Vascular development and hemodynamic force in the mouse yolk sac

Frontiers in Physiology

Volumn 5 AUG, Issue , 2014, Pages

  Garcia, Monica D ^a   Larina, Irina V ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Hemodynamics; Live imaging; Mouse development; Vascular remodeling; Yolk sac

Indexed keywords

CADHERIN; CD31 ANTIGEN; EPHRIN RECEPTOR; NOTCH RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR II; TRANSCRIPTION FACTOR TAL1; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; BIOMECHANICS; BLOOD FLOW VELOCITY; CONFOCAL MICROSCOPY; DEVELOPMENTAL BIOLOGY; EMBRYO CULTURE; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; HEART HEMODYNAMICS; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM; YOLK SAC;

EID: 84906494049     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00308     Document Type: Review

References (94)

1. Adams, R. H., Diella, F., Hennig, S., Helmbacher, F., Deutsch, U., and Klein, R. (2001). The cytoplasmic domain of the ligand ephrinB2 is required for vascular morphogenesis but not cranial neural crest migration. Cell 104, 57-69. doi: 10.1016/S0092-8674(01)00191-X
2. Armulik, A., Abramsson, A., and Betsholtz, C. (2005). Endothelial/pericyte interactions. Circ. Res. 97, 512-523. doi: 10.1161/01.RES.0000182903.16652.d7
3. Carmeliet, P. (2003). Angiogenesis in health and disease. Nat. Med. 9, 653-660. doi: 10.1038/nm0603-653
4. Chen, Z., Milner, T. E., Srinivas, S., Wang, X., Malekafzali, A., van Gemert, M. J., et al. (1997). Noninvasive imaging of in vivo blood flow velocity using optical Doppler tomography. Opt. Lett. 22, 1119-1121. doi: 10.1364/OL.22.001119
5. Conlon, R. A., Reaume, A. G., and Rossant, J. (1995). Notch1 is required for the coordinate segmentation of somites. Development 121, 1533-1545.
6. Conway, D. E., Breckenridge, M. T., Hinde, E., Gratton, E., Chen, C. S., and Schwartz, M. A. (2013). Fluid shear stress on endothelial cells modulates mechanical tension across VE-cadherin and PECAM-1. Curr. Biol. 23, 1024-1030. doi: 10.1016/j.cub.2013.04.049
7. Conway, S. J., Kruzynska-Frejtag, A., Kneer, P. L., Machnicki, M., and Koushik, S. V. (2003). What cardiovascular defect does my prenatal mouse mutant have, and why? Genesis 35, 1-21. doi: 10.1002/gene.10152
8. Coultas, L., Chawengsaksophak, K., and Rossant, J. (2005). Endothelial cells and VEGF in vascular development. Nature 438, 937-945. doi: 10.1038/nature04479
9. Culver, J. C., and Dickinson, M. E. (2010). The effects of hemodynamic force on embryonic development. Microcirculation 17, 164-178. doi: 10.1111/j.1549-8719.2010.00025.x
10. Davis, S., Aldrich, T. H., Jones, P. F., Acheson, A., Compton, D. L., Jain, V., et al. (1996). Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 87, 1161-1169. doi: 10.1016/S0092-8674(00)81812-7
11. Dickson, M. C., Martin, J. S., Cousins, F. M., Kulkarni, A. B., Karlsson, S., and Akhurst, R. J. (1995). Defective haematopoiesis and vasculogenesis in transforming growth factor-ß 1 knock out mice. Development 121, 1845-1854.
