MicroRNAs (miRs) are a class of small (~22 nucleotides), widely distributed, and highly conserved non-coding RNA molecules and play an important post-transcriptional regulatory role by targeting mRNA. Embryonic and induced pluripotent stem cells (ESCs and iPSC, respectively) hold great promise for vascular regenerative therapies. However, several limitations currently prohibit their therapeutic use. The importance of miRs in controlling the gene expression profile of a particular cell type is emerging and a multitude of miRs have been identified that play key roles in vascular development and regeneration. A combination of pluripotency transcription factors and different miRs not only enhances the pluripotency of stem cells but also has been reported to enhance their endothelial differentiation. This review will summarize the findings that focus different miR clusters in the induction, maintenance, and directed endothelial differentiation of ESCs and iPSCs.
KeywordsEPCsESCsiPSCmiRsVascular Regeneration
Mehta, D. and Malik, A.B. (2006) Signaling Mechanisms Regulating Endothelial Permeability. Physiological Reviews, 86, 279-367. http://dx.doi.org/10.1152/physrev.00012.2005
Gaengel, K., Genove, G., Armulik, A. and Betsholtz, C. (2009) Endothelial-Mural Cell Signaling in Vascular Development and Angiogenesis. Arteriosclerosis, Thrombosis, and Vascular Biology, 29, 630-638. http://dx.doi.org/10.1161/ATVBAHA.107.161521
Marcelo, K.L., Goldie, L.C. and Hirschi, K.K. (2013) Regulation of Endothelial Cell Differentiation and Specification. Circulation Research, 112, 1272-1287. http://dx.doi.org/10.1161/CIRCRESAHA.113.300506
Fish, J.E. and Wythe, J.D. (2015) The Molecular Regulation of Arteriovenous Specification and Maintenance. Developmental Dynamics, 244, 391-409. http://dx.doi.org/10.1002/dvdy.24252
Fadini, G.P., Losordo, D. and Dimmeler, S. (2012) Critical Reevaluation of Endothelial Progenitor Cell Phenotypes for Therapeutic and Diagnostic Use. Circulation Research, 110, 624-637. http://dx.doi.org/10.1161/CIRCRESAHA.111.243386
Zhou, Y., Yang, F., Yang, M., Xiao, Q. and Zhang, L. (2014) MicroRNAs in Endothelial Development and Differentiation. Stem Cell Research & Therapy, 4, 1000191.
Lewis, B.P., Burge, C.B. and Bartel, D.P. (2005) Conserved Seed Pairing, Often Flanked by Adenosines, Indicates That Thousands of Human Genes Are microRNA Targets. Cell, 120, 15-20. http://dx.doi.org/10.1016/j.cell.2004.12.035
He, L. and Hannon, G.J. (2004) MicroRNAs: Small RNAs with a Big Role in Gene Regulation. Nature Reviews Genetics, 5, 522-531. http://dx.doi.org/10.1038/nrg1379
Lee, Y., Jeon, K., Lee, J.T., Kim, S. and Kim, V.N. (2002) MicroRNA Maturation: Stepwise Processing and Subcellular Localization. EMBO Journal, 21, 4663-4670. http://dx.doi.org/10.1093/emboj/cdf476
Ha, M. and Kim, V.N. (2014) Regulation of microRNA Biogenesis. Nature Reviews Molecular Cell Biology, 15, 509- 524. http://dx.doi.org/10.1038/nrm3838
Pratt, A.J. and MacRae, I.J. (2009) The RNA-Induced Silencing Complex: A Versatile Gene-Silencing Machine. The Journal of Biological Chemistry, 284, 17897-17901. http://dx.doi.org/10.1074/jbc.R900012200
Verdel, A., Jia, S., Gerber, S., Sugiyama, T., Gygi, S., Grewal, S.I. and Moazed, D. (2004) RNAi-Mediated Targeting of Heterochromatin by the RITS Complex. Science, 303, 672-676. http://dx.doi.org/10.1126/science.1093686
Buhler, M., Verdel, A. and Moazed, D. (2006) Tethering RITS to a Nascent Transcript Initiates RNAi- and Heterochromatin-Dependent Gene Silencing. Cell, 125, 873-886. http://dx.doi.org/10.1016/j.cell.2006.04.025
Kozomara, A. and Griffiths-Jones, S. (2014) miRBase: Annotating High Confidence microRNAs Using Deep Sequencing Data. Nucleic Acids Research, 42, D68-D73. http://dx.doi.org/10.1093/nar/gkt1181
