Tumor microenvironment remodeling with a telomere-targeting agent and its cooperative antitumor effects with a nanovaccine

Abstract The nucleoside analogue 6-thio-2'-deoxyguanosine (6-thio-dG, also known as THIO) is a telomere-targeting agent with important clinical potency. It can selectively kill telomerase-positive tumor cells. We previously reported that THIO could successfully induce immunogenic cell death (IC...

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Main Authors: Jing Bai, Mengzhen Wang, Yiming Luo, Biao Duan, Ying Yang, Yuting Fu, Shuqin Li, Zhongqian Yang, Peng Zheng, Tong Yu, Xin Yin, Hongmei Bai, Qiong Long, Yanbing Ma
Format: Article
Language:English
Published: BMC 2025-06-01
Series:Journal of Nanobiotechnology
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Online Access:https://doi.org/10.1186/s12951-025-03471-2
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author Jing Bai
Mengzhen Wang
Yiming Luo
Biao Duan
Ying Yang
Yuting Fu
Shuqin Li
Zhongqian Yang
Peng Zheng
Tong Yu
Xin Yin
Hongmei Bai
Qiong Long
Yanbing Ma
author_facet Jing Bai
Mengzhen Wang
Yiming Luo
Biao Duan
Ying Yang
Yuting Fu
Shuqin Li
Zhongqian Yang
Peng Zheng
Tong Yu
Xin Yin
Hongmei Bai
Qiong Long
Yanbing Ma
author_sort Jing Bai
collection DOAJ
description Abstract The nucleoside analogue 6-thio-2'-deoxyguanosine (6-thio-dG, also known as THIO) is a telomere-targeting agent with important clinical potency. It can selectively kill telomerase-positive tumor cells. We previously reported that THIO could successfully induce immunogenic cell death (ICD) in multiple mouse tumor cell lines. In this study, we further explored the potential impact of THIO on remodeling the tumor microenvironment, regulating anti-tumor immune responses, and its possible synergistic effects with other therapeutic methods, such as tumor vaccines. Our results showed that THIO could also induce ICD in various human tumor cell lines. The induction of ICD in tumor cells promoted the migration and maturation of antigen-presenting cells. Administration of THIO significantly inhibited the growth of established CT26 and TC-1 tumors in mice. Meanwhile, it enhanced the anti-tumor CTL response and reduced the levels of immunosuppressive myeloid-derived suppressor cells (MDSCs) in both the spleen and tumor tissues. Additionally, THIO had a direct inhibitory effect on the proliferation and differentiation of MDSCs. Moreover, when combined with bacterial biomimetic vesicles or a nanovaccine, such as THIO with BBV or different Q11-tumor antigen peptide nanofibers, it exhibited enhanced anti-tumor effects and immune responses compared to monotherapy in either “immune hot” TC-1 tumors or “immune cold” B16-F10 tumors. In summary, THIO has the ability to remodel the tumor microenvironment, exert a specific killing effect on tumor cells, and effectively cooperate with tumor vaccines. This broadens the anti-tumor mechanisms of THIO and provides a promising strategy for improving anti-tumor immunotherapies. Graphical abstract
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publishDate 2025-06-01
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spelling doaj-art-e2d1eaca086a42e8bb1c1b6bfa01244f2025-08-20T03:10:41ZengBMCJournal of Nanobiotechnology1477-31552025-06-0123112110.1186/s12951-025-03471-2Tumor microenvironment remodeling with a telomere-targeting agent and its cooperative antitumor effects with a nanovaccineJing Bai0Mengzhen Wang1Yiming Luo2Biao Duan3Ying Yang4Yuting Fu5Shuqin Li6Zhongqian Yang7Peng Zheng8Tong Yu9Xin Yin10Hongmei Bai11Qiong Long12Yanbing Ma13Institute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical CollegeInstitute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical CollegeKunming Medical UniversityKunming Medical UniversityInstitute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical CollegeInstitute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical CollegeKunming Medical UniversityInstitute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical CollegeInstitute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical CollegeInstitute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical CollegeInstitute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical CollegeInstitute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical CollegeInstitute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical CollegeInstitute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical CollegeAbstract The nucleoside analogue 6-thio-2'-deoxyguanosine (6-thio-dG, also known as THIO) is a telomere-targeting agent with important clinical potency. It can selectively kill telomerase-positive tumor cells. We previously reported that THIO could successfully induce immunogenic cell death (ICD) in multiple mouse tumor cell lines. In this study, we further explored the potential impact of THIO on remodeling the tumor microenvironment, regulating anti-tumor immune responses, and its possible synergistic effects with other therapeutic methods, such as tumor vaccines. Our results showed that THIO could also induce ICD in various human tumor cell lines. The induction of ICD in tumor cells promoted the migration and maturation of antigen-presenting cells. Administration of THIO significantly inhibited the growth of established CT26 and TC-1 tumors in mice. Meanwhile, it enhanced the anti-tumor CTL response and reduced the levels of immunosuppressive myeloid-derived suppressor cells (MDSCs) in both the spleen and tumor tissues. Additionally, THIO had a direct inhibitory effect on the proliferation and differentiation of MDSCs. Moreover, when combined with bacterial biomimetic vesicles or a nanovaccine, such as THIO with BBV or different Q11-tumor antigen peptide nanofibers, it exhibited enhanced anti-tumor effects and immune responses compared to monotherapy in either “immune hot” TC-1 tumors or “immune cold” B16-F10 tumors. In summary, THIO has the ability to remodel the tumor microenvironment, exert a specific killing effect on tumor cells, and effectively cooperate with tumor vaccines. This broadens the anti-tumor mechanisms of THIO and provides a promising strategy for improving anti-tumor immunotherapies. Graphical abstracthttps://doi.org/10.1186/s12951-025-03471-26-thio-2′-deoxyguanosine (THIO)Immunogenic cell death (ICD)Tumor immunotherapyCancer vaccineTumor microenvironment
spellingShingle Jing Bai
Mengzhen Wang
Yiming Luo
Biao Duan
Ying Yang
Yuting Fu
Shuqin Li
Zhongqian Yang
Peng Zheng
Tong Yu
Xin Yin
Hongmei Bai
Qiong Long
Yanbing Ma
Tumor microenvironment remodeling with a telomere-targeting agent and its cooperative antitumor effects with a nanovaccine
Journal of Nanobiotechnology
6-thio-2′-deoxyguanosine (THIO)
Immunogenic cell death (ICD)
Tumor immunotherapy
Cancer vaccine
Tumor microenvironment
title Tumor microenvironment remodeling with a telomere-targeting agent and its cooperative antitumor effects with a nanovaccine
title_full Tumor microenvironment remodeling with a telomere-targeting agent and its cooperative antitumor effects with a nanovaccine
title_fullStr Tumor microenvironment remodeling with a telomere-targeting agent and its cooperative antitumor effects with a nanovaccine
title_full_unstemmed Tumor microenvironment remodeling with a telomere-targeting agent and its cooperative antitumor effects with a nanovaccine
title_short Tumor microenvironment remodeling with a telomere-targeting agent and its cooperative antitumor effects with a nanovaccine
title_sort tumor microenvironment remodeling with a telomere targeting agent and its cooperative antitumor effects with a nanovaccine
topic 6-thio-2′-deoxyguanosine (THIO)
Immunogenic cell death (ICD)
Tumor immunotherapy
Cancer vaccine
Tumor microenvironment
url https://doi.org/10.1186/s12951-025-03471-2
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