Decellularized Periosteum-Derived Hydrogels Promote the Proliferation, Migration and Osteogenic Differentiation of Human Umbilical Cord Mesenchymal Stem Cells

Human umbilical cord mesenchymal stem cells (hUCMSCs) are promising for bone tissue engineering, which have a non-invasive harvesting process, high cell yield, favorable proliferation capacity, and low immunogenicity. However, the osteogenic efficacy of hUCMSCs is relatively lower than that of bone...

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Main Authors: Shuyi Li, Rongli Deng, Tim Forouzanfar, Gang Wu, Daping Quan, Miao Zhou
Format: Article
Language:English
Published: MDPI AG 2022-05-01
Series:Gels
Subjects:
Online Access:https://www.mdpi.com/2310-2861/8/5/294
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author Shuyi Li
Rongli Deng
Tim Forouzanfar
Gang Wu
Daping Quan
Miao Zhou
author_facet Shuyi Li
Rongli Deng
Tim Forouzanfar
Gang Wu
Daping Quan
Miao Zhou
author_sort Shuyi Li
collection DOAJ
description Human umbilical cord mesenchymal stem cells (hUCMSCs) are promising for bone tissue engineering, which have a non-invasive harvesting process, high cell yield, favorable proliferation capacity, and low immunogenicity. However, the osteogenic efficacy of hUCMSCs is relatively lower than that of bone marrow mesenchymal stem cells (BMSCs). Hydrogels from decellularized extracellular matrix (dECM) preserve the biological compositions and functions of natural ECM, which can provide tissue-specific cues to regulate phenotypic expression and cell fate. It is unknown, however, whether hydrogels from periosteum can serve as pro-osteogenic carriers of hUCMSCs. Herein, a decellularized periosteum-derived hydrogel (dPH) was fabricated to reveal the effects of periosteum-specific cues on the bioactivities of hUCMSCs. A widely used non-bone/periosteum-derived ECM hydrogel product, Matrigel, was used as the control group. After decellularization, the absence of nuclei in the histological analysis indicated a successful removal of cellular components, which was also confirmed by DNA content quantification. The storage modulus of dPH increased (from 164.49 ± 29.92 Pa to 855.20 ± 20.67 Pa) with increasing concentration (from 0.5% to 1%). With a highly porous, fibrous microstructure, dPH had a more hydrophilic surface than Matrigel, of which the water contact angle reduced 62.62 ± 0.04%. Furthermore, dPH prominently promoted the initial cellular spreading with a significantly higher cell surface area (1.47-fold), cell spreading length (1.45-fold) and proliferation (approximately 1.05–1.13-fold) of hUCMSCs than those of Matrigel. Additionally, dPH was conducive to cell migration, whereas no cells migrated to Matrigel in the Transwell model. Compared with those of the Matrigel group, the osteogenesis-related genes expression levels (runt-related transcription factor 2 (RUNX2), alkaline phosphatase (ALP), osteopontin (OPN), and osteocalcin (OCN)) and mineralized matrix formation (9.74-fold) of the hUCMSCs significantly increased in the dPH group. Our study indicated that dPH could provide a pro-osteogenic microenvironment for hUCMSCs, thereby revealing a promising application potential to repair bone defects.
