MicroRNA regulation of endothelial homeostasis and commitment - Implications for vascular regeneration strategies using stem cell therapies

Free Radical Biology and Medicine

Volumn 64, Issue , 2013, Pages 52-60

  Scott, Elizabeth ^a   Loya, Komal ^a   Mountford, Joanne ^b   Milligan, Graeme ^c   Baker, Andrew H ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Embryonic stem cells; Free radicals; Induced pluripotent stem cells; MicroRNA; Pluripotency; Regenerative medicine; Vascular endothelial cells

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; ENDOTHELIN 1; EPHRIN A3; EPHRIN RECEPTOR; GROWTH FACTOR RECEPTOR; KARYOPHERIN ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA; MICRORNA 10; MICRORNA 100; MICRORNA 126; MICRORNA 20A; MICRORNA 20B; MICRORNA 210; MICRORNA 221; MICRORNA 222; MICRORNA 27B; MICRORNA 378; NOTCH1 RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; THROMBOSPONDIN 1; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; CELL GROWTH; CELL LINEAGE; CELL MIGRATION; CELL SURVIVAL; EMBRYO DEVELOPMENT; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; HOMEOSTASIS; HUMAN; LEUKOCYTE ADHERENCE; OXIDATIVE STRESS; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; TISSUE REGENERATION; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; VASCULAR DISEASE; VASCULAR ENDOTHELIUM;

CARDIOVASCULAR DISEASE; CVD; EC; EMBRYONIC STEM CELLS; ENDOTHELIAL CELL; ENDOTHELIAL PROGENITOR CELL; EPC; FREE RADICALS; HESC; HUMAN EMBRYONIC STEM CELL; INDUCED PLURIPOTENT STEM CELL; INDUCED PLURIPOTENT STEM CELLS; IPSC; MESC; MICRORNA; MIRNA; MURINE EMBRYONIC STEM CELL; PLURIPOTENCY; REACTIVE OXYGEN SPECIES; REGENERATIVE MEDICINE; ROS; VASCULAR ENDOTHELIAL CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR; VEGF;

ADULT; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICRORNAS; NEOVASCULARIZATION, PHYSIOLOGIC; OXIDATION-REDUCTION; REGENERATION; SIGNAL TRANSDUCTION; VASCULAR DISEASES;

EID: 84885187887     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.04.037     Document Type: Review

References (100)

1. Thomson, J. A.; Itskovitz-Eldor, J.; Shapiro, S. S.; Waknitz, M. A.; Swiergiel, J. J.; Marshall, V. S.; Jones, J. M. Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147; 1998. (Pubitemid 28516247)
2. Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; Yamanaka, S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872; 2007. (Pubitemid 350138099)
3. 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.; Thomson, J. A. Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917-1920; 2007.
4. Lee, R. C.; Feinbaum, R. L.; Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843-854; 1993.
5. Lee, R. C.; Ambros, V. An extensive class of small RNAs in Caenorhabditis elegans. Science 294:862-864; 2001. (Pubitemid 33032105)
6. Wightman, B.; Ha, I.; Ruvkun, G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75:855-862; 1993. (Pubitemid 24014543)
7. Lee, Y.; Kim, M.; Han, J.; Yeom, K. H.; Lee, S.; Baek, S. H.; Kim, V. N. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23:4051-4060; 2004. (Pubitemid 39472426)
8. Lee, Y.; Ahn, C.; Han, J.; Choi, H.; Kim, J.; Yim, J.; Lee, J.; Provost, P.; Radmark, O.; Kim, S.; Kim, V. N. The nuclear RNase III Drosha initiates microRNA processing. Nature 425:415-419; 2003. (Pubitemid 37187272)
9. Lund, E.; Guttinger, S.; Calado, A.; Dahlberg, J. E.; Kutay, U. Nuclear export of microRNA precursors. Science 303:95-98; 2004. (Pubitemid 38055779)
10. Knight, S. W.; Bass, B. L. A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in Caenorhabditis elegans. Science 293:2269-2271; 2001. (Pubitemid 32900239)
11. Guo, H.; Ingolia, N. T.; Weissman, J. S.; Bartel, D. P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466:835-840; 2010.
