A Biomimetic Fibrous Composite Scaffold with Nanotopography-Regulated Mineralization for Bone Defect Repair
The effective regeneration of large bone defects via bone tissue engineering is challenging due to the difficulty in creating an osteogenic microenvironment. Inspired by the fibrillar architecture of the natural extracellular matrix, we developed a nanoscale bioengineering strategy to produce bone f...
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| Veröffentlicht in: | Biomacromolecules 2024-06, Vol.25 (6), p.3784-3794 |
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| creator | Jiang, Kai Wang, Kai Luo, Chuan Su, Biao-Yao Du, Hao Liu, Yao Lei, Jun Luo, En Cardon, Ludwig Edeleva, Mariya Huang, Shi-Shu Xu, Jia-Zhuang Li, Zhong-Ming |
| description | The effective regeneration of large bone defects via bone tissue engineering is challenging due to the difficulty in creating an osteogenic microenvironment. Inspired by the fibrillar architecture of the natural extracellular matrix, we developed a nanoscale bioengineering strategy to produce bone fibril-like composite scaffolds with enhanced osteogenic capability. To activate the surface for biofunctionalization, self-adaptive ridge-like nanolamellae were constructed on poly(ε-caprolactone) (PCL) electrospinning scaffolds via surface-directed epitaxial crystallization. This unique nanotopography with a markedly increased specific surface area offered abundant nucleation sites for Ca2+ recruitment, leading to a 5-fold greater deposition weight of hydroxyapatite than that of the pristine PCL scaffold under stimulated physiological conditions. Bone marrow mesenchymal stem cells (BMSCs) cultured on bone fibril-like scaffolds exhibited enhanced adhesion, proliferation, and osteogenic differentiation in vitro. In a rat calvarial defect model, the bone fibril-like scaffold significantly accelerated bone regeneration, as evidenced by micro-CT, histological histological and immunofluorescence staining. This work provides the way for recapitulating the osteogenic microenvironment in tissue-engineered scaffolds for bone repair. |
| doi_str_mv | 10.1021/acs.biomac.4c00378 |
| format | Article |
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Inspired by the fibrillar architecture of the natural extracellular matrix, we developed a nanoscale bioengineering strategy to produce bone fibril-like composite scaffolds with enhanced osteogenic capability. To activate the surface for biofunctionalization, self-adaptive ridge-like nanolamellae were constructed on poly(ε-caprolactone) (PCL) electrospinning scaffolds via surface-directed epitaxial crystallization. This unique nanotopography with a markedly increased specific surface area offered abundant nucleation sites for Ca2+ recruitment, leading to a 5-fold greater deposition weight of hydroxyapatite than that of the pristine PCL scaffold under stimulated physiological conditions. Bone marrow mesenchymal stem cells (BMSCs) cultured on bone fibril-like scaffolds exhibited enhanced adhesion, proliferation, and osteogenic differentiation in vitro. In a rat calvarial defect model, the bone fibril-like scaffold significantly accelerated bone regeneration, as evidenced by micro-CT, histological histological and immunofluorescence staining. This work provides the way for recapitulating the osteogenic microenvironment in tissue-engineered scaffolds for bone repair.