Endothelial differentiation: Molecular mechanisms of specification and heterogeneity

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 7, 2011, Pages 1476-1484

  Atkins, G Brandon ^a   Jain, Mukesh K ^b   Hamik, Anne ^a  

^a UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^b NONE   (United States)

Author keywords

angiogenesis; biology, developmental; endothelium; vascular biology

Indexed keywords

EPHRIN RECEPTOR B4; MITOGEN ACTIVATED PROTEIN KINASE; NOTCH1 RECEPTOR; NOTCH4 RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; SONIC HEDGEHOG PROTEIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 3;

BRAIN; CELL DIFFERENTIATION; CELL HETEROGENEITY; CLASSIFICATION; ENDOTHELIUM; ENDOTHELIUM CELL; FENESTRATION; HEMANGIOBLAST; HUMAN; KIDNEY EPITHELIUM; LYMPHATIC SYSTEM; MOLECULAR DYNAMICS; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ANIMALS; ARTERIES; BODY PATTERNING; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; LYMPHATIC VESSELS; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; SIGNAL TRANSDUCTION; VEINS;

EID: 79959760473     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.228999     Document Type: Review

References (112)

1. Aitsebaomo J, Portbury AL, Schisler JC, Patterson C. Brothers and sisters: molecular insights into arterial-venous heterogeneity. Circ Res. 2008;103:929-939.
2. Hong CC, Kume T, Peterson RT. Role of crosstalk between phosphatidylinositol 3-kinase and extracellular signal-regulated kinase/mitogenactivated protein kinase pathways in artery-vein specification. Circ Res. 2008;103:573-579.
3. Swift MR, Weinstein BM. Arterial-venous specification during development. Circ Res. 2009;104:576-588.
4. Le Bras A, Vijayaraj P, Oettgen P. Molecular mechanisms of endothelial differentiation. Vasc Med. 2010;15:321-331.
5. Kume T. Specification of arterial, venous, and lymphatic endothelial cells during embryonic development. Histol Histopathol. 2010;25: 637-646.
6. Tammela T, Alitalo K. Lymphangiogenesis: molecular mechanisms and future promise. Cell. 2010;140:460-476.
7. Zhong TP, Childs S, Leu JP, Fishman MC. Gridlock signalling pathway fashions the first embryonic artery. Nature. 2001;414:216-220. (Pubitemid 33051237)
8. Vogeli KM, Jin SW, Martin GR, Stainier DY. A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula. Nature. 2006;443:337-339. (Pubitemid 44435152)
9. Vokes SA, Yatskievych TA, Heimark RL, McMahon J, McMahon AP, Antin PB, Krieg PA. Hedgehog signaling is essential for endothelial tube formation during vasculogenesis. Development. 2004;131: 4371-4380. (Pubitemid 39276203)
10. Jia J, Tong C, Wang B, Luo L, Jiang J. Hedgehog signalling activity of Smoothened requires phosphorylation by protein kinase A and casein kinase I. Nature. 2004;432:1045-1050. (Pubitemid 40052237)
11. Nicoli S, Tobia C, Gualandi L, De Sena G, Presta M. Calcitonin receptor-like receptor guides arterial differentiation in zebrafish. Blood. 2008;111:4965-4972.
12. Yurugi-Kobayashi T, Itoh H, Schroeder T, Nakano A, Narazaki G, Kita F, Yanagi K, Hiraoka-Kanie M, Inoue E, Ara T, Nagasawa T, Just U, Nakao K, Nishikawa S, Yamashita JK. Adrenomedullin/cyclic AMP pathway induces Notch activation and differentiation of arterial endothelial cells from vascular progenitors. Arterioscler Thromb Vasc Biol. 2006;26:1977-1984. (Pubitemid 44253777)
13. Lawson ND, Mugford JW, Diamond BA, Weinstein BM. Phospholipase Cγ-1 is required downstream of vascular endothelial growth factor during arterial development. Genes Dev. 2003;17:1346-1351. (Pubitemid 36666004)
