The Role of miRNA in Stem Cell Pluripotency and Commitment to the Vascular Endothelial Lineage

Microcirculation

Volumn 19, Issue 3, 2012, Pages 196-207

  White, Katie ^a   Kane, Nicole M ^a,c   Milligan, Graeme ^b   Baker, Andrew H ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Angiogenesis; Endothelial cell differentiation; MicroRNA; Pluripotent stem cells

Indexed keywords

ALPHA5 INTEGRIN; CONNECTIVE TISSUE GROWTH FACTOR; DICER; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 3; KRUPPEL LIKE FACTOR 4; LET 7B; MICRORNA; MICRORNA 100; MICRORNA 101; MICRORNA 126; MICRORNA 130; MICRORNA 132; MICRORNA 155; MICRORNA 16; MICRORNA 200B; MICRORNA 210; MICRORNA 218; MICRORNA 296; MICRORNA 322; MICRORNA 424; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P85; THROMBOSPONDIN 1; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSCRIPTION FACTOR 7 LIKE 1; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANGIOGENESIS; CELL ACTIVATION; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL LINEAGE; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL RENEWAL; CELL THERAPY; DOWN REGULATION; ENDOTHELIUM CELL; GENE EXPRESSION; GENE OVEREXPRESSION; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE FUNCTION; HUMAN; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SOMATIC CELL; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; ENDOTHELIAL CELLS; HUMANS; MICRORNAS; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PHYSIOLOGIC; PLURIPOTENT STEM CELLS;

EID: 84859128392     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1111/j.1549-8719.2012.00161.x     Document Type: Review

References (115)

1. Amatschek S, Kriehuber E, Bauer W, Reininger B, Meraner P, Wolpl A, Schweifer N, Haslinger C, Stingl G, Maurer D. Blood and lymphatic endothelial cell-specific differentiation programs are stringently controlled by the tissue environment. Blood 109: 4777-4785, 2007.
2. Anand S, Majeti BK, Acevedo LM, Murphy EA, Mukthavaram R, Scheppke L, Huang M, Shields DJ, Lindquist JN, Lapinski PE, King PD, Weis SM, Cheresh DA. MicroRNA-132-mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis. Nat Med 16: 909-914, 2010.
3. Bartel DP. MicroRNAs: Target recognition and regulatory functions. Cell 136: 215-233, 2009.
4. Benetti R, Gonzalo S, Jaco I, Munoz P, Gonzalez S, Schoeftner S, Murchison E, Andl T, Chen T, Klatt P, Li E, Serrano M, Millar S, Hannon G, Blasco MA. A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases. Nat Struct Mol Biol 15: 268-279, 2008.
5. Bonauer A, Carmona G, Iwasaki M, Mione M, Koyanagi M, Fischer A, Burchfield J, Fox H, Doebele C, Ohtani K, Chavakis E, Potente M, Tjwa M, Urbich C, Zeiher AM, Dimmeler S. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science 324: 1710-1713, 2009.
6. Bueno MaJ, Gamez de Cedran M, Gamez-Lapez G, Parez de Castro I, Di Lisio L, Montes-Moreno S, Martanez N, Guerrero M, Sanchez-Martanez R, Santos J, Pisano DG, Piris MA, Fernandez-Piqueras J, Malumbres M. Combinatorial effects of microRNAs to suppress the Myc oncogenic pathway. Blood 117: 6255-6266, 2011.
7. Caporali A, Meloni M, Völlenkle C, Bonci D, Sala-Newby GB, Addis R, Spinetti G, Losa S, Masson R, Baker AH, Agami R, Le Sage C, Condorelli G, Madeddu P, Martelli F, Emanueli C. Deregulation of microRNA-503 contributes to diabetes mellitus-induced impairment of endothelial function and reparative angiogenesis after limb ischemia: clinical perspective. Circulation 123: 282-291, 2011.