</description><identifier>ISSN: 1525-7797</identifier><identifier>ISSN: 1526-4602</identifier><identifier>EISSN: 1526-4602</identifier><identifier>DOI: 10.1021/acs.biomac.4c00378</identifier><identifier>PMID: 38743836</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>adhesion ; Animals ; Biomimetic Materials - chemistry ; Biomimetic Materials - pharmacology ; biomimetics ; bone formation ; bone marrow ; Bone Regeneration - drug effects ; calcium ; Cell Differentiation ; Cell Proliferation ; Cells, Cultured ; crystallization ; Durapatite - chemistry ; Durapatite - pharmacology ; extracellular matrix ; fluorescent antibody technique ; histology ; hydroxyapatite ; Mesenchymal Stem Cells - cytology ; micro-computed tomography ; mineralization ; nanomaterials ; Osteogenesis - drug effects ; Osteogenesis - physiology ; Polyesters - chemistry ; Rats ; Rats, Sprague-Dawley ; Skull - injuries ; Skull - pathology ; surface area ; Tissue Engineering - methods ; Tissue Scaffolds - chemistry</subject><ispartof>Biomacromolecules, 2024-06, Vol.25 (6), p.3784-3794</ispartof><rights>2024 American Chemical Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a326t-2d8a056bc2d50d65c764844eb278b7c39be1300687f341c57d27f10a054fedbb3</cites><orcidid>0000-0002-4019-612X ; 0000-0001-7203-1453 ; 0000-0001-6803-5216 ; 0000-0001-9888-7014</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://pubs.acs.org/doi/pdf/10.1021/acs.biomac.4c00378$$EPDF$$P50$$Gacs$$H</linktopdf><linktohtml>$$Uhttps://pubs.acs.org/doi/10.1021/acs.biomac.4c00378$$EHTML$$P50$$Gacs$$H</linktohtml><link.rule.ids>314,778,782,2754,27063,27911,27912,56725,56775</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38743836$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jiang, Kai</creatorcontrib><creatorcontrib>Wang, Kai</creatorcontrib><creatorcontrib>Luo, Chuan</creatorcontrib><creatorcontrib>Su, Biao-Yao</creatorcontrib><creatorcontrib>Du, Hao</creatorcontrib><creatorcontrib>Liu, Yao</creatorcontrib><creatorcontrib>Lei, Jun</creatorcontrib><creatorcontrib>Luo, En</creatorcontrib><creatorcontrib>Cardon, Ludwig</creatorcontrib><creatorcontrib>Edeleva, Mariya</creatorcontrib><creatorcontrib>Huang, Shi-Shu</creatorcontrib><creatorcontrib>Xu, Jia-Zhuang</creatorcontrib><creatorcontrib>Li, Zhong-Ming</creatorcontrib><title>A Biomimetic Fibrous Composite Scaffold with Nanotopography-Regulated Mineralization for Bone Defect Repair</title><title>Biomacromolecules</title><addtitle>Biomacromolecules</addtitle><description>The effective regeneration of large bone defects via bone tissue engineering is challenging due to the difficulty in creating an osteogenic microenvironment. Inspired by the fibrillar architecture of the natural extracellular matrix, we developed a nanoscale bioengineering strategy to produce bone fibril-like composite scaffolds with enhanced osteogenic capability. To activate the surface for biofunctionalization, self-adaptive ridge-like nanolamellae were constructed on poly(ε-caprolactone) (PCL) electrospinning scaffolds via surface-directed epitaxial crystallization. This unique nanotopography with a markedly increased specific surface area offered abundant nucleation sites for Ca2+ recruitment, leading to a 5-fold greater deposition weight of hydroxyapatite than that of the pristine PCL scaffold under stimulated physiological conditions. Bone marrow mesenchymal stem cells (BMSCs) cultured on bone fibril-like scaffolds exhibited enhanced adhesion, proliferation, and osteogenic differentiation in vitro. In a rat calvarial defect model, the bone fibril-like scaffold significantly accelerated bone regeneration, as evidenced by micro-CT, histological histological and immunofluorescence staining. This work provides the way for recapitulating the osteogenic microenvironment in tissue-engineered scaffolds for bone repair.