Novel Arf1 Inhibitors Drive Cancer Stem Cell Aging and Potentiate Anti‐Tumor Immunity

Abstract The small G protein Arf1 has been identified as playing a selective role in supporting cancer stem cells (CSCs), making it an attractive target for cancer therapy. However, the current Arf1 inhibitors have limited translational potential due to their high toxicity and low specificity. In th...

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Main Authors: Yuetong Wang, Qiaoming Li, Yahui Ding, Chenfei Luo, Jun Yang, Na Wang, Ning Jiang, Tiange Yao, Guohao Wang, Guoming Shi, Steven X. Hou
Format: Article
Language:English
Published: Wiley 2024-10-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202404442
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author Yuetong Wang
Qiaoming Li
Yahui Ding
Chenfei Luo
Jun Yang
Na Wang
Ning Jiang
Tiange Yao
Guohao Wang
Guoming Shi
Steven X. Hou
author_facet Yuetong Wang
Qiaoming Li
Yahui Ding
Chenfei Luo
Jun Yang
Na Wang
Ning Jiang
Tiange Yao
Guohao Wang
Guoming Shi
Steven X. Hou
author_sort Yuetong Wang
collection DOAJ
description Abstract The small G protein Arf1 has been identified as playing a selective role in supporting cancer stem cells (CSCs), making it an attractive target for cancer therapy. However, the current Arf1 inhibitors have limited translational potential due to their high toxicity and low specificity. In this study, two new potent small‐molecule inhibitors of Arf1, identified as DU101 and DU102, for cancer therapy are introduced. Preclinical tumor models demonstrate that these inhibitors triggered a cascade of aging in CSCs and enhance anti‐tumor immunity in mouse cancer and PDX models. Through single‐cell sequencing, the remodeling of the tumor immune microenvironment induced by these new Arf1 inhibitors is analyzed and an increase in tumor‐associated CD8+ CD4+ double‐positive T (DPT) cells is identified. These DPT cells exhibit superior features of active CD8 single‐positive T cells and a higher percentage of TCF1+PD‐1+, characteristic of stem‐like T cells. The frequency of tumor‐infiltrating stem‐like DPT cells correlates with better disease‐free survival (DFS) in cancer patients, indicating that these inhibitors may offer a novel cancer immunotherapy strategy by converting the cold tumor immune microenvironment into a hot one, thus expanding the potential for immunotherapy in cancer patients.
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spelling doaj-art-3123fbd059c74f3b8874b217b59b71682025-08-20T02:10:42ZengWileyAdvanced Science2198-38442024-10-011139n/an/a10.1002/advs.202404442Novel Arf1 Inhibitors Drive Cancer Stem Cell Aging and Potentiate Anti‐Tumor ImmunityYuetong Wang0Qiaoming Li1Yahui Ding2Chenfei Luo3Jun Yang4Na Wang5Ning Jiang6Tiange Yao7Guohao Wang8Guoming Shi9Steven X. Hou10Department of Cell and Developmental Biology at School of Life Sciences State Key Laboratory of Genetic Engineering Institute of Metabolism and Integrative Biology Human Phenome Institute Department of Liver Surgery and Transplantation of Liver Cancer Institute at Zhongshan Hospital Fudan University Shanghai 200438 ChinaDepartment of Cell and Developmental Biology at School of Life Sciences State Key Laboratory of Genetic Engineering Institute of Metabolism and Integrative Biology Human Phenome Institute Department of Liver Surgery and Transplantation of Liver Cancer Institute at Zhongshan Hospital Fudan University Shanghai 200438 ChinaDepartment of Cell and Developmental Biology at School of Life Sciences State Key Laboratory of Genetic Engineering Institute of Metabolism and Integrative Biology Human Phenome Institute Department of Liver Surgery and Transplantation of Liver Cancer Institute at Zhongshan Hospital Fudan University Shanghai 200438 ChinaDepartment of Cell and Developmental Biology at School of Life Sciences State Key Laboratory of Genetic Engineering Institute of Metabolism and Integrative Biology Human Phenome Institute Department of Liver Surgery and Transplantation of Liver Cancer Institute at Zhongshan Hospital Fudan University Shanghai 200438 ChinaDepartment of Cell and Developmental Biology at School of Life Sciences State Key Laboratory of Genetic Engineering Institute of Metabolism and Integrative Biology Human Phenome Institute Department of Liver Surgery and Transplantation of Liver Cancer Institute at Zhongshan