Role of extracellular vesicles from adipose tissue‐ and bone marrow‐mesenchymal stromal cells in endothelial proliferation and chondrogenesis

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Abstract

The secretome of mesenchymal stromal cells (MSCs) derived from different tissue sources is considered an innovative therapeutic tool for regenerative medicine. Although adipose tissue‐and bone marrow‐derived MSCs (ADSCs and BMSCs, respectively) share many biological features, the different tissue origins can be mirrored by variations in their secretory profile, and in particular in the secreted extracellular vesicles (EVs). In this study, we carried out a detailed and comparative characterization of middle‐ and small‐sized EVs (mEVs and sEVs, respectively) released by either ADSCs or BMSCs. Their involvement in an endochondral ossification setting was investigated using ex vivo metatarsal culture models that allowed to explore both blood vessel sprouting and bone growth plate dynamics. Although EVs separated from both cell sources presented similar characteristics in terms of size, concentration, and marker expression, they exhibited different characteristics in terms of protein content and functional effects. ADSC‐EVs overexpressed pro‐angiogenic factors in comparison to the BMSC‐counterpart, and, consequently, they were able to induce a significant increase in endothelial cord outgrowth. On the other hand, BMSC‐EVs contained a higher amount of pro‐differentiation and chemotactic proteins, and they were able to prompt growth plate organization. The present study highlights the importance of selecting the appropriate cell source of EVs for targeted therapeutic applications.

Abstract

This study shows how the differences among bone marrow‐ and adipose tissue‐derived mesenchymal stromal cells (BMSCs and ADSCs, respectively) are mirrored in the corresponding extracellular vesicles (EVs). The role of ADSCs‐ and BMSCs‐derived EVs in an endochondral ossification setting was investigated using ex vivo metatarsal culture models that allowed to explore both blood vessel sprouting and bone growth plate dynamics.

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Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines

Clotilde Théry, Kenneth W Witwer, Elena Aikawa … (2019)

ABSTRACT The last decade has seen a sharp increase in the number of scientific publications describing physiological and pathological functions of extracellular vesicles (EVs), a collective term covering various subtypes of cell-released, membranous structures, called exosomes, microvesicles, microparticles, ectosomes, oncosomes, apoptotic bodies, and many other names. However, specific issues arise when working with these entities, whose size and amount often make them difficult to obtain as relatively pure preparations, and to characterize properly. The International Society for Extracellular Vesicles (ISEV) proposed Minimal Information for Studies of Extracellular Vesicles (“MISEV”) guidelines for the field in 2014. We now update these “MISEV2014” guidelines based on evolution of the collective knowledge in the last four years. An important point to consider is that ascribing a specific function to EVs in general, or to subtypes of EVs, requires reporting of specific information beyond mere description of function in a crude, potentially contaminated, and heterogeneous preparation. For example, claims that exosomes are endowed with exquisite and specific activities remain difficult to support experimentally, given our still limited knowledge of their specific molecular machineries of biogenesis and release, as compared with other biophysically similar EVs. The MISEV2018 guidelines include tables and outlines of suggested protocols and steps to follow to document specific EV-associated functional activities. Finally, a checklist is provided with summaries of key points.

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Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement.

M Dominici, K Le Blanc, I. Mueller … (2006)

The considerable therapeutic potential of human multipotent mesenchymal stromal cells (MSC) has generated markedly increasing interest in a wide variety of biomedical disciplines. However, investigators report studies of MSC using different methods of isolation and expansion, and different approaches to characterizing the cells. Thus it is increasingly difficult to compare and contrast study outcomes, which hinders progress in the field. To begin to address this issue, the Mesenchymal and Tissue Stem Cell Committee of the International Society for Cellular Therapy proposes minimal criteria to define human MSC. First, MSC must be plastic-adherent when maintained in standard culture conditions. Second, MSC must express CD105, CD73 and CD90, and lack expression of CD45, CD34, CD14 or CD11b, CD79alpha or CD19 and HLA-DR surface molecules. Third, MSC must differentiate to osteoblasts, adipocytes and chondroblasts in vitro. While these criteria will probably require modification as new knowledge unfolds, we believe this minimal set of standard criteria will foster a more uniform characterization of MSC and facilitate the exchange of data among investigators.