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spelling doaj.art-0eaef1ec70cb46d18d12005a17a056112023-11-23T11:07:47ZengMDPI AGGels2310-28612022-05-018529410.3390/gels8050294Decellularized Periosteum-Derived Hydrogels Promote the Proliferation, Migration and Osteogenic Differentiation of Human Umbilical Cord Mesenchymal Stem CellsShuyi Li0Rongli Deng1Tim Forouzanfar2Gang Wu3Daping Quan4Miao Zhou5Department of Stomatology, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Science, Guangzhou 510080, ChinaPCFM Laboratory, School of Chemistry and School of Materials Science and Engineering, Sun Yat-sen University, Guangzhou 510006, ChinaDepartment of Oral and Maxillofacial Surgery/Pathology, Amsterdam UMC and Academic Center for Dentistry Amsterdam (ACTA), Amsterdam Movement Science, Vrije Universiteit Amsterdam, 1081 LA Amsterdam, The NetherlandsDepartment of Oral Cell Biology, Academic Center for Dentistry Amsterdam (ACTA), University of Amsterdam and Vrije Universiteit Amsterdam, 1081 LA Amsterdam, The NetherlandsPCFM Laboratory, School of Chemistry and School of Materials Science and Engineering, Sun Yat-sen University, Guangzhou 510006, ChinaDepartment of Stomatology, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Science, Guangzhou 510080, ChinaHuman umbilical cord mesenchymal stem cells (hUCMSCs) are promising for bone tissue engineering, which have a non-invasive harvesting process, high cell yield, favorable proliferation capacity, and low immunogenicity. However, the osteogenic efficacy of hUCMSCs is relatively lower than that of bone marrow mesenchymal stem cells (BMSCs). Hydrogels from decellularized extracellular matrix (dECM) preserve the biological compositions and functions of natural ECM, which can provide tissue-specific cues to regulate phenotypic expression and cell fate. It is unknown, however, whether hydrogels from periosteum can serve as pro-osteogenic carriers of hUCMSCs. Herein, a decellularized periosteum-derived hydrogel (dPH) was fabricated to reveal the effects of periosteum-specific cues on the bioactivities of hUCMSCs. A widely used non-bone/periosteum-derived ECM hydrogel product, Matrigel, was used as the control group. After decellularization, the absence of nuclei in the histological analysis indicated a successful removal of cellular components, which was also confirmed by DNA content quantification. The storage modulus of dPH increased (from 164.49 ± 29.92 Pa to 855.20 ± 20.67 Pa) with increasing concentration (from 0.5% to 1%). With a highly porous, fibrous microstructure, dPH had a more hydrophilic surface than Matrigel, of which the water contact angle reduced 62.62 ± 0.04%. Furthermore, dPH prominently promoted the initial cellular spreading with a significantly higher cell surface area (1.47-fold), cell spreading length (1.45-fold) and proliferation (approximately 1.05–1.13-fold) of hUCMSCs than those of Matrigel. Additionally, dPH was conducive to cell migration, whereas no cells migrated to Matrigel in the Transwell model. Compared with those of the Matrigel group, the osteogenesis-related genes expression levels (runt-related transcription factor 2 (RUNX2), alkaline phosphatase (ALP), osteopontin (OPN), and osteocalcin (OCN)) and mineralized matrix formation (9.74-fold) of the hUCMSCs significantly increased in the dPH group. Our study indicated that dPH could provide a pro-osteogenic microenvironment for hUCMSCs, thereby revealing a promising application potential to repair bone defects.https://www.mdpi.com/2310-2861/8/5/294periosteumdecellularized extracellular matrix-derived hydrogelsMatrigelhUCMSCsosteogenic differentiation
spellingShingle Shuyi Li
Rongli Deng
Tim Forouzanfar
Gang Wu
Daping Quan
Miao Zhou
Decellularized Periosteum-Derived Hydrogels Promote the Proliferation, Migration and Osteogenic Differentiation of Human Umbilical Cord Mesenchymal Stem Cells
Gels
periosteum
decellularized extracellular matrix-derived hydrogels
Matrigel
hUCMSCs
osteogenic differentiation
title Decellularized Periosteum-Derived Hydrogels Promote the Proliferation, Migration and Osteogenic Differentiation of Human Umbilical Cord Mesenchymal Stem Cells
title_full Decellularized Periosteum-Derived Hydrogels Promote the Proliferation, Migration and Osteogenic Differentiation of Human Umbilical Cord Mesenchymal Stem Cells
title_fullStr Decellularized Periosteum-Derived Hydrogels Promote the Proliferation, Migration and Osteogenic Differentiation of Human Umbilical Cord Mesenchymal Stem Cells
title_full_unstemmed Decellularized Periosteum-Derived Hydrogels Promote the Proliferation, Migration and Osteogenic Differentiation of Human Umbilical Cord Mesenchymal Stem Cells
title_short Decellularized Periosteum-Derived Hydrogels Promote the Proliferation, Migration and Osteogenic Differentiation of Human Umbilical Cord Mesenchymal Stem Cells
title_sort decellularized periosteum derived hydrogels promote the proliferation migration and osteogenic differentiation of human umbilical cord mesenchymal stem cells
topic periosteum
decellularized extracellular matrix-derived hydrogels
Matrigel
hUCMSCs
osteogenic differentiation
url https://www.mdpi.com/2310-2861/8/5/294
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