Sun, G. and Gerecht, S. (2009) Vascular Regeneration: Engineering the Stem Cell Microenvironment. Regenerative Medicine, 4, 435-447. http://dx.doi.org/10.2217/rme.09.1
Yang, Z. and Wu, J. (2007) MicroRNAs and Regenerative Medicine. DNA and Cell Biology, 26, 257-264. http://dx.doi.org/10.1089/dna.2006.0548
Isner, J.M. and Asahara, T. (1999) Angiogenesis and Vasculo-genesis as Therapeutic Strategies for Postnatal Neovascularization. Journal of Clinical Investigation, 103, 1231-1236. http://dx.doi.org/10.1172/JCI6889
Zhang, L. and Xu, Q. (2014) Stem/Progenitor Cells in Vascular Regeneration. Arteriosclerosis, Thrombosis, and Vascular Biology, 34, 1114-1119. http://dx.doi.org/10.1161/ATVBAHA.114.303809
Guiducci, S., Distler, O., Distler, J.H. and Matucci-Cerinic, M. (2008) Mechanisms of Vascular Damage in SSc— Implications for Vascular Treatment Strategies. Rheumatology (Oxford), 47, v18-v20. http://dx.doi.org/10.1093/rheumatology/ken267
Ang, Y.S., Tsai, S.Y., Lee, D.F., Monk, J., Su, J., Ratnakumar, K., Ding, J., Ge, Y., Darr, H., Chang, B., Wang, J., Rendl, M., Bernstein, E., Schaniel, C. and Lemischka, I.R. (2011) Wdr5 Mediates Self-Renewal and Reprogramming via the Embryonic Stem Cell Core Transcriptional Network. Cell, 145, 183-197. http://dx.doi.org/10.1016/j.cell.2011.03.003
Bar-Nur, O., Russ, H.A., Efrat, S. and Benvenisty, N. (2011) Epigenetic Memory and Preferential Lineage-Specific Differentiation in Induced Pluripotent Stem Cells Derived from Human Pancreatic Islet Beta Cells. Cell Stem Cell, 9, 17-23. http://dx.doi.org/10.1016/j.stem.2011.06.007
Hirai, H., Tani, T., Katoku-Kikyo, N., Kellner, S., Karian, P., Firpo, M. and Kikyo, N. (2011) Radical Acceleration of Nuclear Reprogramming by Chromatin Remodeling with the Transactivation Domain of MyoD. Stem Cells, 29, 1349-1361. http://dx.doi.org/10.1002/stem.684
Wang, S. and Olson, E.N. (2009) AngiomiRs—Key Regulators of Angiogenesis. Current Opinion in Genetics & Development, 19, 205-211. http://dx.doi.org/10.1016/j.gde.2009.04.002
Yang, W.J., Yang, D.D., Na, S., Sandusky, G.E., Zhang, Q. and Zhao, G. (2005) Dicer Is Required for Embryonic Angiogenesis during Mouse Development. The Journal of Biological Chemistry, 280, 9330-9335. http://dx.doi.org/10.1074/jbc.M413394200
Suárez, Y., Fernandez-Hernando, C., Pober, J.S. and Sessa, W.C. (2007) Dicer Dependent microRNAs Regulate Gene Expression and Functions in Human Endothelial Cells. Circulation Research, 100, 1164-1173. http://dx.doi.org/10.1161/01.RES.0000265065.26744.17
Kuehbacher, A., Urbich, C., Zeiher, A.M. and Dimmeler, S. (2007) Role of Dicer and Drosha for Endothelial microRNA Expression and Angiogenesis. Circulation Research, 101, 59-68. http://dx.doi.org/10.1161/CIRCRESAHA.107.153916
Suárez, Y., Fernandez-Hernando, C., Yu, J., Gerber, S.A., Harrison, K.D., Pober, J.S., Iruela-Arispe, M.L., Merkenschlager, M. and Sessa, W.C. (2008) Dicer-Dependent Endothelial microRNAs Are Necessary for Postnatal Angiogenesis. Proceedings of the National Academy of Sciences of the United States of America, 105, 14082-14087. http://dx.doi.org/10.1073/pnas.0804597105
Wang, S., Aurora, A.B., Johnson, B.A., Qi, X., McAnally, J., Hill, J.A., Richardson, J.A., Bassel-Duby, R. and Olson, E.N. (2008) The Endothelial-Specific microRNA miR-126 Governs Vascular Integrity and Angiogenesis. Developmental Cell, 15, 261-271. http://dx.doi.org/10.1016/j.devcel.2008.07.002
Santulli, G., Wronska, A., Uryu, K., Diacovo, T.G., Gao, M., Marx, S.O., Kitajewski, J., Chilton, J.M., Akat, K.M., Tuschl, T., Marks, A.R. and Totary-Jain, H. (2014) A Selective microRNA-Based Strategy Inhibits Restenosis While Preserving Endothelial Function. Journal of Clinical Investigation, 124, 4102-4114. http://dx.doi.org/10.1172/JCI76069
