Endothelial heterogeneity in the umbilico-placental unit: DNA methylation as an innuendo of epigenetic diversity

Frontiers in Pharmacology

Volumn 5 MAR, Issue , 2014, Pages

  Casanello, Paola ^a   Schneider, Daniela ^a   Herrera, Emilio A ^b   Uauy, Ricardo ^a   Krause, Bernardo J ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

Author keywords

Artery; Endothelial; Epigenetics; Placenta; Umbilical; Vein

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN 1; FIBROBLAST GROWTH FACTOR 2; HISTONE DEACETYLASE; HISTONE LYSINE METHYLTRANSFERASE; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN; VASCULOTROPIN A; VON WILLEBRAND FACTOR;

ANGIOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN STRUCTURE; DNA METHYLATION; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM; ENDOTHELIUM CELL; ENZYME ACTIVITY; EPIGENETICS; GENE EXPRESSION; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; MICROCIRCULATION; PHENOTYPE; PLACENTA; PROTEIN EXPRESSION; PROTEIN PROCESSING; REVIEW; UMBILICAL VEIN ENDOTHELIAL CELL; UMBILICUS;

EID: 84897952664     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2014.00049     Document Type: Review

References (97)

1. Aird, W. C. (2012). Endothelial cell heterogeneity. Cold Spring Harb. Perspect. Med. 2:a006429. doi: 10.1101/cshperspect.a006429.
2. Alexander, M. R., and Owens, G. K. (2012). Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annu. Rev. Physiol. 74, 13-40. doi: 10.1146/annurev-physiol-012110-142315.
3. Andersen, M. R., Simonsen, U., Uldbjerg, N., Aalkjaer, C., and Stender, S. (2009). Smoking cessation early in pregnancy and birth weight, length, head circumference, and endothelial nitric oxide synthase activity in umbilical and chorionic vessels: an observational study of healthy singleton pregnancies. Circulation 119, 857-864. doi: 10.1161/CIRCULATIONAHA.107.755769.
4. Aranguren, X. L., Agirre, X., Beerens, M., Coppiello, G., Uriz, M., Vandersmissen, I., et al. (2013). Unraveling a novel transcription factor code determining the human arterial-specific endothelial cell signature. Blood 122, 3982-3992. doi: 10.1182/blood-2013-02-483255.
5. Atkins, G. B., Jain, M. K., and Hamik, A. (2011). Endothelial differentiation: molecular mechanisms of specification and heterogeneity. Arterioscler. Thromb. Vasc. Biol. 31, 1476-1484. doi: 10.1161/ATVBAHA.111.228999.
6. Banerjee, S., and Bacanamwo, M. (2010). DNA methyltransferase inhibition induces mouse embryonic stem cell differentiation into endothelial cells. Exp. Cell Res. 316, 172-180. doi: 10.1016/j.yexcr.2009.08.011.
7. Barkefors, I., Le Jan, S., Jakobsson, L., Hejll, E., Carlson, G., Johansson, H., et al. (2008). Endothelial cell migration in stable gradients of vascular endothelial growth factor A and fibroblast growth factor 2: effects on chemotaxis and chemokinesis. J. Biol. Chem. 283, 13905-13912. doi: 10.1074/jbc.M704917200.
8. Brouillet, S., Hoffmann, P., Benharouga, M., Salomon, A., Schaal, J. P., Feige, J. J., et al. (2010). Molecular characterization of EG-VEGF-mediated angiogenesis: differential effects on microvascular and macrovascular endothelial cells. Mol. Biol. Cell 21, 2832-2843. doi: 10.1091/mbc.E10-01-0059.
9. Burton, G. J. (2009). Oxygen, the Janus gas; its effects on human placental development and function. J. Anat. 215, 27-35. doi: 10.1111/j.1469-7580.2008.00978.x.
10. Burton, G. J., Charnock-Jones, D. S., and Jauniaux, E. (2009). Regulation of vascular growth and function in the human placenta. Reproduction 138, 895-902. doi: 10.1530/REP-09-0092.
11. Buschmann, I., Pries, A., Styp-Rekowska, B., Hillmeister, P., Loufrani, L., Henrion, D., et al. (2010). Pulsatile shear and Gja5 modulate arterial identity and remodeling events during flow-driven arteriogenesis. Development 137, 2187-2196. doi: 10.1242/dev.045351.
