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      Effects of mesenchymal stem cells from human induced pluripotent stem cells on differentiation, maturation, and function of dendritic cells

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          Abstract

          Background

          Mesenchymal stem cells (MSCs) have potent immunomodulatory effects on multiple immune cells and have great potential in treating immune disorders. Induced pluripotent stem cells (iPSCs) serve as an unlimited and noninvasive source of MSCs, and iPSC-MSCs have been reported to have more advantages and exhibit immunomodulation on T lymphocytes and natural killer cells. However, the effects of iPSC-MSCs on dendritic cells (DCs) are unclear. The aim of this study is to investigate the effects of iPSC-MSCs on the differentiation, maturation, and function of DCs.

          Methods

          Human monocyte-derived DCs were induced and cultured in the presence or absence of iPSC-MSCs. Flow cytometry was used to analyze the phenotype and functions of DCs, and enzyme-linked immunosorbent assay (ELISA) was used to study cytokine production.

          Results

          In this study, we successfully induced MSCs from different clones of human iPSCs. iPSC-MSCs exhibited a higher proliferation rate with less cell senescence than BM-MSCs. iPSC-MSCs inhibited the differentiation of human monocyte-derived DCs by both producing interleukin (IL)-10 and direct cell contact. Furthermore, iPSC-MSCs did not affect immature DCs to become mature DCs, but modulated their functional properties by increasing their phagocytic ability and inhibiting their ability to stimulate proliferation of lymphocytes. More importantly, iPSC-MSCs induced the generation of IL-10-producing regulatory DCs in the process of maturation, which was mostly mediated by a cell-cell contact mechanism.

          Conclusions

          Our results indicate an important role for iPSC-MSCs in the modulation of DC differentiation and function, supporting the clinical application of iPSC-MSCs in DC-mediated immune diseases.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13287-017-0499-0) contains supplementary material, which is available to authorized users.

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          Most cited references23

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          Generation of functional human pancreatic β cells in vitro.

          Felicia W Pagliuca, Jeffrey Millman, Mads Gürtler … (2014)
          The generation of insulin-producing pancreatic β cells from stem cells in vitro would provide an unprecedented cell source for drug discovery and cell transplantation therapy in diabetes. However, insulin-producing cells previously generated from human pluripotent stem cells (hPSC) lack many functional characteristics of bona fide β cells. Here, we report a scalable differentiation protocol that can generate hundreds of millions of glucose-responsive β cells from hPSC in vitro. These stem-cell-derived β cells (SC-β) express markers found in mature β cells, flux Ca(2+) in response to glucose, package insulin into secretory granules, and secrete quantities of insulin comparable to adult β cells in response to multiple sequential glucose challenges in vitro. Furthermore, these cells secrete human insulin into the serum of mice shortly after transplantation in a glucose-regulated manner, and transplantation of these cells ameliorates hyperglycemia in diabetic mice. Copyright © 2014 Elsevier Inc. All rights reserved.
          Article 0 comments Cited 716 times – based on 0 reviews     Review now
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            Mesenchymal stem cells in the Wharton's jelly of the human umbilical cord.

            Hwai-Shi Wang, Shih-Chieh Hung, Shu-Tine Peng … (2004)
            The Wharton's jelly of the umbilical cord contains mucoid connective tissue and fibroblast-like cells. Using flow cytometric analysis, we found that mesenchymal cells isolated from the umbilical cord express matrix receptors (CD44, CD105) and integrin markers (CD29, CD51) but not hematopoietic lineage markers (CD34, CD45). Interestingly, these cells also express significant amounts of mesenchymal stem cell markers (SH2, SH3). We therefore investigated the potential of these cells to differentiate into cardiomyocytes by treating them with 5-azacytidine or by culturing them in cardiomyocyte-conditioned medium and found that both sets of conditions resulted in the expression of cardiomyocyte markers, namely N-cadherin and cardiac troponin I. We also showed that these cells have multilineage potential and that, under suitable culture conditions, are able to differentiate into cells of the adipogenic and osteogenic lineages. These findings may have a significant impact on studies of early human cardiac differentiation, functional genomics, pharmacological testing, cell therapy, and tissue engineering by helping to eliminate worrying ethical and technical issues.
            Article 0 comments Cited 356 times – based on 0 reviews     Review now
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              Human bone marrow derived mesenchymal stem cells do not undergo transformation after long-term in vitro culture and do not exhibit telomere maintenance mechanisms.