Yan, T., Cui, K., Huang, X., Ding, S., Zheng, Y., Luo, Q., Liu, X. and Zou, L. (2014) Assessment of Therapeutic Efficacy of miR-126 with Contrast-Enhanced Ultrasound in Preeclampsia Rats. Placenta, 35, 23-29. http://dx.doi.org/10.1016/j.placenta.2013.10.017
Sessa, R., Seano, G., di Blasio, L., Gagliardi, P.A., Isella, C., Medico, E., Cotelli, F., Bussolino, F. and Primo, L. (2012) The miR-126 Regulates Angiopoietin-1 Signaling and Vessel Maturation by Targeting p85β. Biochimica et Biophysica Acta, 1823, 1925-1935. http://dx.doi.org/10.1016/j.bbamcr.2012.07.011
Mogilyansky, E. and Rigoutsos, I. (2013) The miR-17/92 Cluster: A Comprehensive Update on Its Genomics, Genetics, Functions and Increasingly Important and Numerous Roles in Health and Disease. Cell Death & Differentiation, 20, 1603-1614. http://dx.doi.org/10.1038/cdd.2013.125
Mendell, J.T. (2008) miRiad Roles for the miR-17-92 Cluster in Development and Disease. Cell, 133, 217-222. http://dx.doi.org/10.1016/j.cell.2008.04.001
Dews, M., Homayouni, A., Yu, D., Murphy, D., Sevignani, C., Wentzel, E., Furth, E.E., Lee, W.M., Enders, G.H., Mendell, J.T. and Thomas-Tikhonenko, A. (2006) Augmentation of Tumor Angiogenesis by a Myc-Activated microRNA Cluster. Nature Genetics, 38, 1060-1065. http://dx.doi.org/10.1038/ng1855
Doebele, C., Bonauer, A., Fischer, A., Scholz, A., Reiss, Y., Urbich, C., Hofmann, W.K., Zeiher, A.M. and Dimmeler, S. (2010) Members of the microRNA-17-92 Cluster Exhibit a Cell-Intrinsic Anti-angiogenic Function in Endothelial Cells. Blood, 115, 4944-4950. http://dx.doi.org/10.1182/blood-2010-01-264812
Kaluza, D., Kroll, J., Gesierich, S., Manavski, Y., Boeckel, J.N., Doebele, C., Zelent, A., Rossig, L., Zeiher, A.M., Augustin, H.G., Urbich, C. and Dimmeler, S. (2013) Histone Deacetylase 9 Promotes Angiogenesis by Targeting the Antiangiogenic microRNA-17-92 Cluster in Endothelial Cells. Arteriosclerosis, Thrombosis, and Vascular Biology, 33, 533-543. http://dx.doi.org/10.1161/ATVBAHA.112.300415
Yin, K.J., Olsen, K., Hamblin, M., Zhang, J., Schwendeman, S.P. and Chen, Y.E. (2012) Vascular Endothelial Cell- Specific microRNA-15a Inhibits Angiogenesis in Hindlimb Ischemia. The Journal of Biological Chemistry, 287, 27055-27064. http://dx.doi.org/10.1074/jbc.M112.364414
Spinetti, G., Fortunato, O., Caporali, A., Shantikumar, S., Marchetti, M., Meloni, M., Descamps, B., Floris, I., Sangalli, E., Vono, R., Faglia, E., Specchia, C., Pintus, G., Madeddu, P. and Emanueli, C. (2013) MicroRNA-15a and microRNA-16 Impair Human Circulating Proangiogenic Cell Functions and Are Increased in the Proangiogenic Cells and Serum of Patients with Critical Limb Ischemia. Circulation Research, 112, 335-346. http://dx.doi.org/10.1161/CIRCRESAHA.111.300418
Chen, Y. and Gorski, D.H. (2008) Regulation of Angiogenesis through a microRNA (miR-130a) That Down-Regulates Antiangiogenic Homeobox Genes GAX and HOXA5. Blood, 111, 1217-1226. http://dx.doi.org/10.1182/blood-2007-07-104133
Richart, A., Loyer, X., Neri, T., Howangyin, K., Guerin, C.L., Ngkelo, A., Bakker, W., Zlatanova, I., Rouanet, M., Vilar, J., Levy, B., Rothenberg, M., Mallat, Z., Puceat, M. and Silvestre, J.S. (2014) MicroRNA-21 Coordinates Human Multipotent Cardiovascular Progenitors Therapeutic Potential. Stem Cells, 32, 2908-2922. http://dx.doi.org/10.1002/stem.1789
Xu, X., Kriegel, A.J., Jiao, X., Liu, H., Bai, X., Olson, J., Liang, M. and Ding, X. (2014) miR-21 in Ischemia/Reperfusion Injury: A Double-Edged Sword? Physiological Genomics, 46, 789-797. http://dx.doi.org/10.1152/physiolgenomics.00020.2014
