Molecular Pathways Governing Development of Vascular Endothelial Cells from ES/iPS Cells

Stem Cell Reviews and Reports

Volumn 9, Issue 5, 2013, Pages 586-598

  Tan, Keai Sinn ^a,b   Tamura, Kiyomi ^c   Lai, Mei I ^b   Veerakumarasivam, Abhimanyu ^b,d   Nakanishi, Yoichi ^a   Ogawa, Minetaro ^c   Sugiyama, Daisuke ^a  

^a KYUSHU UNIVERSITY HOSPITAL   (Japan)

^b UNIVERSITY PUTRA MALAYSIA   (Malaysia)

^c KUMAMOTO UNIVERSITY   (Japan)

^d PERDANA UNIVERSITY   (Malaysia)

Author keywords

Differentiation; Embryonic stem cells; Endothelial cells; Induced pluripotent stem cells; Molecular pathways

Indexed keywords

IPS;

ARTICLE; BLOOD VESSEL; CELL DIFFERENTIATION; CYTOLOGY; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PLURIPOTENT STEM CELL; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER;

BLOOD VESSELS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MYOCYTES, SMOOTH MUSCLE; SIGNAL TRANSDUCTION;

EID: 84884812307     PISSN: 15508943     EISSN: 15586804     Source Type: Journal    
DOI: 10.1007/s12015-013-9450-7     Document Type: Article

References (105)

