Stem Cell Extracellular Matrix-Modified Decellularized Tendon Slices Facilitate the Migration of Bone Marrow Mesenchymal Stem Cells

Yao, Xuan; Ning, Liang-Ju; He, Shu-Kun; Cui, Jing; Hu, Ruo-Nan; Zhang, Yi; Zhang, Yanjing; Luo, Jingcong; Ding, Wei; Qin, Tingwu

doi:10.1021/acsbiomaterials.9b00064

Cited by 16 publications

(15 citation statements)

References 54 publications

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“…11,12,53 Our previous study also demonstrated that TDSCs could secrete chemokines similar to BMSCs, including SDF-1 and monocyte chemotactic protein 1, and decellularized tendon slices coated with TDSC-derived ECM notably improved BMSC migration compared with decellularized tendon slices. 66 In our study, the results of immunofluorescence staining showed that the hDCB-ECM group could recruit more endogenous stromal cells than the other 3 groups. However, there was no difference in stromal cell recruitment between the hDCB group and the DCB group.…”

Section: Discussionsupporting

confidence: 47%

“…In general, our results and previous studies demonstrated that SDF-1 from ECM could recruit endogenous stromal cells, and biglycan from ECM could further induce multidirectional differentiation of recruited stromal cells to promote healing of the tendon-bone interface. 66,68 Although the hDCB group had more new formation of bone and fibrocartilage than the DCB group, there was no significant difference in the results of micro-CT and biomechanical testing between the 2 groups. However, hDCB-ECM significantly improved the ultimate tensile stress and Young modulus of the tendon-bone interface compared with DCB.…”

Section: Discussionmentioning

confidence: 87%

“…57 Our previous studies also showed that TDSCs cultured on decellularized tendon slices could secrete stromal cell-derived factor 1 (SDF-1) and monocyte chemotactic protein 1, which promoted stem cell recruitment. 66 However, whether the scaffold coated with TDSC-derived ECM can repair tendon-bone interface lacks investigation. From this perspective, we used the bioactive TDSC-derived ECM to modify the DCB part (DCB-ECM) of hDCB, which could improve the effect of scaffolds.…”

mentioning

confidence: 99%

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Hierarchically Demineralized Cortical Bone Combined With Stem Cell–Derived Extracellular Matrix for Regeneration of the Tendon-Bone Interface

Ning

Yao

et al. 2021

Am J Sports Med

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Background: Poor healing of the tendon-bone interface after rotator cuff repair is one of the main causes of surgical failure. Previous studies demonstrated that demineralized cortical bone (DCB) could improve healing of the enthesis. Purpose: To evaluate the outcomes of hierarchically demineralized cortical bone (hDCB) coated with stem cell–derived extracellular matrix (hDCB-ECM) in the repair of the rotator cuff in a rabbit model. Study Design: Controlled laboratory study. Methods: Tendon-derived stem cells (TDSCs) were isolated, cultured, and identified. Then, hDCB was prepared by the graded demineralization procedure. Finally, hDCB-ECM was fabricated via 2-week cell culture and decellularization, and the morphologic features and biochemical compositions of the hDCB-ECM were evaluated. A total of 24 rabbits (48 samples) were randomly divided into 4 groups: control, DCB, hDCB, and hDCB-ECM. All rabbits underwent bilateral detachment of the infraspinatus tendon, and the tendon-bone interface was repaired with or without scaffolds. After surgery, 8 rabbits were assessed by immunofluorescence staining at 2 weeks, and the others were assessed by micro–computed tomography (CT) examination, immunohistochemical staining, histological staining, and biomechanical testing at 12 weeks. Results: TDSCs were identified to have universal stem cell characteristics including cell markers, clonogenicity, and multilineage differentiation. The hDCB-ECM contained 3 components (bone, partial DCB, and DCB coated with ECM) with a gradient of calcium and phosphorus elements, and the ECM had stromal cell-derived factor 1, biglycan, and fibromodulin. Macroscopic observations demonstrated the absence of infection and rupture around the enthesis. The results of immunofluorescence staining showed that hDCB-ECM promoted stromal cell recruitment. Results of micro-CT analysis, immunohistochemical staining, and histological staining showed that hDCB-ECM enhanced bone and fibrocartilage formation at the tendon-bone interface. Biomechanical analysis showed that the hDCB-ECM group had higher ultimate tensile stress and Young modulus than the DCB group. Conclusion: The administration of hDCB-ECM promoted healing of the tendon-bone interface. Clinical Relevance: hDCB-ECM could provide useful information for the design of scaffolds to repair the tendon-bone interface, and further studies are needed to determine its effectiveness.