Schaper, W. (2009) Collateral Circulation: Past and Present. Basic Research in Cardiology, 104, 5-21. http://dx.doi.org/10.1007/s00395-008-0760-x
Hans, F.P., Moser, M., Bode, C. and Grundmann, S. (2010) MicroRNA Regulation of Angiogenesis and Arteriogenesis. Trends in Cardiovascular Medicine, 20, 253-262. http://dx.doi.org/10.1016/j.tcm.2011.12.001
Weber, M., Baker, M.B., Moore, J.P. and Searles, C.D. (2010) MiR-21 Is Induced in Endothelial Cells by Shear Stress and Modulates Apoptosis and eNOS Activity. Biochemical and Bi-ophysical Research Communications, 393, 643-648. http://dx.doi.org/10.1016/j.bbrc.2010.02.045
Ji, R., Cheng, Y., Yue, J., Yang, J., Liu, X., Chen, H., Dean, D.B. and Zhang, C. (2007) MicroRNA Expression Signature and Anti-sense-Mediated Depletion Reveal an Essential Role of MicroRNA in Vascular Neointimal Lesion Formation. Circulation Research, 100, 1579-1588. http://dx.doi.org/10.1161/CIRCRESAHA.106.141986
Meng, F., Henson, R., Wehbe-Janek, H., Ghoshal, K., Jacob, S.T. and Patel, T. (2007) MicroRNA-21 Regulates Expression of the PTEN Tumor Suppressor Gene in Human Hepatocellular Cancer. Gastroenterology, 133, 647-658. http://dx.doi.org/10.1053/j.gastro.2007.05.022
Hutcheson, R., Chaplin, J., Hutcheson, B., Borthwick, F., Proctor, S., Gebb, S., Jadhav, R., Smith, E., Russell, J.C. and Rocic, P. (2014) miR-21 Normalizes Vascular Smooth Muscle Proliferation and Improves Coronary Collateral Growth in Metabolic Syndrome. The FASEB Journal, 28, 4088-4099. http://dx.doi.org/10.1096/fj.14-251223
Landskroner-Eiger, S., Qiu, C., Perrotta, P., Siragusa, M., Lee, M.Y., Ul-rich, V., Luciano, A.K., Zhuang, Z.W., Corti, F., Simons, M., Montgomery, R.L., Wu, D., Yu, J. and Sessa, W.C. (2015) Endothelial miR-17 Approximately 92 Cluster Negatively Regulates Arteriogenesis via miRNA-19 Repression of WNT Signaling. Proceedings of the National Academy of Sciences of the United States of America, 112, 12812-12817. http://dx.doi.org/10.1073/pnas.1507094112
Pankratz, F., Bemtgen, X., Zeiser, R., Leonhardt, F., Kreuzaler, S., Hilgendorf, I., Smolka, C., Helbing, T., Hoefer, I., Esser, J.S., Kustermann, M., Moser, M., Bode, C. and Grundmann, S. (2015) MicroRNA-155 Exerts Cell-Specific Antiangiogenic but Proarteriogenic Effects during Adaptive Neovascularization. Circulation, 131, 1575-1589. http://dx.doi.org/10.1161/CIRCULATIONAHA.114.014579
Eisenhardt, S.U., Weiss, J.B., Smolka, C., Maxeiner, J., Pankratz, F., Bemtgen, X., Kustermann, M., Thiele, J.R., Schmidt, Y., Bjoern Stark, G., Moser, M., Bode, C. and Grundmann, S. (2015) MicroRNA-155 Aggravates Ischemia- Reperfusion Injury by Modulation of Inflammatory Cell Recruitment and the Respiratory Oxidative Burst. Basic Research in Cardiology, 110, 32. http://dx.doi.org/10.1007/s00395-015-0490-9
Grundmann, S., Hans, F.P., Kinniry, S., Heinke, J., Helbing, T., Bluhm, F., Sluijter, J.P., Hoefer, I., Pasterkamp, G., Bode, C. and Moser, M. (2011) MicroRNA-100 Regulates Neovascular-ization by Suppression of Mammalian Target of Rapamycin in Endothelial and Vascular Smooth Muscle Cells. Circulation, 123, 999-1009. http://dx.doi.org/10.1161/CIRCULATIONAHA.110.000323
Leonhardt, F., Grundmann, S., Behe, M., Bluhm, F., Dumont, R.A., Braun, F., Fani, M., Riesner, K., Prinz, G., Hechinger, A.K., Gerlach, U.V., Dierbach, H., Penack, O., Schmitt-Graff, A., Finke, J., Weber, W.A. and Zeiser, R. (2013) Inflammatory Neovascularization during Graft-versus-Host Disease Is Regulated by Alphav Integrin and miR-100. Blood, 121, 3307-3318. http://dx.doi.org/10.1182/blood-2012-07-442665