14. Hong CC, Peterson QP, Hong JY, Peterson RT. Artery/vein specification is governed by opposing phosphatidylinositol-3 kinase and MAP kinase/ERK signaling. Curr Biol. 2006;16:1366-1372. (Pubitemid 43975369)
15. Hayashi H, Kume T. Foxc transcription factors directly regulate Dll4 and Hey2 expression by interacting with the VEGF-Notch signaling pathways in endothelial cells. PLoS One. 2008;3:e2401.
16. Seo S, Fujita H, Nakano A, Kang M, Duarte A, Kume T. The forkhead transcription factors, Foxc1 and Foxc2, are required for arterial specification and lymphatic sprouting during vascular development. Dev Biol. 2006;294:458-470. (Pubitemid 43884821)
17. Gale NW, Dominguez MG, Noguera I, Pan L, Hughes V, Valenzuela DM, Murphy AJ, Adams NC, Lin HC, Holash J, Thurston G, Yancopoulos GD. Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc Natl Acad Sci USA. 2004;101:15949-15954. (Pubitemid 39507907)
18. Sorensen I, Adams RH, Gossler A. DLL1-mediated Notch activation regulates endothelial identity in mouse fetal arteries. Blood. 2009;113: 5680-5688.
19. Fischer A, Schumacher N, Maier M, Sendtner M, Gessler M. The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev. 2004;18:901-911. (Pubitemid 38529659)
20. Kokubo H, Miyagawa-Tomita S, Nakazawa M, Saga Y, Johnson RL. Mouse hesr1 and hesr2 genes are redundantly required to mediate Notch signaling in the developing cardiovascular system. Dev Biol. 2005;278: 301-309. (Pubitemid 40175030)
21. Weinstein BM, Stemple DL, Driever W, Fishman MC. Gridlock, a localized heritable vascular patterning defect in the zebrafish. Nat Med. 1995;1:1143-1147.
22. Cermenati S, Moleri S, Cimbro S, Corti P, Del Giacco L, Amodeo R, Dejana E, Koopman P, Cotelli F, Beltrame M. Sox18 and Sox7 play redundant roles in vascular development. Blood. 2008;111:2657-2666.
23. Herpers R, van de Kamp E, Duckers HJ, Schulte-Merker S. Redundant roles for sox7 and sox18 in arteriovenous specification in zebrafish. Circ Res. 2008;102:12-15.
24. Pendeville H, Winandy M, Manfroid I, Nivelles O, Motte P, Pasque V, Peers B, Struman I, Martial JA, Voz ML. Zebrafish Sox7 and Sox18 function together to control arterial-venous identity. Dev Biol. 2008;317: 405-416.
25. Wang HU, Chen ZF, Anderson DJ. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell. 1998;93:741-753. (Pubitemid 28257581)
26. Adams RH, Wilkinson GA, Weiss C, Diella F, Gale NW, Deutsch U, Risau W, Klein R. Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev. 1999; 13:295-306. (Pubitemid 29095801)
27. Moyon D, Pardanaud L, Yuan L, Breant C, Eichmann A. Plasticity of endothelial cells during arterial-venous differentiation in the avian embryo. Development. 2001;128:3359-3370. (Pubitemid 32910388)
28. Herzog Y, Kalcheim C, Kahane N, Reshef R, Neufeld G. Differential expression of neuropilin-1 and neuropilin-2 in arteries and veins. Mech Dev. 2001;109:115-119. (Pubitemid 33035924)
29. Kitsukawa T, Shimizu M, Sanbo M, Hirata T, Taniguchi M, Bekku Y, Yagi T, Fujisawa H. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron. 1997;19:995-1005. (Pubitemid 27512361)
30. Kawasaki T, Kitsukawa T, Bekku Y, Matsuda Y, Sanbo M, Yagi T, Fujisawa H. A requirement for neuropilin-1 in embryonic vessel formation. Development. 1999;126:4895-4902.
31. Jones EA, Yuan L, Breant C, Watts RJ, Eichmann A. Separating genetic and hemodynamic defects in neuropilin 1 knockout embryos. Development. 2008;135:2479-2488.
32. Mukouyama YS, Gerber HP, Ferrara N, Gu C, Anderson DJ. Peripheral nerve-derived VEGF promotes arterial differentiation via neuropilin 1-mediated positive feedback. Development. 2005;132:941-952. (Pubitemid 40484929)