12. Dirnagl, U., Villringer, A., and Einhaupl, K. M. (1992). In vivo confocal scanning laser microscopy of the cerebral microcirculation. J. Microsc. 165, 147-157. doi: 10.1111/j.1365-2818.1992.tb04312.x
13. Drake, C. J., and Fleming, P. A. (2000). Vasculogenesis in the day 6.5 to 9.5 mouse embryo. Blood 95, 1671-1679.
14. Dumont, D. J., Fong, G. H., Puri, M. C., Gradwohl, G., Alitalo, K., and Breitman, M. L. (1995). Vascularization of the mouse embryo: a study of flk-1, tek, tie, and vascular endothelial growth factor expression during development. Dev. Dyn. 203, 80-92. doi: 10.1002/aja.1002030109
15. Dumont, D. J., Gradwohl, G., Fong, G. H., Puri, M. C., Gertsenstein, M., Auerbach, A., et al. (1994). Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev. 8, 1897-1909. doi: 10.1101/gad.8.16.1897
16. Dumont, D. J., Yamaguchi, T. P., Conlon, R. A., Rossant, J., and Breitman, M. L. (1992). tek, a novel tyrosine kinase gene located on mouse chromosome 4, is expressed in endothelial cells and their presumptive precursors. Oncogene 7, 1471-1480.
17. Duncan, G. S., Andrew, D. P., Takimoto, H., Kaufman, S. A., Yoshida, H., Spellberg, J., et al. (1999). Genetic evidence for functional redundancy of Platelet/Endothelial cell adhesion molecule-1 (PECAM-1): CD31-deficient mice reveal PECAM-1-dependent and PECAM-1-independent functions. J. Immunol. 162, 3022-3030.
18. Dvorak, H. F., Brown, L. F., Detmar, M., and Dvorak, A. M. (1995). Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am. J. Pathol. 146, 1029-1039.
19. Dyer, M. A., Farrington, S. M., Mohn, D., Munday, J. R., and Baron, M. H. (2001). Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify prospective neurectodermal cell fate in the mouse embryo. Development 128, 1717-1730.
20. Fischer, A., Schumacher, N., Maier, M., Sendtner, M., and Gessler, M. (2004). The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev. 18, 901-911. doi: 10.1101/gad.291004
21. Fraser, S. T., Hadjantonakis, A. K., Sahr, K. E., Willey, S., Kelly, O. G., Jones, E. A., et al. (2005). Using a histone yellow fluorescent protein fusion for tagging and tracking endothelial cells in ES cells and mice. Genesis 42, 162-171. doi: 10.1002/gene.20139
22. Gaengel, K., Genove, G., Armulik, A., and Betsholtz, C. (2009). Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler. Thromb. Vasc. Biol. 29, 630-638. doi: 10.1161/ATVBAHA.107.161521
23. Gale, N. W., Dominguez, M. G., Noguera, I., Pan, L., Hughes, V., Valenzuela, D. M., et al. (2004). Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc. Natl. Acad. Sci. U.S.A. 101, 15949-15954. doi: 10.1073/pnas.0407290101
24. Gale, N. W., Thurston, G., Hackett, S. F., Renard, R., Wang, Q., McClain, J., et al. (2002). Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Dev. Cell 3, 411-423. doi: 10.1016/S1534-5807(02)00217-4
25. Garcia, M. D., Udan, R. S., Hadjantonakis, A. K., and Dickinson, M. E. (2011). Live imaging of mouse embryos. Cold Spring Harb. Protoc. 2011, 366-372. doi: 10.1101/pdb.top104
26. Gerety, S. S., and Anderson, D. J. (2002). Cardiovascular ephrinB2 function is essential for embryonic angiogenesis. Development 129, 1397-1410.
27. Gerety, S. S., Wang, H. U., Chen, Z. F., and Anderson, D. J. (1999). Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol. Cell 4, 403-414. doi: 10.1016/S1097-2765(00)80342-1
28. Gory-Faure, S., Prandini, M. H., Pointu, H., Roullot, V., Pignot-Paintrand, I., Vernet, M., et al. (1999). Role of vascular endothelial-cadherin in vascular morphogenesis. Development 126, 2093-2102.
29. Gridley, T. (2010). "Chapter nine - notch signaling in the vasculature," in Current Topics in Developmental Biology, ed K. Raphael (Waltham, MA: Academic Press), 277-309.