Welten, S.M., Bastiaansen, A.J., de Jong, R.C., de Vries, M.R., Peters, E.A., Boonstra, M.C., Sheikh, S.P., La Monica, N., Kandimalla, E.R., Quax, P.H. and Nossent, A.Y. (2014) Inhibition of 14q32 MicroRNAs miR-329, miR-487b, miR-494, and miR-495 Increases Neovascularization and Blood Flow Recovery after Ischemia. Circulation Research, 115, 696-708. http://dx.doi.org/10.1161/CIRCRESAHA.114.304747
Lei, Z., van Mil, A., Brandt, M.M., Grundmann, S., Hoefer, I., Smits, M., El Azzouzi, H., Fukao, T., Cheng, C., Doevendans, P.A. and Sluijter, J.P. (2015) MicroRNA-132/212 Family Enhances Arteriogenesis after Hindlimb Ischaemia through Modulation of the Ras-MAPK Pathway. Journal of Cellular and Molecular Medicine, 19, 1994-2005. http://dx.doi.org/10.1111/jcmm.12586
Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., Witzenbichler, B., Schatteman, G. and Isner, J.M. (1997) Isolation of Putative Progenitor Endothelial Cells for Angiogenesis. Science, 275, 964-967. http://dx.doi.org/10.1126/science.275.5302.964
Minami, Y., Satoh, M., Maesawa, C., Takahashi, Y., Tabuchi, T., Itoh, T. and Nakamura, M. (2009) Effect of Atorvastatin on microRNA 221/222 Expression in Endothelial Progenitor Cells Obtained from Patients with Coronary Artery Disease. European Journal of Clinical Investigation, 39, 359-367. http://dx.doi.org/10.1111/j.1365-2362.2009.02110.x
Zhang, X., Mao, H., Chen, J.Y., Wen, S., Li, D., Ye, M. and Lv, Z. (2013) Increased Expression of microRNA-221 Inhibits PAK1 in Endothelial Progenitor Cells and Impairs Its Function via c-Raf/MEK/ERK Pathway. Biochemical and Biophysical Research Communications, 431, 404-408. http://dx.doi.org/10.1016/j.bbrc.2012.12.157
Zuo, K., Li, M., Zhang, X., Lu, C., Wang, S., Zhi, K. and He, B. (2015) MiR-21 Suppresses Endothelial Progenitor Cell Proliferation by Activating the TGFbeta Signaling Pathway via Down-Regulation of WWP1. International Journal of Clinical and Experimental Pathology, 8, 414-422.
Meng, S., Cao, J.T., Zhang, B., Zhou, Q., Shen, C.X. and Wang, C.Q. (2012) Down-Regulation of microRNA-126 in Endothelial Progenitor Cells from Diabetes Patients, Impairs Their Functional Properties, via Target Gene Spred-1. Journal of Molecular and Cellular Cardiology, 53, 64-72. http://dx.doi.org/10.1016/j.yjmcc.2012.04.003
Ye, M., Li, D., Yang, J., Xie, J., Yu, F., Ma, Y., Zhu, X., Zhao, J. and Lv, Z. (2015) MicroRNA-130a Targets MAP3K12 to Modulate Diabetic Endothelial Progenitor Cell Function. Cellular Physiology and Biochemistry, 36, 712- 726. http://dx.doi.org/10.1159/000430132
Tabuchi, T., Satoh, M., Itoh, T. and Nakamura, M. (2012) MicroRNA-34a Regulates the Longevity-Associated Protein SIRT1 in Coronary Artery Disease: Effect of Statins on SIRT1 and microRNA-34a Expression. Clinical Science, 123, 161-171. http://dx.doi.org/10.1042/CS20110563
Zhao, T., Li, J. and Chen, A.F. (2010) MicroRNA-34a Induces Endothelial Progenitor Cell Senescence and Impedes Its Angiogenesis via Suppressing Silent Information Regulator 1. American Journal of Physiology—Endocrinology and Metabolism, 299, E110-E116. http://dx.doi.org/10.1152/ajpendo.00192.2010
Zhu, S., Deng, S., Ma, Q., Zhang, T., Jia, C., Zhuo, D., Yang, F., Wei, J., Wang, L., Dykxhoorn, D.M., Hare, J.M., Goldschmidt-Clermont, P.J. and Dong, C. (2013) MicroRNA-10A* and MicroRNA-21 Modulate Endothelial Progenitor Cell Senescence via Suppressing High-Mobility Group A2. Circulation Research, 112, 152-164. http://dx.doi.org/10.1161/CIRCRESAHA.112.280016
Zheng, Y. and Xu, Z. (2014) MicroRNA-22 Induces Endothelial Progenitor Cell Senescence by Targeting AKT3. Cellular Physiology and Biochemistry, 34, 1547-1555. http://dx.doi.org/10.1159/000366358