12. Cordes, K. R.; Sheehy, N. T.; White, M. P.; Berry, E. C.; Morton, S. U.; Muth, A. N.; Lee, T. H.; Miano, J. M.; Ivey, K. N.; Srivastava, D. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 460:705-710; 2009.
13. Iorio, M. V.; Croce, C. M. MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol. Med 4:143-159; 2012.
14. Rottiers, V.; Naar, A. M. MicroRNAs in metabolism and metabolic disorders. Nat. Rev. Mol. Cell Biol. 13:239-250; 2012.
15. Ono, K.; Kuwabara, Y.; Han, J. MicroRNAs and cardiovascular diseases. FEBS J. 278:1619-1633; 2011.
16. Wang, S.; Aurora, A. B.; Johnson, B. A.; Qi, X.; McAnally, J.; Hill, J. A.; Richardson, J. A.; Bassel-Duby, R.; Olson, E. N. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev. Cell 15:261-271; 2008.
17. Jakob, P.; Landmesser, U. Role of microRNAs in stem/progenitor cells and cardiovascular repair. Cardiovasc. Res. 93:614-622; 2012.
18. Suarez, Y.; Fernandez-Hernando, C.; Pober, J. S.; Sessa, W. C. Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ. Res. 100:1164-1173; 2007. (Pubitemid 46684129)
19. Suarez, Y.; Fernandez-Hernando, C.; Yu, J.; Gerber, S. A.; Harrison, K. D.; Pober, J. S.; Iruela-Arispe, M. L.; Merkenschlager, M.; Sessa, W. C. Dicerdependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc. Natl. Acad. Sci. USA 105:14082-14087; 2008.
20. Kuehbacher, A.; Urbich, C.; Zeiher, A. M.; Dimmeler, S. Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ. Res. 101:59-68; 2007. (Pubitemid 47094624)
21. Harris, T. A.; Yamakuchi, M.; Ferlito, M.; Mendell, J. T.; Lowenstein, C. J. MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc. Natl. Acad. Sci. USA 105:1516-1521; 2008. (Pubitemid 351346546)
22. Sessa, R.; Seano, G.; di Blasio, L.; Gagliardi, P. A.; Isella, C.; Medico, E.; Cotelli, F.; Bussolino, F.; Primo, L. The miR-126 regulates angiopoietin-1 signaling and vessel maturation by targeting p85beta. Biochim. Biophys. Acta 1823:1925-1935; 2012.
23. Dews, M.; Homayouni, A.; Yu, D.; Murphy, D.; Sevignani, C.; Wentzel, E.; Furth, E. E.; Lee, W. M.; Enders, G. H.; Mendell, J. T.; Thomas-Tikhonenko, A. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat. Genet. 38:1060-1065; 2006. (Pubitemid 44325933)
24. Chen, Y.; Gorski, D. H. Regulation of angiogenesis through a microRNA (miR-130a) that down-regulates antiangiogenic homeobox genes GAX and HOXA5. Blood 111:1217-1226; 2008. (Pubitemid 351213403)
25. Wurdinger, T.; Tannous, B. A.; Saydam, O.; Skog, J.; Grau, S.; Soutschek, J.; Weissleder, R.; Breakefield, X. O.; Krichevsky, A. M. miR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells. Cancer Cell 14:382-393; 2008.
26. Hassel, D.; Cheng, P.; White, M. P.; Ivey, K. N.; Kroll, J.; Augustin, H. G.; Katus, H. A.; Stainier, D. Y.; Srivastava, D. MicroRNA-10 regulates the angiogenic behavior of zebrafish and human endothelial cells by promoting vascular endothelial growth factor signaling. Circ. Res. 111: 1421-1433; 2012.
27. Fasanaro, P.; D'Alessandra, Y.; Di Stefano, V.; Melchionna, R.; Romani, S.; Pompilio, G.; Capogrossi, M. C.; 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.