30. He, C., Hu, H., Braren, R., Fong, S.-Y., Trumpp, A., Carlson, T. R., et al. (2008). c-myc in the hematopoietic lineage is crucial for its angiogenic function in the mouse embryo. Development 135, 2467-2477. doi: 10.1242/dev.020131
31. Huang, C., Sheikh, F., Hollander, M., Cai, C., Becker, D., Chu, P.-H., et al. (2003). Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis. Development 130, 6111-6119. doi: 10.1242/dev.00831
32. Jakobsson, L., and van Meeteren, L. A. (2013). Transforming growth factor ß family members in regulation of vascular function: in the light of vascular conditional knockouts. Exp. Cell Res. 319, 1264-1270. doi: 10.1016/j.yexcr.2013.02.015
33. Jones, E. A., Baron, M. H., Fraser, S. E., and Dickinson, M. E. (2005). Dynamic in vivo imaging of mammalian hematovascular development using whole embryo culture. Methods Mol. Med. 105, 381-394. doi: 10.1385/1-59259-826-9:381
34. Jones, E. A. V., Baron, M. H., Fraser, S. E., and Dickinson, M. E. (2004). Measuring hemodynamic changes during mammalian development. Am. J. Physiol. Heart Circ. Physiol. 287, H1561-H1569. doi: 10.1152/ajpheart.00081.2004
35. Kappel, A., Schlaeger, T. M., Flamme, I., Orkin, S. H., Risau, W., and Breier, G. (2000). Role of SCL/Tal-1, GATA, and ets transcription factor binding sites for the regulation of flk-1 expression during murine vascular development. Blood 96, 3078-3085.
36. Klagsbrun, M., and Soker, S. (1993). VEGF/VPF: the angiogenesis factor found? Curr. Biol. 3, 699-702. doi: 10.1016/0960-9822(93)90073-W
37. Klein, R. (2012). Eph/ephrin signalling during development. Development 139, 4105-4109. doi: 10.1242/dev.074997
38. Kleinfeld, D., Mitra, P. P., Helmchen, F., and Denk, W. (1998). Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. Proc. Natl. Acad. Sci. U.S.A. 95, 15741-15746. doi: 10.1073/pnas.95.26.15741
39. Korhonen, J., Polvi, A., Partanen, J., and Alitalo, K. (1994). The mouse tie receptor tyrosine kinase gene: expression during embryonic angiogenesis. Oncogene 9, 395-403.
40. Koushik, S. V., Wang, J., Rogers, R., Moskophidis, D., Lambert, N. A., Creazzo, T. L., et al. (2001). Targeted inactivation of the sodium-calcium exchanger (Ncx1) results in the lack of a heartbeat and abnormal myofibrillar organization. FASEB J. 15, 1209-1211. doi: 10.1096/fj.00-0696fje
41. Krebs, L. T., Xue, Y., Norton, C. R., Shutter, J. R., Maguire, M., Sundberg, J. P., et al. (2000). Notch signaling is essential for vascular morphogenesis in mice. Genes Dev. 14, 1343-1352. doi: 10.1101/gad.14.11.1343
42. Larina, I. V., and Dickinson, M. E. (2012). In vivo imaging of the developing mouse embryonic vasculature. Methods Mol. Biol. 872, 205-215. doi: 10.1007/978-1-61779-797-2_14
43. Larina, I. V., Ivers, S., Syed, S., Dickinson, M. E., and Larin, K. V. (2009a). Hemodynamic measurements from individual blood cells in early mammalian embryos with Doppler swept source OCT. Opt. Lett. 34, 986-988. doi: 10.1364/OL.34.000986
44. Larina, I. V., Shen, W., Kelly, O. G., Hadjantonakis, A. K., Baron, M. H., and Dickinson, M. E. (2009b). A membrane associated mCherry fluorescent reporter line for studying vascular remodeling and cardiac function during murine embryonic development. Anat. Rec. (Hoboken). 292, 333-341. doi: 10.1002/ar.20821
45. Larina, I. V., Sudheendran, N., Ghosn, M., Jiang, J., Cable, A., Larin, K. V., et al. (2008). Live imaging of blood flow in mammalian embryos using Doppler swept-source optical coherence tomography. J. Biomed. Opt. 13:060506. doi: 10.1117/1.3046716