Boyette, L.B., Creasey, O.A., Guzik, L., Lozito, T. and Tuan, R.S. (2014) Human Bone Marrow-Derived Mesenchymal Stem Cells Display Enhanced Clonogenicity but Impaired Differentiation with Hypoxic Preconditioning. Stem Cells Translational Medicine, 3, 241-254. http://dx.doi.org/10.5966/sctm.2013-0079
Goretti, E., Rolland-Turner, M., Leonard, F., Zhang, L., Wagner, D.R. and Devaux, Y. (2013) MicroRNA-16 Affects Key Functions of Human Endothelial Progenitor Cells. Journal of Leukocyte Biology, 93, 645-655. http://dx.doi.org/10.1189/jlb.1012511
Obi, S., Yamamoto, K. and Ando, J. (2014) Effects of Shear Stress on Endothelial Progenitor Cells. Journal of Biomedical Nanotechnology, 10, 2586-2597. http://dx.doi.org/10.1166/jbn.2014.2014
Cheng, B.B., Qu, M.J., Wu, L.L., Shen, Y., Yan, Z.Q., Zhang, P., Qi, Y.X. and Jiang, Z.L. (2014) MicroRNA-34a Targets Forkhead Box j2 to Modulate Differentiation of Endothelial Progenitor Cells in Response to Shear Stress. Journal of Molecular and Cellular Cardiology, 74, 4-12. http://dx.doi.org/10.1016/j.yjmcc.2014.04.016
Qiang, L., Hong, L., Ningfu, W., Huaihong, C. and Jing, W. (2013) Expression of miR-126 and miR-508-5p in Endothelial Progenitor Cells Is Associated with the Prognosis of Chronic Heart Failure Patients. International Journal of Cardiology, 168, 2082-2088. http://dx.doi.org/10.1016/j.ijcard.2013.01.160
Goerke, S.M., Kiefer, L.S., Stark, G.B., Simunovic, F. and Finkenzeller, G. (2015) miR-126 Modulates Angiogenic Growth Parameters of Peripheral Blood Endothelial Progenitor Cells. The Journal of Biological Chemistry, 396, 245-252. http://dx.doi.org/10.1515/hsz-2014-0259
Meng, Q., Wang, W., Yu, X., Li, W., Kong, L., Qian, A., Li, C. and Li, X. (2015) Upregulation of MicroRNA-126 Contributes to Endothelial Progenitor Cell Function in Deep Vein Thrombosis via Its Target PIK3R2. Journal of Cellular Biochemistry, 116, 1613-1623. http://dx.doi.org/10.1002/jcb.25115
Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., Waknitz, M.A., Swiergiel, J.J., Marshall, V.S. and Jones, J.M. (1998) Embryonic Stem Cell Lines Derived from Human Blastocysts. Science, 282, 1145-1147. http://dx.doi.org/10.1126/science.282.5391.1145
Houbaviy, H.B., Murray, M.F. and Sharp, P.A. (2003) Embryonic Stem Cell-Specific MicroRNAs. Developmental Cell, 5, 351-358. http://dx.doi.org/10.1016/S1534-5807(03)00227-2
Gruber, A.J., Grandy, W.A., Balwierz, P.J., Dimitrova, Y.A., Pachkov, M., Ciaudo, C., Nimwegen, E. and Zavolan, M. (2014) Embryonic Stem Cell-Specific microRNAs Contribute to Pluripotency by Inhibiting Regulators of Multiple Differentiation Pathways. Nucleic Acids Research, 42, 9313-9326. http://dx.doi.org/10.1093/nar/gku544
Kanellopoulou, C., Muljo, S.A., Kung, A.L., Ganesan, S., Drapkin, R., Jenuwein, T., Livingston, D.M. and Rajewsky, K. (2005) Dicer-Deficient Mouse Embryonic Stem Cells Are Defective in Differentiation and Centromeric Silencing. Genes & Development, 19, 489-501. http://dx.doi.org/10.1101/gad.1248505
Judson, R.L., Babiarz, J.E., Venere, M. and Blelloch, R. (2009) Embryonic Stem Cell-Specific microRNAs Promote Induced Pluripotency. Nature Biotechnology, 27, 459-461. http://dx.doi.org/10.1038/nbt.1535
Stadler, B., Ivanovska, I., Mehta, K., Song, S., Nelson, A., Tan, Y., Mathieu, J., Darby, C., Blau, C.A., Ware, C., Peters, G., Miller, D.G., Shen, L., Cleary, M.A. and Ruohola-Baker, H. (2010) Characteri-zation of microRNAs Involved in Embryonic Stem Cell States. Stem Cells and Development, 19, 935-950. http://dx.doi.org/10.1089/scd.2009.0426
Jia, W., Chen, W. and Kang, J. (2013) The Functions of microRNAs and Long Non-Coding RNAs in Embryonic and Induced Pluripotent Stem Cells. Genomics Proteomics Bioinformatics, 11, 275-283. http://dx.doi.org/10.1016/j.gpb.2013.09.004