1. Patan, S. (2001). Vasculogenesis and angiogenesis as mechanisms of vascular network formation, growth and remodeling. Journal of Neuro-Oncology, 50(1-2), 1-15.
2. Benedito, R., Trindade, A., Hirashima, M., Henrique, D., da Costa, L. L., Rossant, J., et al. (2008). Loss of Notch signalling induced by Dll4 causes arterial calibre reduction by increasing endothelial cell response to angiogenic stimuli. BMC Developmental Biology, 8(117), 1-15.
3. Wang, H. U., Chen, Z. F., & Anderson, D. J. (1998). Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell, 93(5), 741-753.
4. Chong, D. C., Koo, Y., Xu, K., Fu, S., & Cleaver, O. (2011). Stepwise arteriovenous fate acquisition during mammalian vasculogenesis. Developmental Dynamics, 240(9), 2153-2165.
5. Hamada, K., Oike, Y., Ito, Y., Maekawa, H., Miyata, K., Shimomura, T., et al. (2003). Distinct roles of ephrin-B2 forward and EphB4 reverse signaling in endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology, 23(2), 190-197.
6. Choi, K., Yu, J., Smuga-Otto, K., Salvagiotto, G., Rehrauer, W., Vodyanik, M., et al. (2009). Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells, 27, 559-567.
7. Moyon, D., Pardanaud, L., Yuan, L., Breant, C., & Eichmann, A. (2001). Plasticity of endothelial cells during arterial-venous differentiation in the avian embryo. Development, 128, 3359-3370.
8. Lawson, N. D., Vogel, A. M., & Weinstein, B. M. (2002). Sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Developmental Cell, 3(1), 127-136.
9. Liu, Z., Shirakawa, T., Li, Y., Soma, A., Oka, M., Dotto, G. P., et al. (2003). Regulation of Notch1 and Dll4 by vascular endothelial growth factor in arterial endothelial cells: implications for modulating arteriogenesis and angiogenesis. Molecular and Cellular Biology, 23(1), 14-25.
10. Risau, W., Sariola, H., Zerwes, H. G., Sasse, J., Ekblom, P., Kemler, R., et al. (1988). Vasculogenesis and angiogenesis in embryonic-stem-cell-derived embryoid bodies. Development, 102(3), 471-478.
11. Walthall, S. L., Moses, M., & Horabin, J. I. (2007). A large complex containing patched and smoothened initiates hedgehog signaling in drosophila. Journal of Cell Science, 120(Pt 5), 826-837.
12. Chen, Y., & Struhl, G. (1996). Dual roles for patched in sequestering and transducing hedgehog. Cell, 87(3), 553-563.
13. Kanda, S., Mochizuki, Y., Suematsu, T., Miyata, Y., Nomata, K., & Kanetake, H. (2003). Sonic hedgehog induces capillary morphogenesis by endothelial cells through phosphoinositide 3-kinase. The Journal of Biological Chemistry, 278(10), 8244-8249.
14. Wilkinson, R. N., Koudijs, M. J., Patient, R. K., Ingham, P. W., Schulte-Merker, S., & van Eeden, F. J. (2012). Hedgehog signaling via a calcitonin receptor-like receptor can induce arterial differentiation independently of VEGF signaling in zebrafish. Blood, 120(2), 477-488.
15. Li, X., & Eriksson, U. (2011). Novel VEGF family members: VEGF-B, VEGF-C and VEGF-D. The International Journal of Biochemistry & Cell Biology, 33(4), 421-426.
16. Lanahan, A. A., Hermans, K., Claes, F., Kerley-Hamilton, J. S., Zhuang, Z. W., Giordano, F. J., et al. (2010). VEGF receptor 2 endocytic trafficking regulates arterial morphogenesis. Developmental Cell, 18(5), 713-724.
17. Petrova, T. V., Makinen, T., & Alitalo, K. (1999). Signaling via vascular endothelial growth factor receptors. Experimental Cell Research, 253(1), 117-130.
18. Shima, D. T., Kuroki, M., Deutsch, U., Ng, Y., Adamis, A. P., & Amore, P. A. D. (1996). The mouse gene for vascular endothelial growth factor. Genomic structure, definition of the transcriptional unit, and characterization of transcriptional and post-transcriptional regulatory sequences. The Journal of Biological Chemistry, 271(7), 3877-3883.