8. Carmeliet P. Angiogenesis in health and disease. Nat Med 9: 653-660, 2003.
9. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature 473: 298-307, 2011.
10. Chamorro-Jorganes A, Araldi E, Penalva LO, Sandhu D, Fernandez-Hernando C, Suarez Y. MicroRNA-16 and microRNA-424 regulate cell-autonomous angiogenic functions in endothelial cells via targeting vascular endothelial growth factor receptor-2 and fibroblast growth factor receptor-1. Arterioscler Thromb Vasc Biol 31: 2595-2606, 2011.
11. Chan YC, Khanna S, Roy S, Sen CK. miR-200b targets Ets-1 and is down-regulated by hypoxia to induce angiogenic response of endothelial cells. J Biol Chem 286: 2047-2056, 2011.
12. Chen S-J, Chang C-M, Tsai S-K, Chang Y-L, Chou S-J, Huang S-S, Tai L-K, Chen Y-C, Ku H-H, Li H-Y, Chiou S-H. Functional improvement of focal cerebral ischemia injury by subdural transplantation of induced pluripotent stem cells with fibrin glue. Stem Cells Dev 19: 1757-1767, 2011.
13. Chen Y, Gorski DH. Regulation of angiogenesis through a microRNA (miR-130a) that down-regulates antiangiogenic homeobox genes GAX and HOXA5. Blood 111: 1217-1226, 2008.
14. Chen J-F, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang D-Z. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 38: 228-233, 2006.
15. Chen C, Ridzon D, Lee C-T, Blake J, Sun Y, Strauss W. Defining embryonic stem cell identity using differentiation-related microRNAs and their potential targets. Mamm Genome 18: 316-327, 2007.
16. Cheng W, Liu T, Jiang F, Liu C, Zhao X, Gao Y, Wang H, Liu Z. microRNA-155 regulates angiotensin II type 1 receptor expression in umbilical vein endothelial cells from severely pre-eclamptic pregnant women. Int J Mol Med 27: 393-399, 2011.
17. Chhabra R, Dubey R, Saini N. Cooperative and individualistic functions of the microRNAs in the miR-23a∼27a∼24-2 cluster and its implication in human diseases. Mol Cancer 9: 232, 2010.
18. Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, Lee T-H, Miano JM, Ivey KN, Srivastava D. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 460: 705-710, 2009.
19. Cui Y, Han Z, Yi H, Song G, Hao C, Xia H, Ma X. MicroRNA-181b and microRNA-9 mediate arsenic-induced angiogenesis via NRP1. J Cell Physiol 227: 772-783, 2012.
20. Davis BN, Hilyard AC, Lagna G, Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454: 56-61, 2008.
21. Davis-Dusenbery BN, Hata A. Mechanisms of control of microRNA biogenesis. J Biochem 148: 381-392, 2010.
22. Dentelli P, Rosso A, Orso F, Olgasi C, Taverna D, Brizzi MF. microRNA-222 controls neovascularization by regulating signal transducer and activator of transcription 5A expression. Arterioscler Thromb Vasc Biol 30: 1562-1568, 2010.
23. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth EE, Lee WM, Enders GH, Mendell JT, Thomas-Tikhonenko A. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 38: 1060-1065, 2006.
24. Doebele C, Bonauer A, Fischer A, Scholz A, Reiss Y, Urbich C, Hofmann W-K, Zeiher AM, Dimmeler S. Members of the microRNA-17-92 cluster exhibit a cell-intrinsic antiangiogenic function in endothelial cells. Blood 115: 4944-4950, 2010.
25. Evseenko D, Zhu Y, Schenke-Layland K, Kuo J, Latour B, Ge S, Scholes J, Dravid G, Li X, MacLellan WR, Crooks GM. Mapping the first stages of mesoderm commitment during differentiation of human embryonic stem cells. Proc Natl Acad Sci U S A 107: 13742-13747, 2010.
26. Fasanaro P, D'Alessandra Y, Di Stefano V, Melchionna R, Romani S, Pompilio G, Capogrossi MC, Martelli F. MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem 283: 15878-15883, 2008.