Card, D.A., Hebbar, P.B., Li, L., Trotter, K.W., Komatsu, Y., Mishina, Y. and Archer, T.K. (2008) Oct4/Sox2-Regulated miR-302 Targets Cyclin D1 in Human Embryonic Stem Cells. Molecular and Cellular Biology, 28, 6426-6438. http://dx.doi.org/10.1128/MCB.00359-08
Anokye-Danso, F., Trivedi, C.M., Juhr, D., Gupta, M., Cui, Z., Tian, Y., Zhang, Y., Yang, W., Gruber, P.J., Epstein, J.A. and Morrisey, E.E. (2011) Highly Efficient miRNA-Mediated Reprogramming of Mouse and Human Somatic Cells to Pluripotency. Cell Stem Cell, 8, 376-388. http://dx.doi.org/10.1016/j.stem.2011.03.001
Li, M.A. and He, L. (2012) microRNAs as Novel Regulators of Stem Cell Pluripotency and Somatic Cell Reprogramming. Bioessays, 34, 670-680. http://dx.doi.org/10.1002/bies.201200019
Tay, Y., Zhang, J., Thomson, A.M., Lim, B. and Rigoutsos, I. (2008) MicroRNAs to Nanog, Oct4 and Sox2 Coding Regions Modulate Embryonic Stem Cell Differentiation. Nature, 455, 1124-1128. http://dx.doi.org/10.1038/nature07299
Singh, S.K., Kagalwala, M.N., Parker-Thornburg, J., Adams, H. and Majumder, S. (2008) REST Maintains Self- Renewal and Pluripotency of Embryonic Stem Cells. Nature, 453, 223-227. http://dx.doi.org/10.1038/nature06863
Xu, N., Papagiannakopoulos, T., Pan, G., Thomson, J.A. and Kosik, K.S. (2009) MicroRNA-145 Regulates OCT4, SOX2, and KLF4 and Represses Pluripotency in Human Embryonic Stem Cells. Cell, 137, 647-658. http://dx.doi.org/10.1016/j.cell.2009.02.038
Yoo, J.K., Kim, J., Choi, S.J., Noh, H.M., Kwon, Y.D., Yoo, H., Yi, H.S., Chung, H.M. and Kim, J.K. (2012) Discovery and Characterization of Novel microRNAs during Endothelial Differentiation of Human Embryonic Stem Cells. Stem Cells and Development, 21, 2049-2057. http://dx.doi.org/10.1089/scd.2011.0500
Kane, N.M., Howard, L., Descamps, B., Meloni, M., McClure, J., Lu, R., McCahill, A., Breen, C., Mackenzie, R.M., Delles, C., Mountford, J.C., Milligan, G., Emanueli, C. and Baker, A.H. (2012) Role of microRNAs 99b, 181a, and 181b in the Differentiation of Human Embryonic Stem Cells to Vascular Endothelial Cells. Stem Cells, 30, 643-654. http://dx.doi.org/10.1002/stem.1026
Wang, L., Su, W., Du, W., Xu, Y., Wang, L., Kong, D., Han, Z., Zheng, G. and Li, Z. (2015) Gene and MicroRNA Profiling of Human Induced Pluripotent Stem Cell-Derived Endothelial Cells. Stem Cell Reviews and Reports, 11, 219- 227. http://dx.doi.org/10.1007/s12015-014-9582-4
Treguer, K., Heinrich, E.M., Ohtani, K., Bonauer, A. and Dimmeler, S. (2012) Role of the microRNA-17-92 Cluster in the Endothelial Differentiation of Stem Cells. Journal of Vascular Research, 49, 447-460. http://dx.doi.org/10.1159/000339429
Luo, Z., Wen, G., Wang, G., Pu, X., Ye, S., Xu, Q., Wang, W. and Xiao, Q. (2013) MicroRNA-200C and -150 Play an Important Role in Endothelial Cell Differentiation and Vasculogenesis by Targeting Transcription Repressor ZEB1. Stem Cells, 31, 1749-1762. http://dx.doi.org/10.1002/stem.1448
Gill, J.G., Langer, E.M., Lindsley, R.C., Cai, M., Murphy, T.L. and Murphy, K.M. (2012) Snail Promotes the Cell-Autonomous Generation of Flk1+ Endothelial Cells through the Repression of the microRNA-200 Family. Stem Cells and Development, 21, 167-176. http://dx.doi.org/10.1089/scd.2011.0194
Shi, X., Richard, J., Zirbes, K.M., Gong, W., Lin, G., Kyba, M., Thomson, J.A., Koyano-Nakagawa, N. and Garry, D.J. (2014) Cooperative Interaction of Etv2 and Gata2 Regulates the Development of Endothelial and Hematopoietic Lineages. Developmental Biology, 389, 208-218. http://dx.doi.org/10.1016/j.ydbio.2014.02.018
Moore, J.C., Sheppard-Tindell, S., Shestopalov, I.A., Yamazoe, S., Chen, J.K. and Lawson, N.D. (2013) Post- Transcriptional Mechanisms Contribute to Etv2 Repression during Vascular Development. Developmental Biology, 384, 128-140. http://dx.doi.org/10.1016/j.ydbio.2013.08.028