28. Murai, K. K.; Pasquale, E. B. 'Eph'ective signaling: forward, reverse and crosstalk. J. Cell Sci. 116: 2823-2832; 2003. (Pubitemid 36926971)
29. Lou, Y. L.; Guo, F.; Liu, F.; Gao, F. L.; Zhang, P. Q.; Niu, X.; Guo, S. C.; Yin, J. H.; Wang, Y.; Deng, Z. F. miR-210 activates notch signaling pathway in angiogenesis induced by cerebral ischemia. Mol. Cell. Biochem. 370:45-51; 2012.
30. Lou, Y.; Gao, F.; Xie, A.; Guo, F.; Deng, Z.; Wang, Y. [MicroRNA-210 modified human umbilical vein endothelial cells induce capillary formation]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 26:587-591; 2012.
31. Lee, D. Y.; Deng, Z.; Wang, C. H.; Yang, B. B. MicroRNA-378 promotes cell survival, tumor growth, and angiogenesis by targeting SuFu and Fus-1 expression. Proc. Natl. Acad. Sci. USA 104:20350-20355; 2007.
32. Taylor, M. D.; Liu, L.; Raffel, C.; Hui, C. C.; Mainprize, T. G.; Zhang, X.; Agatep, R.; Chiappa, S.; Gao, L.; Lowrance, A.; Hao, A.; Goldstein, A. M.; Stavrou, T.; Scherer, S. W.; Dura, W. T.; Wainwright, B.; Squire, J. A.; Rutka, J. T.; Hogg, D. Mutations in SUFU predispose to medulloblastoma. Nat. Genet. 31:306-310; 2002.
33. Taylor, M. D.; Zhang, X.; Liu, L.; Hui, C. C.; Mainprize, T. G.; Scherer, S. W.; Wainwright, B.; Hogg, D.; Rutka, J. T. Failure of a medulloblastoma- derived mutant of SUFU to suppress WNT signaling. Oncogene 23:4577-4583; 2004. (Pubitemid 38850405)
34. Uno, F.; Sasaki, J.; Nishizaki, M.; Carboni, G.; Xu, K.; Atkinson, E. N.; Kondo, M.; Minna, J. D.; Roth, J. A.; Ji, L. Myristoylation of the fus1 protein is required for tumor suppression in human lung cancer cells. Cancer Res. 64: 2969-2976; 2004. (Pubitemid 38581390)
35. Poliseno, L.; Tuccoli, A.; 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.
36. Gorski, D. H.; LePage, D. F.; Patel, C. V.; Copeland, N. G.; Jenkins, N. A.; Walsh, K. Molecular cloning of a diverged homeobox gene that is rapidly down-regulated during the G0/G1 transition in vascular smooth muscle cells. Mol. Cell. Biol. 13:3722-3733; 1993. (Pubitemid 23157309)
37. van Grunsven, L. A.; Michiels, C.; Van de Putte, T.; Nelles, L.; Wuytens, G.; Verschueren, K.; Huylebroeck, D. Interaction between Smad-interacting protein-1 and the corepressor C-terminal binding protein is dispensable for transcriptional repression of E-cadherin. J. Biol. Chem. 278:26135-26145; 2003. (Pubitemid 36835383)
38. Chen, Y.; Banda, M.; Speyer, C. L.; Smith, J. S.; Rabson, A. B.; Gorski, D. H. Regulation of the expression and activity of the antiangiogenic homeobox gene GAX/MEOX2 by ZEB2 and microRNA-221. Mol. Cell. Biol. 30:3902-3913; 2010.
39. Iaconetti, C.; Polimeni, A.; Sorrentino, S.; Sabatino, J.; Pironti, G.; Esposito, G.; Curcio, A.; Indolfi, C. Inhibition of miR-92a increases endothelial proliferation and migration in vitro as well as reduces neointimal proliferation in vivo after vascular injury. Basic Res. Cardiol. 107:296; 2012.