19. Tischer, E., Mitchell, R., Hartman, T., Silva, M., Gospodarowiczs, D., Fiddes, J. C., et al. (1991). The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. The Journal of Biological Chemistry, 266(18), 11947-11954.
20. Ng, Y., Rohan, R., Sunday, M. E., Demello, D. E., & Amore, P. A. D. (2001). Differential expression of VEGF isoforms in mouse during development and in the adult. Developmental Dynamics, 220, 112-121.
21. Stalmans, I., Ng, Y., Rohan, R., Fruttiger, M., Bouché, A., Ÿuce, A., et al. (2002). Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. The Journal of Clinical Investigation, 109(3), 327-336.
22. Lai, E. C. (2004). Notch signaling: control of cell communication and cell fate. Development, 131(5), 965-973.
23. Fischer, A., Schumacher, N., Maier, M., Sendtner, M., & Gessler, M. (2004). The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes & Development, 18(8), 901-911.
24. Kokubo, H., Miyagawa-Tomita, S., Nakazawa, M., Saga, Y., & Johnson, R. L. (2005). Mouse hesr1 and hesr2 genes are redundantly required to mediate Notch signaling in the developing cardiovascular system. Developmental Biology, 278(2), 301-309.
25. Iso, T., Hamamori, Y., & Kedes, L. (2003). Notch signaling in vascular development. Arteriosclerosis, Thrombosis, and Vascular Biology, 23(4), 543-553.
26. Villa, N., Walker, L., Lindsell, C. E., Gasson, J., Iruela-Arispe, M. L., & Weinmaster, G. (2001). Vascular expression of Notch pathway receptors and ligands is restricted to arterial vessels. Mechanisms of Development, 108(1-2), 161-164.
27. Shutter, J. R., Scully, S., Fan, W., Richards, W. G., Kitajewski, J., Deblandre, G. A., et al. (2000). Dll4, a novel Notch ligand expressed in arterial endothelium. Genes & Development, 14(11), 1313-1318.
28. Liu, Z. J., Shirakawa, T., Li, Y., Soma, A., Oka, M., Dotto, G. P., et al. (2003). Regulation of Notch1 and Dll4 by vascular endothelial growth factor in arterial endothelial cells: implications for modulating arteriogenesis and angiogenesis. Molecular Cell. Biology, 23(1), 14-25.
29. Hong, C. C., Peterson, Q. P., Hong, J. Y., & Peterson, R. T. (2006). Artery/vein specification is governed by opposing phosphatidylinositol-3 kinase and MAP kinase/ERK signaling. Current Biology, 16(13), 1366-1372.
30. Hayashi, H., & Kume, T. (2008). Foxc transcription factors directly regulate Dll4 and Hey2 expression by interacting with the VEGF-Notch signaling pathways in endothelial cells. PLoS One, 3(6), e2401.
31. Gessler, M., Knobeloch, K. P., Helisch, A., Amann, K., Schumacher, N., Rohde, E., et al. (2002). Mouse gridlock: no aortic coarctation or deficiency, but fatal cardiac defects in Hey2 -/- mice. Current Biology, 12(18), 1601-1604.
32. Donovan, J., Kordylewska, A., Jan, Y. N., & Utset, M. F. (2002). Tetralogy of fallot and other congenital heart defects in Hey2 mutant mice. Current Biology, 12(18), 1605-1610.
33. Sakata, Y., Kamei, Y. C. N., Nakagami, H., Bronson, R., Liao, J. K., & Chin, M. T. (2002). Ventricular septal defect and cardiomyopathy in mice lacking the transcription factor CHF1/Hey2. Proceedings of the National Academy of Sciences of the United States of America, 99(25), 16197-16202.
34. Diez, H., Fischer, A., Winkler, A., Hu, C.-J., Hatzopoulos, A. K., Breier, G., et al. (2007). Hypoxia-mediated activation of Dll4-Notch-Hey2 signaling in endothelial progenitor cells and adoption of arterial cell fate. Experimental Cell Research, 313(1), 1-9.
35. You, L., Lin, F., Lee, C. T., DeMayo, F. J., Tsai, M., & Tsai, S. Y. (2005). Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature Biotechnology, 435, 98-104.
36. Lee, C. T. (2005). Loss of the nuclear orphan receptor COUP-TFII results in the formation of arteriovenous malformations. University of Alberta Health Sciences Journal, 2(2), 3-6.
37. Bach, T. L., Barsigian, C., Chalupowicz, D. G., Busler, D., Yaen, C. H., Grant, D. S., et al. (1998). VE-Cadherin mediates endothelial cell capillary tube formation in fibrin and collagen gels. Experimental Cell Research, 238(2), 324-334.
