Effects of Extracellular Vesicles from Osteogenic Differentiated Human BMSCs on Osteogenic and Adipogenic Differentiation Capacity of Naïve Human BMSCs

Osteoporosis, or steroid-induced osteonecrosis of the hip, is accompanied by increased bone marrow adipogenesis. Such a disorder of adipogenic/osteogenic differentiation, affecting bone-marrow-derived mesenchymal stem cells (BMSCs), contributes to bone loss during aging. Here, we investigated the ef...

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Main Authors: Chenglong Wang, Sabine Stöckl, Shushan Li, Marietta Herrmann, Christoph Lukas, Yvonne Reinders, Albert Sickmann, Susanne Grässel
Format: Article
Language:English
Published: MDPI AG 2022-08-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/11/16/2491
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author Chenglong Wang
Sabine Stöckl
Shushan Li
Marietta Herrmann
Christoph Lukas
Yvonne Reinders
Albert Sickmann
Susanne Grässel
author_facet Chenglong Wang
Sabine Stöckl
Shushan Li
Marietta Herrmann
Christoph Lukas
Yvonne Reinders
Albert Sickmann
Susanne Grässel
author_sort Chenglong Wang
collection DOAJ
description Osteoporosis, or steroid-induced osteonecrosis of the hip, is accompanied by increased bone marrow adipogenesis. Such a disorder of adipogenic/osteogenic differentiation, affecting bone-marrow-derived mesenchymal stem cells (BMSCs), contributes to bone loss during aging. Here, we investigated the effects of extracellular vesicles (EVs) isolated from human (h)BMSCs during different stages of osteogenic differentiation on the osteogenic and adipogenic differentiation capacity of naïve (undifferentiated) hBMSCs. We observed that all EV groups increased viability and proliferation capacity and suppressed the apoptosis of naïve hBMSCs. In particular, EVs derived from hBMSCs at late-stage osteogenic differentiation promoted the osteogenic potential of naïve hBMSCs more effectively than EVs derived from naïve hBMSCs (naïve EVs), as indicated by the increased gene expression of COL1A1 and OPN. In contrast, the adipogenic differentiation capacity of naïve hBMSCs was inhibited by treatment with EVs from osteogenic differentiated hBMSCs. Proteomic analysis revealed that osteogenic EVs and naïve EVs contained distinct protein profiles, with pro-osteogenic and anti-adipogenic proteins encapsulated in osteogenic EVs. We speculate that osteogenic EVs could serve as an intercellular communication system between bone- and bone-marrow adipose tissue, for transporting osteogenic factors and thus favoring pro-osteogenic processes. Our data may support the theory of an endocrine circuit with the skeleton functioning as a ductless gland.
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spelling doaj.art-2f3f6a50af514076968a12b7238597912023-11-30T21:06:24ZengMDPI AGCells2073-44092022-08-011116249110.3390/cells11162491Effects of Extracellular Vesicles from Osteogenic Differentiated Human BMSCs on Osteogenic and Adipogenic Differentiation Capacity of Naïve Human BMSCsChenglong Wang0Sabine Stöckl1Shushan Li2Marietta Herrmann3Christoph Lukas4Yvonne Reinders5Albert Sickmann6Susanne Grässel7Department of Orthopedic Surgery, Experimental Orthopedics, Centre for Medical Biotechnology (ZMB), University of Regensburg, 93053 Regensburg, GermanyDepartment of Orthopedic Surgery, Experimental Orthopedics, Centre for Medical Biotechnology (ZMB), University of Regensburg, 93053 Regensburg, GermanyDepartment of Orthopedic Surgery, Experimental Orthopedics, Centre for Medical Biotechnology (ZMB), University of Regensburg, 93053 Regensburg, GermanyIZKF Group Tissue Reg. in Musculoskeletal Dis., University Hospital & Bernhard-Heine-Centrum for Locomotion Res., University of Würzburg, 97070 Würzburg, GermanyDepartment of Orthopedic Surgery, Experimental Orthopedics, Centre