Siglec-15 antibody–GM-CSF chimera suppresses tumor progression via reprogramming tumor-associated macrophages

Background Sialic acid-binding immunoglobulin-like lectin (Siglec)-15-expressing tumor-associated macrophages (TAMs) drive immunosuppression in the tumor microenvironment (TME), promoting CD8+ T cell exhaustion and limiting immunotherapy efficacy. Both blockade of immune checkpoint molecule Siglec-1...

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Main Authors: Jun Li, Hongyan Li, Zemeng Ma, Xiaoyao Hao, Wenwen Dai, Jinyu Liu, Mingjiu Chen, Shuang Qu, Quanli Zhang, Jiajing Luo, Shouyong Gu, Dihan Zhu, Ke Zen
Format: Article
Language:English
Published: BMJ Publishing Group 2025-04-01
Series:Journal for ImmunoTherapy of Cancer
Online Access:https://jitc.bmj.com/content/13/4/e010580.full
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author Jun Li
Hongyan Li
Zemeng Ma
Xiaoyao Hao
Wenwen Dai
Jinyu Liu
Mingjiu Chen
Shuang Qu
Quanli Zhang
Jiajing Luo
Shouyong Gu
Dihan Zhu
Ke Zen
author_facet Jun Li
Hongyan Li
Zemeng Ma
Xiaoyao Hao
Wenwen Dai
Jinyu Liu
Mingjiu Chen
Shuang Qu
Quanli Zhang
Jiajing Luo
Shouyong Gu
Dihan Zhu
Ke Zen
author_sort Jun Li
collection DOAJ
description Background Sialic acid-binding immunoglobulin-like lectin (Siglec)-15-expressing tumor-associated macrophages (TAMs) drive immunosuppression in the tumor microenvironment (TME), promoting CD8+ T cell exhaustion and limiting immunotherapy efficacy. Both blockade of immune checkpoint molecule Siglec-15 and promotion of granulocyte-macrophage colony-stimulating factor (GM-CSF) have been respectively employed in anticancer immunotherapy.Methods Murine CT26 or MC38 cancer cells were used to establish subcutaneous tumor models in BALB/c or C57BL/6 mice. Tumors were treated with anti-Siglec-15 antibody–GM-CSF chimera (anti-S15×GM CSF) or anti-Siglec-15 antibody via intraperitoneal injection. The TME was analyzed by flow cytometry and ELISA for immune cell infiltration and cytokine levels. Biodistribution and half-life of anti-S15×GM CSF were assessed by intravenous injection in tumor-bearing mice, with GM-CSF levels measured by ELISA. Macrophage reprogramming and antigen presentation were evaluated using bone marrow-derived macrophages and human peripheral blood mononuclear cell-derived macrophages treated with anti-S15×GM CSF, followed by flow cytometry and immunofluorescence assays.Results Here we report that anti-S15×GM CSF displays superior function to suppress the progression of Siglec-15-overexpressing MC38 colon cancer engrafted in mice compared to anti-Siglec-15 antibody or GM-CSF alone. Different from the injected GM-CSF which is distributed broadly in various organs and tissues of mouse, the injected anti-S15×GM CSF is preferentially accumulated in Siglec-15-positive tumor cells and TAMs. Anti-S15×GM CSF not only extends the half-life of GM-CSF in vivo, but also reduces the off-target effect of GM-CSF through TAM-specific delivery. In addition to Siglec-15 blockade, anti-S15×GM CSF effectively reprograms immunosuppressive TAMs to a proinflammatory phenotype, enhancing antigen presentation by macrophages to activate T cells.Conclusions In summary, our results reveal that anti-S15×GM CSF may serve as an effective therapeutic approach for solid tumors.
