Synergistic effect of ultrasound and reinforced electrical environment by bioinspired periosteum for enhanced osteogenesis via immunomodulation of macrophage polarization through Piezo1

The periosteum plays a vital role in repairing bone defects. Researchers have demonstrated the existence of electrical potential in the periosteum and native bone, indicating that electrical signals are essential for functional bone regeneration. However, the clinical use of external electrical trea...

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Main Authors: Jiang, Ting, Yu, Fei, Zhou, Yuqi, Li, Ruomei, Zheng, Mengting, Jiang, Yangyang, Li, Zhenxia, Pan, Jun, Ouyang, Ningjuan
Other Authors: School of Physical and Mathematical Sciences
Format: Article
Language:English
Published: 2024
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Online Access:https://hdl.handle.net/10356/180507
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Institution: Nanyang Technological University
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spelling sg-ntu-dr.10356-1805072024-10-14T15:35:20Z Synergistic effect of ultrasound and reinforced electrical environment by bioinspired periosteum for enhanced osteogenesis via immunomodulation of macrophage polarization through Piezo1 Jiang, Ting Yu, Fei Zhou, Yuqi Li, Ruomei Zheng, Mengting Jiang, Yangyang Li, Zhenxia Pan, Jun Ouyang, Ningjuan School of Physical and Mathematical Sciences Physics Piezoelectric periosteum Electrical environment The periosteum plays a vital role in repairing bone defects. Researchers have demonstrated the existence of electrical potential in the periosteum and native bone, indicating that electrical signals are essential for functional bone regeneration. However, the clinical use of external electrical treatments has been limited due to their inconvenience and inefficacy. As an alternative, low-intensity pulsed ultrasound (LIPUS) is a noninvasive form of physical therapy that enhances bone regeneration. Furthermore, the wireless activation of piezoelectric biomaterials through ultrasound stimulation would generate electric charges precisely at the defect area, compensating for the insufficiency of external electrical stimulation and potentially promoting bone regeneration through the synergistic effect of mechanical and electrical stimulation. However, the optimal integration of LIPUS with an appropriate piezoelectric periosteum is yet to be explored. Herein, the BaTiO3/multiwalled-carbon nanotubes/collagen (BMC) membranes have been fabricated, possessing physicochemical properties including improved surface hydrophilicity, enhanced mechanical performance, ideal piezoelectricity, and outstanding biocompatibility, all of which are conducive to bone regeneration. When combined with LIPUS, the endogenous electrical microenvironment of native bone was recreated. After that, the wireless-generated electrical signals, along with the mechanical signals induced by LIPUS, were transferred to macrophages and activated Ca2+ influx through Piezo1. Ultimately, the regenerative effect of the BMC membrane with LIPUS stimulation (BMC + L) was confirmed in a mouse cranial defect model. Together, this research presents a co-engineering strategy that involves fabricating a novel biomimetic periosteum and utilizing the synergistic effect of ultrasound to enhance bone regeneration, which is achieved through the reinforcement of the electrical environment and the immunomodulation of macrophage polarization. Published version This work was supported by the National Natural Science Foundation of China (82101047), and Fundamental Research program funding of Ninth People’s Hospital affiliated with Shanghai Jiao Tong University School of Medicine (JYZZ138, JYZZ085B). Additional support was received from the Shanghai Key Laboratory of Translational Medicine on Ear and Nose Diseases (14DZ2260300), Shanghai’s Top Priority Research Center (2022ZZ01017), and CAMS Innovation Fund for Medical Sciences (CIFMS, 2019–12M-5-037). 2024-10-09T07:33:22Z 2024-10-09T07:33:22Z 2024 Journal Article Jiang, T., Yu, F., Zhou, Y., Li, R., Zheng, M., Jiang, Y., Li, Z., Pan, J. & Ouyang, N. (2024). Synergistic effect of ultrasound and reinforced electrical environment by bioinspired periosteum for enhanced osteogenesis via immunomodulation of macrophage polarization through Piezo1. Materials Today Bio, 27, 101147-. https://dx.doi.org/10.1016/j.mtbio.2024.101147 2590-0064 https://hdl.handle.net/10356/180507 10.1016/j.mtbio.2024.101147 2-s2.0-85197523274 27 101147 en Materials Today Bio © 2024 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC license (http://creativecommons.org/licenses/bync/4.0/). application/pdf
