Oncolytic Vaccinia Virus Armed with GM-CSF and IL-7 Enhances Antitumor Immunity in Pancreatic Cancer

<b>Objectives:</b> Pancreatic cancer remains a therapeutic challenge due to its immunosuppressive microenvironment and treatment resistance. This study aimed to develop a novel recombinant oncolytic vaccinia virus (VVL-GL7) co-expressing granulocyte-macrophage colony-stimulating factor (...

Full description

Saved in:
Bibliographic Details
Main Authors: Wenyi Yan, Yujing Xuan, Ruimin Wang, Ziyan Huan, Yu Guo, Huilin Dun, Lihua Xu, Ruxia Han, Xianlei Sun, Lingling Si, Nicholas Robert Lemoine, Yaohe Wang, Pengju Wang
Format: Article
Language:English
Published: MDPI AG 2025-04-01
Series:Biomedicines
Subjects:
Online Access:https://www.mdpi.com/2227-9059/13/4/882
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849711971786555392
author Wenyi Yan
Yujing Xuan
Ruimin Wang
Ziyan Huan
Yu Guo
Huilin Dun
Lihua Xu
Ruxia Han
Xianlei Sun
Lingling Si
Nicholas Robert Lemoine
Yaohe Wang
Pengju Wang
author_facet Wenyi Yan
Yujing Xuan
Ruimin Wang
Ziyan Huan
Yu Guo
Huilin Dun
Lihua Xu
Ruxia Han
Xianlei Sun
Lingling Si
Nicholas Robert Lemoine
Yaohe Wang
Pengju Wang
author_sort Wenyi Yan
collection DOAJ
description <b>Objectives:</b> Pancreatic cancer remains a therapeutic challenge due to its immunosuppressive microenvironment and treatment resistance. This study aimed to develop a novel recombinant oncolytic vaccinia virus (VVL-GL7) co-expressing granulocyte-macrophage colony-stimulating factor (GM-CSF) and interleukin-7 (IL-7), designed to enhance anti-tumor immunity and synergize with immune checkpoint inhibitors. <b>Methods:</b> VVL-GL7 was constructed through CRISPR/Cas9-mediated knockout of TK and A49 genes, combined with the simultaneous insertion of dual cytokine-encoding cassettes. Anti-tumor efficacy was evaluated in vitro and in vivo using C57BL/6 mouse and Syrian hamster pancreatic cancer models. Comprehensive immune profiling evaluated CD8<sup>+</sup> T-cell and macrophage infiltration dynamics while simultaneously assessing memory T-cell differentiation patterns using flow cytometry. Preclinical combination studies of VVL-GL7 and the PD-1 immune checkpoint inhibitor were systematically evaluated in a syngeneic pancreatic cancer model. <b>Results:</b> VVL-GL7 exhibited potent oncolytic activity, inducing significant tumor regression in both preclinical models. VVL-GL7 therapy significantly augmented CD8<sup>+</sup> T-cell and macrophage infiltration within the tumor microenvironment, while concomitantly driving memory T-cell differentiation. The synergistic effects of VVL-GL7 and the PD-1 blockade further improved therapeutic outcomes, resulting in significantly higher tumor remission rates compared to monotherapy and achieving complete tumor regression in pancreatic cancer models. <b>Conclusions:</b> VVL-GL7 reprograms the immunosuppressive tumor microenvironment and synergizes with anti-PD-1 antibodies to overcome resistance in pancreatic cancer.