33. Lanner F, Sohl M, Farnebo F. Functional arterial and venous fate is determined by graded VEGF signaling and notch status during embryonic stem cell differentiation. Arterioscler Thromb Vasc Biol. 2007;27:487-493.
34. Lawson ND, Vogel AM, Weinstein BM. Sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev Cell. 2002;3:127-136. (Pubitemid 34778401)
35. Blum S, Issbruker K, Willuweit A, Hehlgans S, Lucerna M, Mechtcheriakova D, Walsh K, von der Ahe D, Hofer E, Clauss M. An inhibitory role of the phosphatidylinositol 3-kinase-signaling pathway in vascular endothelial growth factor-induced tissue factor expression. J Biol Chem. 2001;276:33428-33434.
36. Liu ZJ, Xiao M, Balint K, Soma A, Pinnix CC, Capobianco AJ, Velazquez OC, Herlyn M. Inhibition of endothelial cell proliferation by Notch1 signaling is mediated by repressing MAPK and PI3K/Akt pathways and requires MAML1. FASEB J. 2006;20:1009-1011.
37. Liu ZJ, Shirakawa T, Li Y, Soma A, Oka M, Dotto GP, Fairman RM, Velazquez OC, Herlyn M. Regulation of Notch1 and Dll4 by vascular endothelial growth factor in arterial endothelial cells: implications for modulating arteriogenesis and angiogenesis. Mol Cell Biol. 2003;23: 14-25. (Pubitemid 36008497)
38. You LR, Lin FJ, Lee CT, DeMayo FJ, Tsai MJ, Tsai SY. Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature. 2005;435:98-104. (Pubitemid 40655915)
39. Lin FJ, Chen X, Qin J, Hong YK, Tsai MJ, Tsai SY. Direct transcriptional regulation of neuropilin-2 by COUP-TFII modulates multiple steps in murine lymphatic vessel development. J Clin Invest. 2010;120: 1694-1707.
40. Wigle JT, Harvey N, Detmar M, Lagutina I, Grosveld G, Gunn MD, Jackson DG, Oliver G. An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J. 2002;21:1505-1513. (Pubitemid 34614607)
41. Gale NW, Prevo R, Espinosa J, Ferguson DJ, Dominguez MG, Yancopoulos GD, Thurston G, Jackson DG. Normal lymphatic development and function in mice deficient for the lymphatic hyaluronan receptor LYVE-1. Mol Cell Biol. 2007;27:595-604. (Pubitemid 46080127)
42. Francois M, Caprini A, Hosking B, Orsenigo F, Wilhelm D, Browne C, Paavonen K, Karnezis T, Shayan R, Downes M, Davidson T, Tutt D, Cheah KS, Stacker SA, Muscat GE, Achen MG, Dejana E, Koopman P. Sox18 induces development of the lymphatic vasculature in mice. Nature. 2008;456:643-647.
43. Wigle JT, Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell. 1999;98:769-778. (Pubitemid 29446894)
44. Oliver G. Lymphatic vasculature development. Nat Rev Immunol. 2004; 4:35-45. (Pubitemid 38084130)
45. Hermans K, Claes F, Vandevelde W, Zheng W, Geudens I, Orsenigo F, De Smet F, Gjini E, Anthonis K, Ren B, Kerjaschki D, Autiero M, Ny A, Simons M, Dewerchin M, Schulte-Merker S, Dejana E, Alitalo K, Carmeliet P. Role of synectin in lymphatic development in zebrafish and frogs. Blood. 2010;116:3356-3366.
46. Pedrioli DM, Karpanen T, Dabouras V, Jurisic G, van de Hoek G, Shin JW, Marino D, Kalin RE, Leidel S, Cinelli P, Schulte-Merker S, Brandli AW, Detmar M. miR-31 functions as a negative regulator of lymphatic vascular lineage-specific differentiation in vitro and vascular development in vivo. Mol Cell Biol. 2010;30:3620-3634.
47. Tammela T, Enholm B, Alitalo K, Paavonen K. The biology of vascular endothelial growth factors. Cardiovasc Res. 2005;65:550-563. (Pubitemid 40138976)
48. Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV, Jeltsch M, Jackson DG, Talikka M, Rauvala H, Betsholtz C, Alitalo K. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol. 2004;5:74-80. (Pubitemid 38081471)
