Martinostat as a novel HDAC inhibitor to overcome tyrosine kinase inhibitor resistance in chronic myeloid leukemia

Abstract Background Chronic myeloid leukemia (CML) remains a therapeutic challenge, particularly in patients who develop resistance to standard tyrosine kinase inhibitors (TKIs) such as imatinib. Here, we present the first demonstration of the potent anti-leukemic activity of the histone deacetylase...

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Main Authors: Haeun Yang, Vladimir Li, Su Jung Park, Sang Won Cheon, Anne Lorant, Aloran Mazumder, Jin Young Lee, Barbora Orlikova-Boyer, Claudia Cerella, Christo Christov, Gilbert Kirsch, Dag Erlend Olberg, Guy Bormans, Hyoung Jin Kang, Byung Woo Han, Michael Schnekenburger, Marc Diederich
Format: Article
Language:English
Published: BMC 2025-07-01
Series:Clinical Epigenetics
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Online Access:https://doi.org/10.1186/s13148-025-01921-0
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author Haeun Yang
Vladimir Li
Su Jung Park
Sang Won Cheon
Anne Lorant
Aloran Mazumder
Jin Young Lee
Barbora Orlikova-Boyer
Claudia Cerella
Christo Christov
Gilbert Kirsch
Dag Erlend Olberg
Guy Bormans
Hyoung Jin Kang
Byung Woo Han
Michael Schnekenburger
Marc Diederich
author_facet Haeun Yang
Vladimir Li
Su Jung Park
Sang Won Cheon
Anne Lorant
Aloran Mazumder
Jin Young Lee
Barbora Orlikova-Boyer
Claudia Cerella
Christo Christov
Gilbert Kirsch
Dag Erlend Olberg
Guy Bormans
Hyoung Jin Kang
Byung Woo Han
Michael Schnekenburger
Marc Diederich
author_sort Haeun Yang
collection DOAJ
description Abstract Background Chronic myeloid leukemia (CML) remains a therapeutic challenge, particularly in patients who develop resistance to standard tyrosine kinase inhibitors (TKIs) such as imatinib. Here, we present the first demonstration of the potent anti-leukemic activity of the histone deacetylase (HDAC) inhibitor martinostat in both TKI-sensitive and TKI-resistant CML. Methods and results Structural and biochemical analyses confirmed the efficient and selective binding of martinostat to HDAC isoenzyme ligand-binding pockets, resulting in histone and tubulin hyperacetylation in both imatinib-sensitive and resistant CML cells, outperforming vorinostat, a clinically used HDAC inhibitor (HDACi). It selectively impaired CML cell proliferation and viability and induced apoptosis across various CML models, including resistant cell models and patient blasts, with minimal toxicity to healthy cells and low developmental toxicity in zebrafish. In addition to its single-agent efficacy, martinostat demonstrated enhanced anticancer effects when combined with imatinib, both in vitro and in vivo, significantly reducing tumor growth in resistant CML xenograft models. Mechanistically, mRNA-seq data showed that martinostat disrupted key survival signaling pathways and amplified apoptotic responses, contributing to its anticancer activity. Conclusions These findings highlight the potential of martinostat as a selective, low-toxicity HDACi that, combined with TKIs, could provide an effective strategy to overcome drug resistance in CML and improve therapeutic outcomes.