12. Chaddha, V., Viero, S., Huppertz, B., and Kingdom, J. (2004). Developmental biology of the placenta and the origins of placental insufficiency. Semin. Fetal Neonatal Med. 9, 357-369. doi: 10.1016/j.siny.2004.03.006.
13. Chan, Y., Fish, J. E., D'abreo, C., Lin, S., Robb, G. B., Teichert, A. M., et al. (2004). The cell-specific expression of endothelial nitric-oxide synthase: a role for DNA methylation. J. Biol. Chem. 279, 35087-35100. doi: 10.1074/jbc.M405063200.
14. Chang, S., Young, B. D., Li, S., Qi, X., Richardson, J. A., and Olson, E. N. (2006). Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase 10. Cell 126, 321-334. doi: 10.1016/j.cell.2006.05.040.
15. Chen, S., Feng, B., George, B., Chakrabarti, R., Chen, M., and Chakrabarti, S. (2010). Transcriptional coactivator p300 regulates glucose-induced gene expression in endothelial cells. Am. J. Physiol. Endocrinol. Metab. 298, E127-E137. doi: 10.1152/ajpendo.00432.2009.
16. Coulet, F., Nadaud, S., Agrapart, M., and Soubrier, F. (2003). Identification of hypoxia-response element in the human endothelial nitric-oxide synthase gene promoter. J. Biol. Chem. 278, 46230-46240. doi: 10.1074/jbc.M305420200.
17. Demir, R., Seval, Y., and Huppertz, B. (2007). Vasculogenesis and angiogenesis in the early human placenta. Acta Histochem. 109, 257-265. doi: 10.1016/j.acthis.2007.02.008.
18. Dennery, P. A. (2010). Oxidative stress in development: nature or nurture? Free Radic. Biol. Med. 49, 1147-1151. doi: 10.1016/j.freeradbiomed.2010.07.011.
19. Deroanne, C. F., Bonjean, K., Servotte, S., Devy, L., Colige, A., Clausse, N., et al. (2002). Histone deacetylases inhibitors as anti-angiogenic agents altering vascular endothelial growth factor signaling. Oncogene 21, 427-436. doi: 10.1038/sj.onc.1205108.
20. Diehl, F., Rossig, L., Zeiher, A. M., Dimmeler, S., and Urbich, C. (2007). The histone methyltransferase MLL is an upstream regulator of endothelial-cell sprout formation. Blood 109, 1472-1478. doi: 10.1182/blood-2006-08-039651.
21. Dutta, D., Ray, S., Vivian, J. L., and Paul, S. (2008). Activation of the VEGFR1 chromatin domain: an angiogenic signal-ETS1/HIF-2alpha regulatory axis. J. Biol. Chem. 283, 25404-25413. doi: 10.1074/jbc.M804349200.
22. Egorova, A. D., Deruiter, M. C., De Boer, H. C., Van De Pas, S., Gittenberger-De Groot, A. C., Van Zonneveld, A. J., et al. (2012). Endothelial colony-forming cells show a mature transcriptional response to shear stress. In Vitro Cell. Dev. Biol. Anim. 48, 21-29. doi: 10.1007/s11626-011-9470-z.
23. El-Osta, A., Brasacchio, D., Yao, D., Pocai, A., Jones, P. L., Roeder, R. G., et al. (2008). Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J. Exp. Med. 205, 2409-2417. doi: 10.1084/jem.20081188.
24. Fish, J. E., and Marsden, P. A. (2006). Endothelial nitric oxide synthase: insight into cell-specific gene regulation in the vascular endothelium. Cell. Mol. Life Sci. 63, 144-162. doi: 10.1007/s00018-005-5421-8.
25. Fish, J. E., Matouk, C. C., Rachlis, A., Lin, S., Tai, S. C., D'abreo, C., et al. (2005). The expression of endothelial nitric-oxide synthase is controlled by a cell-specific histone code. J. Biol. Chem. 280, 24824-24838. doi: 10.1074/jbc.M502115200.
26. Fish, J. E., Matouk, C. C., Yeboah, E., Bevan, S. C., Khan, M., Patil, K., et al. (2007). Hypoxia-inducible expression of a natural cis-antisense transcript inhibits endothelial nitric-oxide synthase. J. Biol. Chem. 282, 15652-15666. doi: 10.1074/jbc.M608318200.
