Development and validation of a disulfidptosis-related genes signature for predicting outcomes and immunotherapy in acute myeloid leukemia

BackgroundAcute myeloid leukemia (AML) is a hematopoietic malignancy with poor outcomes and high recurrence. Disulfidptosis, a novel form of programmed cell death driven by aberrant disulfide bonds and F-actin collapse, provides insights into cancer progression and treatment.MethodsWe investigated t...

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Main Authors: Han Gong, Ying Zhang, Xusheng Wu, Yiming Pan, Mingwei Wang, Xiaofeng He, Jing Liu, Zhong Liu, Ling Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-04-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2025.1513040/full
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author Han Gong
Han Gong
Ying Zhang
Xusheng Wu
Yiming Pan
Yiming Pan
Mingwei Wang
Mingwei Wang
Xiaofeng He
Jing Liu
Zhong Liu
Zhong Liu
Ling Li
author_facet Han Gong
Han Gong
Ying Zhang
Xusheng Wu
Yiming Pan
Yiming Pan
Mingwei Wang
Mingwei Wang
Xiaofeng He
Jing Liu
Zhong Liu
Zhong Liu
Ling Li
author_sort Han Gong
collection DOAJ
description BackgroundAcute myeloid leukemia (AML) is a hematopoietic malignancy with poor outcomes and high recurrence. Disulfidptosis, a novel form of programmed cell death driven by aberrant disulfide bonds and F-actin collapse, provides insights into cancer progression and treatment.MethodsWe investigated the correlation network and prognostic values of disulfidptosis-related genes (DRGs) in AML. Unsupervised clustering was performed to reveal distinct disulfidptosis-related AML subtypes. We implemented the differential analysis and enrichment analysis to explore the difference of the distinct subtypes in biological processes. Least absolute shrinkage and selection operator (LASSO) Cox model was used to generate a disulfidptosis-related signature. We employed the ESTIMATE, CIBERSORT, and scRNA analyses to assess the tumor microenvironment of AML. Moreover, experiments validated the functions of PTPN6 and CSK in OCI-AML2 cells.ResultsWe identified 10 prognostic DRGs and revealed two disulfidptosis subtypes. DRGs significantly affected immune processes like interferon-gamma response and MHC class II antigen presentation. LASSO algorithm was implemented to established a 6-gene signature (HLA-DRB5, CCDC124, PTPN6, HLA-DMA, CSK, ISG15) that predicted prognosis in two validation cohorts more robustly than other signatures. Disulfidptosis was correlated with tumor microenvironment immune cells, especially monocytes. The two risk subgroups differed significantly in susceptibilities of multiple chemotherapy drugs, indicating disulfidptosis as a potential therapeutic target. Knockdown of PTPN6 and CSK inhibited the proliferation of AML cells and increased apoptosis.ConclusionsOur study provides insights into DRG prognoses and immunomodulation, establishing a robust 6-gene risk model for predicting AML outcomes that may enhance precision medicine and treatment strategies.
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spelling doaj-art-ed8e61eee112437a92665bd61a69bde22025-08-20T03:05:53ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-04-011610.3389/fimmu.2025.15130401513040Development and validation of a disulfidptosis-related genes signature for predicting outcomes and immunotherapy in acute myeloid leukemiaHan Gong0Han Gong1Ying Zhang2Xusheng Wu3Yiming Pan4Yiming Pan5Mingwei Wang6Mingwei Wang7Xiaofeng He8Jing Liu9Zhong Liu10Zhong Liu11Ling Li12Institute of Blood Transfusion, Chinese Academy of Medical Sciences and Peking Union Medical College, Chengdu, ChinaDepartment of Hematology, The Second Xiangya Hospital, Molecular Biology Research Center, School of Life Sciences, Hunan Province Key Laboratory of Basic and Applied Hematology, Central South University, Changsha, ChinaThe Institute of Medical Information (IMI) & Library, Chinese Academy of Medical Sciences and Peking Union Medical, Beijing, ChinaShenzhen Health Development Research and Data Management Center, Shenzhen, ChinaInstitute of Blood Transfusion, Chinese Academy of Medical Sciences and Peking Union Medical College, Chengdu, ChinaKey laboratory of transfusion adverse reactions, Chinese Academy of Medical Sciences, Chengdu, ChinaInstitute of Blood Transfusion, Chinese Academy of Medical Sciences and Peking Union Medical College, Chengdu, ChinaKey