Novel Quaternary Ammonium Salt‐Linked STING Agonist Antibody‐Drug Conjugate: Synergistic Activation of Tumor Immunity with Mitigated Off‐Target Toxicity

Abstract Immune‐stimulating antibody conjugate (ISACs) incorporating STING agonists as payloads leverage both the targeting capability of the Fab region and the Fc region‐mediated tumor antigen‐dependent immune activation. Herein, a novel class of ISACs is reported, generated by engineering a quater...

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Main Authors: Yu Long, Borui Tang, Fei Xie, Lianqi Liu, Yangyihua Zhou, Jingwen Dong, Jianfeng Wang, Cuicui Sun, Yuting Wang, Ruoqi Li, Na Zhang, Liping Li, Longlong Luo, Junhai Xiao, Wu Zhong, Dian Xiao, Hongbin Deng, Xinbo Zhou
Format: Article
Language:English
Published: Wiley 2025-08-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202502270
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author Yu Long
Borui Tang
Fei Xie
Lianqi Liu
Yangyihua Zhou
Jingwen Dong
Jianfeng Wang
Cuicui Sun
Yuting Wang
Ruoqi Li
Na Zhang
Liping Li
Longlong Luo
Junhai Xiao
Wu Zhong
Dian Xiao
Hongbin Deng
Xinbo Zhou
author_facet Yu Long
Borui Tang
Fei Xie
Lianqi Liu
Yangyihua Zhou
Jingwen Dong
Jianfeng Wang
Cuicui Sun
Yuting Wang
Ruoqi Li
Na Zhang
Liping Li
Longlong Luo
Junhai Xiao
Wu Zhong
Dian Xiao
Hongbin Deng
Xinbo Zhou
author_sort Yu Long
collection DOAJ
description Abstract Immune‐stimulating antibody conjugate (ISACs) incorporating STING agonists as payloads leverage both the targeting capability of the Fab region and the Fc region‐mediated tumor antigen‐dependent immune activation. Herein, a novel class of ISACs is reported, generated by engineering a quaternary ammonium‐cleavable linker to conjugate diABZI STING agonist 3 (dSA3) with the HER2‐targeting antibody Trastuzumab. The optimized ISAC (TZ‐dSA3‐12) demonstrated high potency, stability, enhanced solubility, and reduced off‐target toxicity. The data showed that TZ‐dSA3‐12 potently activates the STING pathway in the tumor microenvironment through the synergistic action of the Fab and Fc regions of antibodies (activity switch‐on). In contrast, TZ‐dSA3‐12 exhibited ≈75 fold lower activity than dSA3 in normal immune cells, where activation relies solely on the Fc region without Fab‐mediated tumor antigen binding (activity switch‐off). Furthermore, systemic administration of TZ‐dSA3‐12 at a dose (1 mg kg−1) elicited robust and sustained antitumor effect in a manner dependent on the activation of innate immunity and adaptive immunity, including macrophages, dendritic cells (DCs) and CD8+ T cells, while minimizing systemic cytokine release. Notably, TZ‐dSA3‐12 also induced immunological memory to combat the growth of rechallenged tumors. This innovative quaternary ammonium‐linked STING agonist‐ISAC represents a promising avenue for the future development of STING‐targeted immunotherapy.
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spelling doaj-art-c32a48e95cb7457c9bdcef8cd1d6367a2025-08-23T14:15:47ZengWileyAdvanced Science2198-38442025-08-011231n/an/a10.1002/advs.202502270Novel Quaternary Ammonium Salt‐Linked STING Agonist Antibody‐Drug Conjugate: Synergistic Activation of Tumor Immunity with Mitigated Off‐Target ToxicityYu Long0Borui Tang1Fei Xie2Lianqi Liu3Yangyihua Zhou4Jingwen Dong5Jianfeng Wang6Cuicui Sun7Yuting Wang8Ruoqi Li9Na Zhang10Liping Li11Longlong Luo12Junhai Xiao13Wu Zhong14Dian Xiao15Hongbin Deng16Xinbo Zhou17College of Pharmacy Qingdao University Qingdao 266071 ChinaSchool of Pharmaceutical Sciences Capital Medical University Beijing 100069 ChinaNational Engineering Research Center for the Emergency Drug Academy of Military Medical Sciences Beijing 100850 ChinaNational Engineering Research Center for the Emergency Drug Academy of Military Medical Sciences Beijing 100850 ChinaAcademy of Military Medical Sciences Beijing 100850 ChinaInstitute of Medicinal Biotechnology Chinese Academy of Medical Sciences & Peking Union Medical College Beijing 100050 ChinaNational Engineering Research Center for the Emergency Drug Academy of Military Medical Sciences Beijing 100850 ChinaInstitute of Medicinal Biotechnology Chinese Academy of Medical Sciences & Peking Union Medical College Beijing 100050 ChinaInstitute of Medicinal Biotechnology Chinese Academy of Medical Sciences & Peking Union Medical College Beijing 100050 ChinaInstitute of Medicinal Biotechnology Chinese Academy