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series Journal for ImmunoTherapy of Cancer
spelling doaj-art-476b8d49d00547bbb284058bbd8e2d462025-08-20T03:08:25ZengBMJ Publishing GroupJournal for ImmunoTherapy of Cancer2051-14262025-04-0113410.1136/jitc-2024-010580Siglec-15 antibody–GM-CSF chimera suppresses tumor progression via reprogramming tumor-associated macrophagesJun Li0Hongyan Li1Zemeng Ma2Xiaoyao Hao3Wenwen Dai4Jinyu Liu5Mingjiu Chen6Shuang Qu7Quanli Zhang8Jiajing Luo9Shouyong Gu10Dihan Zhu11Ke Zen12Biosion Inc, Nanjing, Jiangsu 210024, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Nanjing University School of Life Sciences, Nanjing, Jiangsu 210093, ChinaState Key Laboratory of Natural Medicines, School of Life Science and Technology, China Pharmaceutical University, Nanjing, 639 Longmian Avenue, Nanjing, Jiangsu 211198, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Nanjing University School of Life Sciences, Nanjing, Jiangsu 210093, ChinaBiosion Inc, Nanjing, Jiangsu 210024, ChinaBiosion Inc, Nanjing, Jiangsu 210024, ChinaBiosion Inc, Nanjing, Jiangsu 210024, ChinaGeriatric Hospital of Nanjing Medical University, Nanjing, Jiangsu 210024, ChinaState Key Laboratory of Natural Medicines, School of Life Science and Technology, China Pharmaceutical University, Nanjing, 639 Longmian Avenue, Nanjing, Jiangsu 211198, ChinaMedical School of Nanjing University, Nanjing, 10993, Jiangsu Province, ChinaGeriatric Hospital of Nanjing Medical University, Nanjing, Jiangsu 210024, ChinaState Key Laboratory of Natural Medicines, School of Life Science and Technology, China Pharmaceutical University, Nanjing, 639 Longmian Avenue, Nanjing, Jiangsu 211198, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Nanjing University School of Life Sciences, Nanjing, Jiangsu 210093, ChinaBackground Sialic acid-binding immunoglobulin-like lectin (Siglec)-15-expressing tumor-associated macrophages (TAMs) drive immunosuppression in the tumor microenvironment (TME), promoting CD8+ T cell exhaustion and limiting immunotherapy efficacy. Both blockade of immune checkpoint molecule Siglec-15 and promotion of granulocyte-macrophage colony-stimulating factor (GM-CSF) have been respectively employed in anticancer immunotherapy.Methods Murine CT26 or MC38 cancer cells were used to establish subcutaneous tumor models in BALB/c or C57BL/6 mice. Tumors were treated with anti-Siglec-15 antibody–GM-CSF chimera (anti-S15×GM CSF) or anti-Siglec-15 antibody via intraperitoneal injection. The TME was analyzed by flow cytometry and ELISA for immune cell infiltration and cytokine levels. Biodistribution and half-life of anti-S15×GM CSF were assessed by intravenous injection in tumor-bearing mice, with GM-CSF levels measured by ELISA. Macrophage reprogramming and antigen presentation were evaluated using bone marrow-derived macrophages and human peripheral blood mononuclear cell-derived macrophages treated with anti-S15×GM CSF, followed by flow cytometry and immunofluorescence assays.Results Here we report that anti-S15×GM CSF displays superior function to suppress the progression of Siglec-15-overexpressing MC38 colon cancer engrafted in mice compared to anti-Siglec-15 antibody or GM-CSF alone. Different from the injected GM-CSF which is distributed broadly in various organs and tissues of mouse, the injected anti-S15×GM CSF is preferentially accumulated in Siglec-15-positive tumor cells and TAMs. Anti-S15×GM CSF not only extends the half-life of GM-CSF in vivo, but also reduces the off-target effect of GM-CSF through TAM-specific delivery. In addition to Siglec-15 blockade, anti-S15×GM CSF effectively reprograms immunosuppressive TAMs to a proinflammatory phenotype, enhancing antigen presentation by macrophages to activate T cells.Conclusions In summary, our results reveal that anti-S15×GM CSF may serve as an effective therapeutic approach for solid tumors.https://jitc.bmj.com/content/13/4/e010580.full
spellingShingle Jun Li
Hongyan Li
Zemeng Ma
Xiaoyao Hao
Wenwen Dai
Jinyu Liu
Mingjiu Chen
Shuang Qu
Quanli Zhang
Jiajing Luo
Shouyong Gu
Dihan Zhu
Ke Zen
Siglec-15 antibody–GM-CSF chimera suppresses tumor progression via reprogramming tumor-associated macrophages
Journal for ImmunoTherapy of Cancer
title Siglec-15 antibody–GM-CSF chimera suppresses tumor progression via reprogramming tumor-associated macrophages
title_full Siglec-15 antibody–GM-CSF chimera suppresses tumor progression via reprogramming tumor-associated macrophages
title_fullStr Siglec-15 antibody–GM-CSF chimera suppresses tumor progression via reprogramming tumor-associated macrophages
title_full_unstemmed Siglec-15 antibody–GM-CSF chimera suppresses tumor progression via reprogramming tumor-associated macrophages
title_short Siglec-15 antibody–GM-CSF chimera suppresses tumor progression via reprogramming tumor-associated macrophages
title_sort siglec 15 antibody gm csf chimera suppresses tumor progression via reprogramming tumor associated macrophages
url https://jitc.bmj.com/content/13/4/e010580.full
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