Light-controlled pyroptosis via redox-responsive microneedles enhances photodynamic–epigenetic immunotherapy in breast cancer

Despite the potential of photodynamic therapy in breast cancer treatment, inadequate immunogenicity and inefficient pyroptosis induction remain critical limitations. To address this, we developed dissolvable microneedles (MNs) for localized co-delivery of decitabine (DEC) and glutathione (GSH)-respo...

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Main Authors: Hang Yu, Yiqing Chen, Jinjin Yin, Zhongwen Yuan, Senling Feng, Yanrong Duan, Pengke Yan, Shengyao Liu, Wenting Zhu
Format: Article
Language:English
Published: Elsevier 2025-10-01
Series:Materials Today Bio
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Online Access:http://www.sciencedirect.com/science/article/pii/S2590006425007288
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author Hang Yu
Yiqing Chen
Jinjin Yin
Zhongwen Yuan
Senling Feng
Yanrong Duan
Pengke Yan
Shengyao Liu
Wenting Zhu
author_facet Hang Yu
Yiqing Chen
Jinjin Yin
Zhongwen Yuan
Senling Feng
Yanrong Duan
Pengke Yan
Shengyao Liu
Wenting Zhu
author_sort Hang Yu
collection DOAJ
description Despite the potential of photodynamic therapy in breast cancer treatment, inadequate immunogenicity and inefficient pyroptosis induction remain critical limitations. To address this, we developed dissolvable microneedles (MNs) for localized co-delivery of decitabine (DEC) and glutathione (GSH)-responsive photosensitizer nanoparticles (HPPH-ss-NPs), aiming to potentiate immunogenic pyroptosis in breast cancer. The MNs enabled spatiotemporal control of DEC (dissolution-dependent release) and HPPH-ss-NPs (GSH-triggered activation), enhancing tumor drug levels with reduced systemic exposure. Mechanistically, DEC restored pyroptosis executioner gasdermin E (GSDME) expression, while HPPH-ss-NPs depleted intracellular GSH and generated caspase-3-activating ROS under light irradiation. The synergistic action triggered GSDME-dependent pyroptosis, releasing immunostimulatory DAMPs that increased mature dendritic cells and tumor-infiltrating CD8+ T cells. In orthotopic models, (DEC + HPPH-ss-NPs)@MNs suppressed primary tumor growth, while combining with anti-PD-1 synergistically inhibited tumor recurrence and lung metastasis, establishing durable systemic immunity. This MN-based platform establishes a localized photodynamic-epigenetic crosstalk to convert immunologically inert tumors into pyroptosis-driven immunogenic niches, providing a strategy for combinatorial breast cancer therapy.
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spelling doaj-art-632d0d1c1f404a37a026fa89094cdbbe2025-08-20T04:00:27ZengElsevierMaterials Today Bio2590-00642025-10-013410215810.1016/j.mtbio.2025.102158Light-controlled pyroptosis via redox-responsive microneedles enhances photodynamic–epigenetic immunotherapy in breast cancerHang Yu0Yiqing Chen1Jinjin Yin2Zhongwen Yuan3Senling Feng4Yanrong Duan5Pengke Yan6Shengyao Liu7Wenting Zhu8Department of Pharmacy, Biomedicine Research Center, Guangdong Provincial Key Laboratory of Major Obstetric Diseases, Guangdong Provincial Clinical Research Center for Obstetrics and Gynecology, The Third Affiliated Hospital, Guangzhou Medical University, Guangzhou, 510150, ChinaDepartment of Neurosurgery and Neurosurgical Disease Research Centre, The Second Affiliated Hospital of Guangzhou Medical University, Guangzhou, 510006, ChinaDepartment of Pharmacy, Biomedicine Research Center, Guangdong Provincial Key Laboratory of Major Obstetric Diseases, Guangdong Provincial Clinical Research Center for Obstetrics and Gynecology, The Third Affiliated Hospital, Guangzhou Medical University, Guangzhou, 510150, ChinaDepartment of Pharmacy, Biomedicine Research Center, Guangdong Provincial Key Laboratory of Major Obstetric Diseases, Guangdong Provincial Clinical Research Center for Obstetrics and Gynecology, The Third Affiliated Hospital, Guangzhou Medical University, Guangzhou, 510150, ChinaDepartment of Pharmacy, Biomedicine Research Center, Guangdong Provincial Key Laboratory of Major Obstetric Diseases, Guangdong