49. Othman-Hassan K, Patel K, Papoutsi M, Rodriguez-Niedenfuhr M, Christ B, Wilting J. Arterial identity of endothelial cells is controlled by local cues. Dev Biol. 2001;237:398-409. (Pubitemid 32881130)
50. Roca C, Adams RH. Regulation of vascular morphogenesis by Notch signaling. Genes Dev. 2007;21:2511-2524. (Pubitemid 47607663)
51. Lee S, Choi I, Hong YK. Heterogeneity and plasticity of lymphatic endothelial cells. Semin Thromb Hemost. 2010;36:352-361.
52. Oliver G, Srinivasan RS. Endothelial cell plasticity: how to become and remain a lymphatic endothelial cell. Development. 2010;137: 363-372.
53. Johnson NC, Dillard ME, Baluk P, McDonald DM, Harvey NL, Frase SL, Oliver G. Lymphatic endothelial cell identity is reversible and its maintenance requires Prox1 activity. Genes Dev. 2008;22: 3282-3291.
54. Hong YK, Harvey N, Noh YH, Schacht V, Hirakawa S, Detmar M, Oliver G. Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate. Dev Dyn. 2002;225:351-357. (Pubitemid 35265813)
55. Petrova TV, Makinen T, Makela TP, Saarela J, Virtanen I, Ferrell RE, Finegold DN, Kerjaschki D, Yla-Herttuala S, Alitalo K. Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J. 2002;21:4593-4599. (Pubitemid 34984346)
56. Kang J, Yoo J, Lee S, Tang W, Aguilar B, Ramu S, Choi I, Otu HH, Shin JW, Dotto GP, Koh CJ, Detmar M, Hong YK. An exquisite cross-control mechanism among endothelial cell fate regulators directs the plasticity and heterogeneity of lymphatic endothelial cells. Blood. 2010;116:140-150.
57. Aird WC. Phenotypic heterogeneity of the endothelium: I: structure, function, and mechanisms. Circ Res. 2007;100:158-173. (Pubitemid 46208717)
58. Aird WC. Phenotypic heterogeneity of the endothelium: II: representative vascular beds. Circ Res. 2007;100:174-190. (Pubitemid 46208718)
59. Molema G. Heterogeneity in endothelial responsiveness to cytokines, molecular causes, and pharmacological consequences. Semin Thromb Hemost. 2010;36:246-264.
60. Davies PF, Civelek M, Fang Y, Guerraty MA, Passerini AG. Endothelial heterogeneity associated with regional athero-susceptibility and adaptation to disturbed blood flow in vivo. Semin Thromb Hemost. 2010;36: 265-275.
61. Kwaan HC, Samama MM. The significance of endothelial heterogeneity in thrombosis and hemostasis. Semin Thromb Hemost. 2010;36: 286-300.
62. Tse D, Stan RV. Morphological heterogeneity of endothelium. Semin Thromb Hemost. 2010;36:236-245.
63. Dejana E. Endothelial cell-cell junctions: happy together. Nat Rev Mol Cell Biol. 2004;5:261-270. (Pubitemid 38480607)
64. Bazzoni G, Dejana E. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev. 2004;84: 869-901. (Pubitemid 38823769)
65. Stan RV. Structure of caveolae. Biochim Biophys Acta. 2005;1746: 334-348. (Pubitemid 41815027)
66. Parton RG, Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol. 2007;8:185-194.
67. Bendayan M. Morphological and cytochemical aspects of capillary permeability. Microsc Res Tech. 2002;57:327-349. (Pubitemid 34579215)
68. Kathuria H, Cao YX, Ramirez MI, Williams MC. Transcription of the caveolin-1 gene is differentially regulated in lung type I epithelial and endothelial cell lines. A role for ETS proteins in epithelial cell expression. J Biol Chem. 2004;279:30028-30036. (Pubitemid 38937923)
69. Dvorak AM, Kohn S, Morgan ES, Fox P, Nagy JA, Dvorak HF. The vesiculo-vacuolar organelle (VVO): a distinct endothelial cell structure that provides a transcellular pathway for macromolecular extravasation. J Leukoc Biol. 1996;59:100-115. (Pubitemid 26054596)
70. Dvorak AM, Feng D. The vesiculo-vacuolar organelle (VVO). A new endothelial cell permeability organelle. J Histochem Cytochem. 2001; 49:419-432.