27. Fiedler J, Jazbutyte V, Kirchmaier BC, Gupta SK, Lorenzen J, Hartmann D, Galuppo P, Kneitz S, Pena JTG, Sohn-Lee C, Loyer X, Soutschek J, Brand T, Tuschl T, Heineke J, Martin U, Schulte-Merker S, Ertl G, Engelhardt S, Bauersachs J, Thum T. MicroRNA-24 regulates vascularity after myocardial infarction. Circulation 124: 720-730, 2011.
28. Fish JE, Santoro MM, Morton SU, Yu S, Yeh R-F, Wythe JD, Ivey KN, Bruneau BG, Stainier DYR, Srivastava D. miR-126 Regulates angiogenic signalling and vascular integrity. Dev Cell 15: 272-284, 2008.
29. Foshay KM, Gallicano GI. miR-17 family miRNAs are expressed during early mammalian development and regulate stem cell differentiation. Dev Biol 326: 431-443, 2009.
30. Friedman RC, Farh KK-H, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105, 2009.
31. Gangaraju VK, Lin H. MicroRNAs: key regulators of stem cells. Nat Rev Mol Cell Biol 10: 116-125, 2009.
32. Ghosh G, Subramanian IV, Adhikari N, Zhang X, Joshi HP, Basi D, Chandrashekhar YS, Hall JL, Roy S, Zeng Y, Ramakrishnan S. Hypoxia-induced microRNA-424 expression in human endothelial cells regulates HIF-1α isoforms and promotes angiogenesis. J Clin Invest 120: 4141-4154, 2010.
33. Grundmann S, Hans FP, Kinniry S, Heinke J, Helbing T, Bluhm F, Sluijter JPG, Hoefer I, Pasterkamp G, Bode C, Moser M. MicroRNA-100 regulates neovascularization by suppression of mammalian target of rapamycin in endothelial and vascular smooth muscle cells. Circulation 123: 999-1009, 2011.
34. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, Yang X, Amit I, Meissner A, Regev A, Rinn JL, Root DE, Lander ES. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477: 295-300, 2011.
35. Hagan JP, Piskounova E, Gregory RI. Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat Struct Mol Biol 16: 1021-1025, 2009.
36. Harris TA, Yamakuchi M, Ferlito M, Mendell JT, Lowenstein CJ. MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci U S A 105: 1516-1521, 2008.
37. Harris TA, Yamakuchi M, Kondo M, Oettgen P, Lowenstein CJ. Ets-1 and Ets-2 regulate the expression of microRNA-126 in endothelial cells. Arterioscler Thromb Vasc Biol 30: 1990-1997, 2010.
38. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ, Hammond SM. A microRNA polycistron as a potential human oncogene. Nature 435: 828-833, 2005.
39. Heo I, Joo C, Cho J, Ha M, Han J, Kim VN. Lin28 mediates the terminal uridylation of let-7 precursor microRNA. Mol Cell 32: 276-284, 2008.
40. Heusschen R, van Gink M, Griffioen AW, Thijssen VL. MicroRNAs in the tumor endothelium: novel controls on the angioregulatory switchboard. Biochim Biophys Acta 1805: 87-96, 2010.
41. Hirakawa S, Hong Y-K, Harvey N, Schacht V, Matsuda K, Libermann T, Detmar M. Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells. Am J Pathol 162: 575-586, 2003.
42. Hua Z, Lv Q, Ye W, Wong C-KA, Cai G, Gu D, Ji Y, Zhao C, Wang J, Yang BB, Zhang Y. MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS ONE 1: e116, 2006.
43. Humar R, Kiefer FN, Berns H, Resink T, Battegay EJ. Hypoxia enhances vascular cell proliferation and angiogenesis in vitro via rapamycin (mTOR)-dependent signaling. FASEB J 16: 771-780, 2002.
