Kinsenoside‐Loaded Microneedle Accelerates Diabetic Wound Healing by Reprogramming Macrophage Metabolism via Inhibiting IRE1α/XBP1 Signaling Axis

Abstract Continuously bacterial infection, undue oxidative stress, and inflammatory responses in the skin tissue microenvironment determine the delayed healing outcome of diabetic wounds, which remain a tough clinical challenge and need multifaceted therapeutic strategies. In this work, HA‐ADH/HA‐QA...

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Main Authors: Li Lu, Jiewen Liao, Chao Xu, Yuan Xiong, Juan Zhou, Guangji Wang, Ze Lin, Kangkang Zha, Chuanlu Lin, Ruiyin Zeng, Guandong Dai, Qian Feng, Bobin Mi, Guohui Liu
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202502293
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author Li Lu
Jiewen Liao
Chao Xu
Yuan Xiong
Juan Zhou
Guangji Wang
Ze Lin
Kangkang Zha
Chuanlu Lin
Ruiyin Zeng
Guandong Dai
Qian Feng
Bobin Mi
Guohui Liu
author_facet Li Lu
Jiewen Liao
Chao Xu
Yuan Xiong
Juan Zhou
Guangji Wang
Ze Lin
Kangkang Zha
Chuanlu Lin
Ruiyin Zeng
Guandong Dai
Qian Feng
Bobin Mi
Guohui Liu
author_sort Li Lu
collection DOAJ
description Abstract Continuously bacterial infection, undue oxidative stress, and inflammatory responses in the skin tissue microenvironment determine the delayed healing outcome of diabetic wounds, which remain a tough clinical challenge and need multifaceted therapeutic strategies. In this work, HA‐ADH/HA‐QA‐ALD‐based hydrogel microneedle (HAQA‐MN) with antimicrobial and antioxidative activities incorporating kinsenoside (KD) coated with macrophage membrane (M‐KD) targeting inflammation relief is developed to improve the cutaneous micro‐niche. KD is observed to trigger trimethylamine N‐oxide‐irritated proinflammatory macrophages repolarization from M1 state to anti‐inflammatory M2 phenotype, and the underlying mechanism is due to drug‐induced IRE1α/XBP1/HIF‐1α pathway suppression, accompanied by diminution of glycolysis and enhancement of oxidative phosphorylation, resulting in proinflammatory cascade inhibition and anti‐inflammatory signaling enhancement. The hydrazone cross‐linked HAQA‐MN possesses favorable biocompatibility, self‐healing, controlled release of M‐KD and excellent mechanical properties. Moreover, the MN patch remarkedly restrains the survival of E. coli and S. aureus and eliminates hydrogen peroxide to preserve cellular viability. Notably, M‐KD@HAQA‐MN array effectively ameliorates cutaneous inflammation and oxidative stress and facilitate angiogenesis and collagen deposition, thereby accelerating tissue regeneration of diabetic mice with a full‐thickness skin defect model. Collectively, this study highlights a multifunctional MN platform as a promising candidate in clinical application for the treatment of diabetic wounds.
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spelling doaj-art-133d01f6f2b9400baba15fdc6fb9e1fb2025-08-20T03:36:45ZengWileyAdvanced Science2198-38442025-07-011226n/an/a10.1002/advs.202502293Kinsenoside‐Loaded Microneedle Accelerates Diabetic Wound Healing by Reprogramming Macrophage Metabolism via Inhibiting IRE1α/XBP1 Signaling AxisLi Lu0Jiewen Liao1Chao Xu2Yuan Xiong3Juan Zhou4Guangji Wang5Ze Lin6Kangkang Zha7Chuanlu Lin8Ruiyin Zeng9Guandong Dai10Qian Feng11Bobin Mi12Guohui Liu13Department of Orthopedics Union Hospital, Tongji Medical College Huazhong University of Science and Technology Wuhan 430022 ChinaDepartment of Orthopedics Union Hospital, Tongji Medical College Huazhong University of Science and Technology Wuhan 430022 ChinaKey Laboratory of Biorheological Science and Technology Ministry of Education College of Bioengineering Chongqing University Chongqing 400044 ChinaDepartment of Orthopedics Tongji Hospital, Tongji Medical College Huazhong University of Science and Technology Wuhan 430030 ChinaDepartment of Cardiology Hubei Provincial Hospital of Traditional Chinese Medicine Wuhan 430073 ChinaDepartment of Cardiology The Central Hospital of Wuhan, Tongji Medical College Huazhong University of Science and Technology Wuhan 430073 ChinaDepartment of Orthopedics Union Hospital, Tongji Medical College Huazhong University of Science and Technology Wuhan 430022 ChinaDepartment of Orthopedics Union