46. Larsson, J., Goumans, M. J., Sjostrand, L. J., van Rooijen, M. A., Ward, D., Leveen, P., et al. (2001). Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type I receptor-deficient mice. EMBO J. 20, 1663-1673. doi: 10.1093/emboj/20.7.1663
47. Lehoux, S., Castier, Y., and Tedgui, A. (2006). Molecular mechanisms of the vascular responses to haemodynamic forces. J. Intern. Med. 259, 381-392. doi: 10.1111/j.1365-2796.2006.01624.x
48. le Noble, F., Moyon, D., Pardanaud, L., Yuan, L., Djonov, V., Matthijsen, R., et al. (2004). Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development 131, 361-375. doi: 10.1242/dev.00929
49. Letterio, J. J., Geiser, A. G., Kulkarni, A. B., Roche, N. S., Sporn, M. B., and Roberts, A. B. (1994). Maternal rescue of transforming growth factor-beta 1 null mice. Science 264, 1936-1938. doi: 10.1126/science.8009224
50. Leung, D. W., Cachianes, G., Kuang, W. J., Goeddel, D. V., and Ferrara, N. (1989). Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246, 1306-1309. doi: 10.1126/science.2479986
51. Lucitti, J. L., Jones, E. A. V., Huang, C., Chen, J., Fraser, S. E., and Dickinson, M. E. (2007). Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development 134, 3317-3326. doi: 10.1242/dev.02883
52. Mahmud, M. S., Cadotte, D. W., Vuong, B., Sun, C., Luk, T. W., Mariampillai, A., et al. (2013). Review of speckle and phase variance optical coherence tomography to visualize microvascular networks. J. Biomed. Opt. 18:50901. doi: 10.1117/1.JBO.18.5.050901
53. Maisonpierre, P. C., Suri, C., Jones, P. F., Bartunkova, S., Wiegand, S. J., Radziejewski, C., et al. (1997). Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277, 55-60. doi: 10.1126/science.277.5322.55
54. Matsumoto, N., Kubo, A., Liu, H., Akita, K., Laub, F., Ramirez, F., et al. (2006). Developmental regulation of yolk sac hematopoiesis by Kruppel-like factor 6. Blood 107, 1357-1365. doi: 10.1182/blood-2005-05-1916
55. May, S. R., Stewart, N. J., Chang, W., and Peterson, A. S. (2004). A Titin mutation defines roles for circulation in endothelial morphogenesis. Dev. Biol. 270, 31-46. doi: 10.1016/j.ydbio.2004.02.006
56. Newman, P. J., and Newman, D. K. (2003). Signal transduction pathways mediated by PECAM-1: new roles for an old molecule in platelet and vascular cell biology. Arterioscler. Thromb. Vasc. Biol. 23, 953-964. doi: 10.1161/01.ATV.0000071347.69358.D9
57. Nowotschin, S., and Hadjantonakis, A. K. (2010). Cellular dynamics in the early mouse embryo: from axis formation to gastrulation. Curr. Opin. Genet. Dev. 20, 420-427. doi: 10.1016/j.gde.2010.05.008
58. Oh, S. P., Seki, T., Goss, K. A., Imamura, T., Yi, Y., Donahoe, P. K., et al. (2000). Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 97, 2626-2631. doi: 10.1073/pnas.97.6.2626
59. Osawa, M., Masuda, M., Kusano, K.-I., and Fujiwara, K. (2002). Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction: is it a mechanoresponsive molecule? J. Cell Biol. 158, 773-785. doi: 10.1083/jcb.200205049
60. Oshima, M., Oshima, H., and Taketo, M. M. (1996). TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev. Biol. 179, 297-302. doi: 10.1006/dbio.1996.0259
61. Pereira, F. A., Qiu, Y., Zhou, G., Tsai, M. J., and Tsai, S. Y. (1999). The orphan nuclear receptor COUP-TFII is required for angiogenesis and heart development. Genes Dev. 13, 1037-1049. doi: 10.1101/gad.13.8.1037
