Neutrophil-induced pyroptosis promotes survival in patients with hepatoblastoma

Abstract Background Hepatoblastoma (HB) is the predominant hepatic malignancy among children. Despite therapeutic options for HB were gradually refined in recent years, patients with metastasis suffer from an unsatisfactory prognosis. Pyroptosis is a type of programmed and inflammatory necrosis. Neu...

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Main Authors: Tingyi Fu, Jiquan Zhou, Liyuan Yang, Jing Wang, Hui Li, Yuhua Shan, Hongxiang Gao, Chenjie Xie, Dapeng Jiang, Lei Zhang, Ji Ma, Qiuhui Pan, Min Xu, Min Zhang, Song Gu
Format: Article
Language:English
Published: Springer 2025-02-01
Series:Cancer Immunology, Immunotherapy
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Online Access:https://doi.org/10.1007/s00262-024-03922-z
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_version_ 1850029737320120320
author Tingyi Fu
Jiquan Zhou
Liyuan Yang
Jing Wang
Hui Li
Yuhua Shan
Hongxiang Gao
Chenjie Xie
Dapeng Jiang
Lei Zhang
Ji Ma
Qiuhui Pan
Min Xu
Min Zhang
Song Gu
author_facet Tingyi Fu
Jiquan Zhou
Liyuan Yang
Jing Wang
Hui Li
Yuhua Shan
Hongxiang Gao
Chenjie Xie
Dapeng Jiang
Lei Zhang
Ji Ma
Qiuhui Pan
Min Xu
Min Zhang
Song Gu
author_sort Tingyi Fu
collection DOAJ
description Abstract Background Hepatoblastoma (HB) is the predominant hepatic malignancy among children. Despite therapeutic options for HB were gradually refined in recent years, patients with metastasis suffer from an unsatisfactory prognosis. Pyroptosis is a type of programmed and inflammatory necrosis. Neutrophils are crucial in innate immunity, which were shown to be associated with tumor progression. Our study strived to unravel the relationship between neutrophil-induced pyroptosis (NIP) and HB. Methods The clinical and bulk RNA sequencing data of 38 patients with HB were obtained from Shanghai Children’s Medical Center. We established NIP score based on the LASSO regression. The single-cell RNA sequencing data (GSE186975) were used for for key genes identification, cellular communication, and differentiation trajectories of neutrophils. KEGG, GO, GSVA, and ssGSEA enrichment were used to analyze biological functions, including neutrophil extracellular traps (NETs), NOD-like receptors pathway, neutrophil activation, neutrophil-mediated cytotoxicity, and others. Results We constructed a NIP score based on the expression of three genes related to neutrophil and pyroptosis, namely ELANE, CASP1, and NOD2, which was positively correlated with a favorable prognosis of HB. Moreover, we clarified the function of ELANE in HB microenvironmwnt. Immunohistochemistry and transcriptome analysis unraveled a significant correlation between NETs and pyroptosis in HB, suggesting the key role of NETs-related neutrophils in inducing pyroptosis and prolonging survival. We also found upregulated tumor-promoting and immunosuppression-related pathways in the HB microenvironment. In addition, we clarified the growth trajectories and phenotypic changes of neutrophils in the immune microenvironment of HB, which can serve as potential targets for immunotherapy. Conclusions The novel NIP score for patients with HB shows high predictive value for survival. Moreover, we identified biological function, cellular communication, and growth trajectories of neutrophils in HB. Our findings broaden insights into the treatment of HB.