Hospital, Tongji Medical College Huazhong University of Science and Technology Wuhan 430022 ChinaDepartment of Orthopedics Union Hospital, Tongji Medical College Huazhong University of Science and Technology Wuhan 430022 ChinaDepartment of Orthopedics Union Hospital, Tongji Medical College Huazhong University of Science and Technology Wuhan 430022 ChinaDepartment of Orthopaedics Pingshan District People's Hospital of Shenzhen Pingshan General Hospital of Southern Medical University Shenzhen Guangdong 518118 ChinaKey Laboratory of Biorheological Science and Technology Ministry of Education College of Bioengineering Chongqing University Chongqing 400044 ChinaDepartment of Orthopedics Union Hospital, Tongji Medical College Huazhong University of Science and Technology Wuhan 430022 ChinaDepartment of Orthopedics Union Hospital, Tongji Medical College Huazhong University of Science and Technology Wuhan 430022 ChinaAbstract Continuously bacterial infection, undue oxidative stress, and inflammatory responses in the skin tissue microenvironment determine the delayed healing outcome of diabetic wounds, which remain a tough clinical challenge and need multifaceted therapeutic strategies. In this work, HA‐ADH/HA‐QA‐ALD‐based hydrogel microneedle (HAQA‐MN) with antimicrobial and antioxidative activities incorporating kinsenoside (KD) coated with macrophage membrane (M‐KD) targeting inflammation relief is developed to improve the cutaneous micro‐niche. KD is observed to trigger trimethylamine N‐oxide‐irritated proinflammatory macrophages repolarization from M1 state to anti‐inflammatory M2 phenotype, and the underlying mechanism is due to drug‐induced IRE1α/XBP1/HIF‐1α pathway suppression, accompanied by diminution of glycolysis and enhancement of oxidative phosphorylation, resulting in proinflammatory cascade inhibition and anti‐inflammatory signaling enhancement. The hydrazone cross‐linked HAQA‐MN possesses favorable biocompatibility, self‐healing, controlled release of M‐KD and excellent mechanical properties. Moreover, the MN patch remarkedly restrains the survival of E. coli and S. aureus and eliminates hydrogen peroxide to preserve cellular viability. Notably, M‐KD@HAQA‐MN array effectively ameliorates cutaneous inflammation and oxidative stress and facilitate angiogenesis and collagen deposition, thereby accelerating tissue regeneration of diabetic mice with a full‐thickness skin defect model. Collectively, this study highlights a multifunctional MN platform as a promising candidate in clinical application for the treatment of diabetic wounds.https://doi.org/10.1002/advs.202502293diabetic woundinflammationkinsenosidemacrophagemetabolic reprogrammingmicroneedle
spellingShingle Li Lu
Jiewen Liao
Chao Xu
Yuan Xiong
Juan Zhou
Guangji Wang
Ze Lin
Kangkang Zha
Chuanlu Lin
Ruiyin Zeng
Guandong Dai
Qian Feng
Bobin Mi
Guohui Liu
Kinsenoside‐Loaded Microneedle Accelerates Diabetic Wound Healing by Reprogramming Macrophage Metabolism via Inhibiting IRE1α/XBP1 Signaling Axis
Advanced Science
diabetic wound
inflammation
kinsenoside
macrophage
metabolic reprogramming
microneedle
title Kinsenoside‐Loaded Microneedle Accelerates Diabetic Wound Healing by Reprogramming Macrophage Metabolism via Inhibiting IRE1α/XBP1 Signaling Axis
title_full Kinsenoside‐Loaded Microneedle Accelerates Diabetic Wound Healing by Reprogramming Macrophage Metabolism via Inhibiting IRE1α/XBP1 Signaling Axis
title_fullStr Kinsenoside‐Loaded Microneedle Accelerates Diabetic Wound Healing by Reprogramming Macrophage Metabolism via Inhibiting IRE1α/XBP1 Signaling Axis
title_full_unstemmed Kinsenoside‐Loaded Microneedle Accelerates Diabetic Wound Healing by Reprogramming Macrophage Metabolism via Inhibiting IRE1α/XBP1 Signaling Axis
title_short Kinsenoside‐Loaded Microneedle Accelerates Diabetic Wound Healing by Reprogramming Macrophage Metabolism via Inhibiting IRE1α/XBP1 Signaling Axis
title_sort kinsenoside loaded microneedle accelerates diabetic wound healing by reprogramming macrophage metabolism via inhibiting ire1α xbp1 signaling axis
topic diabetic wound
inflammation
kinsenoside
macrophage
metabolic reprogramming
microneedle
url https://doi.org/10.1002/advs.202502293
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