44. Huntzinger E, Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12: 99-110, 2011.
45. Inui M, Martello G, Piccolo S. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 11: 252-263, 2010.
46. Ivey KN, Srivastava D. MicroRNAs as regulators of differentiation and cell fate decisions. Cell Stem Cell 7: 36-41, 2010.
47. James D, Nam H-S, Seandel M, Nolan D, Janovitz T, Tomishima M, Studer L, Lee G, Lyden D, Benezra R, Zaninovic N, Rosenwaks Z, Rabbany SY, Rafii S. Expansion and maintenance of human embryonic stem cell-derived endothelial cells by TGFb inhibition is Id1 dependent. Nat Biotech 28: 161-166, 2010.
48. Kane N, Howard L, Khanin R, McClure J, Breen C, Milligan G. MicroRNAs 99b, 181a and 181b are induced during human embryonic stem cell differentiation to vascular endothelial cells and can enhance differentiation capacity upon differentiation. Heart 97: e7, 2011.
49. Kane NM, Meloni M, Spencer HL, Craig MA, Strehl R, Milligan G, Houslay MD, Mountford JC, Emanueli C, Baker AH. Derivation of endothelial cells from human embryonic stem cells by directed differentiation: Analysis of microRNA and angiogenesis in vitro and in vivo. Arterioscler Thromb Vasc Biol 30: 1389-1397, 2010.
50. Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, Jenuwein T, Livingston DM, Rajewsky K. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 19: 489-501, 2005.
51. Katare R, Riu F, Mitchell K, Gubernator M, Campagnolo P, Cui Y, Fortunato O, Avolio E, Cesselli D, Beltrami AP, Angelini G, Emanueli C, Madeddu P. Transplantation of human pericyte progenitor cells improves the repair of infarcted heart through activation of an angiogenic program involving micro-RNA-132: novelty and significance. Circ Res 109: 894-906, 2011.
52. Kazenwadel J, Michael MZ, Harvey NL. Prox1 expression is negatively regulated by miR-181 in endothelial cells. Blood 116: 2395-2401, 2010.
53. Kelly MA, Hirschi KK. Signaling hierarchy regulating human endothelial cell development. Arterioscler Thromb Vasc Biol 29: 718-724, 2009.
54. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11: 597-610, 2010.
55. Kuehbacher A, Urbich C, Zeiher AM, Dimmeler S. Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ Res 101: 59-68, 2007.
56. Kuhnert F, Mancuso MR, Hampton J, Stankunas K, Asano T, Chen C-Z, Kuo CJ. Attribution of vascular phenotypes of the murine Egfl7 locus to the microRNA miR-126. Development 135: 3989-3993, 2008.
57. Lagarkova MA, Volchkov PY, Philonenko ES, Kiselev SL. Efficient differentiation of hESCs into endothelial cells in vitro is secured by epigenetic changes. Cell Cycle 7: 2929-2935, 2008.
58. Leslie Pedrioli DM, Karpanen T, Dabouras V, Jurisic G, van de Hoek G, Shin JW, Marino D, Kalin RE, Leidel S, Cinelli P, Schulte-Merker S, Brandli AW, Detmar M. miR-31 functions as a negative regulator of lymphatic vascular lineage-specific differentiation in vitro and vascular development in vivo. Mol Cell Biol 30: 3620-3634, 2010.
59. Levenberg S, Golub JS, Amit M, Itskovitz-Eldor J, Langer R. Endothelial cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A 99: 4391-4396, 2002.
60. Li Y, Song Y-H, Li F, Yang T, Lu YW, Geng Y-J. microRNA-221 regulates high glucose-induced endothelial dysfunction. Biochem Biophys Res Comms 381: 81-83, 2009.
61. Li Z, Wu JC, Sheikh AY, Kraft D, Cao F, Xie X, Patel M, Gambhir SS, Robbins RC, Cooke JP, Wu JC. Differentiation, survival, and function of embryonic stem cell derived endothelial cells for ischemic heart disease. Circulation 116: I-46-I-54, 2007.