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spelling doaj-art-bebcacad516949ca8b06f1f0cf9887042025-08-20T02:59:28ZengSpringerCancer Immunology, Immunotherapy1432-08512025-02-0174311910.1007/s00262-024-03922-zNeutrophil-induced pyroptosis promotes survival in patients with hepatoblastomaTingyi Fu0Jiquan Zhou1Liyuan Yang2Jing Wang3Hui Li4Yuhua Shan5Hongxiang Gao6Chenjie Xie7Dapeng Jiang8Lei Zhang9Ji Ma10Qiuhui Pan11Min Xu12Min Zhang13Song Gu14Department of General Surgery, Shanghai Children’s Medical Center, School of Medicine, Shanghai Jiao Tong UniversityDepartment of General Surgery, Shanghai Children’s Medical Center, School of Medicine, Shanghai Jiao Tong UniversityDepartment of General Surgery, Shanghai Children’s Medical Center, School of Medicine, Shanghai Jiao Tong UniversityDepartment of General Surgery, Shanghai Children’s Medical Center, School of Medicine, Shanghai Jiao Tong UniversityKey Laboratory of Pediatric Hematology and Oncology Ministry of Health, Pediatric Translational Medicine Institute, Shanghai Children’s Medical Center Affiliated to Shanghai, Jiao Tong University School of MedicineDepartment of General Surgery, Shanghai Children’s Medical Center, School of Medicine, Shanghai Jiao Tong UniversityDepartment of General Surgery, Shanghai Children’s Medical Center, School of Medicine, Shanghai Jiao Tong UniversityDepartment of General Surgery, Shanghai Children’s Medical Center, School of Medicine, Shanghai Jiao Tong UniversityDepartment of General Surgery, Shanghai Children’s Medical Center, School of Medicine, Shanghai Jiao Tong UniversityDepartment of General Surgery, Shanghai Children’s Medical Center, School of Medicine, Shanghai Jiao Tong UniversityDepartment of Laboratory Medicine, Shanghai Children’s Medical Center, School of Medicine, Shanghai Jiao Tong UniversityDepartment of Laboratory Medicine, Shanghai Children’s Medical Center, School of Medicine, Shanghai Jiao Tong UniversityDepartment of General Surgery, Shanghai Children’s Medical Center, School of Medicine, Shanghai Jiao Tong UniversityPediatric Translational Medicine Institute and Pediatric Congenital Heart Disease Institute, Shanghai Children’s Medical Center Affiliated to Shanghai, Jiao Tong University School of MedicineDepartment of General Surgery, Shanghai Children’s Medical Center, School of Medicine, Shanghai Jiao Tong UniversityAbstract Background Hepatoblastoma (HB) is the predominant hepatic malignancy among children. Despite therapeutic options for HB were gradually refined in recent years, patients with metastasis suffer from an unsatisfactory prognosis. Pyroptosis is a type of programmed and inflammatory necrosis. Neutrophils are crucial in innate immunity, which were shown to be associated with tumor progression. Our study strived to unravel the relationship between neutrophil-induced pyroptosis (NIP) and HB. Methods The clinical and bulk RNA sequencing data of 38 patients with HB were obtained from Shanghai Children’s Medical Center. We established NIP score based on the LASSO regression. The single-cell RNA sequencing data (GSE186975) were used for for key genes identification, cellular communication, and differentiation trajectories of neutrophils. KEGG, GO, GSVA, and ssGSEA enrichment were used to analyze biological functions, including neutrophil extracellular traps (NETs), NOD-like receptors pathway, neutrophil activation, neutrophil-mediated cytotoxicity, and others. Results We constructed a NIP score based on the expression of three genes related to neutrophil and pyroptosis, namely ELANE, CASP1, and NOD2, which was positively correlated with a favorable prognosis of HB. Moreover, we clarified the function of ELANE in HB microenvironmwnt. Immunohistochemistry and transcriptome analysis unraveled a significant correlation between NETs and pyroptosis in HB, suggesting the key role of NETs-related neutrophils in inducing pyroptosis and prolonging survival. We also found upregulated tumor-promoting and immunosuppression-related pathways in the HB microenvironment. In addition, we clarified the growth trajectories and phenotypic changes of neutrophils in the immune microenvironment of HB, which can serve as potential targets for immunotherapy. Conclusions The novel NIP score for patients with HB shows high predictive value for survival. Moreover, we identified biological function, cellular communication, and growth trajectories of neutrophils in HB. Our findings broaden insights into the treatment of HB.https://doi.org/10.1007/s00262-024-03922-zHepatoblastomaPyroptosisELANENeutrophilNeutrophil extracellular traps
spellingShingle Tingyi Fu
Jiquan Zhou
Liyuan Yang
Jing Wang
Hui Li
Yuhua Shan
Hongxiang Gao
Chenjie Xie
Dapeng Jiang
Lei Zhang
Ji Ma
Qiuhui Pan
Min Xu
Min Zhang
Song Gu
Neutrophil-induced pyroptosis promotes survival in patients with hepatoblastoma
Cancer Immunology, Immunotherapy
Hepatoblastoma
Pyroptosis
ELANE
Neutrophil
Neutrophil extracellular traps
title Neutrophil-induced pyroptosis promotes survival in patients with hepatoblastoma
title_full Neutrophil-induced pyroptosis promotes survival in patients with hepatoblastoma
title_fullStr Neutrophil-induced pyroptosis promotes survival in patients with hepatoblastoma
title_full_unstemmed Neutrophil-induced pyroptosis promotes survival in patients with hepatoblastoma
title_short Neutrophil-induced pyroptosis promotes survival in patients with hepatoblastoma
title_sort neutrophil induced pyroptosis promotes survival in patients with hepatoblastoma
topic Hepatoblastoma
Pyroptosis
ELANE
Neutrophil
Neutrophil extracellular traps
url https://doi.org/10.1007/s00262-024-03922-z
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