Periosteal matrix-derived hydrogel promotes bone repair through an early immune regulation coupled with enhanced angio- and osteogenesis

Bone healing is a complex physiological process initiated by early regulation of the inflammatory immunity and entails multiple events including angiogenesis, osteogenic differentiation, and biomineralization. Here, we fabricated an injectable periosteal extracellular matrix (PEM) hydrogel that dyna...

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Published in:	Biomaterials Vol. 227; p. 119552
Main Authors:	Qiu, Pengcheng, Li, Mobai, Chen, Kai, Fang, Bin, Chen, Pengfei, Tang, Zhibin, Lin, Xianfeng, Fan, Shunwu
Format:	Journal Article
Language:	English
Published:	Netherlands Elsevier Ltd 01.01.2020
Subjects:	Angiogenesis Animals bioactive properties biocompatible materials Biomineralization blood vessels body fluids bone formation Bone Regeneration bones Cell Differentiation collagen Decellularized periosteum matrix hydrogel Early inflammatory immune regulation extracellular matrix Hydrogels immunity in vitro studies Macrophages osteoblasts Osteogenesis Rats Tissue Engineering Biomineralization Decellularized periosteum matrix hydrogel Angiogenesis Early inflammatory immune regulation Macrophages Bone regeneration
ISSN:	0142-9612, 1878-5905, 1878-5905
Online Access:	Get full text
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Abstract	Bone healing is a complex physiological process initiated by early regulation of the inflammatory immunity and entails multiple events including angiogenesis, osteogenic differentiation, and biomineralization. Here, we fabricated an injectable periosteal extracellular matrix (PEM) hydrogel that dynamically integrates multiple biological functions and, therefore, acts at different stages of the fracture healing process. PEM hydrogels were fully characterized compared with a collagen I hydrogel. The effects of PEM hydrogels on the different phases of the healing process were assessed in vitro. PEM hydrogels induced the recruitment and M2-polarization of macrophages, promoted the differentiation of MSCs into endothelial-like cells, HUVEC tube formation, osteogenic differentiation of primary calvarial osteoblasts and MSCs, and mineralization after being immersed in simulated body fluid. The dynamic and multiphase effects of the hydrogels were evaluated using a rat critical-sized calvarial defect model in vivo. During the early phase of repair, PEM hydrogels facilitated the M1-to-M2 transition of macrophages. As bone repair progressed, PEM hydrogels promoted blood vessel migration, the development of relative larger blood vessels, and functional vascularization. These effects were also verified in a subcutaneous embedding model. Eventually, PEM hydrogels promoted mature bone formation in large bone defects to a greater extent than collagen I hydrogels. These biological effects coordinated well with the natural process of bone regeneration. Thus, PEM hydrogels may serve as promising biomaterials in bone tissue engineering. •Prolonged M1 phase and an M2 transformation failure occur in critical size bone defects.•PEM hydrogels participate in early immune regulation of bone repair and promotes M1-to-M2 transition of macrophages.•PEM hydrogels play a promoting role in the process angiogenesis and osteogenic differentiation of bone repair.•PEM hydrogels coordinate and guide several overlapping bone regeneration events.•PEM hydrogels showed superior bone healing properties.