62. Petrova, T. V., Makinen, T., and Alitalo, K. (1999). Signaling via vascular endothelial growth factor receptors. Exp. Cell Res. 253, 117-130. doi: 10.1006/excr.1999.4707
63. Poole, T. J., Finkelstein, E. B., and Cox, C. M. (2001). The role of FGF and VEGF in angioblast induction and migration during vascular development. Dev. Dyn. 220, 1-17. doi: 10.1002/1097-0177(2000)9999:9999<::AID-DVDY1087>3.0.CO;2-2
64. Porcher, C., Swat, W., Rockwell, K., Fujiwara, Y., Alt, F. W., and Orkin, S. H. (1996). The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 86, 47-57. doi: 10.1016/S0092-8674(00)80076-8
65. Risau, W. (1997). Mechanisms of angiogenesis. Nature 386, 671-674. doi: 10.1038/386671a0
66. Risau, W., and Flamme, I. (1995). Vasculogenesis. Annu. Rev. Cell Dev. Biol. 11, 73-91. doi: 10.1146/annurev.cb.11.110195.000445
67. Robb, L., Lyons, I., Li, R., Hartley, L., Köntgen, F., Harvey, R. P., et al. (1995). Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc. Natl. Acad. Sci. U.S.A. 92, 7075-7079. doi: 10.1073/pnas.92.15.7075
68. Sato, T. N., Qin, Y., Kozak, C. A., and Audus, K. L. (1993). Tie-1 and tie-2 define another class of putative receptor tyrosine kinase genes expressed in early embryonic vascular system. Proc. Natl. Acad. Sci. U.S.A. 90, 9355-9358. doi: 10.1073/pnas.90.20.9355
69. Sato, T. N., Tozawa, Y., Deutsch, U., Wolburg-Buchholz, K., Fujiwara, Y., Gendron-Maguire, M., et al. (1995). Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 376, 70-74. doi: 10.1038/376070a0
70. Satyanarayana, A., Gudmundsson, K. O., Chen, X., Coppola, V., Tessarollo, L., Keller, J. R., et al. (2010). RapGEF2 is essential for embryonic hematopoiesis but dispensable for adult hematopoiesis. Blood 116, 2921-2931. doi: 10.1182/blood-2010-01-262964
71. Schnurch, H., and Risau, W. (1993). Expression of tie-2, a member of a novel family of receptor tyrosine kinases, in the endothelial cell lineage. Development 119, 957-968.
72. Shalaby, F., Ho, J., Stanford, W. L., Fischer, K. D., Schuh, A. C., Schwartz, L., et al. (1997). A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 89, 981-990. doi: 10.1016/S0092-8674(00)80283-4
73. Shay-Salit, A., Shushy, M., Wolfovitz, E., Yahav, H., Breviario, F., Dejana, E., et al. (2002). VEGF receptor 2 and the adherens junction as a mechanical transducer in vascular endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 99, 9462-9467. doi: 10.1073/pnas.142224299
74. Shibuya, M., and Claesson-Welsh, L. (2006). Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Exp. Cell Res. 312, 549-560. doi: 10.1016/j.yexcr.2005.11.012
75. Shivdasani, R. A., Mayer, E. L., and Orkin, S. H. (1995). Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature 373, 432-434. doi: 10.1038/373432a0
76. Solnica-Krezel, L., and Sepich, D. S. (2012). Gastrulation: making and shaping germ layers. Annu. Rev. Cell Dev. Biol. 28, 687-717. doi: 10.1146/annurev-cellbio-092910-154043
77. Sudheendran, N., Syed, S. H., Dickinson, M. E., Larina, I. V., and Larin, K. V. (2011). Speckle variance OCT imaging of the vasculature in live mammalian embryos. Laser Phys. Lett. 8, 247-252. doi: 10.1002/lapl.201010120
78. Suri, C., Jones, P. F., Patan, S., Bartunkova, S., Maisonpierre, P. C., Davis, S., et al. (1996). Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87, 1171-1180. doi: 10.1016/S0092-8674(00)81813-9
79. Tanaka, M., Chen, Z., Bartunkova, S., Yamasaki, N., and Izumo, S. (1999). The cardiac homeobox gene Csx/Nkx2.5 lies genetically upstream of multiple genes essential for heart development. Development 126, 1269-1280.
