Metabolic Mechanism of Osteogenic Differentiation of Bone Marrow Mesenchymal Stem Cell Regulated by Magnetoelectric Microenvironment

Conventional methods to stimulate the metabolism of bone marrow mesenchymal stem cells (BMSCs) for osteogenic differentiation typically involve systemic mobilization, which faces challenges including limited in vivo half‐life, lack of selectivity, and potential side‐effects. Therefore, localized mod...

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Main Authors: Han Zhao, Fangyu Zhu, Yusi Guo, Xuliang Deng, Wenwen Liu
Format: Article
Language:English
Published: Wiley-VCH 2025-04-01
Series:Small Structures
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Online Access:https://doi.org/10.1002/sstr.202400466
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author Han Zhao
Fangyu Zhu
Yusi Guo
Xuliang Deng
Wenwen Liu
author_facet Han Zhao
Fangyu Zhu
Yusi Guo
Xuliang Deng
Wenwen Liu
author_sort Han Zhao
collection DOAJ
description Conventional methods to stimulate the metabolism of bone marrow mesenchymal stem cells (BMSCs) for osteogenic differentiation typically involve systemic mobilization, which faces challenges including limited in vivo half‐life, lack of selectivity, and potential side‐effects. Therefore, localized modulation of BMSCs represents a more efficient and safer alternative. However, few studies have explored the regulation of a localized stimuli‐responsive microenvironment to activate osteogenic differentiation via mitochondrial pathways and clarified its underlying mechanisms. Herein, a novel strategy to accelerate the metabolic switch of BMSCs in tissue defects through targeted modulation using built‐in magnetoelectric biomaterials is proposed. BMSCs cultured in the magnetoelectric microenvironment exhibited an increased mitochondrial membrane potential, the highest oxygen consumption rate and enhanced adenosine triphosphate production. Furthermore, BMSCs in the magnetoelectric microenvironment demonstrated a successful metabolic switch  of energy resource from glycolysis to oxidative phosphorylation, indicating a strong tendency toward osteogenic differentiation. The highest multiclass metabolite profile, indicating the most active metabolic state, was shown in rats cranial defect model treated with magnetoelectric microenvironment. This research introduces a novel approach to accelerate bone defect repair by targeted modulation of BMSC mitochondria with magnetoelectric microenvironment and provides a promising direction for exploring the intrinsic mechanisms through which the magnetoelectric microenvironment promotes bone regeneration.
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spelling doaj-art-c8a34419b8b24d7f87276c9243b7bba62025-08-20T02:16:55ZengWiley-VCHSmall Structures2688-40622025-04-0164n/an/a10.1002/sstr.202400466Metabolic Mechanism of Osteogenic Differentiation of Bone Marrow Mesenchymal Stem Cell Regulated by Magnetoelectric MicroenvironmentHan Zhao0Fangyu Zhu1Yusi Guo2Xuliang Deng3Wenwen Liu4Department of General Dentistry Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices & NMPA Key Laboratory for Dental Materials No. 22, Zhongguancun South Avenue, Haidian District Beijing 100081 P. R. ChinaDepartment of Geriatric Dentistry Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices & NMPA Key Laboratory for Dental Materials No. 22, Zhongguancun South Avenue, Haidian District Beijing 100081 P. R. ChinaDepartment of Geriatric Dentistry Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices & NMPA Key Laboratory for Dental Materials No. 22, Zhongguancun South Avenue, Haidian District Beijing 100081 P. R. ChinaDepartment of Geriatric Dentistry Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices & NMPA Key Laboratory for Dental Materials No. 22, Zhongguancun South Avenue, Haidian District Beijing 100081 P. R. ChinaDepartment of Geriatric Dentistry Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices & NMPA