AbstractList	Bone healing is a complex physiological process initiated by early regulation of the inflammatory immunity and entails multiple events including angiogenesis, osteogenic differentiation, and biomineralization. Here, we fabricated an injectable periosteal extracellular matrix (PEM) hydrogel that dynamically integrates multiple biological functions and, therefore, acts at different stages of the fracture healing process. PEM hydrogels were fully characterized compared with a collagen I hydrogel. The effects of PEM hydrogels on the different phases of the healing process were assessed in vitro. PEM hydrogels induced the recruitment and M2-polarization of macrophages, promoted the differentiation of MSCs into endothelial-like cells, HUVEC tube formation, osteogenic differentiation of primary calvarial osteoblasts and MSCs, and mineralization after being immersed in simulated body fluid. The dynamic and multiphase effects of the hydrogels were evaluated using a rat critical-sized calvarial defect model in vivo. During the early phase of repair, PEM hydrogels facilitated the M1-to-M2 transition of macrophages. As bone repair progressed, PEM hydrogels promoted blood vessel migration, the development of relative larger blood vessels, and functional vascularization. These effects were also verified in a subcutaneous embedding model. Eventually, PEM hydrogels promoted mature bone formation in large bone defects to a greater extent than collagen I hydrogels. These biological effects coordinated well with the natural process of bone regeneration. Thus, PEM hydrogels may serve as promising biomaterials in bone tissue engineering.Bone healing is a complex physiological process initiated by early regulation of the inflammatory immunity and entails multiple events including angiogenesis, osteogenic differentiation, and biomineralization. Here, we fabricated an injectable periosteal extracellular matrix (PEM) hydrogel that dynamically integrates multiple biological functions and, therefore, acts at different stages of the fracture healing process. PEM hydrogels were fully characterized compared with a collagen I hydrogel. The effects of PEM hydrogels on the different phases of the healing process were assessed in vitro. PEM hydrogels induced the recruitment and M2-polarization of macrophages, promoted the differentiation of MSCs into endothelial-like cells, HUVEC tube formation, osteogenic differentiation of primary calvarial osteoblasts and MSCs, and mineralization after being immersed in simulated body fluid. The dynamic and multiphase effects of the hydrogels were evaluated using a rat critical-sized calvarial defect model in vivo. During the early phase of repair, PEM hydrogels facilitated the M1-to-M2 transition of macrophages. As bone repair progressed, PEM hydrogels promoted blood vessel migration, the development of relative larger blood vessels, and functional vascularization. These effects were also verified in a subcutaneous embedding model. Eventually, PEM hydrogels promoted mature bone formation in large bone defects to a greater extent than collagen I hydrogels. These biological effects coordinated well with the natural process of bone regeneration. Thus, PEM hydrogels may serve as promising biomaterials in bone tissue engineering. Bone healing is a complex physiological process initiated by early regulation of the inflammatory immunity and entails multiple events including angiogenesis, osteogenic differentiation, and biomineralization. Here, we fabricated an injectable periosteal extracellular matrix (PEM) hydrogel that dynamically integrates multiple biological functions and, therefore, acts at different stages of the fracture healing process. PEM hydrogels were fully characterized compared with a collagen I hydrogel. The effects of PEM hydrogels on the different phases of the healing process were assessed in vitro. PEM hydrogels induced the recruitment and M2-polarization of macrophages, promoted the differentiation of MSCs into endothelial-like cells, HUVEC tube formation, osteogenic differentiation of primary calvarial osteoblasts and MSCs, and mineralization after being immersed in simulated body fluid. The dynamic and multiphase effects of the hydrogels were evaluated using a rat critical-sized calvarial defect model in vivo. During the early phase of repair, PEM hydrogels facilitated the M1-to-M2 transition of macrophages. As bone repair progressed, PEM hydrogels promoted blood vessel migration, the development of relative larger blood vessels, and functional vascularization. These effects were also verified in a subcutaneous embedding model. Eventually, PEM hydrogels promoted mature bone formation in large bone defects to a greater extent than collagen I hydrogels. These biological effects coordinated well with the natural process of bone regeneration. Thus, PEM hydrogels may serve as promising biomaterials in bone tissue engineering. •Prolonged M1 phase and an M2 transformation failure occur in critical size bone defects.•PEM hydrogels participate in early immune regulation of bone repair and promotes M1-to-M2 transition of macrophages.•PEM hydrogels play a promoting role in the process angiogenesis and osteogenic differentiation of bone repair.•PEM hydrogels coordinate and guide several overlapping bone regeneration events.•PEM hydrogels showed superior bone healing properties. Bone healing is a complex physiological process initiated by early regulation of the inflammatory immunity and entails multiple events including angiogenesis, osteogenic differentiation, and biomineralization. Here, we fabricated an injectable periosteal extracellular matrix (PEM) hydrogel that dynamically integrates multiple biological functions and, therefore, acts at different stages of the fracture healing process. PEM hydrogels were fully characterized compared with a collagen I hydrogel. The effects of PEM hydrogels on the different phases of the healing process were assessed in vitro. PEM hydrogels induced the recruitment and M2-polarization of macrophages, promoted the differentiation of MSCs into endothelial-like cells, HUVEC tube formation, osteogenic differentiation of primary calvarial osteoblasts and MSCs, and mineralization after being immersed in simulated body fluid. The dynamic and multiphase effects of the hydrogels were evaluated using a rat critical-sized calvarial defect model in vivo. During the early phase of repair, PEM hydrogels facilitated the M1-to-M2 transition of macrophages. As bone repair progressed, PEM hydrogels promoted blood vessel migration, the development of relative larger blood vessels, and functional vascularization. These effects were also verified in a subcutaneous embedding model. Eventually, PEM hydrogels promoted mature bone formation in large bone defects to a greater extent than collagen I hydrogels. These biological effects coordinated well with the natural process of bone regeneration. Thus, PEM hydrogels may serve as promising biomaterials in bone tissue engineering.