62. Lu S-J, Feng Q, Caballero S, Chen Y, Moore MAS, Grant MB, Lanza R. Generation of functional hemangioblasts from human embryonic stem cells. Nat Methods 4: 501-509, 2007.
63. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, Guenther MG, Johnston WK, Wernig M, Newman J, Calabrese JM, Dennis LM, Volkert TL, Gupta S, Love J, Hannett N, Sharp PA, Bartel DP, Jaenisch R, Young RA. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134: 521-533, 2008.
64. Melton C, Judson RL, Blelloch R. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 463: 621-626, 2010.
65. Mendell JT. miRiad roles for the miR-17-92 cluster in development and disease. Cell 133: 217-222, 2008.
66. Menghini R, Casagrande V, Cardellini M, Martelli E, Terrinoni A, Amati F, Vasa-Nicotera M, Ippoliti A, Novelli G, Melino G, Lauro R, Federici M. MicroRNA 217 modulates endothelial cell senescence via Silent Information Regulator 1. Circulation 120: 1524-1532, 2009.
67. Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ. Characterization of Dicer-deficient murine embryonic stem cells. Proc Natl Acad Sci U S A 102: 12135-12140, 2005.
68. Newman MA, Thomson JM, Hammond SM. Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA 14: 1539-1549, 2008.
69. Nicoli S, Standley C, Walker P, Hurlstone A, Fogarty KE, Lawson ND. MicroRNA-mediated integration of haemodynamics and Vegf signalling during angiogenesis. Nature 464: 1196-1200, 2010.
70. Nourse MB, Halpin DE, Scatena M, Mortisen DJ, Tulloch NL, Hauch KD, Torok-Storb B, Ratner BD, Pabon L, Murry CE. VEGF induces differentiation of functional endothelium from human embryonic stem cells. Arterioscler Thromb Vasc Biol 30: 80-89, 2010.
71. Oettgen P. Regulation of vascular inflammation and remodeling by ETS factors. Circ Res 99: 1159-1166, 2006.
72. Otsuka M, Zheng M, Hayashi M, Lee J-D, Yoshino O, Lin S, Han J. Impaired microRNA processing causes corpus luteum insufficiency and infertility in mice. J Clin Invest 118: 1944-1954, 2008.
73. Poliseno LTA, Mariani L, Evangelista M, Citti L, Woods K, Mercatanti A, Hammond S, Rainaldi G. MicroRNAs modulate the angiogenic properties of HUVECs. Blood 108: 3068-3071, 2006.
74. Prado-Lopez S, Conesa A, Armiñán A, Martínez-Losa M, Escobedo-Lucea C, Gandia C, Tarazona S, Melguizo D, Blesa D, Montaner D, Sanz-González S, Sepúlveda P, Götz S, O'Connor JE, Moreno R, Dopazo J, Burks DJ, Stojkovic M. Hypoxia promotes efficient differentiation of human embryonic stem cells to functional endothelium. Stem Cells 28: 407-418, 2010.
75. Pulkkinen K, Malm T, Turunen M, Koistinaho J, Ylä-Herttuala S. Hypoxia induces microRNA miR-210 in vitro and in vivo: Ephrin-A3 and neuronal pentraxin 1 are potentially regulated by miR-210. FEBS Lett 582: 2397-2401, 2008.
76. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403: 901-906, 2000.
77. Ren J, Jin P, Wang E, Marincola F, Stroncek D. MicroRNA and gene expression patterns in the differentiation of human embryonic stem cells. J Transl Med 7: 20, 2009.
78. Risau W, Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol 11: 73-91, 1995.
79. Roesli C, Mumprecht V, Neri D, Detmar M. Identification of the surface-accessible, lineage-specific vascular proteome by two-dimensional peptide mapping. FASEB J 22: 1933-1944, 2008.
80. Rybak A, Fuchs H, Smirnova L, Brandt C, Pohl EE, Nitsch R, Wulczyn FG. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol 10: 987-993, 2008.