              Maria Bernardo, Nadia Zaffaroni, Francesca Novara … (2007)
              Significant improvement in the understanding of mesenchymal stem cell (MSC) biology has opened the way to their clinical use. However, concerns regarding the possibility that MSCs undergo malignant transformation have been raised. We investigated the susceptibility to transformation of human bone marrow (BM)-derived MSCs at different in vitro culture time points. MSCs were isolated from BM of 10 healthy donors and propagated in vitro until reaching either senescence or passage (P) 25. MSCs in the senescence phase were closely monitored for 8 to 12 weeks before interrupting the cultures. The genetic characterization of MSCs was investigated through array-comparative genomic hybridization (array-CGH), conventional karyotyping, and subtelomeric fluorescent in situ hybridization analysis both before and after prolonged culture. MSCs were tested for the expression of telomerase activity, human telomerase reverse transcriptase (hTERT) transcripts, and alternative lengthening of telomere (ALT) mechanism at different passages. A huge variability in terms of proliferative capacity and MSCs life span was noted between donors. In eight of 10 donors, MSCs displayed a progressive decrease in proliferative capacity until reaching senescence. In the remaining two MSC samples, the cultures were interrupted at P25 to pursue data analysis. Array-CGH and cytogenetic analyses showed that MSCs expanded in vitro did not show chromosomal abnormalities. Telomerase activity and hTERT transcripts were not expressed in any of the examined cultures and telomeres shortened during the culture period. ALT was not evidenced in the MSCs tested. BM-derived MSCs can be safely expanded in vitro and are not susceptible to malignant transformation, thus rendering these cells suitable for cell therapy approaches.
              Article 0 comments Cited 169 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Wen-Xiang Gao: sungao8829@126.com
                Yue-Qi Sun: aqi1733@163.com
                Jianbo Shi: tsjbent@163.com
                Cheng-Lin Li: allylin521@163.com
                Shu-Bin Fang: smufang@163.com
                Dan Wang: drwangdan@qq.com
                Xue-Quan Deng: docdxq@163.com
                Weiping Wen: wenwp@mail.sysu.edu.cn
                Qing-Ling Fu: 86-20-87333733 , fuqingl@mail.sysu.edu.cn
                Journal
                Journal ID (nlm-ta): Stem Cell Res Ther
                Journal ID (iso-abbrev): Stem Cell Res Ther
                Title: Stem Cell Research & Therapy
                Publisher: BioMed Central (London )
                ISSN (Electronic): 1757-6512
                Publication date (Electronic): 2 March 2017
                Publication date PMC-release: 2 March 2017
                Publication date Collection: 2017
                Volume: 8
                Electronic Location Identifier: 48
                Affiliations
                [1 ]ISNI 0000 0001 2360 039X, GRID grid.12981.33, , Otorhinolaryngology Hospital, The First Affiliated Hospital, Sun Yat-sen University, ; Guangzhou, Guangdong People’s Republic of China
                [2 ]GRID grid.412615.5, Centre for Stem Cell Clinical Research and Application, , The First Affiliated Hospital, Sun Yat-sen University, ; Guangzhou, Guangdong People’s Republic of China
                Article
                Publisher ID: 499
                DOI: 10.1186/s13287-017-0499-0
                PMC ID: 5333407
                PubMed ID: 28253916
                SO-VID: 14ea7d9b-665a-4b9e-abc3-d228587ad012
                Copyright © © The Author(s). 2017
                License:

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                Date received : 24 October 2016
                Date revision received : 11 January 2017
                Date accepted : 9 February 2017
                Funding
                Funded by: NSFC for Excellent Young Scholars
                Award ID: 81322012
                Award Recipient :
                Funded by: NSFC
                Award ID: 81470069
                Award ID: 81500768
                Award Recipient :
                Funded by: NSFC
                Award ID: 81273272
                Award Recipient :
                Funded by: grants from the Science and Technology Foundation of Guangdong Province
                Award ID: 2015B020225001
                Award Recipient :
                Funded by: National Science Foundation of Guangdong Province
                Award ID: 2014A030313051
                Award ID: 2014A030310392
                Award Recipient :
                Funded by: Fundamental Research Funds for the Central Universities
                Award ID: 15ykcj11c
                Award Recipient :
                Categories
                Subject: Research
                Custom metadata
                issue-copyright-statement © The Author(s) 2017

                ScienceOpen disciplines: Molecular medicine
                Keywords: mesenchymal stem cells,induced pluripotent cells,dendritic cells,immunomodulatory effect
                Data availability:
                ScienceOpen disciplines: Molecular medicine
                Keywords: mesenchymal stem cells, induced pluripotent cells, dendritic cells, immunomodulatory effect

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