Mesenchymal stem cell-derived exosomes have altered microRNA profiles and induce osteogenic differentiation depending on the stage of differentiation
Human mesenchymal stem cell (hMSC)-derived exosomes have shown regenerative effects, but their role in osteogenesis and the underlying mechanism are yet to be determined. In this study, we examined the time-course secretion of exosomes by hMSCs during the entire process of osteogenic differentiation...
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| description | Human mesenchymal stem cell (hMSC)-derived exosomes have shown regenerative effects, but their role in osteogenesis and the underlying mechanism are yet to be determined. In this study, we examined the time-course secretion of exosomes by hMSCs during the entire process of osteogenic differentiation. Exosomes derived from hMSCs in various stages of osteogenic differentiation committed homotypic cells to differentiate towards osteogenic lineage, but only exosomes from late stages of osteogenic differentiation induced extracellular matrix mineralisation. Exosomes from expansion and early and late stages of osteogenic differentiation were internalised by a subpopulation of hMSCs. MicroRNA profiling revealed a set of differentially expressed exosomal microRNAs from the late stage of osteogenic differentiation, which were osteogenesis related. Target prediction demonstrated that these microRNAs enriched pathways involved in regulation of osteogenic differentiation and general mechanisms how exosomes exert their functions, such as "Wnt signalling pathway" and "endocytosis". Taken together, the results show that MSCs secrete exosomes with different biological properties depending on differentiation stage of their parent cells. The exosomal cargo transferred from MSCs in the late stage of differentiation induces osteogenic differentiation and mineralisation. Moreover, it is suggested that the regulatory effect on osteogenesis by exosomes is at least partly exerted by exosomal microRNA. |
| doi_str_mv | 10.1371/journal.pone.0193059 |
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In this study, we examined the time-course secretion of exosomes by hMSCs during the entire process of osteogenic differentiation. Exosomes derived from hMSCs in various stages of osteogenic differentiation committed homotypic cells to differentiate towards osteogenic lineage, but only exosomes from late stages of osteogenic differentiation induced extracellular matrix mineralisation. Exosomes from expansion and early and late stages of osteogenic differentiation were internalised by a subpopulation of hMSCs. MicroRNA profiling revealed a set of differentially expressed exosomal microRNAs from the late stage of osteogenic differentiation, which were osteogenesis related. Target prediction demonstrated that these microRNAs enriched pathways involved in regulation of osteogenic differentiation and general mechanisms how exosomes exert their functions, such as "Wnt signalling pathway" and "endocytosis". Taken together, the results show that MSCs secrete exosomes with different biological properties depending on differentiation stage of their parent cells. The exosomal cargo transferred from MSCs in the late stage of differentiation induces osteogenic differentiation and mineralisation. Moreover, it is suggested that the regulatory effect on osteogenesis by exosomes is at least partly exerted by exosomal microRNA.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0193059</identifier><identifier>PMID: 29447276</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>angiogenesis ; Biocompatibility ; Biological effects ; Biological properties ; Biology and Life Sciences ; Biomaterials Science ; Biomaterialvetenskap ; Biomedical materials ; Bone marrow ; Cell differentiation ; cells ; Differentiation ; Endocytosis ; Engineering and Technology ; Exosomes ; expression ; Extracellular matrix ; extracellular vesicles ; Fractures ; Gene expression ; Genetic aspects ; human bone-marrow ; mediated transfer ; Medicine and Health Sciences ; Mesenchyme ; MicroRNA ; MicroRNAs ; Mineralization ; mir-31 ; miRNA ; Nanoparticles ; neural cells ; Osteogenesis ; Osteoporosis ; Physiological aspects ; Physiology ; regeneration ; Ribonucleic acid ; RNA ; Secretion ; Signal transduction ; Signaling ; Skin & tissue grafts ; Stem cells ; stromal ; Tissue engineering ; Wnt protein</subject><ispartof>PloS one, 2018-02, Vol.13 (2), p.e0193059-e0193059</ispartof><rights>COPYRIGHT 2018 Public Library of Science</rights><rights>2018 Wang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2018 Wang et al 2018 Wang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c730t-be9acf670329ab22ffcc3d0f9ae52e93d0952563d57be4273121223cd682815a3</citedby><cites>FETCH-LOGICAL-c730t-be9acf670329ab22ffcc3d0f9ae52e93d0952563d57be4273121223cd682815a3</cites><orcidid>0000-0001-7808-4572</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5814093/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5814093/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29447276$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://gup.ub.gu.se/publication/265354$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Xiaoqin</creatorcontrib><creatorcontrib>Omar, Omar</creatorcontrib><creatorcontrib>Vazirisani, Forugh</creatorcontrib><creatorcontrib>Thomsen, Peter</creatorcontrib><creatorcontrib>Ekström, Karin</creatorcontrib><title>Mesenchymal stem cell-derived exosomes have altered microRNA profiles and induce osteogenic differentiation depending on the stage of differentiation</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Human mesenchymal stem cell (hMSC)-derived exosomes have shown regenerative effects, but their role in osteogenesis and the underlying mechanism are yet to be determined. In this study, we examined the time-course secretion of exosomes by hMSCs during the entire process of osteogenic differentiation. Exosomes derived from hMSCs in various stages of osteogenic differentiation committed homotypic cells to differentiate towards osteogenic lineage, but only exosomes from late stages of osteogenic differentiation induced extracellular matrix mineralisation. Exosomes from expansion and early and late stages of osteogenic differentiation were internalised by a subpopulation of hMSCs. MicroRNA profiling revealed a set of differentially expressed exosomal microRNAs from the late stage of osteogenic differentiation, which were osteogenesis related. Target prediction demonstrated that these microRNAs enriched pathways involved in regulation of osteogenic differentiation and general mechanisms how exosomes exert their functions, such as "Wnt signalling pathway" and "endocytosis". Taken together, the results show that MSCs secrete exosomes with different biological properties depending on differentiation stage of their parent cells. The exosomal cargo transferred from MSCs in the late stage of differentiation induces osteogenic differentiation and mineralisation. Moreover, it is suggested that the regulatory effect on osteogenesis by exosomes is at least partly exerted by exosomal microRNA.