Hospital Fudan University Shanghai 200438 ChinaDepartment of Cell and Developmental Biology at School of Life Sciences State Key Laboratory of Genetic Engineering Institute of Metabolism and Integrative Biology Human Phenome Institute Department of Liver Surgery and Transplantation of Liver Cancer Institute at Zhongshan Hospital Fudan University Shanghai 200438 ChinaDepartment of Cell and Developmental Biology at School of Life Sciences State Key Laboratory of Genetic Engineering Institute of Metabolism and Integrative Biology Human Phenome Institute Department of Liver Surgery and Transplantation of Liver Cancer Institute at Zhongshan Hospital Fudan University Shanghai 200438 ChinaDepartment of Cell and Developmental Biology at School of Life Sciences State Key Laboratory of Genetic Engineering Institute of Metabolism and Integrative Biology Human Phenome Institute Department of Liver Surgery and Transplantation of Liver Cancer Institute at Zhongshan Hospital Fudan University Shanghai 200438 ChinaThe Basic Research Laboratory Center for Cancer Research National Cancer Institute at Frederick National Institutes of Health Frederick MD 21702 USADepartment of Cell and Developmental Biology at School of Life Sciences State Key Laboratory of Genetic Engineering Institute of Metabolism and Integrative Biology Human Phenome Institute Department of Liver Surgery and Transplantation of Liver Cancer Institute at Zhongshan Hospital Fudan University Shanghai 200438 ChinaDepartment of Cell and Developmental Biology at School of Life Sciences State Key Laboratory of Genetic Engineering Institute of Metabolism and Integrative Biology Human Phenome Institute Department of Liver Surgery and Transplantation of Liver Cancer Institute at Zhongshan Hospital Fudan University Shanghai 200438 ChinaAbstract The small G protein Arf1 has been identified as playing a selective role in supporting cancer stem cells (CSCs), making it an attractive target for cancer therapy. However, the current Arf1 inhibitors have limited translational potential due to their high toxicity and low specificity. In this study, two new potent small‐molecule inhibitors of Arf1, identified as DU101 and DU102, for cancer therapy are introduced. Preclinical tumor models demonstrate that these inhibitors triggered a cascade of aging in CSCs and enhance anti‐tumor immunity in mouse cancer and PDX models. Through single‐cell sequencing, the remodeling of the tumor immune microenvironment induced by these new Arf1 inhibitors is analyzed and an increase in tumor‐associated CD8+ CD4+ double‐positive T (DPT) cells is identified. These DPT cells exhibit superior features of active CD8 single‐positive T cells and a higher percentage of TCF1+PD‐1+, characteristic of stem‐like T cells. The frequency of tumor‐infiltrating stem‐like DPT cells correlates with better disease‐free survival (DFS) in cancer patients, indicating that these inhibitors may offer a novel cancer immunotherapy strategy by converting the cold tumor immune microenvironment into a hot one, thus expanding the potential for immunotherapy in cancer patients.https://doi.org/10.1002/advs.202404442anti‐tumor immunityArf1 inhibitorcancer stem cellsuperior T cellstrans‐cellular signaling
spellingShingle Yuetong Wang
Qiaoming Li
Yahui Ding
Chenfei Luo
Jun Yang
Na Wang
Ning Jiang
Tiange Yao
Guohao Wang
Guoming Shi
Steven X. Hou
Novel Arf1 Inhibitors Drive Cancer Stem Cell Aging and Potentiate Anti‐Tumor Immunity
Advanced Science
anti‐tumor immunity
Arf1 inhibitor
cancer stem cell
superior T cells
trans‐cellular signaling
title Novel Arf1 Inhibitors Drive Cancer Stem Cell Aging and Potentiate Anti‐Tumor Immunity
title_full Novel Arf1 Inhibitors Drive Cancer Stem Cell Aging and Potentiate Anti‐Tumor Immunity
title_fullStr Novel Arf1 Inhibitors Drive Cancer Stem Cell Aging and Potentiate Anti‐Tumor Immunity
title_full_unstemmed Novel Arf1 Inhibitors Drive Cancer Stem Cell Aging and Potentiate Anti‐Tumor Immunity
title_short Novel Arf1 Inhibitors Drive Cancer Stem Cell Aging and Potentiate Anti‐Tumor Immunity
title_sort novel arf1 inhibitors drive cancer stem cell aging and potentiate anti tumor immunity
topic anti‐tumor immunity
Arf1 inhibitor
cancer stem cell
superior T cells
trans‐cellular signaling
url https://doi.org/10.1002/advs.202404442
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