38. Fung, Y. C. (1969). Blood flow in the capillary bed. Journal of Biomechanics, 2(4), 353-372.
39. Ross, M. H., & Pawlina, W. (2010). Histology: A text and atlas. Baltimore: Wolters Kluwer.
40. Svistounov, D., Zykova, S. N., Cogger, V. C., Warren, A., McMahon, A. C., Fraser, R., et al. (2012). In P. R. Kelishadi (Ed.), Liver sinusoidal endothelial cells and regulation of blood lipoproteins, in dyslipidemia - from prevention to treatment, InTech.
41. Svistounov, D., Warren, A., McNerney, G. P., Owen, D. M., Zencak, D., Zykova, S. N., et al. (2012). The relationship between fenestrations, sieve plates and rafts in liver sinusoidal endothelial cells. PloS One, 7(9), e46134.
42. Ding, B., Nolan, D. J., Butler, J. M., James, D., Alexander, O., Rosenwaks, Z., et al. (2010). Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature, 468(7321), 310-315.
43. Gordon, E. J., Gale, N. W., & Harvey, N. L. (2008). Expression of the hyaluronan receptor LYVE-1 is not restricted to the lymphatic vasculature; LYVE-1 is also expressed on embryonic blood vessels. Developmental Dynamics, 237(7), 1901-1909.
44. Mouta Carreira, C., Nasser, S. M., di Tomaso, E., Padera, T. P., Boucher, Y., Tomarev, S. I., et al. (2001). LYVE-1 is not restricted to the lymph vessels: expression in normal liver blood sinusoids and down-regulation in human liver cancer and cirrhosis. Cancer Research, 61(22), 8079-8084.
45. Glienke, J., Sturz, A., Menrad, A., & Thierauch, K. H. (2002). CRIM1 is involved in endothelial cell capillary formation in vitro and is expressed in blood vessels in vivo. Mechanisms of Development, 119(2), 165-175.
46. Zhou, Q., Heinke, J., Vargas, A., Winnik, S., Krauss, T., Bode, C., et al. (2007). ERK signaling is a central regulator for BMP-4 dependent capillary sprouting. Cardiovascular Research, 76(3), 390-399.
47. Oliver, G., & Srinivasan, R. S. (2010). Endothelial cell plasticity: how to become and remain a lymphatic endothelial cell. Development (Cambridge, England), 137(3), 363-372.
48. Pepper, M. S., & Skobe, M. (2003). Lymphatic endothelium: morphological, molecular and functional properties. The Journal of Cell Biology, 163(2), 209-213.
49. Wang, Y., & Oliver, G. (2010). Current views on the function of the lymphatic vasculature in health and disease. Genes & Development, 24(19), 2115-2126.
50. Srinivasan, R. S., Dillard, M. E., Lagutin, O. V., Lin, F., Tsai, S., Tsai, M., et al. (2007). Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes & Development, 21(19), 2422-2432.
51. François, M., Caprini, A., Hosking, B., Orsenigo, F., Wilhelm, D., Browne, C., et al. (2008). Sox18 induces development of the lymphatic vasculature in mice. Nature, 456(7222), 643-647.
52. Yang, Y., García-Verdugo, J. M., Soriano-Navarro, M., Srinivasan, R. S., Scallan, J. P., Singh, M. K., et al. (2012). Lymphatic endothelial progenitors bud from the cardinal vein and intersomitic vessels in mammalian embryos. Blood, 120(11), 2340-2348.
53. Karkkainen, M. J., Haiko, P., Sainio, K., Partanen, J., Taipale, J., Petrova, T. V., et al. (2004). Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nature Immunology, 5(1), 74-80.
54. Srinivasan, R. S., Geng, X., Yang, Y., Wang, Y., Mukatira, S., Studer, M., et al. (2010). The nuclear hormone receptor Coup-TFII is required for the initiation and early maintenance of Prox1 expression in lymphatic endothelial cells. Genes & Development, 24(7), 696-707.
55. Yamazaki, T., Yoshimatsu, Y., Morishita, Y., Miyazono, K., & Watabe, T. (2009). COUP-TFII regulates the functions of Prox1 in lymphatic endothelial cells through direct interaction. Genes to Cells: Devoted to Molecular and Cellular Mechanisms, 14(3), 425-434.