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Physics
Piezoelectric periosteum
Electrical environment
spellingShingle Physics
Piezoelectric periosteum
Electrical environment
Jiang, Ting
Yu, Fei
Zhou, Yuqi
Li, Ruomei
Zheng, Mengting
Jiang, Yangyang
Li, Zhenxia
Pan, Jun
Ouyang, Ningjuan
Synergistic effect of ultrasound and reinforced electrical environment by bioinspired periosteum for enhanced osteogenesis via immunomodulation of macrophage polarization through Piezo1
description The periosteum plays a vital role in repairing bone defects. Researchers have demonstrated the existence of electrical potential in the periosteum and native bone, indicating that electrical signals are essential for functional bone regeneration. However, the clinical use of external electrical treatments has been limited due to their inconvenience and inefficacy. As an alternative, low-intensity pulsed ultrasound (LIPUS) is a noninvasive form of physical therapy that enhances bone regeneration. Furthermore, the wireless activation of piezoelectric biomaterials through ultrasound stimulation would generate electric charges precisely at the defect area, compensating for the insufficiency of external electrical stimulation and potentially promoting bone regeneration through the synergistic effect of mechanical and electrical stimulation. However, the optimal integration of LIPUS with an appropriate piezoelectric periosteum is yet to be explored. Herein, the BaTiO3/multiwalled-carbon nanotubes/collagen (BMC) membranes have been fabricated, possessing physicochemical properties including improved surface hydrophilicity, enhanced mechanical performance, ideal piezoelectricity, and outstanding biocompatibility, all of which are conducive to bone regeneration. When combined with LIPUS, the endogenous electrical microenvironment of native bone was recreated. After that, the wireless-generated electrical signals, along with the mechanical signals induced by LIPUS, were transferred to macrophages and activated Ca2+ influx through Piezo1. Ultimately, the regenerative effect of the BMC membrane with LIPUS stimulation (BMC + L) was confirmed in a mouse cranial defect model. Together, this research presents a co-engineering strategy that involves fabricating a novel biomimetic periosteum and utilizing the synergistic effect of ultrasound to enhance bone regeneration, which is achieved through the reinforcement of the electrical environment and the immunomodulation of macrophage polarization.
author2 School of Physical and Mathematical Sciences
author_facet School of Physical and Mathematical Sciences
Jiang, Ting
Yu, Fei
Zhou, Yuqi
Li, Ruomei
Zheng, Mengting
Jiang, Yangyang
Li, Zhenxia
Pan, Jun
Ouyang, Ningjuan
format Article
author Jiang, Ting
Yu, Fei
Zhou, Yuqi
Li, Ruomei
Zheng, Mengting
Jiang, Yangyang
Li, Zhenxia
Pan, Jun
Ouyang, Ningjuan
author_sort Jiang, Ting
title Synergistic effect of ultrasound and reinforced electrical environment by bioinspired periosteum for enhanced osteogenesis via immunomodulation of macrophage polarization through Piezo1
title_short Synergistic effect of ultrasound and reinforced electrical environment by bioinspired periosteum for enhanced osteogenesis via immunomodulation of macrophage polarization through Piezo1
title_full Synergistic effect of ultrasound and reinforced electrical environment by bioinspired periosteum for enhanced osteogenesis via immunomodulation of macrophage polarization through Piezo1
title_fullStr Synergistic effect of ultrasound and reinforced electrical environment by bioinspired periosteum for enhanced osteogenesis via immunomodulation of macrophage polarization through Piezo1
title_full_unstemmed Synergistic effect of ultrasound and reinforced electrical environment by bioinspired periosteum for enhanced osteogenesis via immunomodulation of macrophage polarization through Piezo1
title_sort synergistic effect of ultrasound and reinforced electrical environment by bioinspired periosteum for enhanced osteogenesis via immunomodulation of macrophage polarization through piezo1
publishDate 2024
url https://hdl.handle.net/10356/180507
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