27. Fish, J. E., Yan, M. S., Matouk, C. C., St Bernard, R., Ho, J. J., Gavryushova, A., et al. (2010). Hypoxic repression of endothelial nitric-oxide synthase transcription is coupled with eviction of promoter histones. J. Biol. Chem. 285, 810-826. doi: 10.1074/jbc.M109.067868.
28. Fowden, A. L., Forhead, A. J., Coan, P. M., and Burton, G. J. (2008). The placenta and intrauterine programming. J. Neuroendocrinol. 20, 439-450. doi: 10.1111/j.1365-2826.2008.01663.x.
29. Freyer, C., and Renfree, M. B. (2009). The mammalian yolk sac placenta. J. Exp. Zool. B Mol. Dev. Evol. 312, 545-554. doi: 10.1002/jez.b.21239.
30. Gallicchio, M., Argyriou, S., Ianches, G., Filonzi, E. L., Zoellner, H., Hamilton, J. A., et al. (1994). Stimulation of PAI-1 expression in endothelial cells by cultured vascular smooth muscle cells. Arterioscler. Thromb. 14, 815-823. doi: 10.1161/01.ATV.14.5.815.
31. Gan, Y., Shen, Y. H., Wang, J., Wang, X., Utama, B., and Wang, X. L. (2005). Role of histone deacetylation in cell-specific expression of endothelial nitric-oxide synthase. J. Biol. Chem. 280, 16467-16475. doi: 10.1074/jbc.M412960200.
32. Gibney, E. R., and Nolan, C. M. (2010). Epigenetics and gene expression. Heredity (Edinb.) 105, 4-13. doi: 10.1038/hdy.2010.54.
33. Ha, C. H., Jhun, B. S., Kao, H. Y., and Jin, Z. G. (2008). VEGF stimulates HDAC7 phosphorylation and cytoplasmic accumulation modulating matrix metalloproteinase expression and angiogenesis. Arterioscler. Thromb. Vasc. Biol. 28, 1782-1788. doi: 10.1161/ATVBAHA.108.172528.
34. Hoffmann, J., Dimmeler, S., and Haendeler, J. (2003). Shear stress increases the amount of S-nitrosylated molecules in endothelial cells: important role for signal transduction. FEBS Lett. 551, 153-158. doi: 10.1016/S0014-5793(03)00917-7.
35. Illi, B., Nanni, S., Scopece, A., Farsetti, A., Biglioli, P., Capogrossi, M. C., et al. (2003). Shear stress-mediated chromatin remodeling provides molecular basis for flow-dependent regulation of gene expression. Circ. Res. 93, 155-161. doi: 10.1161/01.RES.0000080933.82105.29.
36. Illi, B., Scopece, A., Nanni, S., Farsetti, A., Morgante, L., Biglioli, P., et al. (2005). Epigenetic histone modification and cardiovascular lineage programming in mouse embryonic stem cells exposed to laminar shear stress. Circ. Res. 96, 501-508. doi: 10.1161/01.RES.0000159181.06379.63.
37. Ito, M., Itakura, A., Ohno, Y., Nomura, M., Senga, T., Nagasaka, T., et al. (2002). Possible activation of the renin-angiotensin system in the feto-placental unit in preeclampsia. J. Clin. Endocrinol. Metab. 87, 1871-1878. doi: 10.1210/jcem.87.4.8422.
38. Jamaluddin, M. D., Chen, I., Yang, F., Jiang, X., Jan, M., Liu, X., et al. (2007). Homocysteine inhibits endothelial cell growth via DNA hypomethylation of the cyclin A gene. Blood 110, 3648-3655. doi: 10.1182/blood-2007-06-096701.
39. Jiang, Y. Z., Wang, K., Li, Y., Dai, C. F., Wang, P., Kendziorski, C., et al. (2013). Enhanced cellular responses and distinct gene profiles in human fetoplacental artery endothelial cells under chronic low oxygen. Biol. Reprod. 89, 133. doi: 10.1095/biolreprod.113.110551.
40. Jin, G., Bausch, D., Knightly, T., Liu, Z., Li, Y., Liu, B., et al. (2011). Histone deacetylase inhibitors enhance endothelial cell sprouting angiogenesis in vitro. Surgery 150, 429-435. doi: 10.1016/j.surg.2011.07.001.