Provincial Clinical Research Center for Obstetrics and Gynecology, The Third Affiliated Hospital, Guangzhou Medical University, Guangzhou, 510150, ChinaDepartment of Pharmacy, Biomedicine Research Center, Guangdong Provincial Key Laboratory of Major Obstetric Diseases, Guangdong Provincial Clinical Research Center for Obstetrics and Gynecology, The Third Affiliated Hospital, Guangzhou Medical University, Guangzhou, 510150, ChinaDepartment of Pharmacy, Biomedicine Research Center, Guangdong Provincial Key Laboratory of Major Obstetric Diseases, Guangdong Provincial Clinical Research Center for Obstetrics and Gynecology, The Third Affiliated Hospital, Guangzhou Medical University, Guangzhou, 510150, China; Corresponding author.Department of Spine Surgery, The Second Affiliated Hospital of Guangzhou Medical University, Guangzhou, 510260, China; Corresponding author.Department of Pharmacy, Biomedicine Research Center, Guangdong Provincial Key Laboratory of Major Obstetric Diseases, Guangdong Provincial Clinical Research Center for Obstetrics and Gynecology, The Third Affiliated Hospital, Guangzhou Medical University, Guangzhou, 510150, China; Corresponding author.Despite the potential of photodynamic therapy in breast cancer treatment, inadequate immunogenicity and inefficient pyroptosis induction remain critical limitations. To address this, we developed dissolvable microneedles (MNs) for localized co-delivery of decitabine (DEC) and glutathione (GSH)-responsive photosensitizer nanoparticles (HPPH-ss-NPs), aiming to potentiate immunogenic pyroptosis in breast cancer. The MNs enabled spatiotemporal control of DEC (dissolution-dependent release) and HPPH-ss-NPs (GSH-triggered activation), enhancing tumor drug levels with reduced systemic exposure. Mechanistically, DEC restored pyroptosis executioner gasdermin E (GSDME) expression, while HPPH-ss-NPs depleted intracellular GSH and generated caspase-3-activating ROS under light irradiation. The synergistic action triggered GSDME-dependent pyroptosis, releasing immunostimulatory DAMPs that increased mature dendritic cells and tumor-infiltrating CD8+ T cells. In orthotopic models, (DEC + HPPH-ss-NPs)@MNs suppressed primary tumor growth, while combining with anti-PD-1 synergistically inhibited tumor recurrence and lung metastasis, establishing durable systemic immunity. This MN-based platform establishes a localized photodynamic-epigenetic crosstalk to convert immunologically inert tumors into pyroptosis-driven immunogenic niches, providing a strategy for combinatorial breast cancer therapy.http://www.sciencedirect.com/science/article/pii/S2590006425007288Soluble microneedlePyroptosisPhotodynamic therapyGlutathione depletionBreast cancer
spellingShingle Hang Yu
Yiqing Chen
Jinjin Yin
Zhongwen Yuan
Senling Feng
Yanrong Duan
Pengke Yan
Shengyao Liu
Wenting Zhu
Light-controlled pyroptosis via redox-responsive microneedles enhances photodynamic–epigenetic immunotherapy in breast cancer
Materials Today Bio
Soluble microneedle
Pyroptosis
Photodynamic therapy
Glutathione depletion
Breast cancer
title Light-controlled pyroptosis via redox-responsive microneedles enhances photodynamic–epigenetic immunotherapy in breast cancer
title_full Light-controlled pyroptosis via redox-responsive microneedles enhances photodynamic–epigenetic immunotherapy in breast cancer
title_fullStr Light-controlled pyroptosis via redox-responsive microneedles enhances photodynamic–epigenetic immunotherapy in breast cancer
title_full_unstemmed Light-controlled pyroptosis via redox-responsive microneedles enhances photodynamic–epigenetic immunotherapy in breast cancer
title_short Light-controlled pyroptosis via redox-responsive microneedles enhances photodynamic–epigenetic immunotherapy in breast cancer
title_sort light controlled pyroptosis via redox responsive microneedles enhances photodynamic epigenetic immunotherapy in breast cancer
topic Soluble microneedle
Pyroptosis
Photodynamic therapy
Glutathione depletion
Breast cancer
url http://www.sciencedirect.com/science/article/pii/S2590006425007288
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