Targeting the Adenosine‐Mediated Metabolic Immune Checkpoint with Engineered Probiotic for Enhanced Chemo‐Immunotherapy

Abstract Immunotherapy has revolutionized cancer treatment by leveraging the patient's immune system, yet its efficacy is often hampered by the immunosuppressive tumor microenvironment (TME). Adenosine, a key player in this milieu, suppresses immune cell activity via cAMP signaling. Here, an in...

Full description

Saved in:
Bibliographic Details
Main Authors: Jinhui Wang, Jing Wang, Zhijie Yu, Hongyu Wen, Chensi Zhao, Jiayong Zhong, Chuanle Xiao, Yingqiu Li, Jianqiao Xu, Jinquan Wang, Zong‐Wan Mao, Wei Xia
Format: Article
Language:English
Published: Wiley 2025-04-01
Series:Advanced Science
Subjects:
Online Access:https://doi.org/10.1002/advs.202411813
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849700976467902464
author Jinhui Wang
Jing Wang
Zhijie Yu
Hongyu Wen
Chensi Zhao
Jiayong Zhong
Chuanle Xiao
Yingqiu Li
Jianqiao Xu
Jinquan Wang
Zong‐Wan Mao
Wei Xia
author_facet Jinhui Wang
Jing Wang
Zhijie Yu
Hongyu Wen
Chensi Zhao
Jiayong Zhong
Chuanle Xiao
Yingqiu Li
Jianqiao Xu
Jinquan Wang
Zong‐Wan Mao
Wei Xia
author_sort Jinhui Wang
collection DOAJ
description Abstract Immunotherapy has revolutionized cancer treatment by leveraging the patient's immune system, yet its efficacy is often hampered by the immunosuppressive tumor microenvironment (TME). Adenosine, a key player in this milieu, suppresses immune cell activity via cAMP signaling. Here, an innovative strategy to remodel the TME using a genetically engineered strain of Escherichia coli Nissle 1917 that expresses adenosine deaminase on its surface under hypoxic conditions is presented. This engineered probiotic targets tumors, converts immunosuppressive adenosine to inosine, and enhances anti‐tumor immune responses. In vivo, the engineered probiotic significantly improved immune cell infiltration and demonstrated synergistic effects with low‐dose doxorubicin in both subcutaneous and orthotopic mouse colorectal cancer model. Furthermore, the engineered probiotic modulated the TME, promoting a shift from M2‐like to M1‐like macrophages and increasing effector T cell populations. These findings highlight the potential of using engineered probiotics for metabolic modulation of the TME, offering a novel approach for enhancing cancer immunotherapy.
format Article
id doaj-art-c6bacb531d9e4f218ab20af62fbb13f9
institution DOAJ
issn 2198-3844
language English
publishDate 2025-04-01
publisher Wiley
record_format Article
series Advanced Science
spelling doaj-art-c6bacb531d9e4f218ab20af62fbb13f92025-08-20T03:18:05ZengWileyAdvanced Science2198-38442025-04-011215n/an/a10.1002/advs.202411813Targeting the Adenosine‐Mediated Metabolic Immune Checkpoint with Engineered Probiotic for Enhanced Chemo‐ImmunotherapyJinhui Wang0Jing Wang1Zhijie Yu2Hongyu Wen3Chensi Zhao4Jiayong Zhong5Chuanle Xiao6Yingqiu Li7Jianqiao Xu8Jinquan Wang9Zong‐Wan Mao10Wei Xia11MOE Key Laboratory of Bioinorganic and Synthetic Chemistry IGCME School of Chemistry Sun Yat‐Sen University Guangzhou 510006 ChinaMOE Key Laboratory of Bioinorganic and Synthetic Chemistry IGCME School of Chemistry Sun Yat‐Sen University Guangzhou 510006 ChinaGuangdong Key Laboratory of Advanced Drug Delivery School of Bioscience and Biopharmaceutics Guangdong Pharmaceutical University Guangzhou 510006 ChinaMOE Key Laboratory of Bioinorganic and Synthetic Chemistry IGCME School of Chemistry Sun Yat‐Sen University Guangzhou 510006 ChinaState Key Laboratory of Biocontrol School of Life Sciences Sun Yat‐sen University Guangzhou 510006 ChinaState Key Laboratory of Ophthalmology Zhongshan Ophthalmic Center Guangdong Provincial Key Laboratory of Ophthalmology and Visual Science Sun Yat‐sen University Guangzhou 510060 ChinaState Key Laboratory of Ophthalmology Zhongshan Ophthalmic Center Guangdong Provincial Key Laboratory of Ophthalmology and Visual Science Sun Yat‐sen University Guangzhou 510060 ChinaState Key Laboratory of Biocontrol School of Life Sciences Sun Yat‐sen University Guangzhou 510006 ChinaMOE Key Laboratory of Bioinorganic and Synthetic Chemistry IGCME School of Chemistry Sun Yat‐Sen University Guangzhou 510006 ChinaGuangdong Key Laboratory of Advanced Drug Delivery School of Bioscience and Biopharmaceutics Guangdong Pharmaceutical University Guangzhou 510006 ChinaMOE