laboratory of transfusion adverse reactions, Chinese Academy of Medical Sciences, Chengdu, ChinaShenzhen Health Development Research and Data Management Center, Shenzhen, ChinaDepartment of Hematology, The Second Xiangya Hospital, Molecular Biology Research Center, School of Life Sciences, Hunan Province Key Laboratory of Basic and Applied Hematology, Central South University, Changsha, ChinaInstitute of Blood Transfusion, Chinese Academy of Medical Sciences and Peking Union Medical College, Chengdu, ChinaKey laboratory of transfusion adverse reactions, Chinese Academy of Medical Sciences, Chengdu, ChinaDepartment of Blood Transfusion, Affiliated Hospital of Southwest Jiaotong University, The Third People's Hospital of Chengdu, Chengdu, Sichuan, ChinaBackgroundAcute myeloid leukemia (AML) is a hematopoietic malignancy with poor outcomes and high recurrence. Disulfidptosis, a novel form of programmed cell death driven by aberrant disulfide bonds and F-actin collapse, provides insights into cancer progression and treatment.MethodsWe investigated the correlation network and prognostic values of disulfidptosis-related genes (DRGs) in AML. Unsupervised clustering was performed to reveal distinct disulfidptosis-related AML subtypes. We implemented the differential analysis and enrichment analysis to explore the difference of the distinct subtypes in biological processes. Least absolute shrinkage and selection operator (LASSO) Cox model was used to generate a disulfidptosis-related signature. We employed the ESTIMATE, CIBERSORT, and scRNA analyses to assess the tumor microenvironment of AML. Moreover, experiments validated the functions of PTPN6 and CSK in OCI-AML2 cells.ResultsWe identified 10 prognostic DRGs and revealed two disulfidptosis subtypes. DRGs significantly affected immune processes like interferon-gamma response and MHC class II antigen presentation. LASSO algorithm was implemented to established a 6-gene signature (HLA-DRB5, CCDC124, PTPN6, HLA-DMA, CSK, ISG15) that predicted prognosis in two validation cohorts more robustly than other signatures. Disulfidptosis was correlated with tumor microenvironment immune cells, especially monocytes. The two risk subgroups differed significantly in susceptibilities of multiple chemotherapy drugs, indicating disulfidptosis as a potential therapeutic target. Knockdown of PTPN6 and CSK inhibited the proliferation of AML cells and increased apoptosis.ConclusionsOur study provides insights into DRG prognoses and immunomodulation, establishing a robust 6-gene risk model for predicting AML outcomes that may enhance precision medicine and treatment strategies.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1513040/fullacute myeloid leukemiadisulfidptosis-related genesprognosisrisk modelimmunomodulationtumor microenvironment
spellingShingle Han Gong
Han Gong
Ying Zhang
Xusheng Wu
Yiming Pan
Yiming Pan
Mingwei Wang
Mingwei Wang
Xiaofeng He
Jing Liu
Zhong Liu
Zhong Liu
Ling Li
Development and validation of a disulfidptosis-related genes signature for predicting outcomes and immunotherapy in acute myeloid leukemia
Frontiers in Immunology
acute myeloid leukemia
disulfidptosis-related genes
prognosis
risk model
immunomodulation
tumor microenvironment
title Development and validation of a disulfidptosis-related genes signature for predicting outcomes and immunotherapy in acute myeloid leukemia
title_full Development and validation of a disulfidptosis-related genes signature for predicting outcomes and immunotherapy in acute myeloid leukemia
title_fullStr Development and validation of a disulfidptosis-related genes signature for predicting outcomes and immunotherapy in acute myeloid leukemia
title_full_unstemmed Development and validation of a disulfidptosis-related genes signature for predicting outcomes and immunotherapy in acute myeloid leukemia
title_short Development and validation of a disulfidptosis-related genes signature for predicting outcomes and immunotherapy in acute myeloid leukemia
title_sort development and validation of a disulfidptosis related genes signature for predicting outcomes and immunotherapy in acute myeloid leukemia
topic acute myeloid leukemia
disulfidptosis-related genes
prognosis
risk model
immunomodulation
tumor microenvironment
url https://www.frontiersin.org/articles/10.3389/fimmu.2025.1513040/full
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