71. Simionescu M, Simionescu N, Palade GE. Morphometric data on the endothelium of blood capillaries. J Cell Biol. 1974;60:128-152.
72. Stan RV, Kubitza M, Palade GE. PV-1 is a component of the fenestral and stomatal diaphragms in fenestrated endothelia. Proc Natl Acad Sci USA. 1999;96:13203-13207.
73. Stan RV, Tkachenko E, Niesman IR. PV1 is a key structural component for the formation of the stomatal and fenestral diaphragms. Mol Biol Cell. 2004;15:3615-3630. (Pubitemid 38989701)
74. Ioannidou S, Deinhardt K, Miotla J, Bradley J, Cheung E, Samuelsson S, Ng YS, Shima DT. An in vitro assay reveals a role for the diaphragm protein PV-1 in endothelial fenestra morphogenesis. Proc Natl Acad Sci USA. 2006;103:16770-16775. (Pubitemid 44737328)
75. Stan RV. Endothelial stomatal and fenestral diaphragms in normal vessels and angiogenesis. J Cell Mol Med. 2007;11:621-643. (Pubitemid 47313310)
76. Braet F, Wisse E. Structural and functional aspects of liver sinusoidal endothelial cell fenestrae: a review. Comp Hepatol. 2002;1:1.
77. Haraldsson B, Jeansson M. Glomerular filtration barrier. Curr Opin Nephrol Hypertens. 2009;18:331-335.
78. Levidiotis V, Power DA. New insights into the molecular biology of the glomerular filtration barrier and associated disease. Nephrology (Carlton). 2005;10:157-166. (Pubitemid 40776276)
79. Weinbaum S, Tarbell JM, Damiano ER. The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng. 2007;9: 121-167. (Pubitemid 350246654)
80. Bulger RE, Eknoyan G, Purcell DJ, II, Dobyan DC. Endothelial characteristics of glomerular capillaries in normal, mercuric chlorideinduced, and gentamicin-induced acute renal failure in the rat. J Clin Invest. 1983;72:128-141. (Pubitemid 13026636)
81. Kriz W. Fenestrated glomerular capillaries are unique. J Am Soc Nephrol. 2008;19:1439-1440.
82. Ichimura K, Stan RV, Kurihara H, Sakai T. Glomerular endothelial cells form diaphragms during development and pathologic conditions. J Am Soc Nephrol. 2008;19:1463-1471.
83. Satchell SC, Braet F. Glomerular endothelial cell fenestrations: an integral component of the glomerular filtration barrier. Am J Physiol Renal Physiol. 2009;296:F947-F956.
84. Breier G, Albrecht U, Sterrer S, Risau W. Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development. 1992;114:521-532.
85. Roberts WG, Palade GE. Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci. 1995;108:2369-2379.
86. Roberts WG, Palade GE. Neovasculature induced by vascular endothelial growth factor is fenestrated. Cancer Res. 1997;57:765-772. (Pubitemid 27085664)
87. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, Gerber HP, Kikkawa Y, Miner JH, Quaggin SE. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest. 2003;111:707-716. (Pubitemid 36278589)
88. Eremina V, Baelde HJ, Quaggin SE. Role of the VEGF-a signaling pathway in the glomerulus: evidence for crosstalk between components of the glomerular filtration barrier. Nephron Physiol. 2007; 106:32-37.
89. Eremina V, Jefferson JA, Kowalewska J, Hochster H, Haas M, Weisstuch J, Richardson C, Kopp JB, Kabir MG, Backx PH, Gerber HP, Ferrara N, Barisoni L, Alpers CE, Quaggin SE. VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med. 2008;358: 1129-1136. (Pubitemid 351398487)
90. Pallone TL, Turner MR, Edwards A, Jamison RL. Countercurrent exchange in the renal medulla. Am J Physiol Regul Integr Comp Physiol. 2003;284:R1153-R1175. (Pubitemid 36457558)
91. Pallone TL, Zhang Z, Rhinehart K. Physiology of the renal medullary microcirculation. Am J Physiol Renal Physiol. 2003;284:F253-F266. (Pubitemid 36114688)