Key Laboratory of Bioinorganic and Synthetic Chemistry IGCME School of Chemistry Sun Yat‐Sen University Guangzhou 510006 ChinaMOE Key Laboratory of Bioinorganic and Synthetic Chemistry IGCME School of Chemistry Sun Yat‐Sen University Guangzhou 510006 ChinaAbstract Immunotherapy has revolutionized cancer treatment by leveraging the patient's immune system, yet its efficacy is often hampered by the immunosuppressive tumor microenvironment (TME). Adenosine, a key player in this milieu, suppresses immune cell activity via cAMP signaling. Here, an innovative strategy to remodel the TME using a genetically engineered strain of Escherichia coli Nissle 1917 that expresses adenosine deaminase on its surface under hypoxic conditions is presented. This engineered probiotic targets tumors, converts immunosuppressive adenosine to inosine, and enhances anti‐tumor immune responses. In vivo, the engineered probiotic significantly improved immune cell infiltration and demonstrated synergistic effects with low‐dose doxorubicin in both subcutaneous and orthotopic mouse colorectal cancer model. Furthermore, the engineered probiotic modulated the TME, promoting a shift from M2‐like to M1‐like macrophages and increasing effector T cell populations. These findings highlight the potential of using engineered probiotics for metabolic modulation of the TME, offering a novel approach for enhancing cancer immunotherapy.https://doi.org/10.1002/advs.202411813adenosine deaminasechemo‐immunotherapyengineered probioticmetabolic modulationtumor microenvironment
spellingShingle Jinhui Wang
Jing Wang
Zhijie Yu
Hongyu Wen
Chensi Zhao
Jiayong Zhong
Chuanle Xiao
Yingqiu Li
Jianqiao Xu
Jinquan Wang
Zong‐Wan Mao
Wei Xia
Targeting the Adenosine‐Mediated Metabolic Immune Checkpoint with Engineered Probiotic for Enhanced Chemo‐Immunotherapy
Advanced Science
adenosine deaminase
chemo‐immunotherapy
engineered probiotic
metabolic modulation
tumor microenvironment
title Targeting the Adenosine‐Mediated Metabolic Immune Checkpoint with Engineered Probiotic for Enhanced Chemo‐Immunotherapy
title_full Targeting the Adenosine‐Mediated Metabolic Immune Checkpoint with Engineered Probiotic for Enhanced Chemo‐Immunotherapy
title_fullStr Targeting the Adenosine‐Mediated Metabolic Immune Checkpoint with Engineered Probiotic for Enhanced Chemo‐Immunotherapy
title_full_unstemmed Targeting the Adenosine‐Mediated Metabolic Immune Checkpoint with Engineered Probiotic for Enhanced Chemo‐Immunotherapy
title_short Targeting the Adenosine‐Mediated Metabolic Immune Checkpoint with Engineered Probiotic for Enhanced Chemo‐Immunotherapy
title_sort targeting the adenosine mediated metabolic immune checkpoint with engineered probiotic for enhanced chemo immunotherapy
topic adenosine deaminase
chemo‐immunotherapy
engineered probiotic
metabolic modulation
tumor microenvironment
url https://doi.org/10.1002/advs.202411813
work_keys_str_mv AT jinhuiwang targetingtheadenosinemediatedmetabolicimmunecheckpointwithengineeredprobioticforenhancedchemoimmunotherapy
AT jingwang targetingtheadenosinemediatedmetabolicimmunecheckpointwithengineeredprobioticforenhancedchemoimmunotherapy
AT zhijieyu targetingtheadenosinemediatedmetabolicimmunecheckpointwithengineeredprobioticforenhancedchemoimmunotherapy
AT hongyuwen targetingtheadenosinemediatedmetabolicimmunecheckpointwithengineeredprobioticforenhancedchemoimmunotherapy
AT chensizhao targetingtheadenosinemediatedmetabolicimmunecheckpointwithengineeredprobioticforenhancedchemoimmunotherapy
AT jiayongzhong targetingtheadenosinemediatedmetabolicimmunecheckpointwithengineeredprobioticforenhancedchemoimmunotherapy
AT chuanlexiao targetingtheadenosinemediatedmetabolicimmunecheckpointwithengineeredprobioticforenhancedchemoimmunotherapy
AT yingqiuli targetingtheadenosinemediatedmetabolicimmunecheckpointwithengineeredprobioticforenhancedchemoimmunotherapy
AT jianqiaoxu targetingtheadenosinemediatedmetabolicimmunecheckpointwithengineeredprobioticforenhancedchemoimmunotherapy
AT jinquanwang targetingtheadenosinemediatedmetabolicimmunecheckpointwithengineeredprobioticforenhancedchemoimmunotherapy
AT zongwanmao targetingtheadenosinemediatedmetabolicimmunecheckpointwithengineeredprobioticforenhancedchemoimmunotherapy
AT weixia targetingtheadenosinemediatedmetabolicimmunecheckpointwithengineeredprobioticforenhancedchemoimmunotherapy