format Article
id doaj-art-e42abfffbe3b4c92ae91eeeffd9375f7
institution DOAJ
issn 2227-9059
language English
publishDate 2025-04-01
publisher MDPI AG
record_format Article
series Biomedicines
spelling doaj-art-e42abfffbe3b4c92ae91eeeffd9375f72025-08-20T03:14:27ZengMDPI AGBiomedicines2227-90592025-04-0113488210.3390/biomedicines13040882Oncolytic Vaccinia Virus Armed with GM-CSF and IL-7 Enhances Antitumor Immunity in Pancreatic CancerWenyi Yan0Yujing Xuan1Ruimin Wang2Ziyan Huan3Yu Guo4Huilin Dun5Lihua Xu6Ruxia Han7Xianlei Sun8Lingling Si9Nicholas Robert Lemoine10Yaohe Wang11Pengju Wang12Sino-British Research Centre for Molecular Oncology, National Centre for International Research in Cell and Gene Therapy, State Key Laboratory of Esophageal Cancer Prevention & Treatment, School of Basic Medical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou 450001, ChinaSino-British Research Centre for Molecular Oncology, National Centre for International Research in Cell and Gene Therapy, State Key Laboratory of Esophageal Cancer Prevention & Treatment, School of Basic Medical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou 450001, ChinaDepartment of Pathology, Zhengzhou People’s Hospital, Fifth Clinical Medical College of Henan University of Chinese Medicine, Zhengzhou 450003, ChinaSino-British Research Centre for Molecular Oncology, National Centre for International Research in Cell and Gene Therapy, State Key Laboratory of Esophageal Cancer Prevention & Treatment, School of Basic Medical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou 450001, ChinaSino-British Research Centre for Molecular Oncology, National Centre for International Research in Cell and Gene Therapy, State Key Laboratory of Esophageal Cancer Prevention & Treatment, School of Basic Medical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou 450001, ChinaSino-British Research Centre for Molecular Oncology, National Centre for International Research in Cell and Gene Therapy, State Key Laboratory of Esophageal Cancer Prevention & Treatment, School of Basic Medical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou 450001, ChinaSino-British Research Centre for Molecular Oncology, National Centre for International Research in Cell and Gene Therapy, State Key Laboratory of Esophageal Cancer Prevention & Treatment, School of Basic Medical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou 450001, ChinaSino-British Research Centre for Molecular Oncology, National Centre for International Research in Cell and Gene Therapy, State Key Laboratory of Esophageal Cancer Prevention & Treatment, School of Basic Medical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou 450001, ChinaSino-British Research Centre for Molecular Oncology, National Centre for International Research in Cell and Gene Therapy, State Key Laboratory of Esophageal Cancer Prevention & Treatment, School of Basic Medical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou 450001, ChinaSino-British Research Centre for Molecular Oncology, National Centre for International Research in Cell and Gene Therapy, State Key Laboratory of Esophageal Cancer Prevention & Treatment, School of Basic Medical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou 450001, ChinaSino-British Research Centre for Molecular Oncology, National Centre for International Research in Cell and Gene Therapy, State Key Laboratory of Esophageal Cancer Prevention & Treatment, School of Basic Medical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou 450001, ChinaSino-British Research Centre for Molecular Oncology, National Centre for International Research in Cell and Gene Therapy, State Key Laboratory of Esophageal Cancer Prevention & Treatment, School of Basic Medical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou 450001, ChinaSino-British Research Centre for Molecular Oncology, National Centre for International Research in Cell and Gene Therapy, State Key Laboratory of Esophageal Cancer Prevention & Treatment, School of Basic Medical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou 450001, China<b>Objectives:</b> Pancreatic cancer remains a therapeutic challenge due to its immunosuppressive microenvironment