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Biological properties of extracellular vesicles and their physiological functions

María Yañez-Mó, Pia Siljander, Zoraida Andreu … (2015)

In the past decade, extracellular vesicles (EVs) have been recognized as potent vehicles of intercellular communication, both in prokaryotes and eukaryotes. This is due to their capacity to transfer proteins, lipids and nucleic acids, thereby influencing various physiological and pathological functions of both recipient and parent cells. While intensive investigation has targeted the role of EVs in different pathological processes, for example, in cancer and autoimmune diseases, the EV-mediated maintenance of homeostasis and the regulation of physiological functions have remained less explored. Here, we provide a comprehensive overview of the current understanding of the physiological roles of EVs, which has been written by crowd-sourcing, drawing on the unique EV expertise of academia-based scientists, clinicians and industry based in 27 European countries, the United States and Australia. This review is intended to be of relevance to both researchers already working on EV biology and to newcomers who will encounter this universal cell biological system. Therefore, here we address the molecular contents and functions of EVs in various tissues and body fluids from cell systems to organs. We also review the physiological mechanisms of EVs in bacteria, lower eukaryotes and plants to highlight the functional uniformity of this emerging communication system.

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Author and article information

Contributors

Roberta Tasso: roberta.tasso@unige.it

Chiara Gentili:

ORCID: https://orcid.org/0000-0001-6745-3782

chiara.gentili@unige.it

Journal

Journal ID (nlm-ta): Stem Cells Transl Med

Journal ID (iso-abbrev): Stem Cells Transl Med

Journal ID (doi): 10.1002/(ISSN)2157-6580

Journal ID (publisher-id): SCT3

Title: Stem Cells Translational Medicine

Publisher: John Wiley & Sons, Inc. (Hoboken, USA )

ISSN (Print): 2157-6564

ISSN (Electronic): 2157-6580

Publication date (Electronic): 04 September 2021

Publication date Collection: December 2021

Volume: 10

Issue: 12 ( doiID: 10.1002/sct3.v10.12 )

Pages: 1680-1695

Affiliations

[ ¹ ] Department of Experimental Medicine (DIMES) University of Genova Genoa Italy

[ ² ] U.O. Cellular Oncology IRCCS Ospedale Policlinico San Martino Genoa Italy

[ ³ ] U.O. Molecular Pathology IRCCS Ospedale Policlinico San Martino Genoa Italy

Author notes

[*] [* ] Correspondence

Roberta Tasso, PhD and Chiara Gentili, PhD, Department of Experimental Medicine, University of Genova, 16132, Genoa, Italy.

Email: roberta.tasso@ 123456unige.it (R.T.) and chiara.gentili@ 123456unige.it (C.G.)

Author information

Cansu Gorgun https://orcid.org/0000-0002-0460-2952

Maria Elisabetta Federica Palamà https://orcid.org/0000-0001-5585-137X

Chiara Gentili https://orcid.org/0000-0001-6745-3782

Article

Publisher ID: SCT312992

DOI: 10.1002/sctm.21-0107

PMC ID: 8641083

PubMed ID: 34480533

SO-VID: 212534dc-aee1-4389-9bb9-799aea5fb691

License:

This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

History

Date revision received : 15 June 2021

Date received : 19 March 2021

Date accepted : 06 July 2021

Page count

Figures: 8, Tables: 0, Pages: 16, Words: 9373

Funding

Funded by: Marie Sklodowska—Curie

Award ID: 721432 CarBon

Funded by: European Union's Horizon 2020

Award ID: 874671

Custom metadata

source-schema-version-number 2.0

cover-date December 2021

details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:6.0.9 mode:remove_FC converted:03.12.2021

Keywords: cartilage and bone development,ex vivo metatarsal culture model,extracellular vesicles,mesenchymal stromal cells,regenerative medicine

Data availability:

Keywords: cartilage and bone development, ex vivo metatarsal culture model, extracellular vesicles, mesenchymal stromal cells, regenerative medicine

Role of extracellular vesicles from adipose tissue‐ and bone marrow‐mesenchymal stromal cells in endothelial proliferation and chondrogenesis

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Bacterial extracellular vesicles

Most cited references 63

Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines

Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement.

Biological properties of extracellular vesicles and their physiological functions

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