40. Hua, Z.; Lv, Q.; Ye, W.; Wong, C. K.; Cai, G.; Gu, D.; Ji, Y.; Zhao, C.; Wang, J.; Yang, B. B.; Zhang, Y. MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS One 1:e116; 2006.
41. Grundmann, S.; Hans, F. P.; Kinniry, S.; Heinke, J.; Helbing, T.; Bluhm, F.; Sluijter, J. P.; 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.
42. Humar, R.; Kiefer, F. N.; Berns, H.; Resink, T. J.; Battegay, E. J. Hypoxia enhances vascular cell proliferation and angiogenesis in vitro via rapamycin (mTOR)-dependent signaling. FASEB J 16:771-780; 2002. (Pubitemid 34615125)
43. Wigle, J. T.; Oliver, G. Prox1 function is required for the development of the murine lymphatic system. Cell 98:769-778; 1999. (Pubitemid 29446894)
44. Kazenwadel, J.; Michael, M. Z.; Harvey, N. L. Prox1 expression is negatively regulated by miR-181 in endothelial cells. Blood 116: 2395-2401; 2010.
45. Sun, X.; Icli, B.; Wara, A. K.; Belkin, N.; He, S.; Kobzik, L.; Hunninghake, G. M.; Vera, M. P.; Blackwell, T. S.; Baron, R. M.; Feinberg, M. W. MicroRNA-181b regulates NF-kappaB-mediated vascular inflammation. J. Clin. Invest. 122:1973-1990; 2012.
46. Fang, Y.; Shi, C.; Manduchi, E.; Civelek, M.; Davies, P. F. MicroRNA-10a regulation of proinflammatory phenotype in athero-susceptible endothelium in vivo and in vitro. Proc. Natl. Acad. Sci. USA 107:13450-13455; 2010.
47. Fang, Y.; Davies, P. F. Site-specific microRNA-92a regulation of Kruppel-like factors 4 and 2 in atherosusceptible endothelium. Arterioscler. Thromb. Vasc. Biol. 32:979-987; 2012.
48. Caporali, A.; Meloni, M.; Vollenkle, C.; Bonci, D.; Sala-Newby, G. B.; Addis, R.; Spinetti, G.; Losa, S.; Masson, R.; Baker, A. H.; 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. Circulation 123:282-291; 2011.
49. Feng, B.; Chakrabarti, S. miR-320 regulates glucose-induced gene expression in diabetes. ISRN Endocrinol 2012:549875; 2012.
50. Li, Y.; Song, Y. H.; Li, F.; Yang, T.; Lu, Y. W.; Geng, Y. J. MicroRNA-221 regulates high glucose-induced endothelial dysfunction. Biochem. Biophys. Res. Commun. 381:81-83; 2009.
51. Shi, Q.; Rafii, S.; Wu, M. H.; Wijelath, E. S.; Yu, C.; Ishida, A.; Fujita, Y.; Kothari, S.; Mohle, R.; Sauvage, L. R.; Moore, M. A.; Storb, R. F.; Hammond, W. P. Evidence for circulating bone marrow-derived endothelial cells. Blood 92:362-367; 1998. (Pubitemid 28323695)
52. Zhang, Q. W.; Kandic, I.; Kutryk, M. J. Dysregulation of angiogenesis-related microRNAs in endothelial progenitor cells from patients with coronary artery disease. Biochem. Biophys. Res. Commun. 405:42-46; 2011.
53. Kanellopoulou, C.; Muljo, S. A.; Kung, A. L.; Ganesan, S.; Drapkin, R.; Jenuwein, T.; Livingston, D. M.; Rajewsky, K. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19:489-501; 2005. (Pubitemid 40256280)
54. Murchison, E. P.; Partridge, J. F.; Tam, O. H.; Cheloufi, S.; Hannon, G. J. Characterization of Dicer-deficient murine embryonic stem cells. Proc. Natl. Acad. Sci. USA 102:12135-12140; 2005. (Pubitemid 41291141)
55. 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. (Pubitemid 46328490)
56. Qi, J.; Yu, J. Y.; Shcherbata, H. R.; Mathieu, J.; Wang, A. J.; Seal, S.; Zhou, W.; Stadler, B. M.; Bourgin, D.; Wang, L.; Nelson, A.; Ware, C.; Raymond, C.; Lim, L. P.; Magnus, J.; Ivanovska, I.; Diaz, R.; Ball, A.; Cleary, M. A.; Ruohola-Baker, H. microRNAs regulate human embryonic stem cell division. Cell Cycle 8:3729-3741; 2009.