80. Tzima, E., Del Pozo, M. A., Kiosses, W. B., Mohamed, S. A., Li, S., Chien, S., et al. (2002). Activation of Rac1 by shear stress in endothelial cells mediates both cytoskeletal reorganization and effects on gene expression. EMBO J. 21, 6791-6800. doi: 10.1093/emboj/cdf688
81. Tzima, E., del Pozo, M. A., Shattil, S. J., Chien, S., and Schwartz, M. A. (2001). Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment. EMBO J. 20, 4639-4647. doi: 10.1093/emboj/20.17.4639
82. Tzima, E., Irani-Tehrani, M., Kiosses, W. B., Dejana, E., Schultz, D. A., Engelhardt, B., et al. (2005). A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437, 426-431. doi: 10.1038/nature03952
83. Tzima, E., Kiosses, W. B., del Pozo, M. A., and Schwartz, M. A. (2003). Localized Cdc42 activation, detected using a novel assay, mediates microtubule organizing center positioning in endothelial cells in response to fluid shear stress. J. Biol. Chem. 278, 31020-31023. doi: 10.1074/jbc.M301179200
84. Udan, R. S., Culver, J. C., and Dickinson, M. E. (2013a). Understanding vascular development. Wiley Interdiscip. Rev. Dev. Biol. 2, 327-346. doi: 10.1002/wdev.91
85. Udan, R. S., Vadakkan, T. J., and Dickinson, M. E. (2013b). Dynamic responses of endothelial cells to changes in blood flow during vascular remodeling of the mouse yolk sac. Development 140, 4041-4050. doi: 10.1242/dev.096255
86. Urness, L. D., Sorensen, L. K., and Li, D. Y. (2000). Arteriovenous malformations in mice lacking activin receptor-like kinase-1. Nat. Genet. 26, 328-331. doi: 10.1038/81634
87. Valenzuela, D. M., Griffiths, J. A., Rojas, J., Aldrich, T. H., Jones, P. F., Zhou, H., et al. (1999). Angiopoietins 3 and 4: diverging gene counterparts in mice and humans. Proc. Natl. Acad. Sci. U.S.A. 96, 1904-1909. doi: 10.1073/pnas.96.5.1904
88. Villa, N., Walker, L., Lindsell, C. E., Gasson, J., Iruela-Arispe, M. L., and Weinmaster, G. (2001). Vascular expression of Notch pathway receptors and ligands is restricted to arterial vessels. Mech. Dev. 108, 161-164. doi: 10.1016/S0925-4773(01)00469-5
89. Visvader, J. E., Fujiwara, Y., and Orkin, S. H. (1998). Unsuspected role for the T-cell leukemia protein SCL/tal-1 in vascular development. Genes Dev. 12, 473-479. doi: 10.1101/gad.12.4.473
90. Wakimoto, K., Kobayashi, K., Kuro-o, M., Yao, A., Iwamoto, T., Yanaka, N., et al. (2000). Targeted disruption of Na+/Ca2+ Exchanger gene leads to cardiomyocyte apoptosis and defects in heartbeat. J. Biol. Chem. 275, 36991-36998. doi: 10.1074/jbc.M004035200
91. Wang, H. U., Chen, Z. F., and 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, 741-753. doi: 10.1016/S0092-8674(00)81436-1
92. Xue, Y., Gao, X., Lindsell, C. E., Norton, C. R., Chang, B., Hicks, C., et al. (1999). Embryonic lethality and vascular defects in mice lacking the notch ligand jagged1. Hum. Mol. Genet. 8, 723-730. doi: 10.1093/hmg/8.5.723
93. Yang, X., Castilla, L. H., Xu, X., Li, C., Gotay, J., Weinstein, M., et al. (1999). Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5. Development 126, 1571-1580.
94. You, L.-R., Lin, F.-J., Lee, C. T., DeMayo, F. J., Tsai, M.-J., and Tsai, S. Y. (2005). Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature 435, 98-104. doi: 10.1038/nature03511