Intratumoral Brevibacillus parabrevis enhances antitumor immunity by inhibiting NK cell ferroptosis in hepatocellular carcinoma

Abstract It is known that intestinal flora affects the number and function of NK cells through metabolites, thereby regulating the response of tumors to chemotherapy or immunotherapy. However, little is known about whether intratumoral bacteria are involved in NK cell-mediated antitumor immunity. In...

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Main Authors: Banglun Pan, Xiaoxia Zhang, Dongjie Ye, Yuxin Yao, Zhu Zhang, Yue Luo, Hao Wu, Xiaoqian Wang, Nanhong Tang
Format: Article
Language:English
Published: Nature Publishing Group 2025-05-01
Series:Cell Death and Disease
Online Access:https://doi.org/10.1038/s41419-025-07733-7
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author Banglun Pan
Xiaoxia Zhang
Dongjie Ye
Yuxin Yao
Zhu Zhang
Yue Luo
Hao Wu
Xiaoqian Wang
Nanhong Tang
author_facet Banglun Pan
Xiaoxia Zhang
Dongjie Ye
Yuxin Yao
Zhu Zhang
Yue Luo
Hao Wu
Xiaoqian Wang
Nanhong Tang
author_sort Banglun Pan
collection DOAJ
description Abstract It is known that intestinal flora affects the number and function of NK cells through metabolites, thereby regulating the response of tumors to chemotherapy or immunotherapy. However, little is known about whether intratumoral bacteria are involved in NK cell-mediated antitumor immunity. In this study, 2bRAD-M analysis was performed on patient hepatocellular carcinoma and paired tissues to determine the composition of the intratumoral microbiota. Mass cytometry, flow cytometry, co-immunoprecipitation, immunoblotting, immunofluorescence, and DNA pull-down assays were used to evaluate the relationship between intratumoral bacteria, ferroptosis, and NK cell activity in Hu-SRC mice. Here, we found that the intratumoral B. parabrevis inhibited NK cell ferroptosis by promoting lipolysis into acetyl-CoA. Mechanistically, B. parabrevis catalyzed the acetylation of RORC, enhancing its binding to the NEDD4L promoter. NEDD4L induced ubiquitination of iron transporters SLC39A14, SLC39A8, and STEAP3. Functionally, B. parabrevis induced NK cells to differentiate into adaptability, cytotoxicity, and heat shock phenotypes, inhibiting the terminal phenotype and changing the tumor microenvironment from “cold” to “hot”. In conclusion, B. parabrevis enhanced the antitumor response of NK cells by regulating post-translational modifications. Our study identified a new strategy for utilizing intratumor bacteria for clinical treatment.
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spelling doaj-art-015791e88f7b40e5b3a1cf2ce8afca662025-08-20T02:34:07ZengNature Publishing GroupCell Death and Disease2041-48892025-05-0116111410.1038/s41419-025-07733-7Intratumoral Brevibacillus parabrevis enhances antitumor immunity by inhibiting NK cell ferroptosis in hepatocellular carcinomaBanglun Pan0Xiaoxia Zhang1Dongjie Ye2Yuxin Yao3Zhu Zhang4Yue Luo5Hao Wu6Xiaoqian Wang7Nanhong Tang8Department of Hepatobiliary Surgery and Fujian Institute of Hepatobiliary Surgery, Fujian Medical University Union HospitalDepartment of Hepatobiliary Surgery and Fujian Institute of Hepatobiliary Surgery, Fujian Medical University Union HospitalDepartment of Hepatobiliary Surgery and Fujian Institute of Hepatobiliary Surgery, Fujian Medical University Union HospitalDepartment of Hepatobiliary Surgery and Fujian Institute of Hepatobiliary Surgery, Fujian Medical University Union HospitalDepartment of Hepatobiliary Surgery and Fujian Institute of Hepatobiliary Surgery, Fujian Medical University Union HospitalDepartment of Hepatobiliary Surgery and Fujian Institute of Hepatobiliary Surgery, Fujian Medical University Union HospitalDepartment of Hepatobiliary Surgery and Fujian Institute of Hepatobiliary Surgery, Fujian Medical University Union HospitalDepartment of Hepatobiliary Surgery and Fujian Institute of Hepatobiliary Surgery, Fujian Medical University Union HospitalDepartment of Hepatobiliary Surgery and Fujian Institute of Hepatobiliary Surgery, Fujian Medical University Union HospitalAbstract It is known that intestinal flora affects the number and function of NK cells through metabolites, thereby regulating the response of tumors to chemotherapy or immunotherapy. However, little is known about whether intratumoral bacteria are involved in NK cell-mediated antitumor immunity. In this study, 2bRAD-M analysis was performed on patient hepatocellular carcinoma and paired tissues to determine the composition of the intratumoral microbiota. Mass cytometry, flow cytometry, co-immunoprecipitation, immunoblotting, immunofluorescence, and DNA pull-down assays were used to evaluate the relationship between intratumoral bacteria, ferroptosis, and NK cell activity in Hu-SRC mice. Here, we found that the intratumoral B. parabrevis inhibited NK cell ferroptosis by promoting lipolysis into acetyl-CoA. Mechanistically, B. parabrevis catalyzed the acetylation of RORC, enhancing its binding to the NEDD4L promoter. NEDD4L induced ubiquitination of iron transporters SLC39A14, SLC39A8, and STEAP3. Functionally, B. parabrevis induced NK cells to differentiate into adaptability, cytotoxicity, and heat shock phenotypes, inhibiting the terminal phenotype and changing the tumor microenvironment from “cold” to “hot”. In conclusion, B. parabrevis enhanced the antitumor response of NK cells by regulating post-translational modifications. Our study identified a new strategy for utilizing intratumor bacteria for clinical treatment.https://doi.org/10.1038/s41419-025-07733-7
spellingShingle Banglun Pan
Xiaoxia Zhang
Dongjie Ye
Yuxin Yao
Zhu Zhang
Yue Luo
Hao Wu
Xiaoqian Wang
Nanhong Tang
Intratumoral Brevibacillus parabrevis enhances antitumor immunity by inhibiting NK cell ferroptosis in hepatocellular carcinoma
Cell Death and Disease
title Intratumoral Brevibacillus parabrevis enhances antitumor immunity by inhibiting NK cell ferroptosis in hepatocellular carcinoma
title_full Intratumoral Brevibacillus parabrevis enhances antitumor immunity by inhibiting NK cell ferroptosis in hepatocellular carcinoma
title_fullStr Intratumoral Brevibacillus parabrevis enhances antitumor immunity by inhibiting NK cell ferroptosis in hepatocellular carcinoma
title_full_unstemmed Intratumoral Brevibacillus parabrevis enhances antitumor immunity by inhibiting NK cell ferroptosis in hepatocellular carcinoma
title_short Intratumoral Brevibacillus parabrevis enhances antitumor immunity by inhibiting NK cell ferroptosis in hepatocellular carcinoma
title_sort intratumoral brevibacillus parabrevis enhances antitumor immunity by inhibiting nk cell ferroptosis in hepatocellular carcinoma
url https://doi.org/10.1038/s41419-025-07733-7
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