Enhanced cardioprotection by human endometrium mesenchymal stem cells driven by exosomal MicroRNA-21

Stem Cells Translational Medicine

Volumn 6, Issue 1, 2017, Pages 209-222

  Wang, Kan ^a,b   Jiang, Zhi ^c   Webster, Keith A ^d   Chen, Jinghai ^b,e   Hu, Hengxun ^a,b   Zhou, Yu ^a,b   Zhao, Jing ^a,b   Wang, Lihan ^a,b   Wang, Yingchao ^a,b   Zhong, Zhiwei ^a,b   Ni, Cheng ^a,b   Li, Qingju ^a,b   Xiang, Charlie ^e   Zhang, Ling ^a,b   Wu, Rongrong ^a,b   Zhu, Wei ^a,b   Yu, Hong ^a,b   Hu, Xinyang ^a,b   Wang, Jian’An ^a,b  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b Provincial Key Laboratory of Cardiovascular Research of Zhejiang Province   (China)

^c GUIZHOU PROVINCIAL PEOPLE'S HOSPITAL   (China)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^e ZHEJIANG UNIVERSITY   (China)

Author keywords

Adipose; Bone marrow; Cell therapy; Endometrium; Mesenchymal stem cells; Myocardial infarction

Indexed keywords

DEUBIQUITINASE; FIBROBLAST GROWTH FACTOR 18; KRUPPEL LIKE FACTOR 6; MEMBRANE RECEPTOR; MICRORNA 21; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN BCL 2; PROTEIN KINASE YES; RIBOSOME PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN 2; SPROUTY PROTEIN; STAT3 PROTEIN; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR YAP1; TRANSIENT RECEPTOR POTENTIAL CHANNEL 2; CARDIOTONIC AGENT; MICRORNA; MIRN21 MICRORNA, HUMAN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAPILLARY DENSITY; CELL SURVIVAL; CELL THERAPY; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENDOMETRIUM CELL; EXOSOME; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; HEART INFARCTION; HEART PROTECTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MESENCHYMAL STEM CELL; MICROARRAY ANALYSIS; NONHUMAN; PARACRINE SIGNALING; PHASE CONTRAST MICROSCOPY; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; TUNEL ASSAY; VIRUS INFECTION; WESTERN BLOTTING; ADIPOSE TISSUE; ANIMAL; BIOLOGICAL MODEL; BONE MARROW CELL; CARDIAC MUSCLE CELL; CYTOLOGY; ENDOCYTOSIS; ENDOMETRIUM; FEMALE; GENETICS; METABOLISM; PATHOLOGY; REPRODUCIBILITY; SPRAGUE DAWLEY RAT; UMBILICAL VEIN ENDOTHELIAL CELL;

ADIPOSE TISSUE; ANIMALS; BONE MARROW CELLS; CARDIOTONIC AGENTS; ENDOCYTOSIS; ENDOMETRIUM; EXOSOMES; FEMALE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MESENCHYMAL STEM CELLS; MICRORNAS; MODELS, BIOLOGICAL; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; PARACRINE COMMUNICATION; RATS, SPRAGUE-DAWLEY; REPRODUCIBILITY OF RESULTS;

EID: 85017391075     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2015-0386     Document Type: Article

References (43)