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spelling doaj-art-55e3b4b6583e4f24a2e684f874bdcbed2025-08-20T03:05:09ZengBMCClinical Epigenetics1868-70832025-07-0117112710.1186/s13148-025-01921-0Martinostat as a novel HDAC inhibitor to overcome tyrosine kinase inhibitor resistance in chronic myeloid leukemiaHaeun Yang0Vladimir Li1Su Jung Park2Sang Won Cheon3Anne Lorant4Aloran Mazumder5Jin Young Lee6Barbora Orlikova-Boyer7Claudia Cerella8Christo Christov9Gilbert Kirsch10Dag Erlend Olberg11Guy Bormans12Hyoung Jin Kang13Byung Woo Han14Michael Schnekenburger15Marc Diederich16Research Institute of Pharmaceutical Sciences and Natural Products Research Institute, College of Pharmacy, Seoul National UniversityResearch Institute of Pharmaceutical Sciences and Natural Products Research Institute, College of Pharmacy, Seoul National UniversityResearch Institute of Pharmaceutical Sciences and Natural Products Research Institute, College of Pharmacy, Seoul National UniversityResearch Institute of Pharmaceutical Sciences and Natural Products Research Institute, College of Pharmacy, Seoul National UniversityLaboratoire de Biologie Moléculaire et Cellulaire du CancerResearch Institute of Pharmaceutical Sciences and Natural Products Research Institute, College of Pharmacy, Seoul National UniversityResearch Institute of Pharmaceutical Sciences and Natural Products Research Institute, College of Pharmacy, Seoul National UniversityLaboratoire de Biologie Moléculaire et Cellulaire du CancerLaboratoire de Biologie Moléculaire et Cellulaire du CancerService d’Histologie, Faculté de Médicine, Université de Lorraine, INSERM U1256 NGEREUMR CNRS 7053 LC2M, University of LorraineNorsk Medisinsk Syklotronsenter ASLaboratory for Radiopharmaceutical Research, Department of Pharmaceutical and Pharmacological Sciences, KU LeuvenDepartment of Pediatrics, Seoul National University College of Medicine, Seoul National University Cancer Research Institute, Seoul National University Children’s HospitalResearch Institute of Pharmaceutical Sciences and Natural Products Research Institute, College of Pharmacy, Seoul National UniversityLaboratoire de Biologie Moléculaire et Cellulaire du CancerResearch Institute of Pharmaceutical Sciences and Natural Products Research Institute, College of Pharmacy, Seoul National UniversityAbstract Background Chronic myeloid leukemia (CML) remains a therapeutic challenge, particularly in patients who develop resistance to standard tyrosine kinase inhibitors (TKIs) such as imatinib. Here, we present the first demonstration of the potent anti-leukemic activity of the histone deacetylase (HDAC) inhibitor martinostat in both TKI-sensitive and TKI-resistant CML. Methods and results Structural and biochemical analyses confirmed the efficient and selective binding of martinostat to HDAC isoenzyme ligand-binding pockets, resulting in histone and tubulin hyperacetylation in both imatinib-sensitive and resistant CML cells, outperforming vorinostat, a clinically used HDAC inhibitor (HDACi). It selectively impaired CML cell proliferation and viability and induced apoptosis across various CML models, including resistant cell models and patient blasts, with minimal toxicity to healthy cells and low developmental toxicity in zebrafish. In addition to its single-agent efficacy, martinostat demonstrated enhanced anticancer effects when combined with imatinib, both in vitro and in vivo, significantly reducing tumor growth in resistant CML xenograft models. Mechanistically, mRNA-seq data showed that martinostat disrupted key survival signaling pathways and amplified apoptotic responses, contributing to its anticancer activity. Conclusions These findings highlight the potential of martinostat as a selective, low-toxicity HDACi that, combined with TKIs, could provide an effective strategy to overcome drug resistance in CML and improve therapeutic outcomes.https://doi.org/10.1186/s13148-025-01921-0Chronic myeloid leukemiaHDAC inhibitorsImatinib resistanceCell deathCombination treatment
spellingShingle Haeun Yang
Vladimir Li
Su Jung Park
Sang Won Cheon
Anne Lorant
Aloran Mazumder
Jin Young Lee
Barbora Orlikova-Boyer
Claudia Cerella
Christo Christov
Gilbert Kirsch
Dag Erlend Olberg
Guy Bormans
Hyoung Jin Kang
Byung Woo Han
Michael Schnekenburger
Marc Diederich
Martinostat as a novel HDAC inhibitor to overcome tyrosine kinase inhibitor resistance in chronic myeloid leukemia
Clinical Epigenetics
Chronic myeloid leukemia
HDAC inhibitors
Imatinib resistance
Cell death
Combination treatment
title Martinostat as a novel HDAC inhibitor to overcome tyrosine kinase inhibitor resistance in chronic myeloid leukemia
title_full Martinostat as a novel HDAC inhibitor to overcome tyrosine kinase inhibitor resistance in chronic myeloid leukemia
title_fullStr Martinostat as a novel HDAC inhibitor to overcome tyrosine kinase inhibitor resistance in chronic myeloid leukemia
title_full_unstemmed Martinostat as a novel HDAC inhibitor to overcome tyrosine kinase inhibitor resistance in chronic myeloid leukemia
title_short Martinostat as a novel HDAC inhibitor to overcome tyrosine kinase inhibitor resistance in chronic myeloid leukemia
title_sort martinostat as a novel hdac inhibitor to overcome tyrosine kinase inhibitor resistance in chronic myeloid leukemia
topic Chronic myeloid leukemia
HDAC inhibitors
Imatinib resistance
Cell death
Combination treatment
url https://doi.org/10.1186/s13148-025-01921-0
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