92. Engelhardt B. Development of the blood-brain barrier. Cell Tissue Res. 2003;314:119-129. (Pubitemid 37409918)
93. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis. 2010; 37:13-25.
94. Paolinelli R, Corada M, Orsenigo F, Dejana E. The molecular basis of the blood brain barrier differentiation and maintenance: is it still a mystery? Pharmacol Res. 2011;63:165-171.
95. Lee HS, Han J, Bai HJ, Kim KW. Brain angiogenesis in developmental and pathological processes: regulation, molecular and cellular communication at the neurovascular interface. FEBS J. 2009;276:4622-4635.
96. Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev. 2005;57:173-185. (Pubitemid 41043883)
97. Armulik A, Genove G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, He L, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C. Pericytes regulate the blood-brain barrier. Nature. 2010;468: 557-561.
98. Daneman R, Zhou L, Kebede AA, Barres BA. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature. 2010;468: 562-566.
99. Lee SW, Kim WJ, Choi YK, Song HS, Son MJ, Gelman IH, Kim YJ, Kim KW. SSeCKS regulates angiogenesis and tight junction formation in blood-brain barrier. Nat Med. 2003;9:900-906. (Pubitemid 36889933)
100. Liebner S, Plate KH. Differentiation of the brain vasculature: the answer came blowing by the Wnt. J Angiogenes Res. 2010;2:1.
101. Daneman R, Agalliu D, Zhou L, Kuhnert F, Kuo CJ, Barres BA. Wnt/beta-catenin signaling is required for CNS, but not non-CNS, angiogenesis. Proc Natl Acad Sci USA. 2009;106:641-646.
102. Stenman JM, Rajagopal J, Carroll TJ, Ishibashi M, McMahon J, McMahon AP. Canonical Wnt signaling regulates organ-specific assembly and differentiation of CNS vasculature. Science. 2008;322:1247-1250.
103. Liebner S, Corada M, Bangsow T, Babbage J, Taddei A, Czupalla CJ, Reis M, Felici A, Wolburg H, Fruttiger M, Taketo MM, von Melchner H, Plate KH, Gerhardt H, Dejana E. Wnt/beta-catenin signaling controls development of the blood-brain barrier. J Cell Biol. 2008;183:409-417.
104. Franco CA, Liebner S, Gerhardt H. Vascular morphogenesis: a Wnt for every vessel? Curr Opin Genet Dev. 2009;19:476-483.
105. Gimbrone MA Jr. Vascular endothelium, hemodynamic forces, and atherogenesis. Am J Pathol. 1999;155:1-5.
106. Gimbrone MA Jr, Topper JN, Nagel T, Anderson KR, Garcia-Cardena G. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann N Y Acad Sci. 2000;902:230-239; discussion 239-240.
107. Topper JN, Cai J, Falb D, Gimbrone MA Jr. Identification of vascular endothelial genes differentially responsive to fluid mechanical stimuli: cyclooxygenase-2, manganese superoxide dismutase, and endothelial cell nitric oxide synthase are selectively up-regulated by steady laminar shear stress. Proc Natl Acad Sci USA. 1996;93:10417-10422.
108. Takada Y, Shinkai F, Kondo S, Yamamoto S, Tsuboi H, Korenaga R, Ando J. Fluid shear stress increases the expression of thrombomodulin by cultured human endothelial cells. Biochem Biophys Res Commun. 1994;205:1345-1352.
109. Neish AS, Williams AJ, Palmer HJ, Whitley MZ, Collins T. Functional analysis of the human vascular cell adhesion molecule 1 promoter. J Exp Med. 1992;176:1583-1593.
110. Collins T, Cybulsky MI. NF-κB: pivotal mediator or innocent bystander in atherogenesis? J Clin Invest. 2001;107:255-264. (Pubitemid 32157955)
111. Atkins GB, Jain MK. Role of Kruppel-like transcription factors in endothelial biology. Circ Res. 2007;100:1686-1695. (Pubitemid 46987860)
112. Berg DK, Smith CS, Pearton DJ, Wells DN, Broadhurst R, Donnison M, Pfeffer PL. Trophectoderm lineage determination in cattle. Dev Cell. 2011;20:244-255.