and treatment resistance. This study aimed to develop a novel recombinant oncolytic vaccinia virus (VVL-GL7) co-expressing granulocyte-macrophage colony-stimulating factor (GM-CSF) and interleukin-7 (IL-7), designed to enhance anti-tumor immunity and synergize with immune checkpoint inhibitors. <b>Methods:</b> VVL-GL7 was constructed through CRISPR/Cas9-mediated knockout of TK and A49 genes, combined with the simultaneous insertion of dual cytokine-encoding cassettes. Anti-tumor efficacy was evaluated in vitro and in vivo using C57BL/6 mouse and Syrian hamster pancreatic cancer models. Comprehensive immune profiling evaluated CD8<sup>+</sup> T-cell and macrophage infiltration dynamics while simultaneously assessing memory T-cell differentiation patterns using flow cytometry. Preclinical combination studies of VVL-GL7 and the PD-1 immune checkpoint inhibitor were systematically evaluated in a syngeneic pancreatic cancer model. <b>Results:</b> VVL-GL7 exhibited potent oncolytic activity, inducing significant tumor regression in both preclinical models. VVL-GL7 therapy significantly augmented CD8<sup>+</sup> T-cell and macrophage infiltration within the tumor microenvironment, while concomitantly driving memory T-cell differentiation. The synergistic effects of VVL-GL7 and the PD-1 blockade further improved therapeutic outcomes, resulting in significantly higher tumor remission rates compared to monotherapy and achieving complete tumor regression in pancreatic cancer models. <b>Conclusions:</b> VVL-GL7 reprograms the immunosuppressive tumor microenvironment and synergizes with anti-PD-1 antibodies to overcome resistance in pancreatic cancer.https://www.mdpi.com/2227-9059/13/4/882oncolytic virusvaccinia virusGM-CSFIL-7pancreatic cancer
spellingShingle Wenyi Yan
Yujing Xuan
Ruimin Wang
Ziyan Huan
Yu Guo
Huilin Dun
Lihua Xu
Ruxia Han
Xianlei Sun
Lingling Si
Nicholas Robert Lemoine
Yaohe Wang
Pengju Wang
Oncolytic Vaccinia Virus Armed with GM-CSF and IL-7 Enhances Antitumor Immunity in Pancreatic Cancer
Biomedicines
oncolytic virus
vaccinia virus
GM-CSF
IL-7
pancreatic cancer
title Oncolytic Vaccinia Virus Armed with GM-CSF and IL-7 Enhances Antitumor Immunity in Pancreatic Cancer
title_full Oncolytic Vaccinia Virus Armed with GM-CSF and IL-7 Enhances Antitumor Immunity in Pancreatic Cancer
title_fullStr Oncolytic Vaccinia Virus Armed with GM-CSF and IL-7 Enhances Antitumor Immunity in Pancreatic Cancer
title_full_unstemmed Oncolytic Vaccinia Virus Armed with GM-CSF and IL-7 Enhances Antitumor Immunity in Pancreatic Cancer
title_short Oncolytic Vaccinia Virus Armed with GM-CSF and IL-7 Enhances Antitumor Immunity in Pancreatic Cancer
title_sort oncolytic vaccinia virus armed with gm csf and il 7 enhances antitumor immunity in pancreatic cancer
topic oncolytic virus
vaccinia virus
GM-CSF
IL-7
pancreatic cancer
url https://www.mdpi.com/2227-9059/13/4/882
work_keys_str_mv AT wenyiyan oncolyticvacciniavirusarmedwithgmcsfandil7enhancesantitumorimmunityinpancreaticcancer
AT yujingxuan oncolyticvacciniavirusarmedwithgmcsfandil7enhancesantitumorimmunityinpancreaticcancer
AT ruiminwang oncolyticvacciniavirusarmedwithgmcsfandil7enhancesantitumorimmunityinpancreaticcancer
AT ziyanhuan oncolyticvacciniavirusarmedwithgmcsfandil7enhancesantitumorimmunityinpancreaticcancer
AT yuguo oncolyticvacciniavirusarmedwithgmcsfandil7enhancesantitumorimmunityinpancreaticcancer
AT huilindun oncolyticvacciniavirusarmedwithgmcsfandil7enhancesantitumorimmunityinpancreaticcancer
AT lihuaxu oncolyticvacciniavirusarmedwithgmcsfandil7enhancesantitumorimmunityinpancreaticcancer
AT ruxiahan oncolyticvacciniavirusarmedwithgmcsfandil7enhancesantitumorimmunityinpancreaticcancer
AT xianleisun oncolyticvacciniavirusarmedwithgmcsfandil7enhancesantitumorimmunityinpancreaticcancer
AT linglingsi oncolyticvacciniavirusarmedwithgmcsfandil7enhancesantitumorimmunityinpancreaticcancer
AT nicholasrobertlemoine oncolyticvacciniavirusarmedwithgmcsfandil7enhancesantitumorimmunityinpancreaticcancer
AT yaohewang oncolyticvacciniavirusarmedwithgmcsfandil7enhancesantitumorimmunityinpancreaticcancer
AT pengjuwang oncolyticvacciniavirusarmedwithgmcsfandil7enhancesantitumorimmunityinpancreaticcancer