Robinton, D.A. and Daley, G.Q. (2012) The Promise of Induced Pluripotent Stem Cells in Research and Therapy. Nature, 481, 295-305. http://dx.doi.org/10.1038/nature10761
Takahashi, K. and Yamanaka, S. (2006) Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors. Cell, 126, 663-676. http://dx.doi.org/10.1016/j.cell.2006.07.024
Yu, J., Vodyanik, M.A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J.L., Tian, S., Nie, J., Jonsdottir, G.A., Ruotti, V., Stewart, R., Slukvin, I.I. and Thomson, J.A. (2007) Induced Plu-ripotent Stem Cell Lines Derived from Human Somatic Cells. Science, 318, 1917-1920. http://dx.doi.org/10.1126/science.1151526
Wang, Y., Baskerville, S., Shenoy, A., Babiarz, J.E., Baehner, L. and Blelloch, R. (2008) Embryonic Stem Cell-Specific microRNAs Regulate the G1-S Transition and Promote Rapid Proliferation. Nature Genetics, 40, 1478-1483. http://dx.doi.org/10.1038/ng.250
Li, Z., Yang, C.S., Nakashima, K. and Rana, T.M. (2011) Small RNA-Mediated Regulation of iPS Cell Generation. The EMBO Journal, 30, 823-834. http://dx.doi.org/10.1038/emboj.2011.2
Subramanyam, D., Lamouille, S., Judson, R.L., Liu, J.Y., Bucay, N., Derynck, R. and Blelloch, R. (2011) Multiple Targets of miR-302 and miR-372 Promote Reprogramming of Human Fibroblasts to Induced Pluripotent Stem Cells. Nature Biotechnology, 29, 443-448. http://dx.doi.org/10.1038/nbt.1862
Deng, W., Cao, X., Chen, J., Zhang, Z., Yu, Q., Wang, Y., Shao, G., Zhou, J., Gao, X., Yu, J. and Xu, X. (2015) MicroRNA Replacing Oncogenic Klf4 and c-Myc for Generating iPS Cells via Cationized Pleurotus eryngii Polysaccharide-Based Nanotransfection. ACS Applied Materials & Interfaces, 7, 18957-18966. http://dx.doi.org/10.1021/acsami.5b06768
Zhang, Z., Xiang, D., Heriyanto, F., Gao, Y., Qian, Z. and Wu, W.S. (2013) Dissecting the Roles of miR-302/367 Cluster in Cellular Reprogramming Using TALE-Based Repressor and TALEN. Stem Cell Reports, 1, 218-225. http://dx.doi.org/10.1016/j.stemcr.2013.07.002
Lin, S.L., Chang, D.C., Lin, C.H., Ying, S.Y., Leu, D. and Wu, D.T. (2011) Regulation of Somatic Cell Reprogramming through Inducible mir-302 Expression. Nucleic Acids Research, 39, 1054-1065. http://dx.doi.org/10.1093/nar/gkq850
Yang, C.S., Li, Z. and Rana, T.M. (2011) microRNAs Modulate iPS Cell Generation. RNA, 17, 1451-1460. http://dx.doi.org/10.1261/rna.2664111
Choi, Y.J., Lin, C.P., Ho, J.J., He, X., Okada, N., Bu, P., Zhong, Y., Kim, S.Y., Bennett, M.J., Chen, C., Ozturk, A., Hicks, G.G., Hannon, G.J. and He, L. (2011) miR-34 miRNAs Provide a Barrier for Somatic Cell Reprogramming. Nature Cell Biology, 13, 1353-1360. http://dx.doi.org/10.1038/ncb2366
Di Bernardini, E., Campagnolo, P., Margariti, A., Zampetaki, A., Karamariti, E., Hu, Y. and Xu, Q. (2014) Endothelial Lineage Differentiation from Induced Pluripotent Stem Cells Is Regulated by microRNA-21 and Transforming Growth Factor beta2 (TGF-beta2) Pathways. The Journal of Biological Chemistry, 289, 3383-3393. http://dx.doi.org/10.1074/jbc.M113.495531
Li, Z., Margariti, A., Wu, Y., Yang, F., Hu, J., Zhang, L. and Chen, T. (2015) MicroRNA-199a Induces Differentiation of Induced Pluripotent Stem Cells into Endothelial Cells by Targeting Sirtuin 1. Molecular Medicine Reports, 12, 3711-3717.
Chen, T., Margariti, A., Kelaini, S., Cochrane, A., Guha, S.T., Hu, Y., Stitt, A.W., Zhang, L. and Xu, Q. (2015) MicroRNA-199b Modulates Vascular Cell Fate during iPS Cell Differentiation by Targeting the Notch Ligand Jagged1 and Enhancing VEGF Signaling. Stem Cells, 33, 1405-1418. http://dx.doi.org/10.1002/stem.1930