1. Dauwe DF, Janssens SP. Stem cell therapy for the treatment of myocardial infarction. Curr Pharm Des 2011;17:3328-3340
2. MacDonald DJ, Luo J, Saito T et al. Persistence of marrow stromal cells implanted into acutely infarcted myocardium: Observations in a xenotransplant model. J Thorac Cardiovasc Surg 2005;130:1114-1121
3. Atoui R, Shum-Tim D, Chiu RC. Myocardial regenerative therapy: Immunologic basis for the potential “universal donor cells. Ann Thorac Surg 2008;86:327-334
4. Atoui R, Asenjo JF, Duong M et al. Marrow stromal cells as universal donor cells for myocardial regenerative therapy: Their unique immune tolerance. Ann Thorac Surg 2008;85: 571-579
5. Rasmussen JG, Frøbert O, Holst-Hansen C et al. Comparison of human adipose-derived stem cells and bone marrow-derived stem cells in amyocardial infarctionmodel. Cell Transplant 2014;23:195-206
6. Meng X, Ichim TE, Zhong J et al. Endometrial regenerative cells:Anovel stemcell population. J Transl Med 2007;5:57
7. Jiang Z, Hu X, Yu H et al. Human endometrial stem cells confer enhanced myocardial salvage and regeneration by paracrine mechanisms. J Cell Mol Med 2013;17:1247-1260
8. Zhang Z, Wang JA, Xu Y et al. Menstrual blood derived mesenchymal cells ameliorate cardiac fibrosis via inhibition of endothelial to mesenchymal transition in myocardial infarction. Int J Cardiol 2013;168:1711-1714
9. Stoorvogel W, Kleijmeer MJ, Geuze HJ et al. The biogenesis and functions of exosomes. Traffic 2002;3:321-330
10. Ge R, Tan E, Sharghi-Namini S et al. Exosomes in cancermicroenvironment and beyond: Have we overlooked these extracellularmessengers? Cancer Microenviron 2012;5:323-332
11. Valadi H, Ekström K, Bossios A et al. Exosome-mediated transfer ofmRNAs andmicro-RNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007;9:654-659
12. Arslan F, Lai RC, Smeets MB et al. Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Res (Amst) 2013;10:301-312
13. Simpson P, Savion S. Differentiation of rat myocytes in single cell cultures with and without proliferating nonmyocardial cells: Cross-striations, ultrastructure, and chronotropic response to isoproterenol. Circ Res 1982;50:101-116
14. Hu G, Yao H, Chaudhuri AD et al. Exosome-mediated shuttling of microRNA-29 regulates HIV Tat and morphine-mediated neuronal dysfunction. Cell Death Dis 2012;3:e381
15. Hu X, Yu SP, Fraser JL et al. Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J Thorac Cardiovasc Surg 2008;135:799-808
16. Gnecchi M, He H, Liang OD et al. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 2005;11:367-368
17. Kosaka N, Iguchi H, Yoshioka Y et al. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 2010; 285:17442-17452
18. Trajkovic K, Hsu C, Chiantia S et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008;319: 1244-1247
19. Corcoran C, Rani S, O’Brien K et al. Docetaxelresistance in prostate cancer: Evaluating associated phenotypic changes and potential for resistance transfer via exosomes. PLoS One 2012;7:e50999
20. Heeschen C, Lehmann R, Honold J et al. Profoundly reduced neovascularization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation 2004;109:1615-1622
21. Wang Y, Li C, Cheng K et al. Activation of liver X receptor improves viability of adipose-derived mesenchymal stem cells to attenuate myocardial ischemia injury through TLR4/NF-kB and Keap-1/Nrf-2 signaling pathways. Antioxid Redox Signal 2014;21:2543-2557
22. van der Bogt KE, Sheikh AY, Schrepfer S et al. Comparison of different adult stem cell types for treatment of myocardial ischemia. Circulation 2008;118(suppl):S121-S129
23. Hare JM, Traverse JH, Henry TD et al. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol 2009;54:2277-2286
24. Rodrigo SF, van Ramshorst J, Hoogslag GE et al. Intramyocardial injection of autologous bone marrow-derived ex vivo expanded mesenchymal stem cells in acute myocardial infarction patients is feasible and safe up to 5 years of follow-up. J Cardiovasc Transl Res 2013;6:816-825
25. Behfar A, Yamada S, Crespo-Diaz R et al. Guided cardiopoiesis enhances therapeutic benefit of bone marrow human mesenchymal stem cells in chronic myocardial infarction. J Am Coll Cardiol 2010;56:721-734
26. Camussi G, Deregibus MC, Bruno S et al. Exosome/microvesicle-mediated epigenetic reprogramming of cells. Am J Cancer Res 2011; 1:98-110
27. Xin H, Li Y, Liu Z et al. MiR-133b promotes neural plasticity and functional recovery after treatment of stroke with multipotent mesenchymal stromal cells in rats via transfer of exosome-enriched extracellular particles. STEM CELLS 2013;31:2737-2746
28. Roccaro AM, Sacco A, Maiso P et al. BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression. J Clin Invest 2013;123:1542-1555
29. Ono M, Kosaka N, Tominaga N et al. Exosomes from bone marrow mesenchymal stem cells contain a microRNA that promotes dormancy in metastatic breast cancer cells. Sci Signal 2014;7:ra63
30. Kang K, Ma R, Cai W et al. Exosomes secreted from CXCR4 overexpressing mesenchymal stem cells promote cardioprotection via Akt signaling pathway following myocardial infarction. Stem Cells Int 2015;2015: 659890
31. Dhanabal M, Wu F, Alvarez E et al. Recombinant semaphorin 6A-1 ectodomain inhibits in vivo growth factor and tumor cell lineinduced angiogenesis. Cancer Biol Ther 2005;4: 659-668
32. Impagnatiello MA, Weitzer S, Gannon G et al. Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells. J Cell Biol 2001;152:1087-1098
33. Wang Y, Zhang L, Li Y et al. Exosomes/ microvesicles frominduced pluripotent stem cells deliver cardioprotective miRNAs and prevent cardiomyocyte apoptosis in the ischemic myocardium. Int J Cardiol 2015;192:61-69
34. Xu Y, Luo F, Liu Y et al. Exosomal miR-21 derived from arsenite-transformed human bronchial epithelial cells promotes cell proliferation associated with arsenite carcinogenesis. Arch Toxicol 2015;89:1071-1082
35. Liu Y, Nie H, Zhang K et al. A feedback regulatory loop between HIF-1a and miR-21 in response to hypoxia in cardiomyocytes. FEBS Lett 2014;588:3137-3146
36. Liu LZ, Li C, Chen Q et al. MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1a expression. PLoS One 2011;6: e19139
37. Meng F, Henson R, Wehbe-Janek H et al. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 2007;133: 647-658
38. Roy S, Khanna S, Hussain SR et al. Micro-RNA expression in response to murine myocardial infarction: MiR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovasc Res 2009;82:21-29
39. Karantalis V, Hare JM. Use of mesenchymal stem cells for therapy of cardiac disease. Circ Res 2015;116:1413-1430
40. Makkar RR, Smith RR, Cheng K et al. Intracoronarycardiosphere-derivedcells forheartregeneration after myocardial infarction (CADUCEUS): A prospective, randomised phase 1 trial. Lancet 2012;379:895-904
41. Mathiasen AB, Qayyum AA, Jørgensen E et al. Bone marrow-derived mesenchymal stromal cell treatment in patients with severe ischaemic heart failure: A randomized placebocontrolled trial (MSC-HF trial). Eur Heart J 2015; 36:1744-1753
42. Williams AR, Hare JM. Mesenchymal stem cells: Biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ Res 2011;109: 923-940
43. Hu X, Wu R, Jiang Z et al. Leptin signaling is required for augmented therapeutic properties of mesenchymal stem cells conferred by hypoxia preconditioning. STEM CELLS 2014;32: 2702-2713