Unraveling the role of HDAC3 as an immunotherapy prognostic biomarker and therapeutic target in advanced non-small cell lung cancer

Abstract Background This study investigates HDAC3 as a potential immunotherapy biomarker in advanced non-small cell lung cancer (aNSCLC), focusing on its association with treatment response to immune checkpoint inhibitors (ICIs). Methods We employed a multi-phase approach in 78 aNSCLC patients with...

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Main Authors: Liyuan Dai, Liling Huang, Lin Li, Le Tang, Yuankai Shi, Xiaohong Han
Format: Article
Language:English
Published: BMC 2025-06-01
Series:Respiratory Research
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Online Access:https://doi.org/10.1186/s12931-025-03275-w
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author Liyuan Dai
Liling Huang
Lin Li
Le Tang
Yuankai Shi
Xiaohong Han
author_facet Liyuan Dai
Liling Huang
Lin Li
Le Tang
Yuankai Shi
Xiaohong Han
author_sort Liyuan Dai
collection DOAJ
description Abstract Background This study investigates HDAC3 as a potential immunotherapy biomarker in advanced non-small cell lung cancer (aNSCLC), focusing on its association with treatment response to immune checkpoint inhibitors (ICIs). Methods We employed a multi-phase approach in 78 aNSCLC patients with 138 plasma samples, starting with a discovery phase that identified differential autoantibodies (AAbs) using proteomic analysis in responders and non-responders. In the validation phase, we assessed AAb levels at multiple time points. Additionally, immunohistochemistry and multiple immunofluorescence (n = 21) were used to validate HDAC3 expression in FFPE samples, single-cell RNA sequencing (n = 26) was performed to explore gene expression differences, cell and animal experiments were performed. Results We identified 127 differential AAbs, with five key AAbs (HDAC3, METTL21C, HSPB3, SPACA7, and SPPL2B) consistently linked to prognosis pre- and post-treatment (p < 0.05). A risk score model based on these AAbs effectively predicted progression-free survival. Furthermore, HDAC3 expression correlated with significant pathway enrichments and was associated with higher TGFβ1, PD-L1 infiltration and lower CD8+ T cells infiltration (p < 0.05). HDAC3 knockdown significantly inhibited cell proliferation, impaired colony formation, and induced G0/G1 phase arrest in lung cancer cells. Preclinical models demonstrated that RGFP966, an HDAC3 inhibitor, combined with anti–PD-1 therapy enhanced CD8+ T cell infiltration (p < 0.05). Conclusion Our findings underscore HDAC3’s role as a biomarker for predicting ICI response in aNSCLC and suggest its potential as a therapeutic target, paving the way for future studies on HDAC3-targeted therapies to improve immunotherapy outcomes. Clinical trial number not applicable.
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spelling doaj-art-0764cbb02f064ebeb2db340d8bcaf7122025-08-20T03:21:02ZengBMCRespiratory Research1465-993X2025-06-0126111710.1186/s12931-025-03275-wUnraveling the role of HDAC3 as an immunotherapy prognostic biomarker and therapeutic target in advanced non-small cell lung cancerLiyuan Dai0Liling Huang1Lin Li2Le Tang3Yuankai Shi4Xiaohong Han5Department of Medical Oncology, Beijing Key Laboratory of Key Technologies for Early Clinical Trial Evaluation of Innovative Drugs for Major Diseases, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital,Chinese Academy of Medical Sciences & Peking Union Medical CollegeDepartment of Medical Oncology, Beijing Key Laboratory of Key Technologies for Early Clinical Trial Evaluation of Innovative Drugs for Major Diseases, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital,Chinese Academy of Medical Sciences & Peking Union Medical CollegeDepartment of Pathology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences & Peking Union Medical CollegeDepartment of Medical Oncology, Beijing Key Laboratory of Key Technologies for Early Clinical Trial Evaluation of Innovative Drugs for Major