Key Laboratory for Dental Materials No. 22, Zhongguancun South Avenue, Haidian District Beijing 100081 P. R. ChinaConventional methods to stimulate the metabolism of bone marrow mesenchymal stem cells (BMSCs) for osteogenic differentiation typically involve systemic mobilization, which faces challenges including limited in vivo half‐life, lack of selectivity, and potential side‐effects. Therefore, localized modulation of BMSCs represents a more efficient and safer alternative. However, few studies have explored the regulation of a localized stimuli‐responsive microenvironment to activate osteogenic differentiation via mitochondrial pathways and clarified its underlying mechanisms. Herein, a novel strategy to accelerate the metabolic switch of BMSCs in tissue defects through targeted modulation using built‐in magnetoelectric biomaterials is proposed. BMSCs cultured in the magnetoelectric microenvironment exhibited an increased mitochondrial membrane potential, the highest oxygen consumption rate and enhanced adenosine triphosphate production. Furthermore, BMSCs in the magnetoelectric microenvironment demonstrated a successful metabolic switch  of energy resource from glycolysis to oxidative phosphorylation, indicating a strong tendency toward osteogenic differentiation. The highest multiclass metabolite profile, indicating the most active metabolic state, was shown in rats cranial defect model treated with magnetoelectric microenvironment. This research introduces a novel approach to accelerate bone defect repair by targeted modulation of BMSC mitochondria with magnetoelectric microenvironment and provides a promising direction for exploring the intrinsic mechanisms through which the magnetoelectric microenvironment promotes bone regeneration.https://doi.org/10.1002/sstr.202400466bone marrow mesenchymal stem cell metabolismsmagnetoelectric microenvironmentsmetabolic switchesmitochondria functions osteogenic differentiations
spellingShingle Han Zhao
Fangyu Zhu
Yusi Guo
Xuliang Deng
Wenwen Liu
Metabolic Mechanism of Osteogenic Differentiation of Bone Marrow Mesenchymal Stem Cell Regulated by Magnetoelectric Microenvironment
Small Structures
bone marrow mesenchymal stem cell metabolisms
magnetoelectric microenvironments
metabolic switches
mitochondria functions osteogenic differentiations
title Metabolic Mechanism of Osteogenic Differentiation of Bone Marrow Mesenchymal Stem Cell Regulated by Magnetoelectric Microenvironment
title_full Metabolic Mechanism of Osteogenic Differentiation of Bone Marrow Mesenchymal Stem Cell Regulated by Magnetoelectric Microenvironment
title_fullStr Metabolic Mechanism of Osteogenic Differentiation of Bone Marrow Mesenchymal Stem Cell Regulated by Magnetoelectric Microenvironment
title_full_unstemmed Metabolic Mechanism of Osteogenic Differentiation of Bone Marrow Mesenchymal Stem Cell Regulated by Magnetoelectric Microenvironment
title_short Metabolic Mechanism of Osteogenic Differentiation of Bone Marrow Mesenchymal Stem Cell Regulated by Magnetoelectric Microenvironment
title_sort metabolic mechanism of osteogenic differentiation of bone marrow mesenchymal stem cell regulated by magnetoelectric microenvironment
topic bone marrow mesenchymal stem cell metabolisms
magnetoelectric microenvironments
metabolic switches
mitochondria functions osteogenic differentiations
url https://doi.org/10.1002/sstr.202400466
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AT fangyuzhu metabolicmechanismofosteogenicdifferentiationofbonemarrowmesenchymalstemcellregulatedbymagnetoelectricmicroenvironment
AT yusiguo metabolicmechanismofosteogenicdifferentiationofbonemarrowmesenchymalstemcellregulatedbymagnetoelectricmicroenvironment
AT xuliangdeng metabolicmechanismofosteogenicdifferentiationofbonemarrowmesenchymalstemcellregulatedbymagnetoelectricmicroenvironment
AT wenwenliu metabolicmechanismofosteogenicdifferentiationofbonemarrowmesenchymalstemcellregulatedbymagnetoelectricmicroenvironment