</description><subject>adhesion</subject><subject>Animals</subject><subject>Biomimetic Materials - chemistry</subject><subject>Biomimetic Materials - pharmacology</subject><subject>biomimetics</subject><subject>bone formation</subject><subject>bone marrow</subject><subject>Bone Regeneration - drug effects</subject><subject>calcium</subject><subject>Cell Differentiation</subject><subject>Cell Proliferation</subject><subject>Cells, Cultured</subject><subject>crystallization</subject><subject>Durapatite - chemistry</subject><subject>Durapatite - pharmacology</subject><subject>extracellular matrix</subject><subject>fluorescent antibody technique</subject><subject>histology</subject><subject>hydroxyapatite</subject><subject>Mesenchymal Stem Cells - cytology</subject><subject>micro-computed tomography</subject><subject>mineralization</subject><subject>nanomaterials</subject><subject>Osteogenesis - drug effects</subject><subject>Osteogenesis - physiology</subject><subject>Polyesters - chemistry</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Skull - injuries</subject><subject>Skull - pathology</subject><subject>surface area</subject><subject>Tissue Engineering - methods</subject><subject>Tissue Scaffolds - chemistry</subject><issn>1525-7797</issn><issn>1526-4602</issn><issn>1526-4602</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU1v1DAQhi0E6vcf4IB85JLF3_Ye24UWpAJSac-R7YxblyQOtqOq_Pqm3YUjnGYOz_tKMw9CbylZUcLoB-vLysU0WL8SnhCuzSt0QCVTjVCEvX7ZZaP1Wu-jw1LuCSFrLuQe2udGC264OkA_T_HZUhEHqNHj8-hymgvepGFKJVbAP7wNIfUdfoj1Dn-zY6ppSrfZTnePzRXczr2t0OGvcYRs-_jb1phGHFLGZ2kE_BEC-IqvYLIxH6M3wfYFTnbzCN2cf7refG4uv1982ZxeNpYzVRvWGUukcp51knRKeq2EEQIc08Zpz9cOKCdEGR24oF7qjulAyZIRATrn-BF6v-2dcvo1Q6ntEIuHvrcjLNe1nEqumNLU_B8lUgpJjVALyraoz6mUDKGdchxsfmwpaZ99tIuPduuj3flYQu92_bMboPsb-SNgAVZb4Dl8n-Y8Lp_5V-MTMu2Y4w</recordid><startdate>20240610</startdate><enddate>20240610</enddate><creator>Jiang, Kai</creator><creator>Wang, Kai</creator><creator>Luo, Chuan</creator><creator>Su, Biao-Yao</creator><creator>Du, Hao</creator><creator>Liu, Yao</creator><creator>Lei, Jun</creator><creator>Luo, En</creator><creator>Cardon, Ludwig</creator><creator>Edeleva, Mariya</creator><creator>Huang, Shi-Shu</creator><creator>Xu, Jia-Zhuang</creator><creator>Li, Zhong-Ming</creator><general>American Chemical Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0002-4019-612X</orcidid><orcidid>https://orcid.org/0000-0001-7203-1453</orcidid><orcidid>https://orcid.org/0000-0001-6803-5216</orcidid><orcidid>https://orcid.org/0000-0001-9888-7014</orcidid></search><sort><creationdate>20240610</creationdate><title>A Biomimetic Fibrous Composite Scaffold with Nanotopography-Regulated Mineralization for Bone Defect Repair</title><author>Jiang, Kai ; Wang, Kai ; Luo, Chuan ; Su, Biao-Yao ; Du, Hao ; Liu, Yao ; Lei, Jun ; Luo, En ; Cardon, Ludwig ; Edeleva, Mariya ; Huang, Shi-Shu ; Xu, Jia-Zhuang ; Li, Zhong-Ming</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a326t-2d8a056bc2d50d65c764844eb278b7c39be1300687f341c57d27f10a054fedbb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>adhesion</topic><topic>Animals</topic><topic>Biomimetic Materials - chemistry</topic><topic>Biomimetic Materials - pharmacology</topic><topic>biomimetics</topic><topic>bone formation</topic><topic>bone marrow</topic><topic>Bone Regeneration - drug effects</topic><topic>calcium</topic><topic>Cell Differentiation</topic><topic>Cell Proliferation</topic><topic>Cells, Cultured</topic><topic>crystallization</topic><topic>Durapatite - chemistry</topic><topic>Durapatite - pharmacology</topic><topic>extracellular matrix</topic><topic>fluorescent antibody technique</topic><topic>histology</topic><topic>hydroxyapatite</topic><topic>Mesenchymal Stem Cells - cytology</topic><topic>micro-computed tomography</topic><topic>mineralization</topic><topic>nanomaterials</topic><topic>Osteogenesis - drug effects</topic><topic>Osteogenesis - physiology</topic><topic>Polyesters - chemistry</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Skull - injuries</topic><topic>Skull - pathology</topic><topic>surface area</topic><topic>Tissue Engineering - methods</topic><topic>Tissue Scaffolds - chemistry</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jiang, Kai</creatorcontrib><creatorcontrib>Wang, Kai</creatorcontrib><creatorcontrib>Luo, Chuan</creatorcontrib><creatorcontrib>Su, Biao-Yao</creatorcontrib><creatorcontrib>Du, Hao</creatorcontrib><creatorcontrib>Liu, Yao</creatorcontrib><creatorcontrib>Lei, Jun</creatorcontrib><creatorcontrib>Luo, En</creatorcontrib><creatorcontrib>Cardon, Ludwig</creatorcontrib><creatorcontrib>Edeleva, Mariya</creatorcontrib><creatorcontrib>Huang, Shi-Shu</creatorcontrib><creatorcontrib>Xu, Jia-Zhuang</creatorcontrib><creatorcontrib>Li, Zhong-Ming</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Biomacromolecules</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jiang, Kai</au><au>Wang, Kai</au><au>Luo, Chuan</au><au>Su, Biao-Yao</au><au>Du, Hao</au><au>Liu, Yao</au><au>Lei, Jun</au><au>Luo, En</au><au>Cardon, Ludwig</au><au>Edeleva, Mariya</au><au>Huang, Shi-Shu</au><au>Xu, Jia-Zhuang</au><au>Li, Zhong-Ming</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Biomimetic Fibrous Composite Scaffold with Nanotopography-Regulated Mineralization for Bone Defect Repair</atitle><jtitle>Biomacromolecules</jtitle><addtitle>Biomacromolecules</addtitle><date>2024-06-10</date><risdate>2024</risdate><volume>25</volume><issue>6</issue><spage>3784</spage><epage>3794</epage><pages>3784-3794</pages><issn>1525-7797</issn><issn>1526-4602</issn><eissn>1526-4602</eissn><abstract>The effective regeneration of large bone defects via bone tissue engineering is challenging due to the difficulty in creating an osteogenic microenvironment. Inspired by the fibrillar architecture of the natural extracellular matrix, we developed a nanoscale bioengineering strategy to produce bone fibril-like composite scaffolds with enhanced osteogenic capability. To activate the surface for biofunctionalization, self-adaptive ridge-like nanolamellae were constructed on poly(ε-caprolactone) (PCL) electrospinning scaffolds via surface-directed epitaxial crystallization. This unique nanotopography with a markedly increased specific surface area offered abundant nucleation sites for Ca2+ recruitment, leading to a 5-fold greater deposition weight of hydroxyapatite than that of the pristine PCL scaffold under stimulated physiological conditions. Bone marrow mesenchymal stem cells (BMSCs) cultured on bone fibril-like scaffolds exhibited enhanced adhesion, proliferation, and osteogenic differentiation in vitro. In a rat calvarial defect model, the bone fibril-like scaffold significantly accelerated bone regeneration, as evidenced by micro-CT, histological histological and immunofluorescence staining. This work provides the way for recapitulating the osteogenic microenvironment in tissue-engineered scaffolds for bone repair.</abstract><cop>United States</cop><pub>American Chemical Society</pub><pmid>38743836</pmid><doi>10.1021/acs.biomac.4c00378</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-4019-612X</orcidid><orcidid>https://orcid.org/0000-0001-7203-1453</orcidid><orcidid>https://orcid.org/0000-0001-6803-5216</orcidid><orcidid>https://orcid.org/0000-0001-9888-7014</orcidid></addata></record> |
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| subjects | adhesion Animals Biomimetic Materials - chemistry Biomimetic Materials - pharmacology biomimetics bone formation bone marrow Bone Regeneration - drug effects calcium Cell Differentiation Cell Proliferation Cells, Cultured crystallization Durapatite - chemistry Durapatite - pharmacology extracellular matrix fluorescent antibody technique histology hydroxyapatite Mesenchymal Stem Cells - cytology micro-computed tomography mineralization nanomaterials Osteogenesis - drug effects Osteogenesis - physiology Polyesters - chemistry Rats Rats, Sprague-Dawley Skull - injuries Skull - pathology surface area Tissue Engineering - methods Tissue Scaffolds - chemistry |
| title | A Biomimetic Fibrous Composite Scaffold with Nanotopography-Regulated Mineralization for Bone Defect Repair |
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