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Killing tumor-associated bacteria with a liposomal antibiotic generates neoantigens that induce anti-tumor immune responses

by Foote, Michael B. , Zhang, Yu , Huang, Guannan , Miao, Michael Z. , Zhou, Xuefei , Huang, Leaf , Rousseau, Benoit , Le Bihan-Benjamin, Christine , Qiu, Kunyu , Lin, Lin , Khati, Ines , Vargason, Ava , Ting, Jenny P.-Y. , Bousquet, Philippe-Jean , Anselmo, Aaron C. , Arthur, Janelle C. , Wang, Menglin , Sun, Yue , Lee, Kuo-Hsiung , Artz, Oliver , Song, Wantong , Liu, Yun , He, Yongqun , Dumas, Elise , Nguyen, Juliane , Hamy, Anne-Sophie , Armistead, Paul M. , Hilmi, Marc , Reyal, Fabien , Su, Hang , Cheng, Yung-Yi , Guo, Jianfeng

in 631/250/254 / 631/326/41 / 631/67/580 / Agriculture / Anaerobic bacteria / Animal models / Animals / Anti-Bacterial Agents - pharmacology / Anti-Bacterial Agents - therapeutic use / Antibiotics / Antigens, Neoplasm - immunology / Bacteria / Bioinformatics / Biomedical and Life Sciences / Biomedical Engineering/Biotechnology / Biomedicine / Biotechnology / Cancer / CD8 antigen / Cell culture / Cell Line, Tumor / Coliforms / Colon cancer / Colorectal cancer / Colorectal Neoplasms - drug therapy / Colorectal Neoplasms - immunology / Colorectal Neoplasms - microbiology / Dysbacteriosis / E coli / Epitopes / Humans / Immune response / Immunogenicity / Immunotherapy / Immunotherapy - methods / Intestinal microflora / Life Sciences / Liposomes / Lymphocytes / Lymphocytes T / Metastases / Mice / Microbiomes / Microbiota / Microorganisms / Neoantigens / Probiotics / Survival / Tinidazole / Tumors

2024

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Killing tumor-associated bacteria with a liposomal antibiotic generates neoantigens that induce anti-tumor immune responses

2024

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2024

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Journal Article

Killing tumor-associated bacteria with a liposomal antibiotic generates neoantigens that induce anti-tumor immune responses

Foote, Michael B.,

Zhang, Yu,

Huang, Guannan,

Miao, Michael Z.,

Zhou, Xuefei,

Huang, Leaf,

Rousseau, Benoit,

Le Bihan-Benjamin, Christine,

Qiu, Kunyu,

Lin, Lin,

Khati, Ines,

Vargason, Ava,

Ting, Jenny P.-Y.,

Bousquet, Philippe-Jean,

Anselmo, Aaron C.,

Arthur, Janelle C.,

Wang, Menglin,

Sun, Yue,

Lee, Kuo-Hsiung,

Artz, Oliver,

Song, Wantong,

Liu, Yun,

He, Yongqun,

Dumas, Elise,

Nguyen, Juliane,

Hamy, Anne-Sophie,

Armistead, Paul M.,

Hilmi, Marc,

Reyal, Fabien,

Su, Hang,

Cheng, Yung-Yi,

Guo, Jianfeng

2024

Overview

Increasing evidence implicates the tumor microbiota as a factor that can influence cancer progression. In patients with colorectal cancer (CRC), we found that pre-resection antibiotics targeting anaerobic bacteria substantially improved disease-free survival by 25.5%. For mouse studies, we designed an antibiotic silver-tinidazole complex encapsulated in liposomes (LipoAgTNZ) to eliminate tumor-associated bacteria in the primary tumor and liver metastases without causing gut microbiome dysbiosis. Mouse CRC models colonized by tumor-promoting bacteria ( Fusobacterium nucleatum spp.) or probiotics ( Escherichia coli Nissle spp.) responded to LipoAgTNZ therapy, which enabled more than 70% long-term survival in two F. nucleatum -infected CRC models. The antibiotic treatment generated microbial neoantigens that elicited anti-tumor CD8 + T cells. Heterologous and homologous bacterial epitopes contributed to the immunogenicity, priming T cells to recognize both infected and uninfected tumors. Our strategy targets tumor-associated bacteria to elicit anti-tumoral immunity, paving the way for microbiome–immunotherapy interventions. Killing bacteria in tumors boosts survival in a mouse model of colon cancer.

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Publisher

Nature Publishing Group US,Nature Publishing Group

Subject

/ Animals