41. Jin, S. W., and Patterson, C. (2009). The opening act: vasculogenesis and the origins of circulation. Arterioscler. Thromb. Vasc. Biol. 29, 623-629. doi: 10.1161/ATVBAHA.107.161539.
42. Joo, J. E., Hiden, U., Lassance, L., Gordon, L., Martino, D. J., Desoye, G., et al. (2013). Variable promoter methylation contributes to differential expression of key genes in human placenta-derived venous and arterial endothelial cells. BMC Genomics 14:475. doi: 10.1186/1471-2164-14-475.
43. Kaikkonen, M. U., Lam, M. T., and Glass, C. K. (2011). Non-coding RNAs as regulators of gene expression and epigenetics. Cardiovasc. Res. 90, 430-440. doi: 10.1093/cvr/cvr097.
44. Kanki, Y., Kohro, T., Jiang, S., Tsutsumi, S., Mimura, I., Suehiro, J., et al. (2011). Epigenetically coordinated GATA2 binding is necessary for endothelium-specific endomucin expression. EMBO J. 30, 2582-2595. doi: 10.1038/emboj.2011.173.
45. Kim, C. S., Kim, Y. R., Naqvi, A., Kumar, S., Hoffman, T. A., Jung, S. B., et al. (2011). Homocysteine promotes human endothelial cell dysfunction via site-specific epigenetic regulation of p66shc. Cardiovasc. Res. 92, 466-475. doi: 10.1093/cvr/cvr250.
46. Kim, J., Kim, J. Y., Song, K. S., Lee, Y. H., Seo, J. S., Jelinek, J., et al. (2007). Epigenetic changes in estrogen receptor beta gene in atherosclerotic cardiovascular tissues and in-vitro vascular senescence. Biochim. Biophys. Acta 1772, 72-80. doi: 10.1016/j.bbadis.2006.10.004.
47. Kim, M. S., Kwon, H. J., Lee, Y. M., Baek, J. H., Jang, J. E., Lee, S. W., et al. (2001). Histone deacetylases induce angiogenesis by negative regulation of tumor suppressor genes. Nat. Med. 7, 437-443. doi: 10.1038/86507.
48. Klose, R. J., and Bird, A. P. (2006). Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 31, 89-97. doi: 10.1016/j.tibs.2005.12.008.
49. Koch, S., and Claesson-Welsh, L. (2012). Signal transduction by vascular endothelial growth factor receptors. Cold Spring Harb. Perspect. Med. 2:a006502. doi: 10.1101/cshperspect.a006502.
50. Kohli, R. M., and Zhang, Y. (2013). TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502, 472-479. doi: 10.1038/nature12750.
51. Korten, S., Brunssen, C., Poitz, D. M., Grossklaus, S., Brux, M., Schnittler, H. J., et al. (2013). Impact of Hey2 and COUP-TFII on genes involved in arteriovenous differentiation in primary human arterial and venous endothelial cells. Basic Res. Cardiol. 108, 362. doi: 10.1007/s00395-013-0362-0.
52. Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128, 693-705. doi: 10.1016/j.cell.2007.02.005.
53. Krause, B., Sobrevia, L., and Casanello, P. (2009). Epigenetics: new concepts of old phenomena in vascular physiology. Curr. Vasc. Pharmacol. 7, 513-520. doi: 10.2174/157016109789043883.
54. Krause, B. J., Costello, P. M., Munoz-Urrutia, E., Lillycrop, K. A., Hanson, M. A., and Casanello, P. (2013). Role of DNA methyltransferase 1 on the altered eNOS expression in human umbilical endothelium from intrauterine growth restricted fetuses. Epigenetics 8, 944-952. doi: 10.4161/epi.25579.
55. Krause, B. J., Hanson, M. A., and Casanello, P. (2011). Role of nitric oxide in placental vascular development and function. Placenta 32:797-805. doi: 10.1016/j.placenta.2011.06.025.
56. Krause, B. J., Prieto, C. P., Munoz-Urrutia, E., Martin, S. S., Sobrevia, L., and Casanello, P. (2012). Role of arginase-2 and eNOS in the differential vascular reactivity and hypoxia-induced endothelial response in umbilical arteries and veins. Placenta 33:360-366. doi: 10.1016/j.placenta.2012.02.006.