ArticleNumber	119552
Author	Fan, Shunwu Tang, Zhibin Lin, Xianfeng Chen, Kai Chen, Pengfei Fang, Bin Li, Mobai Qiu, Pengcheng
Author_xml	– sequence: 1 givenname: Pengcheng surname: Qiu fullname: Qiu, Pengcheng organization: Department of Orthopaedic Surgery, Sir Run Run Shaw Hospital, Medical College of Zhejiang University, Hangzhou, China – sequence: 2 givenname: Mobai surname: Li fullname: Li, Mobai organization: Department of Orthopaedic Surgery, Sir Run Run Shaw Hospital, Medical College of Zhejiang University, Hangzhou, China – sequence: 3 givenname: Kai surname: Chen fullname: Chen, Kai organization: School of Biomedical Sciences, University of Western Australia, Perth, WA, Australia – sequence: 4 givenname: Bin surname: Fang fullname: Fang, Bin organization: Department of Orthopaedic Surgery, Sir Run Run Shaw Hospital, Medical College of Zhejiang University, Hangzhou, China – sequence: 5 givenname: Pengfei surname: Chen fullname: Chen, Pengfei organization: Department of Orthopaedic Surgery, Sir Run Run Shaw Hospital, Medical College of Zhejiang University, Hangzhou, China – sequence: 6 givenname: Zhibin surname: Tang fullname: Tang, Zhibin organization: Department of Orthopaedic Surgery, Sir Run Run Shaw Hospital, Medical College of Zhejiang University, Hangzhou, China – sequence: 7 givenname: Xianfeng surname: Lin fullname: Lin, Xianfeng email: xianfeng_lin@zju.edu.cn organization: Department of Orthopaedic Surgery, Sir Run Run Shaw Hospital, Medical College of Zhejiang University, Hangzhou, China – sequence: 8 givenname: Shunwu surname: Fan fullname: Fan, Shunwu email: shunwu_fan@zju.edu.cn organization: Department of Orthopaedic Surgery, Sir Run Run Shaw Hospital, Medical College of Zhejiang University, Hangzhou, China
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/31670079$$D View this record in MEDLINE/PubMed
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Keywords	Biomineralization Decellularized periosteum matrix hydrogel Angiogenesis Early inflammatory immune regulation Macrophages Bone regeneration
Language	English
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Snippet	Bone healing is a complex physiological process initiated by early regulation of the inflammatory immunity and entails multiple events including angiogenesis,...
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SubjectTerms	Angiogenesis Animals bioactive properties biocompatible materials Biomineralization blood vessels body fluids bone formation Bone Regeneration bones Cell Differentiation collagen Decellularized periosteum matrix hydrogel Early inflammatory immune regulation extracellular matrix Hydrogels immunity in vitro studies Macrophages osteoblasts Osteogenesis Rats Tissue Engineering
Title	Periosteal matrix-derived hydrogel promotes bone repair through an early immune regulation coupled with enhanced angio- and osteogenesis
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