57. 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.; Baker, A. H. Role of microRNAs 99b, 181a, and 181b in the differentiation of human embryonic stem cells to vascular endothelial cells. Stem Cells 30:643-654; 2012.
58. Chambers, I.; Smith, A. Self-renewal of teratocarcinoma and embryonic stem cells. Oncogene 23:7150-7160; 2004. (Pubitemid 39382149)
59. Marson, A.; Levine, S. S.; Cole, M. F.; Frampton, G. M.; Brambrink, T.; Johnstone, S.; Guenther, M. G.; Johnston, W. K.; Wernig, M.; Newman, J.; Calabrese, J. M.; Dennis, L. M.; Volkert, T. L.; Gupta, S.; Love, J.; Hannett, N.; Sharp, P. A.; Bartel, D. P.; Jaenisch, R.; Young, R. A. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134:521-533; 2008.
60. Houbaviy, H. B.; Murray, M. F.; Sharp, P. A. Embryonic stem cell-specific microRNAs. Dev. Cell 5:351-358; 2003. (Pubitemid 37006477)
61. Lakshmipathy, U.; Love, B.; Goff, L. A.; Jornsten, R.; Graichen, R.; Hart, R. P.; Chesnut, J. D. MicroRNA expression pattern of undifferentiated and differentiated human embryonic stem cells. Stem Cells Dev. 16: 1003-1016; 2007.
62. Mineno, J.; Okamoto, S.; Ando, T.; Sato, M.; Chono, H.; Izu, H.; Takayama, M.; Asada, K.; Mirochnitchenko, O.; Inouye, M.; Kato, I. The expression profile of microRNAs in mouse embryos. Nucleic Acids Res. 34:1765-1771; 2006.
63. Laurent, L. C.; Chen, J.; Ulitsky, I.; Mueller, F. J.; Lu, C.; Shamir, R.; Fan, J. B.; Loring, J. F. Comprehensive microRNA profiling reveals a unique human embryonic stem cell signature dominated by a single seed sequence. Stem Cells 26:1506-1516; 2008.
64. Suh, M. R.; Lee, Y.; Kim, J. Y.; Kim, S. K.; Moon, S. H.; Lee, J. Y.; Cha, K. Y.; Chung, H. M.; Yoon, H. S.; Moon, S. Y.; Kim, V. N.; Kim, K. S. Human embryonic stem cells express a unique set of microRNAs. Dev. Biol. 270: 488-498; 2004. (Pubitemid 38748567)
65. 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.; Ruohola-Baker, H. Characterization of microRNAs involved in embryonic stem cell states. Stem Cells Dev. 19:935-950; 2010.
66. Card, D. A.; Hebbar, P. B.; Li, L.; Trotter, K. W.; Komatsu, Y.; Mishina, Y.; Archer, T. K. Oct4/Sox2-regulated miR-302 targets cyclin D1 in human embryonic stem cells. Mol. Cell. Biol. 28:6426-6438; 2008.
67. Rosa, A.; Brivanlou, A. H. A regulatory circuitry comprised of miR-302 and the transcription factors OCT4 and NR2F2 regulates human embryonic stem cell differentiation. EMBO J 30:237-248; 2011.
68. White, J.; Dalton, S. Cell cycle control of embryonic stem cells. Stem Cell Rev. 1:131-138; 2005. (Pubitemid 43074197)
69. O'Donnell, K. A.; Wentzel, E. A.; Zeller, K. I.; Dang, C. V.; Mendell, J. T. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435:839-843; 2005. (Pubitemid 40839736)
70. Smith, K. N.; Singh, A. M.; Dalton, S. Myc represses primitive endoderm differentiation in pluripotent stem cells. Cell Stem Cell 7:343-354; 2010.