57. Lagarkova, M. A., Shutova, M. V., Bogomazova, A. N., Vassina, E. M., Glazov, E. A., Zhang, P., et al. (2010). Induction of pluripotency in human endothelial cells resets epigenetic profile on genome scale. Cell Cycle 9, 937-946. doi: 10.4161/cc.9.5.10869.
58. Lagarkova, M. A., Volchkov, P. Y., Philonenko, E. S., and Kiselev, S. L. (2008). Efficient differentiation of hESCs into endothelial cells in vitro is secured by epigenetic changes. Cell Cycle 7, 2929-2935. doi: 10.4161/cc.7.18.6700.
59. Lang, I. (2003). Heterogeneity of microvascular endothelial cells isolated from human term placenta and macrovascular umbilical vein endothelial cells. Eur. J. Cell Biol. 82, 163-173. doi: 10.1078/0171-9335-00306.
60. Lang, I., Hartmann, M., Blaschitz, A., Dohr, G., Skofitsch, G., and Desoye, G. (1993). Immunohistochemical evidence for the heterogeneity of maternal and fetal vascular endothelial cells in human full-term placenta. Cell Tissue Res. 274, 211-218. doi: 10.1007/BF00318740.
61. Lang, I., Schweizer, A., Hiden, U., Ghaffari-Tabrizi, N., Hagendorfer, G., Bilban, M., et al. (2008). Human fetal placental endothelial cells have a mature arterial and a juvenile venous phenotype with adipogenic and osteogenic differentiation potential. Differentiation 76, 1031-1043. doi: 10.1111/j.1432-0436.2008.00302.x.
62. Lassance, L., Miedl, H., Konya, V., Heinemann, A., Ebner, B., Hackl, H., et al. (2012). Differential response of arterial and venous endothelial cells to extracellular matrix is modulated by oxygen. Histochem. Cell Biol. doi: 10.1007/s00418-012-0917-4 [Epub ahead of print].
63. le Noble, F., Klein, C., Tintu, A., Pries, A., and Buschmann, I. (2008). Neural guidance molecules, tip cells, and mechanical factors in vascular development. Cardiovasc. Res. 78, 232-241. doi: 10.1093/cvr/cvn058.
64. Lu, X., Le Noble, F., Yuan, L., Jiang, Q., De Lafarge, B., Sugiyama, D., et al. (2004). The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 432, 179-186. doi: 10.1038/nature03080.
65. Lux, C. T., Yoshimoto, M., Mcgrath, K., Conway, S. J., Palis, J., and Yoder, M. C. (2008). All primitive and definitive hematopoietic progenitor cells emerging before E10 in the mouse embryo are products of the yolk sac. Blood 111, 3435-3438. doi: 10.1182/blood-2007-08-107086.
66. Matouk, C. C., and Marsden, P. A. (2008). Epigenetic regulation of vascular endothelial gene expression. Circ. Res. 102, 873-887. doi: 10.1161/CIRCRESAHA.107.171025.
67. Miller, S., Walker, S. W., Arthur, J. R., Lewin, M. H., Pickard, K., Nicol, F., et al. (2002). Selenoprotein expression in endothelial cells from different human vasculature and species. Biochim. Biophys. Acta 1588, 85-93. doi: 10.1016/S0925-4439(02)00143-6.
68. Murthi, P., Hiden, U., Rajaraman, G., Liu, H., Borg, A. J., Coombes, F., et al. (2008). Novel homeobox genes are differentially expressed in placental microvascular endothelial cells compared with macrovascular cells. Placenta 29, 624-630. doi: 10.1016/j.placenta.2008.04.006.
69. Murthi, P., So, M., Gude, N. M., Doherty, V. L., Brennecke, S. P., and Kalionis, B. (2007). Homeobox genes are differentially expressed in macrovascular human umbilical vein endothelial cells and microvascular placental endothelial cells. Placenta 28, 219-223. doi: 10.1016/j.placenta.2006.02.012.
70. Ohtani, K., Vlachojannis, G. J., Koyanagi, M., Boeckel, J. N., Urbich, C., Farcas, R., et al. (2011). Epigenetic regulation of endothelial lineage committed genes in pro-angiogenic hematopoietic and endothelial progenitor cells. Circ. Res. 109, 1219-1229. doi: 10.1161/CIRCRESAHA.111.247304.