56. Tsuji-Tamura, K., Sakamoto, H., & Ogawa, M. (2011). ES cell differentiation as a model to study cell biological regulation of vascular development. In C. Atwood (Ed.), Embryonic stem cells: The hormonal regulation of pluripotency and embryogenesis (pp. 581-606). Vienna: INTECH.
57. Bai, H., & Wang, Z. Z. (2008). Directing human embryonic stem cells to generate vascular progenitor cells generation of blood vessels from hESC. Gene Therapy, 15(89-95).
58. Kane, N. M., Xiao, Q., Baker, A. H., Luo, Z., Xu, Q., & Emanueli, C. (2011). Pluripotent stem cell differentiation into vascular cells: a novel technology with promises for vascular re(generation). Pharmacological Therapy, 129(1), 29-49.
59. Yamamizu, K., Matsunaga, T., Katayama, S., Kataoka, H., Takayama, N., Eto, K., et al. (2012). PKA/CREB signaling triggers initiation of endothelial and hematopoietic cell differentiation via Etv2 induction. Stem Cells, 30(4), 687-696.
60. Rungarunlert, S., Techakumphu, M., Pirity, M. K., & Dinnyes, A. (2009). Embryoid body formation from embryonic and induced pluripotent stem cells. Benefits of Bioreactors, 1(1), 11-21.
61. Kurosawa, H. (2007). Methods for inducing embryoid body formation: in vitro differentiation system of embryonic stem cells. Journal of Bioscience and Bioengineering, 103(5), 389-398.
62. Vittet, D., Prandini, M. H., Berthier, R., Schweitzer, A., Martin-Sisteron, H., Uzan, G., et al. (1996). Embryonic stem cells differentiate in vitro to endothelial cells through successive maturation steps. Blood, 88(9), 3424-3431.
63. Niwa, H., Ogawa, K., Shimosato, D., & Adachi, K. (2009). A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells. Nature Biotechnology, 460, 118-122.
64. Doetschman, T. C., Eistetter, H., Katz, M., Schmidt, W., & Kemler, R. (1985). The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. Journal of Embryology and Experimental Morphology, 87, 27-45.
65. Kim, G. D., Kim, G. J., Seok, J. H., Chung, H. M., Chee, K. M., & Rhee, G. S. (2008). Differentiation of endothelial cells derived from mouse embryoid bodies: a possible in vitro vasculogenesis model. Toxicology Letter, 180(3), 166-173.
66. Trivier, E., Kurz, D. J., Hong, Y., Huang, H. L., & Erusalimsky, J. D. (2004). Differential regulation of telomerase in endothelial cells by fibroblast growth factor-2 and vascular endothelial growth factor-a: association with replicative life span. Annals of the New York Academy of Sciences, 1019, 111-115.
67. Vittet, D., Buchou, T., Schweitzer, A., Dejana, E., & Huber, P. (1997). Targeted null-mutation in the vascular endothelial-cadherin gene impairs the organization of vascular-like structures in embryoid bodies. Proceedings of the National Academy of Sciences of the United States of America, 94, 6273-6278.
68. Yamaguchi, T. P., Dumont, D. J., Conlon, R. A., Breitman, M. L., & Rossant, J. (1993). flk-1, an flt-related receptor tyrosine kinase is an early marker for endothelial cell precursors. Development, 118(2), 489-498.
69. Itskovitz-Eldor, J., Schuldiner, M., Karsenti, D., Eden, A., Yanuka, O., Amit, M., et al. (2000). Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Molecular Medicine (Cambridge, Mass.), 6(2), 88-95.
70. Levenberg, S., Huang, N. F., Lavik, E., Rogers, A. B., Itskovitz-Eldor, J., & Langer, R. (2003). Differentiation of human embryonic stem cells on three-dimensional polymer scaffolds. Proceedings of the National Academy of Sciences, 100(22)), 12741-12746.
71. Levenberg, S., Zoldan, J., Basevitch, Y., & Langer, R. (2007). Endothelial potential of human embryonic stem cells. Blood, 110(3), 806-814.
72. Wang, L., Li, L., Shojaei, F., Levac, K., Cerdan, C., Menendez, P., et al. (2004). Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity, 21(1), 31-41.
73. Levenberg, S., Golub, J. S., Amit, M., Itskovitz-eldor, J., & Langer, R. (2002). Endothelial cells derived from human embryonic stem cells. Proceedings of the National Academic of Sciences, 99(7), 4391-4396.