Diseases, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital,Chinese Academy of Medical Sciences & Peking Union Medical CollegeDepartment of Medical Oncology, Beijing Key Laboratory of Key Technologies for Early Clinical Trial Evaluation of Innovative Drugs for Major Diseases, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital,Chinese Academy of Medical Sciences & Peking Union Medical CollegeClinical Pharmacology Research Center,NMPA Key Laboratory for Clinical Research and Evaluation of Drug, Beijing Key Laboratory of Key Technologies for Early Clinical Trial Evaluation of Innovative Drugs for Major Diseases, Peking Union Medical College Hospital,Chinese Academy of Medical Sciences & Peking Union Medical CollegeAbstract Background This study investigates HDAC3 as a potential immunotherapy biomarker in advanced non-small cell lung cancer (aNSCLC), focusing on its association with treatment response to immune checkpoint inhibitors (ICIs). Methods We employed a multi-phase approach in 78 aNSCLC patients with 138 plasma samples, starting with a discovery phase that identified differential autoantibodies (AAbs) using proteomic analysis in responders and non-responders. In the validation phase, we assessed AAb levels at multiple time points. Additionally, immunohistochemistry and multiple immunofluorescence (n = 21) were used to validate HDAC3 expression in FFPE samples, single-cell RNA sequencing (n = 26) was performed to explore gene expression differences, cell and animal experiments were performed. Results We identified 127 differential AAbs, with five key AAbs (HDAC3, METTL21C, HSPB3, SPACA7, and SPPL2B) consistently linked to prognosis pre- and post-treatment (p < 0.05). A risk score model based on these AAbs effectively predicted progression-free survival. Furthermore, HDAC3 expression correlated with significant pathway enrichments and was associated with higher TGFβ1, PD-L1 infiltration and lower CD8+ T cells infiltration (p < 0.05). HDAC3 knockdown significantly inhibited cell proliferation, impaired colony formation, and induced G0/G1 phase arrest in lung cancer cells. Preclinical models demonstrated that RGFP966, an HDAC3 inhibitor, combined with anti–PD-1 therapy enhanced CD8+ T cell infiltration (p < 0.05). Conclusion Our findings underscore HDAC3’s role as a biomarker for predicting ICI response in aNSCLC and suggest its potential as a therapeutic target, paving the way for future studies on HDAC3-targeted therapies to improve immunotherapy outcomes. Clinical trial number not applicable.https://doi.org/10.1186/s12931-025-03275-wHDAC3AutoantibodyImmunotherapyPrognostic biomarkerNon-small cell lung cancer
spellingShingle Liyuan Dai
Liling Huang
Lin Li
Le Tang
Yuankai Shi
Xiaohong Han
Unraveling the role of HDAC3 as an immunotherapy prognostic biomarker and therapeutic target in advanced non-small cell lung cancer
Respiratory Research
HDAC3
Autoantibody
Immunotherapy
Prognostic biomarker
Non-small cell lung cancer
title Unraveling the role of HDAC3 as an immunotherapy prognostic biomarker and therapeutic target in advanced non-small cell lung cancer
title_full Unraveling the role of HDAC3 as an immunotherapy prognostic biomarker and therapeutic target in advanced non-small cell lung cancer
title_fullStr Unraveling the role of HDAC3 as an immunotherapy prognostic biomarker and therapeutic target in advanced non-small cell lung cancer
title_full_unstemmed Unraveling the role of HDAC3 as an immunotherapy prognostic biomarker and therapeutic target in advanced non-small cell lung cancer
title_short Unraveling the role of HDAC3 as an immunotherapy prognostic biomarker and therapeutic target in advanced non-small cell lung cancer
title_sort unraveling the role of hdac3 as an immunotherapy prognostic biomarker and therapeutic target in advanced non small cell lung cancer
topic HDAC3
Autoantibody
Immunotherapy
Prognostic biomarker
Non-small cell lung cancer
url https://doi.org/10.1186/s12931-025-03275-w
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