71. Orr, A. W., Hastings, N. E., Blackman, B. R., and Wamhoff, B. R. (2010). Complex regulation and function of the inflammatory smooth muscle cell phenotype in atherosclerosis. J. Vasc. Res. 47, 168-180. doi: 10.1159/000250095.
72. Owens, G. K., Kumar, M. S., and Wamhoff, B. R. (2004). Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84, 767-801. doi: 10.1152/physrev.00041.2003.
73. Parenti, A., Morbidelli, L., Cui, X. L., Douglas, J. G., Hood, J. D., Granger, H. J., et al. (1998). Nitric oxide is an upstream signal of vascular endothelial growth factor-induced extracellular signal-regulated kinase1/2 activation in postcapillary endothelium. J. Biol. Chem. 273, 4220-4226. doi: 10.1074/jbc.273.7.4220.
74. Peng, Y., and Jahroudi, N. (2003). The NFY transcription factor inhibits von Willebrand factor promoter activation in non-endothelial cells through recruitment of histone deacetylases. J. Biol. Chem. 278, 8385-8394. doi: 10.1074/jbc.M213156200.
75. Pirola, L., Balcerczyk, A., Tothill, R. W., Haviv, I., Kaspi, A., Lunke, S., et al. (2011). Genome-wide analysis distinguishes hyperglycemia regulated epigenetic signatures of primary vascular cells. Genome Res. 21, 1601-1615. doi: 10.1101/gr.116095.110.
76. Pojoga, L. H., Williams, J. S., Yao, T. M., Kumar, A., Raffetto, J. D., Do Nascimento, G. R., et al. (2011). Histone demethylase LSD1 deficiency during high-salt diet is associated with enhanced vascular contraction, altered NO-cGMP relaxation pathway, and hypertension. Am. J. Physiol. Heart Circ. Physiol. 301, H1862-H1871. doi: 10.1152/ajpheart.00513.2011.
77. Rao, X., Zhong, J., Zhang, S., Zhang, Y., Yu, Q., Yang, P., et al. (2011). Loss of methyl-CpG-binding domain protein 2 enhances endothelial angiogenesis and protects mice against hind-limb ischemic injury. Circulation 123, 2964-2974. doi: 10.1161/CIRCULATIONAHA.110.966408.
78. Rossig, L., Li, H., Fisslthaler, B., Urbich, C., Fleming, I., Forstermann, U., et al. (2002). Inhibitors of histone deacetylation downregulate the expression of endothelial nitric oxide synthase and compromise endothelial cell function in vasorelaxation and angiogenesis. Circ. Res. 91, 837-844. doi: 10.1161/01.RES.0000037983.07158.B1.
79. Rossig, L., Urbich, C., Bruhl, T., Dernbach, E., Heeschen, C., Chavakis, E., et al. (2005). Histone deacetylase activity is essential for the expression of HoxA9 and for endothelial commitment of progenitor cells. J. Exp. Med. 201, 1825-1835. doi: 10.1084/jem.20042097.
80. Ruchko, M. V., Gorodnya, O. M., Pastukh, V. M., Swiger, B. M., Middleton, N. S., Wilson, G. L., et al. (2009). Hypoxia-induced oxidative base modifications in the VEGF hypoxia-response element are associated with transcriptionally active nucleosomes. Free Radic. Biol. Med. 46, 352-359. doi: 10.1016/j.freeradbiomed.2008.09.038.
81. Shahani, T., Lavend'homme, R., Luttun, A., Saint-Remy, J. M., Peerlinck, K., and Jacquemin, M. (2010). Activation of human endothelial cells from specific vascular beds induces the release of a FVIII storage pool. Blood 115, 4902-4909. doi: 10.1182/blood-2009-07-232546.
82. Shalaby, F., Rossant, J., Yamaguchi, T. P., Gertsenstein, M., Wu, X. F., Breitman, M. L., et al. (1995). Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376, 62-66. doi: 10.1038/376062a0.
83. Shizukuda, Y., Tang, S., Yokota, R., and Ware, J. A. (1999). Vascular endothelial growth factor-induced endothelial cell migration and proliferation depend on a nitric oxide-mediated decrease in protein kinase Cdelta activity. Circ. Res. 85, 247-256. doi: 10.1161/01.RES.85.3.247.