71. Foshay, K. M.; Gallicano, G. I. miR-17 family miRNAs are expressed during early mammalian development and regulate stem cell differentiation. Dev. Biol 326:431-443; 2009.
72. Xu, N.; Papagiannakopoulos, T.; Pan, G.; Thomson, J. A.; Kosik, K. S. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137:647-658; 2009.
73. Otsubo, T.; Akiyama, Y.; Hashimoto, Y.; Shimada, S.; Goto, K.; Yuasa, Y. MicroRNA-126 inhibits SOX2 expression and contributes to gastric carcinogenesis. PLoS One 6:e16617; 2011.
74. Calatayud Maldonado, V.; Calatayud Perez, J. B.; Aso Escario, J. Effects of CDP-choline on the recovery of patients with head injury. J. Neurol. Sci. 103 (Suppl):S15-18; 1991.
75. Lin, S. L.; Chang, D. C.; Lin, C. H.; Ying, S. Y.; Leu, D.; Wu, D. T. S. Regulation of somatic cell reprogramming through inducible mir-302 expression. Nucleic Acids Res. 39:1054-1065; 2011.
76. Miyoshi, N.; Ishii, H.; Nagano, H.; Haraguchi, N.; Dewi, D. L.; Kano, Y.; Nishikawa, S.; Tanemura, M.; Mimori, K.; Tanaka, F.; Saito, T.; Nishimura, J.; Takemasa, I.; Mizushima, T.; Ikeda, M.; Yamamoto, H.; Sekimoto, M.; Doki, Y.; Mori, M. Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell 8:633-638; 2011.
77. Kane, N. M.; Meloni, M.; Spencer, H. L.; Craig, M. A.; Strehl, R.; Milligan, G.; Houslay, M. D.; Mountford, J. C.; Emanueli, C.; Baker, A. H. 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.
78. Bonauer, A.; Dimmeler, S. The microRNA-17-92 cluster: still a miracle? Cell Cycle 8:3866-3873; 2009.
79. Treguer, K.; Heinrich, E. M.; Ohtani, K.; Bonauer, A.; Dimmeler, S. Role of the microRNA-17-92 cluster in the endothelial differentiation of stem cells. J. Vasc. Res. 49:447-460; 2012.
80. Howard, L.; Kane, N. M.; Milligan, G.; Baker, A. H. MicroRNAs regulating cell pluripotency and vascular differentiation. Vasc. Pharmacol 55:69-78; 2011.
81. Kong, Y. W.; Ferland-McCollough, D.; Jackson, T. J.; Bushell, M. microRNAs in cancer management. Lancet Oncol. 13:e249-e258; 2012.
82. Fichtlscherer, S.; De Rosa, S.; Fox, H.; Schwietz, T.; Fischer, A.; Liebetrau, C.; Weber, M.; Hamm, C. W.; Roxe, T.; Muller-Ardogan, M.; Bonauer, A.; Zeiher, A. M.; Dimmeler, S. Circulating microRNAs in patients with coronary artery disease. Circ. Res. 107:677-684; 2010.
83. McDonald, R. A.; Hata, A.; MacLean, M. R.; Morrell, N. W.; Baker, A. H. MicroRNA and vascular remodelling in acute vascular injury and pulmonary vascular remodelling. Cardiovasc. Res. 93:594-604; 2012.
84. Rhee, S. G. Redox signaling: hydrogen peroxide as intracellular messenger. Exp. Mol. Med. 31:53-59; 1999. (Pubitemid 29326708)
85. Luczak, K.; Balcerczyk, A.; Soszynski, M.; Bartosz, G. Low concentration of oxidant and nitric oxide donors stimulate proliferation of human endothelial cells in vitro. Cell Biol. Int 28:483-486; 2004. (Pubitemid 38833656)
86. Tojo, T.; Ushio-Fukai, M.; Yamaoka-Tojo, M.; Ikeda, S.; Patrushev, N.; Alexander, R. W. Role of gp91phox (Nox2)-containing NAD(P)H oxidase in angiogenesis in response to hindlimb ischemia. Circulation 111: 2347-2355; 2005. (Pubitemid 40647071)
87. West, X. Z.; Malinin, N. L.; Merkulova, A. A.; Tischenko, M.; Kerr, B. A.; Borden, E. C.; Podrez, E. A.; Salomon, R. G.; Byzova, T. V. Oxidative stress induces angiogenesis by activating TLR2 with novel endogenous ligands. Nature 467:972-976; 2010.