81. Sengupta S, Nie J, Wagner RJ, Yang C, Stewart R, Thomson JA. MicroRNA 92b controls the G1/S checkpoint gene p57 in human embryonic stem cells. Stem Cells 27: 1524-1528, 2009.
82. Shilo S, Roy S, Khanna S, Sen CK. Evidence for the involvement of miRNA in redox regulated angiogenic response of human microvascular endothelial cells. Arterioscler Thromb Vasc Biol 28: 471-477, 2008.
83. Sinkkonen L, Hugenschmidt T, Berninger P, Gaidatzis D, Mohn F, Artus-Revel CG, Zavolan M, Svoboda P, Filipowicz W. MicroRNAs control de novo DNA methylation through regulation of transcriptional repressors in mouse embryonic stem cells. Nat Struct Mol Biol 15: 259-267, 2008.
84. Small EM, Sutherland LB, Rajagopalan KN, Wang S, Olson EN. MicroRNA-218 regulates vascular patterning by modulation of Slit-Robo signaling. Circ Res 107: 1336-1344, 2010.
85. Smith KN, Singh AM, Dalton S. Myc represses primitive endoderm differentiation in pluripotent stem cells. Cell Stem Cell 7: 343-354, 2010.
86. Smits M, Mir SE, Nilsson RJA, van derStoopPM, Niers JM, Marquez VE, Cloos J, Breakefield XO, Krichevsky AM, Noske DP, Tannous BA, Wardinger T. Down-regulation of miR-101 in endothelial cells promotes blood vessel formation through reduced repression of EZH2. PLoS ONE 6: e16282, 2011.
87. Sone M, Itoh H, Yamahara K, Yamashita JK, Yurugi-Kobayashi T, Nonoguchi A, Suzuki Y, Chao T-H, Sawada N, Fukunaga Y, Miyashita K, Park K, Oyamada N, Sawada N, Taura D, Tamura N, Kondo Y, Nito S, Suemori H, Nakatsuji N, Nishikawa S-I, Nakao K. Pathway for differentiation of human embryonic stem cells to vascular cell components and their potential for vascular regeneration. Arterioscler Thromb Vasc Biol 27: 2127-2134, 2007.
88. Stadler B, Ivanovska I, Mehta K, Song S, Nelson A, Tan Y, Mathieu J, Darby C, Blau CA, Ware C, Peters G, Miller DG, Shen L, Cleary MA, Ruohola-Baker H. Characterization of microRNAs involved in embryonic stem cell states. Stem Cells Dev 19: 935-950, 2010.
89. Staton CA, Kumar I, Reed MWR, Brown NJ. Neuropilins in physiological and pathological angiogenesis. J Pathol 212: 237-248, 2007.
90. Suarez Y, Fernandez-Hernando C, Pober JS, Sessa WC. Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ Res 100: 1164-1173, 2007.
91. Suarez Y, Fernandez-Hernando C, Yu J, Gerber SA, Harrison KD, Pober JS, Iruela-Arispe ML, Merkenschlager M, Sessa WC. Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc Natl Acad Sci U S A 105: 14082-14087, 2008.
92. Suarez Y, Wang C, Manes TD, Pober JS. Cutting edge: TNF-induced microRNAs regulate TNF-induced expression of E-selectin and intercellular adhesion molecule-1 on human endothelial cells: feedback control of inflammation. J Immunol 184: 21-25, 2010.
93. Sun T, Wang C, Xing J, Wu D. miR-429 modulates the expression of c-myc in human gastric carcinoma cells. Eur J Cancer 47: 2552-2559, 2011.
94. Taguchi A, Yanagisawa K, Tanaka M, Cao K, Matsuyama Y, Goto H, Takahashi T. Identification of hypoxia-inducible factor-1α as a novel target for miR-17-92 microRNA cluster. Cancer Res 68: 5540-5545, 2008.
95. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676, 2006.