for Medical Biotechnology (ZMB), University of Regensburg, 93053 Regensburg, GermanyLeibniz-Institut für Analytische Wissenschaften–ISAS–e.V., Bunsen-Kirchhoff-Straße 11, 44139 Dortmund, GermanyLeibniz-Institut für Analytische Wissenschaften–ISAS–e.V., Bunsen-Kirchhoff-Straße 11, 44139 Dortmund, GermanyDepartment of Orthopedic Surgery, Experimental Orthopedics, Centre for Medical Biotechnology (ZMB), University of Regensburg, 93053 Regensburg, GermanyOsteoporosis, or steroid-induced osteonecrosis of the hip, is accompanied by increased bone marrow adipogenesis. Such a disorder of adipogenic/osteogenic differentiation, affecting bone-marrow-derived mesenchymal stem cells (BMSCs), contributes to bone loss during aging. Here, we investigated the effects of extracellular vesicles (EVs) isolated from human (h)BMSCs during different stages of osteogenic differentiation on the osteogenic and adipogenic differentiation capacity of naïve (undifferentiated) hBMSCs. We observed that all EV groups increased viability and proliferation capacity and suppressed the apoptosis of naïve hBMSCs. In particular, EVs derived from hBMSCs at late-stage osteogenic differentiation promoted the osteogenic potential of naïve hBMSCs more effectively than EVs derived from naïve hBMSCs (naïve EVs), as indicated by the increased gene expression of COL1A1 and OPN. In contrast, the adipogenic differentiation capacity of naïve hBMSCs was inhibited by treatment with EVs from osteogenic differentiated hBMSCs. Proteomic analysis revealed that osteogenic EVs and naïve EVs contained distinct protein profiles, with pro-osteogenic and anti-adipogenic proteins encapsulated in osteogenic EVs. We speculate that osteogenic EVs could serve as an intercellular communication system between bone- and bone-marrow adipose tissue, for transporting osteogenic factors and thus favoring pro-osteogenic processes. Our data may support the theory of an endocrine circuit with the skeleton functioning as a ductless gland.https://www.mdpi.com/2073-4409/11/16/2491extracellular vesiclesmesenchymal stem cellsosteogenic potentialosteogenic differentiationadipogenic differentiationECM remodeling
spellingShingle Chenglong Wang
Sabine Stöckl
Shushan Li
Marietta Herrmann
Christoph Lukas
Yvonne Reinders
Albert Sickmann
Susanne Grässel
Effects of Extracellular Vesicles from Osteogenic Differentiated Human BMSCs on Osteogenic and Adipogenic Differentiation Capacity of Naïve Human BMSCs
Cells
extracellular vesicles
mesenchymal stem cells
osteogenic potential
osteogenic differentiation
adipogenic differentiation
ECM remodeling
title Effects of Extracellular Vesicles from Osteogenic Differentiated Human BMSCs on Osteogenic and Adipogenic Differentiation Capacity of Naïve Human BMSCs
title_full Effects of Extracellular Vesicles from Osteogenic Differentiated Human BMSCs on Osteogenic and Adipogenic Differentiation Capacity of Naïve Human BMSCs
title_fullStr Effects of Extracellular Vesicles from Osteogenic Differentiated Human BMSCs on Osteogenic and Adipogenic Differentiation Capacity of Naïve Human BMSCs
title_full_unstemmed Effects of Extracellular Vesicles from Osteogenic Differentiated Human BMSCs on Osteogenic and Adipogenic Differentiation Capacity of Naïve Human BMSCs
title_short Effects of Extracellular Vesicles from Osteogenic Differentiated Human BMSCs on Osteogenic and Adipogenic Differentiation Capacity of Naïve Human BMSCs
title_sort effects of extracellular vesicles from osteogenic differentiated human bmscs on osteogenic and adipogenic differentiation capacity of naive human bmscs
topic extracellular vesicles
mesenchymal stem cells
osteogenic potential
osteogenic differentiation
adipogenic differentiation
ECM remodeling
url https://www.mdpi.com/2073-4409/11/16/2491
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