74. James, D., Nam, H., Seandel, M., Nolan, D., Janovitz, T., Tomishima, M., et al. (2010). Expansion and maintenance of human embryonic stem cell - derived endothelial cells by TGFb inhibition is Id1 dependent. Nature Biotechnology, 28(2), 161-167.
75. Yamashita, J., Itoh, H., Hirashima, M., Ogawa, M., Nishikawa, S., Yurugi, T., et al. (2000). Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature, 408, 92-96.
76. Li, Z., Wu, J. C., Sheikh, A. Y., Kraft, D., Cao, F., Xie, X., et al. (2007). Differentiation, survival, and function of embryonic stem cell derived endothelial cells for ischemic heart disease. Circulation, 116(11), I46-I54.
77. Wary, K. K., Thakker, G. D., Humtsoe, J. O., & Yang, J. (2003). Analysis of VEGF-responsive genes involved in the activation of endothelial cells. Molecular Cancer, 2(25), 1-12.
78. Park, S. H., Sakamoto, H., Tsuji-Tamura, K., Furuyama, T., & Ogawa, M. (2009). Foxo1 is essential for in vitro vascular formation from embryonic stem cells. Biochemical and Biophysical Research Communications, 390(3), 861-866.
79. Thomson, J. A., Kalishman, J., Golos, T. G., Durning, M., Harris, C. P., Becker, R. A., et al. (1995). Isolation of a primate embryonic stem cell line. Proceedings of the National Academy of Sciences of the United States of America, 92(17), 7844-7848.
80. Sone, M., Itoh, H., Yamashita, J., Yurugi-Kobayashi, T., Suzuki, Y., Kondo, Y., et al. (2003). Different differentiation kinetics of vascular progenitor cells in primate and mouse embryonic stem cells. Circulation, 107(16), 2085-2088.
81. Sone, M., Itoh, H., Yamahara, K., Yamashita, J. K., Yurugi-Kobayashi, T., Nonoguchi, A., et al. (2007). Pathway for differentiation of human embryonic stem cells to vascular cell components and their potential for vascular regeneration. Arteriosclerosis, Thrombosis, and Vascular Biology, 10, 2127-2134.
82. Gerecht-Nir, S., Ziskind, A., Cohen, S., & Itskovitz-Eldor, J. (2003). Human embryonic stem cells as an in vitro model for human vascular development and the induction of vascular differentiation. Laboratory Investigation, 83(12), 1811-1120.
83. Yamamizu, K., & Yamashita, J. K. (2011). Roles of cyclic adenosine monophosphate signaling in endothelial cell differentiation and arterial-venous specification during vascular development. Circulation Journal, 75(2), 253-260.
84. Zhu, P., Huang, L., Ge, X., Yan, F., Wu, R., & Ao, Q. (2006). Transdifferentiation of pulmonary arteriolar endothelial cells into smooth muscle-like cells regulated by myocardin involved in hypoxia-induced pulmonary vascular remodelling. International Journal of Experimental Pathology, 87(6), 463-474.
85. Marchetti, S., Gimond, C., Iljin, K., Bourcier, C., Alitalo, K., Pouysségur, J., et al. (2002). Endothelial cells genetically selected from differentiating mouse embryonic stem cells incorporate at sites of neovascularization in vivo. Journal of Cell Science, 115(Pt 10), 2075-2085.
86. Niwa, A., Umeda, K., Chang, H., Saito, M., Okita, K., Takahashi, K., et al. (2009). Orderly hematopoietic development of induced pluripotent stem cells via Flk-1(+) hemoangiogenic progenitors. Journal of Cellular Physiology, 221(2), 367-377.
87. Joo, H. J., Kim, H., Park, S. W., Cho, H. J., Kim, H. S., Lim, D. S., et al. (2011). Angiopoietin-1 promotes endothelial differentiation from embryonic stem cells and induced pluripotent stem cells. Blood, 118(8), 2094-2101.
88. Suzuki, H., Shibata, R., Kito, T., Ishii, M., Li, P., Yoshikai, T., et al. (2010). Therapeutic angiogenesis by transplantation of induced pluripotent stem cell-derived Flk-1 positive cells. BMC Cell Biology, 11(72), 1-10.
89. Narazaki, G., Uosaki, H., Teranishi, M., Okita, K., Kim, B., Matsuoka, S., et al. (2008). Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation, 118(5), 498-506.
