses to redirect T cell engagers to target solid tumors
title_full Universal off-the-shelf combination immunotherapy using oncolytic viruses to redirect T cell engagers to target solid tumors
title_fullStr Universal off-the-shelf combination immunotherapy using oncolytic viruses to redirect T cell engagers to target solid tumors
title_full_unstemmed Universal off-the-shelf combination immunotherapy using oncolytic viruses to redirect T cell engagers to target solid tumors
title_short Universal off-the-shelf combination immunotherapy using oncolytic viruses to redirect T cell engagers to target solid tumors
title_sort universal off the shelf combination immunotherapy using oncolytic viruses to redirect t cell engagers to target solid tumors
url https://jitc.bmj.com/content/13/8/e011051.full
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