88. Case, J.; Ingram, D. A.; Haneline, L. S. Oxidative stress impairs endothelial progenitor cell function. Antioxid. Redox Signaling 10:1895-1907; 2008.
89. Ushio-Fukai, M.; Urao, N. Novel role of NADPH oxidase in angiogenesis and stem/progenitor cell function. Antioxid. Redox Signaling 11: 2517-2533; 2009.
90. Geiszt, M. NADPH oxidases: new kids on the block. Cardiovasc. Res. 71:289-299; 2006.
91. Ushio-Fukai, M.; Alexander, R. W. Reactive oxygen species as mediators of angiogenesis signaling - role of NAD(P)H oxidase. Mol. Cell. Biochem 264:85-97; 2004. (Pubitemid 39366107)
92. Shilo, S.; Roy, S.; Khanna, S.; Sen, C. K. Evidence for the involvement of miRNA in redox regulated angiogenic response of human microvascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 28:471-477; 2008.
93. Fu, Y. B.; Zhang, Y.; Wang, Z. Y.; Wang, L. L.; Wei, X. B.; Zhang, B.; Wen, Z. Q.; Fang, H.; Pang, Q.; Yi, F. Regulation of NADPH oxidase activity is associated with miRNA-25-mediated NOX4 expression in experimental diabetic nephropathy. Am. J. Nephrol. 32:581-589; 2010.
94. Zhang, X.; Ng, W. L.; Wang, P.; Tian, L.; Werner, E.; Wang, H.; Doetsch, P.; Wang, Y. MicroRNA-21 modulates the levels of reactive oxygen species by targeting SOD3 and TNFalpha. Cancer Res. 72:4707-4713; 2012.
95. Ji, A. R.; Ku, S. Y.; Cho, M. S.; Kim, Y. Y.; Kim, Y. J.; Oh, S. K.; Kim, S. H.; Moon, S. Y.; Choi, Y. M. Reactive oxygen species enhance differentiation of human embryonic stem cells into mesendodermal lineage. Exp. Mol. Med. 42: 175-186; 2010.
96. Sauer, H.; Bekhite, M. M.; Hescheler, J.; Wartenberg, M. Redox control of angiogenic factors and CD31-positive vessel-like structures in mouse embryonic stem cells after direct current electrical field stimulation. Exp. Cell Res 304:380-390; 2005. (Pubitemid 40321117)
97. Schmelter, M.; Ateghang, B.; Helmig, S.; Wartenberg, M.; Sauer, H. Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-induced cardiovascular differentiation. FASEB J 20:1182-1184; 2006.
98. Lange, S.; Heger, J.; Euler, G.; Wartenberg, M.; Piper, H. M.; Sauer, H. Platelet-derived growth factor BB stimulates vasculogenesis of embryonic stem cell-derived endothelial cells by calcium-mediated generation of reactive oxygen species. Cardiovasc. Res. 81:159-168; 2009.
99. Magenta, A.; Cencioni, C.; Fasanaro, P.; Zaccagnini, G.; Greco, S.; Sarra-Ferraris, G.; Antonini, A.; Martelli, F.; Capogrossi, M. C. miR-200c is upregulated by oxidative stress and induces endothelial cell apoptosis and senescence via ZEB1 inhibition. Cell Death Differ. 18:1628-1639; 2011.
100. Fong, C. Y.; Gauthaman, K.; Bongso, A. Teratomas from pluripotent stem cells: a clinical hurdle. J. Cell. Biochem. 111: 769-781; 2010.