of Medical Sciences & Peking Union Medical College Beijing 100050 ChinaInstitute of Medicinal Biotechnology Chinese Academy of Medical Sciences & Peking Union Medical College Beijing 100050 ChinaInstitute of Medicinal Biotechnology Chinese Academy of Medical Sciences & Peking Union Medical College Beijing 100050 ChinaAcademy of Military Medical Sciences Beijing 100850 ChinaNational Engineering Research Center for the Emergency Drug Academy of Military Medical Sciences Beijing 100850 ChinaNational Engineering Research Center for the Emergency Drug Academy of Military Medical Sciences Beijing 100850 ChinaNational Engineering Research Center for the Emergency Drug Academy of Military Medical Sciences Beijing 100850 ChinaInstitute of Medicinal Biotechnology Chinese Academy of Medical Sciences & Peking Union Medical College Beijing 100050 ChinaNational Engineering Research Center for the Emergency Drug Academy of Military Medical Sciences Beijing 100850 ChinaAbstract Immune‐stimulating antibody conjugate (ISACs) incorporating STING agonists as payloads leverage both the targeting capability of the Fab region and the Fc region‐mediated tumor antigen‐dependent immune activation. Herein, a novel class of ISACs is reported, generated by engineering a quaternary ammonium‐cleavable linker to conjugate diABZI STING agonist 3 (dSA3) with the HER2‐targeting antibody Trastuzumab. The optimized ISAC (TZ‐dSA3‐12) demonstrated high potency, stability, enhanced solubility, and reduced off‐target toxicity. The data showed that TZ‐dSA3‐12 potently activates the STING pathway in the tumor microenvironment through the synergistic action of the Fab and Fc regions of antibodies (activity switch‐on). In contrast, TZ‐dSA3‐12 exhibited ≈75 fold lower activity than dSA3 in normal immune cells, where activation relies solely on the Fc region without Fab‐mediated tumor antigen binding (activity switch‐off). Furthermore, systemic administration of TZ‐dSA3‐12 at a dose (1 mg kg−1) elicited robust and sustained antitumor effect in a manner dependent on the activation of innate immunity and adaptive immunity, including macrophages, dendritic cells (DCs) and CD8+ T cells, while minimizing systemic cytokine release. Notably, TZ‐dSA3‐12 also induced immunological memory to combat the growth of rechallenged tumors. This innovative quaternary ammonium‐linked STING agonist‐ISAC represents a promising avenue for the future development of STING‐targeted immunotherapy.https://doi.org/10.1002/advs.202502270antitumor immunitydiABZI STING agonist 3immune‐stimulating antibody conjugatesquaternary ammonium salt‐linkerstimulator of interferon genes
spellingShingle Yu Long
Borui Tang
Fei Xie
Lianqi Liu
Yangyihua Zhou
Jingwen Dong
Jianfeng Wang
Cuicui Sun
Yuting Wang
Ruoqi Li
Na Zhang
Liping Li
Longlong Luo
Junhai Xiao
Wu Zhong
Dian Xiao
Hongbin Deng
Xinbo Zhou
Novel Quaternary Ammonium Salt‐Linked STING Agonist Antibody‐Drug Conjugate: Synergistic Activation of Tumor Immunity with Mitigated Off‐Target Toxicity
Advanced Science
antitumor immunity
diABZI STING agonist 3
immune‐stimulating antibody conjugates
quaternary ammonium salt‐linker
stimulator of interferon genes
title Novel Quaternary Ammonium Salt‐Linked STING Agonist Antibody‐Drug Conjugate: Synergistic Activation of Tumor Immunity with Mitigated Off‐Target Toxicity
title_full Novel Quaternary Ammonium Salt‐Linked STING Agonist Antibody‐Drug Conjugate: Synergistic Activation of Tumor Immunity with Mitigated Off‐Target Toxicity
title_fullStr Novel Quaternary Ammonium Salt‐Linked STING Agonist Antibody‐Drug Conjugate: Synergistic Activation of Tumor Immunity with Mitigated Off‐Target Toxicity
title_full_unstemmed Novel Quaternary Ammonium Salt‐Linked STING Agonist Antibody‐Drug Conjugate: Synergistic Activation of Tumor Immunity with Mitigated Off‐Target Toxicity
title_short Novel Quaternary Ammonium Salt‐Linked STING Agonist Antibody‐Drug Conjugate: Synergistic Activation of Tumor Immunity with Mitigated Off‐Target Toxicity
title_sort novel quaternary ammonium salt linked sting agonist antibody drug conjugate synergistic activation of tumor immunity with mitigated off target toxicity
topic antitumor immunity
diABZI STING agonist 3
immune‐stimulating antibody conjugates
quaternary ammonium salt‐linker
stimulator of interferon genes
url https://doi.org/10.1002/advs.202502270
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