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Derived Mesenchymal Stem Cells (Mscs) Have a Superior Neuroprotective Capacity Over Fetal Mscs in the Hypoxic-Ischemic Mouse Brain a Maternal and Fetal a a a a KATE E

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Derived Mesenchymal Stem Cells (Mscs) Have a Superior Neuroprotective Capacity Over Fetal Mscs in the Hypoxic-Ischemic Mouse Brain a Maternal and Fetal a a a a KATE E TISSUE ENGINEERING AND REGENERATIVE MEDICINE Embryonic Stem Cell-Derived Mesenchymal Stem Cells (MSCs) Have a Superior Neuroprotective Capacity Over Fetal MSCs in the Hypoxic-Ischemic Mouse Brain a Maternal and Fetal a a a a KATE E. HAWKINS, MICHELANGELO CORCELLI, KATE DOWDING, ANNA M. RANZONI, Medicine Department, a a,b a a c Institute for Women’s Health, FILIPA VLAHOVA, KWAN-LEONG HAU, AVINA HUNJAN, DONALD PEEBLES, PIERRE GRESSENS, c d a a University College London, HENRIK HAGBERG, PAOLO DE COPPI, MARIYA HRISTOVA, PASCALE V. GUILLOT London, United Kingdom; bFaculty of Medicine, Key Words. Pluripotent stem cells • Mesenchymal stem cells • Fetal stem cells • Cell transplantation • Embryonic stem cells • Induced pluripotent stem cells National Heart and Lung Institute, Imperial College London, London, United ABSTRACT Kingdom; cDepartment of Perinatal Imaging and Health, Human mesenchymal stem cells (MSCs) have huge potential for regenerative medicine. In particu- lar, the use of pluripotent stem cell-derived mesenchymal stem cells (PSC-MSCs) overcomes the St. Thomas’ Hospital, King’s hurdle of replicative senescence associated with the in vitro expansion of primary cells and has College London, London, d increased therapeutic benefits in comparison to the use of various adult sources of MSCs in a wide United Kingdom; Stem Cells range of animal disease models. On the other hand, fetal MSCs exhibit faster growth kinetics and and Regenerative Medicine possess longer telomeres and a wider differentiation potential than adult MSCs. Here, for the first Department, Great Ormond time, we compare the therapeutic potential of PSC-MSCs (ES-MSCs from embryonic stem cells) to Street Institute for Child fetal MSCs (AF-MSCs from the amniotic fluid), demonstrating that ES-MSCs have a superior neuro- Health, University College protective potential over AF-MSCs in the mouse brain following hypoxia-ischemia. Further, we London, London, United demonstrate that nuclear factor (NF)-jB-stimulated interleukin (IL)-13 production contributes to Kingdom an increased in vitro anti-inflammatory potential of ES-MSC-conditioned medium (CM) over AF- MSC-CM, thus suggesting a potential mechanism for this observation. Moreover, we show that Correspondence: Kate E. induced pluripotent stem cell-derived MSCs (iMSCs) exhibit many similarities to ES-MSCs, including Hawkins, Ph.D., Maternal and enhanced NF-jB signaling and IL-13 production in comparison to AF-MSCs. Future studies should Fetal Medicine Department, assess whether iMSCs also exhibit similar neuroprotective potential to ES-MSCs, thus presenting a Institute for Women’s Health, potential strategy to overcome the ethical issues associated with the use of embryonic stem cells University College London, 86-96 and providing a potential source of cells for autologous use against neonatal hypoxic-ischemic Chenies Mews, London WC1N encephalopathy in humans. STEM CELLS TRANSLATIONAL MEDICINE 2018;7:439–449 1EH, United Kingdom. Telephone: 44 (0)207 242 9789; e-mail: k. [email protected]; or Pascale V. Guillot, Ph.D., Maternal and Fetal SIGNIFICANCE STATEMENT Medicine Department, Institute Mesenchymal stem cells (MSCs) are currently under assessment in various clinical trials world- for Women’s Health, University wide. Their therapeutic potential is due largely to the factors they secrete. This study shows College London, 86-96 Chenies Mews, London WC1N 1EH, that embryonic stem cell-derived MSCs have increased in vitro anti-inflammatory potential in United Kingdom. Telephone: 44 comparison to amniotic fluid-derived MSCs and that this translates to an increased in vivo neu- (0)207 242; e-mail: p.guillot@ucl. roprotective capacity following hypoxic-ischemic injury of the mouse brain. These findings pro- ac.uk vide new insight into the molecular mechanisms underlying the therapeutic potential of MSCs. By illuminating these molecular mechanisms, this study may have implications for improving Received November 9, 2017; the efficiency of MSC therapies. accepted for publication January 16, 2018; first published February 28, 2018. amniotic fluid [4, 5]. Due to their more primitive http://dx.doi.org/ INTRODUCTION 10.1002/sctm.17-0260 phenotype, fetal MSCs present various advan- Mesenchymal stromal/stem cells (MSCs) are mul- tages over their adult counterparts such as longer This is an open access article under the terms of the Creative tipotent cells found in various tissues throughout telomeres, active telomerase and a greater expan- Commons Attribution-NonCom- development, where they contribute to the repair sion capacity [6]. MSCs, as defined by their plastic mercial-NoDerivs License, which and regeneration of these tissues. Human fetal adherence, tri-lineage differentiation potential, permits use and distribution in MSCs have been isolated from various fetal tis- co-expression of the cell surface markers CD105, any medium, provided the origi- nal work is properly cited, the use sues including first trimester blood, liver, or CD90, and CD73 and absence of expression of is non-commercial and no modifi- bone marrow (BM) [1–3], or from extraembryonic CD34 and CD45 [7], are currently under assess- cations or adaptations are made. tissues such as the placenta, umbilical cord or ment in numerous clinical trials worldwide STEM CELLS TRANSLATIONAL MEDICINE 2018;7:439–449 www.StemCellsTM.com Oc 2018 The Authors STEM CELLS TRANSLATIONAL MEDICINE published by Wiley Periodicals, Inc. on behalf of AlphaMed Press 440 ES-MSCs Are More Neuroprotective than Fetal MSCs targeting a range of disorders from myocardial infarction to stroke (AF)-MSCs. We show that ES-MSCs have an increased neuropro- [8]. However, the specific mechanisms by which they mediate tective capacity compared with AF-MSCs in a perinatal mouse tissue regeneration in a range of disease contexts remain largely hypoxia-ischemia model. Further, we demonstrate in vitro that elusive. increased NF-jB activation in ES-MSCs leads to elevated Increasing evidence suggests that the therapeutic potential of interleukin (IL)-13 production, thus providing a potential mecha- MSCs should not be attributed only to their engraftment and dif- nism for the enhanced neuroprotective capacity of ES-MSCs over ferentiation but also to the release of regenerative paracrine/ AF-MSCs. Finally, we compare these two MSC lines to iMSCs, endocrine factors. These effects of MSCs were first suggested showing that iMSCs also exhibit increased NF-jB activation, con- when, after injection, BM-MSCs exerted therapeutic effects on comitant with elevated IL-13 production and increased anti- the infarcted heart despite being detected largely in the lungs and inflammatory potential in comparison to AF-MSCs. Together, these liver in various murine heart disease models [9, 10]. Furthermore, findings suggest that PSC-MSCs are a promising cell source for use MSC-conditioned medium (CM) has been shown to exert a thera- in therapeutic strategies targeting neonatal hypoxic-ischemic peutic effect in animal models of cardiomyopathy [11] and MSC- encephalopathy (HIE) in humans. derived exosomes have been shown to ameliorate disorders of the brain, kidney, and joints [12–15]. These studies are paving the way for off-the-shelf cell-free therapies, which would have the MATERIALS AND METHODS benefits of being more well defined and standardized than stem Ethics Statements cell treatments. Standardization of cell-free therapies will require a thorough The healthy donors who provided the amniotic fluid in this study understanding of the therapeutic factors that MSCs secrete. One provided written informed consent in accordance with the Decla- key class of molecules released by MSCs are anti-inflammatory ration of Helsinki. The ethical approval given by the Research factors. These include interleukin 1 receptor agonist (IL-1ra) [16], Ethics Committees of Hammersmith & Queen Charlotte Hospitals tumornecrosisfactor(TNF)a-stimulated gene (TSG)6 [8, 17, 18], (2001/6234) was in compliance with U.K. national guidelines prostaglandin (PG)E2 [16–19], indoleamine 2,3-dioxygenase (IDO) (Review of the Guidance on the Research Use of Fetuses and Fetal [20–24], and IL-10 [19]. When in an inflammatory environment, Material [1989], also known as the Polkinghome Guidelines Lon- MSCs produce higher levels of these anti-inflammatory factors, a don: Her Majesty’s Stationary Office, 1989: Cm762) for the collec- phenomenon known as “licensing” [25–27]. Mechanistically, this tion of fetal tissue for research. is likely due to activation of nuclear factor (NF)-jB signaling in All animals were handled in strict accordance with good ani- MSCs leading to transcription of downstream targets which mal practice as defined by the U.K. Home Office Animal Welfare include anti-inflammatory cytokines. To support this idea, Dorron- Legislation (PPL 70/8784), The Institutional Licensing Committee soro et al. [28] have shown that inhibition of NF-jB through of Imperial College London and University College London (UCL) silencing of IjBkinaseortheTNFa receptor TNFR1 abolishes the and the Institutional Research Ethics Committee (Institute of Child capacity of MSCs to regulate T cell proliferation and various groups Health, UCL, London). have shown that Toll-like receptor (TLR) engagement leads to enhanced immunosuppressive properties in human BM-MSCs [18, Cell Culture 29, 30]. Moreover, Tomchuck et al. [31] have demonstrated that Human AF-MSCs were isolated as previously described [4]. Unless NF-jB activation in MSCs leads to increased production of cyto- specified, cells were plated
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