</description><subject>angiogenesis</subject><subject>Biocompatibility</subject><subject>Biological effects</subject><subject>Biological properties</subject><subject>Biology and Life Sciences</subject><subject>Biomaterials Science</subject><subject>Biomaterialvetenskap</subject><subject>Biomedical materials</subject><subject>Bone marrow</subject><subject>Cell differentiation</subject><subject>cells</subject><subject>Differentiation</subject><subject>Endocytosis</subject><subject>Engineering and Technology</subject><subject>Exosomes</subject><subject>expression</subject><subject>Extracellular matrix</subject><subject>extracellular vesicles</subject><subject>Fractures</subject><subject>Gene expression</subject><subject>Genetic aspects</subject><subject>human bone-marrow</subject><subject>mediated transfer</subject><subject>Medicine and Health Sciences</subject><subject>Mesenchyme</subject><subject>MicroRNA</subject><subject>MicroRNAs</subject><subject>Mineralization</subject><subject>mir-31</subject><subject>miRNA</subject><subject>Nanoparticles</subject><subject>neural cells</subject><subject>Osteogenesis</subject><subject>Osteoporosis</subject><subject>Physiological aspects</subject><subject>Physiology</subject><subject>regeneration</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Secretion</subject><subject>Signal transduction</subject><subject>Signaling</subject><subject>Skin & tissue grafts</subject><subject>Stem cells</subject><subject>stromal</subject><subject>Tissue engineering</subject><subject>Wnt 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stem cell-derived exosomes have altered microRNA profiles and induce osteogenic differentiation depending on the stage of differentiation</title><author>Wang, Xiaoqin ; Omar, Omar ; Vazirisani, Forugh ; Thomsen, Peter ; Ekström, Karin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c730t-be9acf670329ab22ffcc3d0f9ae52e93d0952563d57be4273121223cd682815a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>angiogenesis</topic><topic>Biocompatibility</topic><topic>Biological effects</topic><topic>Biological properties</topic><topic>Biology and Life Sciences</topic><topic>Biomaterials Science</topic><topic>Biomaterialvetenskap</topic><topic>Biomedical materials</topic><topic>Bone marrow</topic><topic>Cell differentiation</topic><topic>cells</topic><topic>Differentiation</topic><topic>Endocytosis</topic><topic>Engineering and 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Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Xiaoqin</au><au>Omar, Omar</au><au>Vazirisani, Forugh</au><au>Thomsen, Peter</au><au>Ekström, Karin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mesenchymal stem cell-derived exosomes have altered microRNA profiles and induce osteogenic differentiation depending on the stage of differentiation</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2018-02-15</date><risdate>2018</risdate><volume>13</volume><issue>2</issue><spage>e0193059</spage><epage>e0193059</epage><pages>e0193059-e0193059</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Human mesenchymal stem cell (hMSC)-derived exosomes have shown regenerative effects, but their role in osteogenesis and the underlying mechanism are yet to be determined. In this study, we examined the time-course secretion of exosomes by hMSCs during the entire process of osteogenic differentiation. Exosomes derived from hMSCs in various stages of osteogenic differentiation committed homotypic cells to differentiate towards osteogenic lineage, but only exosomes from late stages of osteogenic differentiation induced extracellular matrix mineralisation. Exosomes from expansion and early and late stages of osteogenic differentiation were internalised by a subpopulation of hMSCs. MicroRNA profiling revealed a set of differentially expressed exosomal microRNAs from the late stage of osteogenic differentiation, which were osteogenesis related. Target prediction demonstrated that these microRNAs enriched pathways involved in regulation of osteogenic differentiation and general mechanisms how exosomes exert their functions, such as "Wnt signalling pathway" and "endocytosis". Taken together, the results show that MSCs secrete exosomes with different biological properties depending on differentiation stage of their parent cells. The exosomal cargo transferred from MSCs in the late stage of differentiation induces osteogenic differentiation and mineralisation. Moreover, it is suggested that the regulatory effect on osteogenesis by exosomes is at least partly exerted by exosomal microRNA.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>29447276</pmid><doi>10.1371/journal.pone.0193059</doi><tpages>e0193059</tpages><orcidid>https://orcid.org/0000-0001-7808-4572</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Public Library of Science (PLoS) Journals Open Access; Free E-Journal (出版社公開部分のみ）; DOAJ Directory of Open Access Journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | angiogenesis Biocompatibility Biological effects Biological properties Biology and Life Sciences Biomaterials Science Biomaterialvetenskap Biomedical materials Bone marrow Cell differentiation cells Differentiation Endocytosis Engineering and Technology Exosomes expression Extracellular matrix extracellular vesicles Fractures Gene expression Genetic aspects human bone-marrow mediated transfer Medicine and Health Sciences Mesenchyme MicroRNA MicroRNAs Mineralization mir-31 miRNA Nanoparticles neural cells Osteogenesis Osteoporosis Physiological aspects Physiology regeneration Ribonucleic acid RNA Secretion Signal transduction Signaling Skin & tissue grafts Stem cells stromal Tissue engineering Wnt protein |
| title | Mesenchymal stem cell-derived exosomes have altered microRNA profiles and induce osteogenic differentiation depending on the stage of differentiation |
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