90. Taura, D., Sone, M., Homma, K., Oyamada, N., Takahashi, K., Tamura, N., et al. (2009). Induction and isolation of vascular cells from human induced pluripotent stem cells-brief report. Arteriosclerosis, Thrombosis, and Vascular Biology, 29(7), 1100-1103.
91. Yu, J., Vodyanik, M. A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J. L., Tian, S., et al. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science (New York, N. Y.), 318(5858), 1917-1920.
92. Byrd, N., Becker, S., Maye, P., Narasimhaiah, R., St-Jacques, B., Zhang, X., et al. (2002). Hedgehog is required for murine yolk sac angiogenesis. Development, 129(2), 361-372.
93. Kelly, M. A., & Hirschi, K. K. (2009). Signaling hierarchy regulating human endothelial cell development. Arteriosclerosis, Thrombosis, and Vascular Biology, 29(5), 718-724.
94. Boyd, N. L., Dhara, S. K., Rekaya, R., Godbey, E. A., Hasneen, K., Rao, R. R., et al. (2007). BMP4 promotes formation of primitive vascular networks in human embryonic stem cell-derived embryoid bodies. Experimental Biology and Medicine (Maywood), 232(6), 833-843.
95. Banerjee, S., Dhara, S. K., & Bacanamwo, M. (2012). Endoglin is a novel endothelial cell specification gene. Stem Cell Research, 8(1), 85-96.
96. Li, D. Y., Sorensen, L. K., Brooke, B. S., Urness, L. D., Davis, E. C., Taylor, D. G., et al. (1999). Defective angiogenesis in mice lacking endoglin. Science, 284(5419), 1534-1537.
97. Carvalho, R. L., Jonker, L., Goumans, M. J., Larsson, J., Bouwman, P., Karlsson, S., et al. (2004). Defective paracrine signalling by TGFbeta in yolk sac vasculature of endoglin mutant mice: a paradigm for hereditary haemorrhagic telangiectasia. Development, 131(24)), 6237-6247.
98. Lanner, F., Sohl, M., & Farnebo, F. (2007). Functional arterial and venous fate is determined by graded VEGF signaling and notch status during embryonic stem cell differentiation. Arteriosclerosis, Thrombosis, and Vascular Biology, 27(3), 487-493.
99. Yurugi-Kobayashi, T., Itoh, H., Schroeder, T., Nakano, A., Narazaki, G., Kita, F., et al. (2006). Adrenomedullin/cyclic AMP pathway induces Notch activation and differentiation of arterial endothelial cells from vascular progenitors. Arteriosclerosis, Thrombosis, and Vascular Biology, 26(9), 1977-1984.
100. Masumura, T., Yamamoto, K., Shimizu, N., Obi, S., & Ando, J. (2009). Shear stress increases expression of the arterial endothelial marker ephrinB2 in murine ES cells via the VEGF-Notch signaling pathways. Arteriosclerosis, Thrombosis, and Vascular Biology, 29(12), 2125-2131.
101. Era, T., Izumi, N., Hayashi, M., Tada, S., Nishikawa, S., & Nishikawa, S. (2008). Multiple mesoderm subsets give rise to endothelial cells, whereas hematopoietic cells are differentiated only from a restricted subset in embryonic stem cell differentiation culture. Stem Cells, 26(2), 401-411.
102. Chiang, P. M., & Wong, P. C. (2011). Differentiation of an embryonic stem cell to hemogenic endothelium by defined factors: essential role of bone morphogenetic protein 4. Development, 138(13), 2833-2843.
103. Harada, K., Yamazaki, T., Iwata, C., Yoshimatsu, Y., Sase, H., Mishima, K., et al. (2009). Identification of targets of Prox1 during in vitro vascular differentiation from embryonic stem cells: functional roles of HoxD8 in lymphangiogenesis. Journal of Cell Science, 122(Pt 21), 3923-3930.
104. Sasaki, T., Mizuochi, C., Horio, Y., Nakao, K., Akashi, K., & Sugiyama, D. (2010). Regulation of hematopoietic cell clusters in the placental niche through SCF/Kit signaling in embryonic mouse. Development, 137(23), 3941-3952.
105. Sugiyama, D., Kulkeaw, K., & Mizuochi, C. (2012). TGF-beta-1 up-regulates extra-cellular matrix production in mouse hepatoblasts. Mechanisms of Development, 30(2-3), 195-206.