96. Tay Y, Zhang J, Thomson AM, Lim B, Rigoutsos I. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455: 1124-1128, 2008.
97. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, Jaenisch R, Sharp PA, Jacks T. Targeted deletion reveals essential and overlapping functions of the miR-17∼92 family of miRNA clusters. Cell 132: 875-886, 2008.
98. Viswanathan SR, Daley GQ, Gregory RI. Selective blockade of microRNA processing by Lin28. Science 320: 97-100, 2008.
99. Vodyanik MA, Bork JA, Thomson JA, Slukvin II. Human embryonic stem cell-derived CD34+ cells: efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood 105: 617-626, 2005.
100. Wang ZZ, Au P, Chen T, Shao Y, Daheron LM, Bai H, Arzigian M, Fukumura D, Jain RK, Scadden DT. Endothelial cells derived from human embryonic stem cells form durable blood vessels in vivo. Nat Biotech 25: 317-318, 2007.
101. Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, Richardson JA, Bassel-Duby R, Olson EN. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell 15: 261-271, 2008.
102. Wang Y, Baskerville S, Shenoy A, Babiarz JE, Baehner L, Blelloch R. Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nat Genet 40: 1478-1483, 2008.
103. Wang Y, Medvid R, Melton C, Jaenisch R, Blelloch R. DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet 39: 380-385, 2007.
104. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, Waldvogel B, Vannier C, Darling D, zur Hausen A, Brunton VG, Morton J, Sansom O, Schuler J, Stemmler MP, Herzberger C, Hopt U, Keck T, Brabletz S, Brabletz T. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 11: 1487-1495, 2009.
105. Won Kim H, Haider HK, Jiang S, Ashraf M. Ischemic preconditioning augments survival of stem cells via miR-210 expression by targeting Caspase-8-associated protein 2. J Biol Chem 284: 33161-33168, 2009.
106. Wu L, Belasco JG. Micro-RNA Regulation of the mammalian lin-28 gene during neuronal differentiation of embryonal carcinoma cells. Mol Cell Biol 25: 9198-9208, 2005.
107. Würdinger T, Tannous BA, Saydam O, Skog J, Grau S, Soutschek J, Weissleder R, Breakefield XO, Krichevsky AM. miR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells. Cancer Cell 14: 382-393, 2008.
108. Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137: 647-658, 2009.
109. Yang WJ, Yang DD, Na S, Sandusky GE, Zhang Q, Zhao G. Dicer is required for embryonic angiogenesis during mouse development. J Biol Chem 280: 9330-9335, 2005.
110. Young RA. Control of the embryonic stem cell state. Cell 144: 940-954, 2011.
111. Zhao T, Li J, Chen AF. MicroRNA-34a induces endothelial progenitor cell senescence and impedes its angiogenesis via suppressing silent information regulator 1. Am J Physiol Endocrinol Metab 299: E110-E116, 2010.
112. Zhao Y, Samal E, Srivastava D. Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 436: 214-220, 2005.
113. Zhou Q, Gallagher R, Ufret-Vincenty R, Li X, Olson EN, Wang S. Regulation of angiogenesis and choroidal neovascularization by members of microRNA-23a-27a-24 clusters. Proc Natl Acad Sci U S A 108: 8287-8292, 2011.
114. Zhu N, Zhang D, Chen S, Liu X, Lin L, Huang X, Guo Z, Liu J, Wang Y, Yuan W, Qin Y. Endothelial enriched microRNAs regulate angiotensin II-induced endothelial inflammation and migration. Atherosclerosis 215: 286-293, 2011.
115. Zou J, Li W-Q, Li Q, Li X-Q, Zhang J-T, Liu G-Q, Chen J, Qiu X-X, Tian F-J, Wang Z-Z, Zhu N, Qin Y-W, Shen B, Liu TX, Jing Q. Two functional microRNA-126s repress a novel target gene p21-activated kinase 1 to regulate vascular integrity in zebrafish. Circ Res 108: 201-209, 2011.