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Section: Discussionsupporting

confidence: 47%

Section: Discussionmentioning

confidence: 87%

mentioning

confidence: 99%

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Hierarchically Demineralized Cortical Bone Combined With Stem Cell–Derived Extracellular Matrix for Regeneration of the Tendon-Bone Interface

Ning

Yao

et al. 2021

Am J Sports Med

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“…The short stimulation time in cell proliferation may be due to the explosive release of biochemical factors from cell-derived ECM (Katagiri et al, 1990;Fujii et al, 2010). Our recent study also demonstrated that the chemokines (SDF-1) in ECM-modified tendon slices showed an initial burst release within 12 h (Yao et al, 2019). A previous study showed that BMSCs seeded on the demineralized region deposited thicker and more aligned collagen than those on the mineralized region (Zhou et al, 2020).…”

Section: Discussionmentioning

confidence: 74%

Segmentally Demineralized Cortical Bone With Stem Cell-Derived Matrix Promotes Proliferation, Migration and Differentiation of Stem Cells in vitro

Ning

et al. 2022

Front. Cell Dev. Biol.

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A recent study has shown that demineralized cortical bone (DCB) did not improve the healing of tendon-bone interface. Considering that there is a gradient of mineral content in the tendon-bone interface, we designed a segmentally demineralized cortical bone (sDCB) scaffold with two different regions: undemineralized cortical bone section within the scaffold (sDCB-B) and complete demineralized cortical bone section within the scaffold (sDCB-D), to mimic the natural structure of the tendon-bone interface. Furthermore, the extracellular matrix (ECM) from tendon-derived stem cells (TDSCs) was used to modify the sDCB-D region of sDCB to construct a novel scaffold (sDCB-ECM) for enhancing the bioactivity of the sDCB-D. The surface topography, elemental distribution, histological structure, and surface elastic modulus of the scaffold were observed using scanning electron microscopy, energy-dispersive X-ray spectroscopy, Fourier transform infrared spectroscopy, histological staining and atomic force microscopy. Cell proliferation of bone marrow mesenchymal stem cells (BMSCs) and TDSCs cultured on scaffolds was evaluated using the Cell Counting kit-8, and cell viability was assessed by Live/Dead cell staining. Cell morphology was detected by fluorescent staining. The ability of the scaffolds to recruit stem cells was tested using transwell migration assay. The expression levels of bone-, cartilage- and tendon-related genes and proteins in stem cells were assessed by the polymerase chain reaction and western blotting. Our results demonstrated that there was a gradient of Ca and P elements in sDCB, and TDSC-derived ECM existed on the surface of the sDCB-D region of sDCB. The sDCB-ECM could promote stem cell proliferation and migration. Moreover, the sDCB-B region of sDCB-ECM could stimulate osteogenic and chondrogenic differentiation of BMSCs, and the sDCB-D-ECM region of sDCB-ECM could stimulate chondrogenic and tenogenic differentiation of TDSCs when compared to DCB. Our study indicated that sDCB-ECM might be a potential bioscaffold to enhance the tendon-bone interface regeneration.

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“…The mixed hydrogel with 75% cECM promoted the cardiac differentiation of human embryonic stem cells with increased expression of troponin T and Cx43, improved striation patterns of cardiac troponin I, and promoted contractile function of cardiac cells. It should be mentioned that most in vitro stem cell and CM studies involved cECM hydrogels were performed by seeding cells on the hydrogel surface 40‐43 . There may exist significant differences of topography and ECM component presentation between surface and inside of hydrogel.…”

Section: Discussionmentioning

confidence: 99%

In vitro comparison of harvesting site effects on cardiac extracellular matrix hydrogels

Mulvany

McMahan

et al. 2021

J Biomedical Materials Res

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Cardiac extracellular matrix (cECM) derived hydrogel has been investigated to treat myocardial infarction through animal studies and clinical trials. The tissue harvesting site commonly selects porcine left ventricle (LV) because heart attack majorly takes place in LV. However, little is known about whether the region of cardiac tissue harvesting is critical for downstream applications. In this work, in vitro studies to compare cECM hydrogels derived from adult porcine whole heart (WH), LV, and right ventricle (RV) were performed. The cECM from WH has similar chemical composition compared with cECM from LV and RV. All three types of cECM hydrogels share many similarities in terms of their microstructure, gelation time, and mechanical properties. WH‐derived cECM hydrogels have larger variations in storage modulus (G′) and complex modulus (G*) compared with the other two types of cECM hydrogels. Both human cardiomyocytes and mesenchymal stem cells could maintain high cell viability on all hydrogels without significant difference. In terms of above results, the cECM hydrogels from WH, LV and RV exhibited similarity in material properties and cell response in vitro. Thus, future fabrication of cECM hydrogels from WH would increase the yield, which would decrease processing time and production cost.

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Stem Cell Extracellular Matrix-Modified Decellularized Tendon Slices Facilitate the Migration of Bone Marrow Mesenchymal Stem Cells

Cited by 16 publications

References 54 publications

Hierarchically Demineralized Cortical Bone Combined With Stem Cell–Derived Extracellular Matrix for Regeneration of the Tendon-Bone Interface

Hierarchically Demineralized Cortical Bone Combined With Stem Cell–Derived Extracellular Matrix for Regeneration of the Tendon-Bone Interface

Segmentally Demineralized Cortical Bone With Stem Cell-Derived Matrix Promotes Proliferation, Migration and Differentiation of Stem Cells in vitro

In vitro comparison of harvesting site effects on cardiac extracellular matrix hydrogels

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