84. Simard, M., Drolet, R., Blomquist, C. H., and Tremblay, Y. (2011). Human type 2 17beta-hydroxysteroid dehydrogenase in umbilical vein and artery endothelial cells: differential inactivation of sex steroids according to the vessel type. Endocrine 40, 203-211. doi: 10.1007/s12020-011-9519-5.
85. Stefulj, J., Panzenboeck, U., Becker, T., Hirschmugl, B., Schweinzer, C., Lang, I., et al. (2009). Human endothelial cells of the placental barrier efficiently deliver cholesterol to the fetal circulation via ABCA1 and ABCG1. Circ. Res. 104, 600-608. doi: 10.1161/CIRCRESAHA.108.185066.
86. Svensson, K. J., Kucharzewska, P., Christianson, H. C., Skold, S., Lofstedt, T., Johansson, M. C., et al. (2011). Hypoxia triggers a proangiogenic pathway involving cancer cell microvesicles and PAR-2-mediated heparin-binding EGF signaling in endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 108, 13147-13152. doi: 10.1073/pnas.1104261108.
87. Takamura, H., Kasai, H., Arita, H., and Kito, M. (1990). Phospholipid molecular species in human umbilical artery and vein endothelial cells. J. Lipid Res. 31, 709-717.
88. Van Rijen, H., Van Kempen, M. J., Analbers, L. J., Rook, M. B., Van Ginneken, A. C., Gros, D., et al. (1997). Gap junctions in human umbilical cord endothelial cells contain multiple connexins. Am. J. Physiol. 272, C117-C130.
89. Veikkola, T., Lohela, M., Ikenberg, K., Makinen, T., Korff, T., Saaristo, A., et al. (2003). Intrinsic versus microenvironmental regulation of lymphatic endothelial cell phenotype and function. FASEB J. 17, 2006-2013. doi: 10.1096/fj.03-0179com.
90. Wang, G. G., Allis, C. D., and Chi, P. (2007a). Chromatin remodeling and cancer, Part I: covalent histone modifications. Trends Mol. Medic. 13, 363-372. doi: 10.1016/j.molmed.2007.07.003.
91. Wang, G. G., Allis, C. D., and Chi, P. (2007b). Chromatin remodeling and cancer, Part II: ATP-dependent chromatin remodeling. Trends Mol. Med. 13, 373-380. doi: 10.1016/j.molmed.2007.07.004.
92. Wang, K., Jiang, Y. Z., Chen, D. B., and Zheng, J. (2009). Hypoxia enhances FGF2-and VEGF-stimulated human placental artery endothelial cell proliferation: roles of MEK1/2/ERK1/2 and PI3K/AKT1 pathways. Placenta 30, 1045-1051. doi: 10.1016/j.placenta.2009.10.007.
93. Wang, W., Ha, C. H., Jhun, B. S., Wong, C., Jain, M. K., and Jin, Z. G. (2010). Fluid shear stress stimulates phosphorylation-dependent nuclear export of HDAC5 and mediates expression of KLF2 and eNOS. Blood 115, 2971-2979. doi: 10.1182/blood-2009-05-224824.
94. Wu, J., Iwata, F., Grass, J. A., Osborne, C. S., Elnitski, L., Fraser, P., et al. (2005). Molecular determinants of NOTCH4 transcription in vascular endothelium. Mol. Cell. Biol. 25, 1458-1474. doi: 10.1128/MCB.25.4.1458-1474.2005.
95. Xu, X. F., Ma, X. L., Shen, Z., Wu, X. L., Cheng, F., and Du, L. Z. (2010). Epigenetic regulation of the endothelial nitric oxide synthase gene in persistent pulmonary hypertension of the newborn rat. J. Hypertens. 28, 2227-2235. doi: 10.1097/HJH.0b013e32833e08f1.
96. Zampetaki, A., Zeng, L., Margariti, A., Xiao, Q., Li, H., Zhang, Z., et al. (2010). Histone deacetylase 3 is critical in endothelial survival and atherosclerosis development in response to disturbed flow. Circulation 121, 132-142. doi: 10.1161/CIRCULATIONAHA.109.890491.
97. 3 is crucial in shear-and VEGF-induced stem cell differentiation toward endothelial cells. J .Cell Biol. 174, 1059-1069. doi: 10.1083/jcb.200605113.